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Recent Advances in the Innate Immunity of Invertebrate Animals

  • Iwanaga, Sadaaki (The Chemo-Sero-Therapeutic Research Institute and Department of Biology, Kyushu University) ;
  • Lee, Bok-Luel (College of Pharmacy, Pusan National University)
  • Published : 2005.03.31
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Abstract

Invertebrate animals, which lack adaptive immune systems, have developed other systems of biological host defense, so called innate immunity, that respond to common antigens on the cell surfaces of potential pathogens. During the past two decades, the molecular structures and functions of various defense components that participated in innate immune systems have been established in Arthropoda, such as, insects, the horseshoe crab, freshwater crayfish, and the protochordata ascidian. These defense molecules include phenoloxidases, clotting factors, complement factors, lectins, protease inhibitors, antimicrobial peptides, Toll receptors, and other humoral factors found mainly in hemolymph plasma and hemocytes. These components, which together compose the innate immune system, defend invertebrate from invading bacterial, fungal, and viral pathogens. This review describes the present status of our knowledge concerning such defensive molecules in invertebrates.

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References

  1. Abraham, E. G. and Jacobs-Lorena, M. (2004) Mosquito midgut barriers to malaria parasite development. Insect Biochem. Mol. Biol. 34, 667-671 https://doi.org/10.1016/j.ibmb.2004.03.019
  2. Aderem, A. and Ulevitch, R. (2000) Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787 https://doi.org/10.1038/35021228
  3. Agarwara, K. L., Kawabata, S., Hirata, M., Miyagi, M., Tsunasawa, S. and Iwanaga, S. (1996) Cysteine protease inhibitor stored in the large granules of horseshoe crab hemocytes: Purification, characterization, cDNA cloning and tissue localization. J. Biochem. (Tokyo), 119, 85-94 https://doi.org/10.1093/oxfordjournals.jbchem.a021220
  4. Agarwara, K. L., Kawabata, S., Miura, Y., Kuroki, Y. and Iwanaga, S. (1996) Limulus intracellular coagulation inhibitor type 3. Purification, characterization, cDNA cloning, and tissue localization. J. Biol. Chem. 271, 23768-23774 https://doi.org/10.1074/jbc.271.39.23768
  5. Ariki, S., Koori, K., Osaki, T., Motoyama, K., Inamori, K. and Kawabata, S. (2004) A serine protease zymogen functions as a pattern-recognition receptor for lipopolysaccharides. Proc. Natl. Acad. Sci. USA 101, 953-958 https://doi.org/10.1073/pnas.0306904101
  6. Armstrong, P. B. (2001) The contribution of proteinase inhibitors to immune defense. Trends Immunol. 22, 47-52 https://doi.org/10.1016/S1471-4906(00)01803-2
  7. Ashida, M. and Brey, P. T. (1998) Recent advances in research on the insect prophenoloxidase cascade; in Molecular Mechanisms of Immune Responses in Insects, Brey, P. T. and Hultmark, D. (eds.), pp. 135-172, Chapman & Hall, New York, USA
  8. Azumi, K., Ishimoto, R., Fujita, T., Nonaka, M. and Yokosawa, H. (2000) Opsonin-independent and -dependent phagocytosis in the ascidian Halocynthia: galactose-specific lectin and complement C3 function as target-dependent opsonins. Zoological Sci. 17, 625-632 https://doi.org/10.2108/zsj.17.625
  9. Azumi, K., Santis, R., Tomaso, A., Rigoutsos, I., Yoshizaki, F., Pinto, M. R., Marino, R., Shida, K., Ikeda, M., Ikeda, M., Arai, M., Inoue, Y., Shimizu, T., Satoh, N., Rokhsar, D. S., Pasquier, L. D., Kasahara, M., Satake, M. and Nonaka, M. (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: 'waiting for Godot'. Immunogenetics. 55, 570-581 https://doi.org/10.1007/s00251-003-0606-5
  10. Bachman E. S. and McClay, D. R. (1996) Molecular cloning of the first metazoan beta-1,3 glucanase from eggs of the sea urchin Strongylocentrotus purpuratus. Proc. Natl. Acad. Sci USA 9c, 6808-6813 https://doi.org/10.1073/pnas.93.13.6808
  11. Bang, F. B. (1956) A bacterial disease of Limulus polyphemus. Bull. Johns Hopkins Hosp. 98, 325-351
  12. Beauregard, K. A., Truong, N. T., Zhang, H., Lin, W. and Beck, G. (2001) The detection and isolation of a novel antimicrobial peptide from the echinoderm, Cucumaria frondosa. Adv. Exp. Med. Biol. 484, 55-62 https://doi.org/10.1007/978-1-4615-1291-2_5
  13. Begum, N., Matsumoto, M., Tsuji, S., Toyoshima, K. and Seya, T. (2000) The primary host defense system across humans, flies and plants. Current Trends in Immunology, 3, 59-74
  14. Beisel, H. G., Kawabata, S., Iwanaga, S., Huber, R. and Bode, W. (1999) Tachylectin-2: crystal structure of a specific GlcNAc/ GalNAc binding lectin involved in the innate immunity host defense of the Japanese horseshoe crab Tachypleus tridentatus. EMBO. J. 18, 2313-2322 https://doi.org/10.1093/emboj/18.9.2313
  15. Bergner, A., Muta, T., Iwanaga, S., Beisel, H. G., Delotto, R. and Bode, W. (1997) Horseshoe crab coagulogen is an invertebrate protein with a nerve growth factor-like domain. Biol. Chem. 378, 283-287 https://doi.org/10.1515/bchm.1997.378.3-4.283
  16. Bergner, A., Oganessyan, V., Muta, T., Iwanaga, S., Typke, D., Huber, R. and Bode, W. (1996) Crystral structure of a coagulogen, the clotting protein from horseshoe crab: a structural homologue of nerve growth factor. EMBO J. 15, 6789-6797
  17. Bogdan, C., Rollinghoff, M. and Diefenbach, A. (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12, 64-76 https://doi.org/10.1016/S0952-7915(99)00052-7
  18. Brennan, C. A. and Anderson, K. V. (2004) Drosophila: the genetics of innate immune recognition and response. Annu. Rev. Immunol. 22, 457-483 https://doi.org/10.1146/annurev.immunol.22.012703.104626
  19. Cannon, J. P., Haire, R. N., Rast, J. P. and Litman, G. W. (2004) The phylogenetic origins of the antigen-binding receptors and somatic diversification mechanisms. Immunol. Rev. 200, 12-22 https://doi.org/10.1111/j.0105-2896.2004.00166.x
  20. Caroll, M. (2004) The complement system in regulation of adaptive immunity. Nature immunology, 5, 981-986 https://doi.org/10.1038/ni1113
  21. Cerenius, L., Bangyeekhun, E., Keyser, P., Soderhall, I. and Söderhall, K. (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plaque fungus, Aphanomyces astaci. Cell. Microbiol. 5, 353-357 https://doi.org/10.1046/j.1462-5822.2003.00282.x
  22. Cerenius, L., Liang, Z., Duvic, B., Keyser, P., Hellman, U., Palva, T., Iwanaga, S. and Soderhall, K. (1994) Structure and biological activity of a 1, 3-$\beta$-D-glucan-binding protein in crustacean blood. J. Biol. Chem. 269, 29462-29467
  23. Cerenius, L. and Soderhall, K. (2002) Early events in crustacean innate immunity. Fish Shellfish Immunology 12, 421-437 https://doi.org/10.1006/fsim.2002.0420
  24. Chiou, S. T., Chen, Y. W., Chen, S. C., Chao, C. F. and Liu, T. Y. (2000) Isolation and characterization of proteins that bind to galactose, lipopolysaccharide of Escherichia coli, and protein A of Staphylococcus aureus from the hemolymph of Tachypleus tridentatus. J. Biol. Chem. 275, 1630-1634 https://doi.org/10.1074/jbc.275.3.1630
  25. Cho, J. H., Homma, K., Kanegasaki, S. and Natori, S. (1999) Activation of human neutrophils by a synthetic anti-microbial peptide, $KLKLLLLLKLK-NH_{2}$, via cell surface calreticulin. Eur. J. Biochem. 266, 878-885 https://doi.org/10.1046/j.1432-1327.1999.00920.x
  26. Cooper, E. L., Kauschke, E. and Cossarizza, A. (2002) Digging for innate immunity since Darwin and Metchnikoff. BioEssays 24, 319-333 https://doi.org/10.1002/bies.10077
  27. Crouch, E., Hatshorn, K. and Ofek, I. (2000) Collections and pulmonary innate immunity. Imm. Rev. 173, 52-56 https://doi.org/10.1034/j.1600-065X.2000.917311.x
  28. Decker, H. and Tuczek, F. (2000) Tyrosinase/catecholoxidase activity of hemocyanins: Structural basis and molecular mechanism. Trends Biochem. Sci. 25, 392-397 https://doi.org/10.1016/S0968-0004(00)01602-9
  29. Dodds, A. W. (2002) Which come first, the lectin/classical pathway or the alternative pathway of complement. Immunobiol. 205, 340-354 https://doi.org/10.1078/0171-2985-00137
  30. Ezekowitz, R. A. B., Day, L. E. and Herman, G. A. (1988) A human mannose-binding protein is an acute-phase reactant that shares sequence homology with other vertebrate lectins. J. Exp. Med. 167, 1034-1046 https://doi.org/10.1084/jem.167.3.1034
  31. Fabrick, J. A., Baker, J. E. and Kanost, M. R. (2004) Innate immunity in a pyralid moth: functional evaluation of domains from a beta-1,3-glucan recognition protein. J. Biol. Chem. 279, 26605-26611 https://doi.org/10.1074/jbc.M403382200
  32. Fujita, T. (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat. Rev. Immunol. 2, 346-353 https://doi.org/10.1038/nri800
  33. Fujitani, N., Kawabata, S., Osaki, T., Kumaki, Y., Demura, M., Nitta, K. and Kawano, K. (2002) Structure of the antimicrobial peptide tachystatin A. J. Biol. Chem. 277, 23651-23657 https://doi.org/10.1074/jbc.M111120200
  34. Fujita, T., Endo, Y. and Nonaka, M. (2004) Primitive complement system--recognition and activation. Mol. Immunol. 41, 103-111 https://doi.org/10.1016/j.molimm.2004.03.026
  35. Gadjeva, M., Thiel, S. and Jensenius, J. C. (2001) The mannanbinding lectin pathway of the innate immune response. Curr. Opin. Immunol. 13, 74-78 https://doi.org/10.1016/S0952-7915(00)00185-0
  36. Gobert, V., Gottar, M., Matskevich, A. A., Rutschmann, S., Royet, J., Belvin, M., Hoffmann, J. A. and Ferrandon, D. (2003) Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302, 2126-2130 https://doi.org/10.1126/science.1085432
  37. Gokudan, S., Muta, T., Tsuda, R., Koori, K., Kawahara, T., Seki, N., Mizunoe, Y., Wai, S. N., Iwanaga, S. and Kawabata, S. (1999) Horseshoe crab acetyl group recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc. Natl. Acad. Sci. USA 96, 10086-10091 https://doi.org/10.1073/pnas.96.18.10086
  38. Greenberg, S. and Grinstein, S. (2002) Phagocytosis and innate immunity. Curr. Opin. Immunol. 14, 136-145 https://doi.org/10.1016/S0952-7915(01)00309-0
  39. Hall, M., Heusden, M. C. and Soderhall, K. (1995) Identification of the major lipoproteins in crayfish hemolymph as proteins involved in immunorecognition and clotting. Biochem. Biophys. Res. Communs. 216, 939-946 https://doi.org/10.1006/bbrc.1995.2711
  40. Hall, M., Wang, R., Antwerpen, R., Sottrup-Jensen, L. and Soderhall, K. (1999) The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc. Natl. Acad. Sci. USA 96, 1965-1970 https://doi.org/10.1073/pnas.96.5.1965
  41. Hata, S., Azumi, K. and Yokosawa, H. (1998) Ascidian phenoloxidase: its release from hemocytes, isolation, characterization and physiological roles. Comp. Biochem. Physiol. 119, 769-776 https://doi.org/10.1016/S0305-0491(98)00054-6
  42. Hoebe, K., Jansen, E. and Beutler, B. (2004) The interface between innate and adaptive immunity. Nat. Immunol. 5, 971- 974 https://doi.org/10.1038/ni1004-971
  43. Hoess, A., Watson, S., Siber, G. R. and Liddington, R. (1993) Crystal structure of an endotoxin-neutralizing protein from the horseshoe crab, Limulus anti-LPS factor at 1.5 A resolution. EMBO J. 12, 3351-3356
  44. Hoffmann, J. A., Kafatos, F. C., Janeway, C. A. Jr. and Ezekowitz, R. A. B. (1999) Phylogenetic perspectives in innate immunity. Science 284, 1313-1318 https://doi.org/10.1126/science.284.5418.1313
  45. Hoffmann, J. A. (2003) The immune response of Drosophila. Nature 426, 33-38 https://doi.org/10.1038/nature02021
  46. Hori, S., Kobayashi, A. and Natori, S. (1997) Monoclonal antibodies against pupa-specific surface antigens of Sarcophaga peregrina (flesh fly) hemocytes. Biochem. Biophys. Res. Commun. 236, 497-501 https://doi.org/10.1006/bbrc.1997.6918
  47. Huang, T., Wang, H., Lee, S. Y., Johansson, M. W., Soderhall, K. and Cerenius, L. (2000) A cell adhesion protein from the crayfish Pacifastacus leniusculus, a serine proteinase homologue similar to Drosophila masquerade. J. Biol. Chem. 275, 9996-10001 https://doi.org/10.1074/jbc.275.14.9996
  48. Hultmark, D. (2003) Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15, 12-19 https://doi.org/10.1016/S0952-7915(02)00005-5
  49. Husted, L. B., Sorensen, E. S., Armstrong, P. B., Quigley, J. P., Kristensen, L. and Sottrup-Jensen, L. (2002) Localization of carbohydrate attachment sites and disulfide bridges in Limulus $\alpha$2-macroglobulin: Evidence for two forms differing primary in their bait region sequences. J. Biol. Chem. 277, 43698-43706 https://doi.org/10.1074/jbc.M208236200
  50. Imler, J. L. and Hoffmann, J. A. (2000) Signaling mechanisms in the antimicrobial host defense of Drosophila. Curr. Opin. Microbiol. 3,16-22 https://doi.org/10.1016/S1369-5274(99)00045-4
  51. Inamori, K., Ariki, S. and Kawabata, S. (2004) A toll-like receptor in horseshoe crabs. Immunol. Rev. 198, 106-115 https://doi.org/10.1111/j.0105-2896.2004.0131.x
  52. Inamori, K., Koori, K., Mishima, C., Muta, T. and Kawabata, S. (2000) A horseshoe crab toll-like receptor structurally related to Drosophila Toll. J. Endotoxin. Res. 2000, 6, 397-399 https://doi.org/10.1177/09680519000060051201
  53. Inamori, K., Saito, T., Iwaki, D., Nagira, T., Iwanaga, S., Arisaka, F. and Kawabata, S. (1999) A newly identified horseshoe crab lectin with specificity for blood group A antigen recognizes specific O-antigens of bacterial lipopolysaccharides. J. Biol. Chem. 274, 3272-3278 https://doi.org/10.1074/jbc.274.6.3272
  54. Iwaki, D., Kawabata, S., Miura, Y., Kato, A., Armstrong, P. B., Quigley, J. P., Nielsen, K. L., Dolmer, K., Sottrup-Jensen, L. and Iwanaga, S. (1996) Molecular cloning of limulus alpha 2- macroglobulin. Eur. J. Biochem. 242, 822-831 https://doi.org/10.1111/j.1432-1033.1996.0822r.x
  55. Iwaki, D., Osaki, T., Mizunoe, Y., Wai, S. N., Iwanaga, S. and Kawabata, S. (1999) Functional and structural diversities of Creactive proteins present in horseshoe crab hemolymph plasma. Eur. J. Biochem. 264, 314-326 https://doi.org/10.1046/j.1432-1327.1999.00588.x
  56. Iwanaga, S. (1993a) Primitive coagulation systems and their message to modem biology. Thromb. Haemost. 70, 48-55
  57. Iwanaga, S. (1993b) The limulus clotting reaction. Curr. Opin. Immunol. 5, 74-82 https://doi.org/10.1016/0952-7915(93)90084-6
  58. Iwanaga, S., Muta, T., Shigenaga, T., Miura, Y., Seki, N., Saito, T. and Kawabata, S. (1994a) Role of hemocyte-derived granular components in invertebrate defense. Ann. NY Acad. Sci. 712, 102-116 https://doi.org/10.1111/j.1749-6632.1994.tb33566.x
  59. Iwanaga, S. (2002) The molecular basis of innate immunity in the horseshoe crab. Curr. Opin. Immunol. 14, 87-95 https://doi.org/10.1016/S0952-7915(01)00302-8
  60. Iwanaga, S. and Kawabata, S. (1998) Evolution and phylogeny of defense molecules associated with innate immunity in horseshoe crab. Front. Biosci. 3, 973-984
  61. Iwanaga, S., Kawabata, S. and Muta, T. (1998) New types of clotting factors and defense molecules found in horseshoe crab hemolymph: their structures and functions. J. Biochem. (Tokyo), 123, 1-15 https://doi.org/10.1093/oxfordjournals.jbchem.a021894
  62. Iwanaga, S., Kawabata, S., Miura, Y., Seki, N., Shigenaga, T. and Muta, T. (1994b) Clotting cascade in the immuno response of horseshoe crab; Phylogenetic Perspectives in Immunity: The Insect Host Defense, Hoffmann, J. and Natori, S. (eds.), pp. 79-96, R. G. Landes Co. Biomedical Publishers, Austin, USA
  63. Iwanaga, S., Morita, T., Harada, T., Niwa, M., Takada, K., Kimura, T. and Sakakibara, S. (1978) Chromogenic substrates for horseshoe crab clotting enzyme. Its application for the assay of bacterial endotoxins. Haemostasis 7, 183-188
  64. Iwanaga, S., Miyata, T., Tokunaga, F. and Muta, T. (1992) Molecular mechanism of hemolymph clotting system in Limulus. Thrombosis Res. 68, 1-32 https://doi.org/10.1016/0049-3848(92)90124-S
  65. Iwasaki, A. and Medzhitov, R. (2004) Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5, 987-995 https://doi.org/10.1038/ni1112
  66. Jiang, H. and Kanost, M. R. (1997) Characterization and functional analysis of 12 naturally occurring reactive site variants of serpin-1 from Manduca sexta. J. Biol. Chem. 272, 1082-1087 https://doi.org/10.1074/jbc.272.2.1082
  67. Johansson, M. W., Keyser, P. and Soderhall, K. (1994) Purification and cDNA cloning of a four-domain Kazal proteinase inhibitor from crayfish blood cells. Eur. J. Biochem, 223, 389-394 https://doi.org/10.1111/j.1432-1033.1994.tb19005.x
  68. Johanson, M. W., Lind, M. I., Holmblad, T., Thörnqist, P.-O. and Soderhall, K. (1995) Peroxinectin, a novel adhesion protein from crayfish blood. Biochem, Biophys. Res. Commun. 216, 1079-1087 https://doi.org/10.1006/bbrc.1995.2731
  69. Jomori, T. and Natori, S., (1991) Molecular cloning of cDNA for lipopolysaccharide-binding protein from the haemolymph of the American cockroach Periplaneta americana. J. Biol. Chem. 266, 13318-13323
  70. Kairies, N., Beisel, H. G., Fuentes-Prior, P., Tsuda, R., Muta, T., Iwanaga, S., Bode, W., Huber, R. and Kawabata, S. (2001) The 2.0 A crystal structure of tachylectin 5A provide evidence for the common origin of the innate immunity and the blood coagulation system. Proc. Natl. Acad. Sci. USA 98, 13519- 13524 https://doi.org/10.1073/pnas.201523798
  71. Kanost, M. R. (1999) Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 23, 291-301 https://doi.org/10.1016/S0145-305X(99)00012-9
  72. Kanost, M. R., Jiang, H. and Yu, X. Q. (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 198, 97-105 https://doi.org/10.1111/j.0105-2896.2004.0121.x
  73. Kawabata, S., Beisel, H. G., Huber, R., Bode, W., Gokudan, S., Muta, T., Tsuda, R., Koori, K., Kawahara, T., Seki, N., Mizunoe, Y., Wai, S. N. and Iwanaga, S. (2001) Role of tachylectins in host defense of the Japanese horseshoe crab Tachypleus tridentatus. Adv. Exp. Med. Biol. 484, 195-202 https://doi.org/10.1007/978-1-4615-1291-2_18
  74. Kawabata, S. and Iwanaga, S (1999) Role of lectins in the innate immunity of horseshoe crab. Dev. Comp. Immunol. 23, 391- 400 https://doi.org/10.1016/S0145-305X(99)00019-1
  75. Kawabata, S., Muta, T. and Iwanaga, S. (1996) Clotting cascade and defense molecules found in the hemolymph of the horseshoe crab; in New Directions in Invertebrate Immunology, Soderhall, K., Iwanaga, S. and Vasta, G. (eds.), pp. 255-283, SOS Publication, Fair Haven, USA
  76. Kawabata, S., Nagayama, R., Hirata, M., Shigenaga, T., Agarwala, K. L., Saito, T., Cho, J., Nakajima, H., Takagi, T. and Iwanaga, S. (1996) Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J. Biochem. (Tokyo) 120, 1253-1260 https://doi.org/10.1093/oxfordjournals.jbchem.a021549
  77. Kawabata, S., Saeki, K. and Iwanaga, S. (1996) Limulus kexin: a new type of kex2-like endoprotease specifically expressed in hemocytes of the horseshoe crab. FEBS Lett. 386, 201-204 https://doi.org/10.1016/0014-5793(96)00440-1
  78. Kawabata, S., Saito, T., Saeki, K., Okino, N., Mizutani, A., Toh, Y. and Iwanaga, S. (1997) cDNA cloning, tissue distribution, and subcellular localization of horseshoe crab big defensin. Biol. Chem. 378, 289-292 https://doi.org/10.1515/bchm.1997.378.3-4.289
  79. Kawabata, S., Tokunaga, F., Kugi, Y., Motoyama, S., Miura, Y., Hirata, M. and Iwanaga, S. (1996) Limulus factor D, a 43-kDa protein isolated from horseshoe crab hemocytes, is a serine protease homologue with antimicrobial activity. FEBS Lett. 398, 146-150 https://doi.org/10.1016/S0014-5793(96)01224-0
  80. Kawabata, S. and Tsuda, R. (2002) Molecular basis of non-self recognition by the horseshoe crab tachylectins. Biochem. Biophys. Acta, 1572, 414-421 https://doi.org/10.1016/S0304-4165(02)00322-7
  81. Kawabata, T., Yasuhara, Y., Ochiai, M., Matsuura, S. and Ashida, M. (1995) Molecular cloning of insect pro-phenoloxidase: a copper-containing protein homologous to arthropod hemocyanin. Proc. Natl. Acad. Sci. USA 92, 7774-7778 https://doi.org/10.1073/pnas.92.17.7774
  82. Kawasaki, H., Nose, T., Muta, T., Iwanaga, S., Shimohigashi, Y. and Kawabata, S. (2000) Head-to-tail polymerization of coagulin, a clottable protein of the horseshoe crab. J. Biol. Chem. 275, 35297-35301 https://doi.org/10.1074/jbc.M006856200
  83. Kenjo, A., Takahashi, M., Matsushita, M., Endo, Y., Nakata, M., Mizuochi, T. and Fujita, T. (2001) Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J. Biol. Chem. 276, 19959-19965 https://doi.org/10.1074/jbc.M011723200
  84. Kim, M. S., Baek, M. J., Lee, M. H., Park, J. W., Lee, S. Y., Soderhall, K. and Lee, B. L. (2002) A new easter-type serine protease cleaves a masquerade-like protein during prophenoloxidase activation in Holotrichia diomphalia larvae. J. Biol. Chem. 277, 39999-40004 https://doi.org/10.1074/jbc.M205508200
  85. Kim, M. S., Byun, M. and Oh, B.-H. (2003) Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster, Nat. Immunol. 4, 787-793 https://doi.org/10.1038/ni952
  86. Krem, M. M. and Cera, E. D. (2002) Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem. Sci. 27, 67-74 https://doi.org/10.1016/S0968-0004(01)02007-2
  87. Krutzik, S. R., Sieling, P. A. and Modlin, R. L. (2001) The role of Toll-like receptors in host defense against microbial infection. Curr. Opin. Immunol. 13, 104-108 https://doi.org/10.1016/S0952-7915(00)00189-8
  88. Kwon, T. H., Kim, M. S., Choi, H. W., Joo, C. H., Cho, M. Y. and Lee, B. L. (2000) A masquerade-like serine proteinase homologue is necessary for phenoloxidase activity in the coleopteran insect, Holotrichia diomphalia larvae. Eur. J. Biochem. 267, 6188-6196 https://doi.org/10.1046/j.1432-1327.2000.01695.x
  89. Lee, S. Y., Moon, H. J., Kurata, S., Kurama, S., Natori, S. and Lee, B. L. (1994) Purification and molecular cloning of cDNA for an inducible antibacterial protein of larvae of a coleopteran insect, Holotricihia diomphalia. J. Biochem. (Tokyo), 115, 82- 86
  90. Lee, S. Y., Moon, H. J., Kawabata, S., Kurata, S., Natori, S. and Lee, B. L. (1995a) A sapecin homologue of Holotrichia diomphalia: Purification, sequencing and determination of disulfide pairs, Biol. Pharm. Bull. 18, 457-459 https://doi.org/10.1248/bpb.18.457
  91. Lee, S. Y., Moon, H. J., Kurata, S., Natori, S. and Lee, B. L. (1995b) Purification and cDNA cloning of an antifungal protein from the hemolymph of Holotrichia diomphalia larvae. Biol. Pharm. Bull. 18, 1049-1052 https://doi.org/10.1248/bpb.18.1049
  92. Lee, S. Y., Cho, M. Y., Hyun, J. H., Lee, K. M., Homma, K. I., Natori, S., Kawabata, S. I., Iwanaga, S. and Lee, B. L. (1998) Molecular cloning of cDNA for pro-phenoloxidase activating factor I, a serine protease is induced by lipopolysaccharide or 1,3-beta-glucan in coleopteran insect, Holotrichia diomphalia larvae. Eur. J. Biochem. 257, 615-621 https://doi.org/10.1046/j.1432-1327.1998.2570615.x
  93. Lee, S. Y., Wang, R. and Soderhall, K. (2000) A lipopolysaccharide and $\beta$-1, 3-glucan binding protein from hemocytes of the freshwater crayfish Pacifastacus leniusculus. Purification, characterization and cDNA cloning. J. Biol. Chem. 275, 1337-1343 https://doi.org/10.1074/jbc.275.2.1337
  94. Lee, S. Y. and Soderhall, K. (2001) Characterization of a pattern recognition protein, a masquerade-like protein, in the freshwater crayfish Pascifastacus leniusculus. J. Immunol. 166, 7319-7326 https://doi.org/10.4049/jimmunol.166.12.7319
  95. Lee, W. J., Lee, J. D., Kravchenko, V. V., Ulevitch, R. J. and Brey, P. T. (1996) Purification and molecular cloning of an inducible gram-negative bacteria-binding protein from the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. USA 93, 7888- 7893 https://doi.org/10.1073/pnas.93.15.7888
  96. Lee, Y. J., Chung, T. J., Park, C. W., Hahn, Y. S., Chung, J. H., Lee, B. L., Han, D. M., Jung, Y. H., Kim, S. and Lee, Y. H. (1996) Structure and expression of the tenecin 3 gene in Tenebrio molitor. Biochem. Biophys. Res. Commun. 218, 6-11 https://doi.org/10.1006/bbrc.1996.0002
  97. Leclerc, V. and Reichhart, J. M. (2004) The immune response of Drosophila melanogaster. Immunol. Rev. 198, 59-71 https://doi.org/10.1111/j.0105-2896.2004.0130.x
  98. Leem, J. Y., Nishimura, C., Kurata, S., Shimada, I., Kobayashi, A. and Natori, S. (1996) Purification and characterization of Nbeta- alanyl-5-S-glutathionyl-3,4-dihydroxyphenylalanine, a novel antibacterial substance of Sarcophaga peregrina (flesh fly). J. Biol. Chem. 271, 13573-13577 https://doi.org/10.1074/jbc.271.23.13573
  99. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M. and Hoffmann, J. A. (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86, 973-983 https://doi.org/10.1016/S0092-8674(00)80172-5
  100. Levin, J. and Bang, F. B. (1964) The role of endotoxin in the extracellular coagulation of Limulus blood. Bull. Johns Hopkins Hosp. 115, 265-274
  101. Liang, Z., Sottrup-Jensen, T., Aspán, A., Hall, M. and Soderhall, K. (1997) Pacifastin, a novel 155kDa heterodimeric proteinase inhibitor. Proc. Natl. Acad. Sci. USA 94, 6682-6687 https://doi.org/10.1073/pnas.94.13.6682
  102. Lindahl, G., Sjobring, U. and Johnsson, E. (2000) Human complement regulators: a major target for pathogenic microorganisms. Curr. Opin. Immunol. 12, 44-61 https://doi.org/10.1016/S0952-7915(99)00049-7
  103. Loker, E. S. and Bayne, C. J. (1999) Molecular studies of the molluscan response to Digenean infection. Adv. Exp. Med. Biol. 484, 209-222
  104. Luster, A. D. (2002) The role of chemokines in linking innate and adaptive immunity. Curr. Opin. Immunol. 14, 129-135 https://doi.org/10.1016/S0952-7915(01)00308-9
  105. Ma, C. and Kanost, M. R. (2000) A beta1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biol. Chem. 275, 7505-7514 https://doi.org/10.1074/jbc.275.11.7505
  106. Matsushita, M. and Fujita, T. (2001) Ficolins and the lectin complement pathway. Immunol. Rev. 180, 78-85 https://doi.org/10.1034/j.1600-065X.2001.1800107.x
  107. Medzhitov, R. and Janeway, C. Jr. (2000) Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173, 89- 97 https://doi.org/10.1034/j.1600-065X.2000.917309.x
  108. Moon, H. J., Lee, S. Y., Kurata, S., Natori, S. and Lee, B. L. (1994) Purification and molecular cloning of cDNA for an inducible antibacterial protein from larvae of the coleopteran, Tenebrio molitor. J. Biochem. (Tokyo) 116, 53-58
  109. Morvan, A., Iwanaga, S., Comps, M. and Bachere, E. (1997) In vitro activity of the Limulus antimicrobial peptide tachyplesin I on marine bivalve pathogens. J. Invertebr. Pathol. 69, 177-182 https://doi.org/10.1006/jipa.1996.4642
  110. Muta, T. and Iwanaga, S. (1996a) Clotting and immune defense in Limulidae. Prog. Mol. Subcell. Biol. 15, 154-189 https://doi.org/10.1007/978-3-642-79735-4_8
  111. Muta, T. and Iwanaga, S. (1996b) The role of hemolymph coagulation in innate immunity. Curr. Opin. Immunol. 8, 41-47 https://doi.org/10.1016/S0952-7915(96)80103-8
  112. Muta, T., Seki, N., Takaki, Y., Hashimoto, R., Oda, T., Iwanaga, A., Tokunaga, F. and Iwanaga, S. (1995) Purified horseshoe crab factor G. Reconstitution and characterization of the (1$\rightarrow$ 3)-beta-D-glucan-sensitive serine protease cascade. J. Biol. Chem. 270, 892-897 https://doi.org/10.1074/jbc.270.2.892
  113. Nagai, T. and Kawabata, S. (2000) A link between blood coagulation and prophenoloxidase activation in arthropod host defense. J. Biol. Chem. 275, 29264-29267 https://doi.org/10.1074/jbc.M002556200
  114. Nagai, T., Osaki, T. and Kawabata, S. (2001) Functional conversion of hemocyanin to phenoloxidase by horseshoe crab antimicrobial peptides. J. Biol. Chem. 276, 27166-27170 https://doi.org/10.1074/jbc.M102596200
  115. Nakajima, Y., Alvarez-Bravo, J., Cho, J., Homma, K., Kanegasaki, S. and Natori, S. (1997) Chemotherapeutic activity of synthetic antimicrobial peptides: correlation between chemotherapeutic activity and neutrophil-activating activity. FEBS Lett. 415, 64- 66 https://doi.org/10.1016/S0014-5793(97)01101-0
  116. Natori. S., Shiraishi, H., Hori, S. and Kobayashi, A. (1999) The roles of Sarcophaga defense molecules in immunity and metamorphosis. Dev. Comp. Immunol. 23, 317-328 https://doi.org/10.1016/S0145-305X(99)00014-2
  117. Nellaiappan, K. and Sugumaran, M. (1996) On the presence of phenoloxidase in the hemolymph of the horseshoe crab, limulus. Comp. Biochem. Physiol. 113, 163-168 https://doi.org/10.1016/0305-0491(95)02047-0
  118. Nonaka, M. (2001) Evolution of the complement system. Curr. Opin. Immunol. 13, 69-73 https://doi.org/10.1016/S0952-7915(00)00184-9
  119. Nonaka, M. and Azumi, K. (1999) Opsonic complement system of the solitary ascidian, Halocynthia roretzi. Dev. Comp. Immunol. 23, 421-427 https://doi.org/10.1016/S0145-305X(99)00021-X
  120. Nonaka, M., Azumi, K., Xin, J., Namikawa-Yamada, C., Sasaki, M., Saiga, H., Dodds, A. W., Sekine, H., Homma, M. K., Matsushita, M., Endo, Y. and Fujita, T. (1999) Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. J. Immunol. 162, 387-391
  121. Nonaka, M. and Yoshizaki, F. (2004) Primitive complement system of invertebrates. Immunol. Rev. 198, 203-215 https://doi.org/10.1111/j.0105-2896.2004.00118.x
  122. Obayashi, T., Tamura, H., Tanaka, S., Ohki, M., Takahashi, M., Arai, M., Matsuda, M. and Kawai, T. (1985) A new chromogenic endotoxin-specific assay using recombined Limulus coagulation enzyme and its clinical application. Clin. Chim. Acta. 149, 55-65 https://doi.org/10.1016/0009-8981(85)90273-6
  123. Ochiai, M. and Ashida, M. (1988) Purification of a beta-1,3- glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 263, 12056-12062
  124. Ohno, S. (1994) MHC evolution and development of a recognition system. Ann. N. Y. Acad. Sci. 712, 13-19 https://doi.org/10.1111/j.1749-6632.1994.tb33558.x
  125. Okino, N., Kawabata, S., Saito, T., Hirata, M., Takagi, T. and Iwanaga, S. (1995) Purification, characterization, and cDNA cloning of a 27-kDa lectin (L10) from horseshoe crab hemocytes. J. Biol. Chem. 270, 31008-31015 https://doi.org/10.1074/jbc.270.52.31008
  126. Osaki, T. and Kawabata, S. (2004) Structure and function of coagulogen, a clottable protein in horseshoe crabs. CMLS, Cell Mol. Life Sci. 61, 1257-1265 https://doi.org/10.1007/s00018-004-3396-5
  127. Osaki, T., Okino, N., Tokunaga, F., Iwanaga, S. and Kawabata, S. (2002) Proline-rich cell surface antigens of horseshoe crab hemocytes are substrates for protein cross-linking with a clotting protein coagulin. J. Biol. Chem. 277, 40084-40090 https://doi.org/10.1074/jbc.M206773200
  128. Osaki, T., Omotezako, M., Nagayama, R., Hirata, M., Iwanaga, S., Kasahara, J., Hattori, J., Ito, I., Sugiyama, H. and Kawabata, S. (1999) Horseshoe crab hemocyte-derived antimicrobial polypeptides, tachystatins, with sequence similarity to spider neurotoxins. J. Biol. Chem. 274, 26172-26178 https://doi.org/10.1074/jbc.274.37.26172
  129. Palsson-Mcdermott, E. M. and Onell, L. J. (2004) Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunol. 113, 153-162 https://doi.org/10.1111/j.1365-2567.2004.01976.x
  130. Pieters, J. (2001) Evasion of host cell defense mechanisms by pathogenic bacteria. Curr. Opin. Immunol. 13, 37-44 https://doi.org/10.1016/S0952-7915(00)00179-5
  131. Saito, T., Hatada, M., Iwanaga, S. and Kawabata, S. (1997) A newly identified horseshoe crab lectin with binding specificity to O-antigen of bacterial lipopolysaccharides. J. Biol. Chem. 272, 30703-30708 https://doi.org/10.1074/jbc.272.49.30703
  132. Saito,T., Kawabata, S., Hirata, M. and Iwanaga, S. (1995) A novel type of limulus lectin-L6. Purification, primary structure, and antibacterial activity. J. Biol. Chem. 270, 14493-14499 https://doi.org/10.1074/jbc.270.24.14493
  133. Salzet, M. (2001) Vertebrate innate immunity resembles a mosaic of invertebrate immune responses. Trends Immunol. 22, 285- 288 https://doi.org/10.1016/S1471-4906(01)01895-6
  134. Smith, L. C. (1999) The complement system in sea urchins. Adv. Exp. Med. Biol. 484, 363-372
  135. Smith, V. J. and Chisholm, J. R. (2001) Antimicrobial proteins in crustaceans. Adv. Exp. Med. Biol. 484, 95-112 https://doi.org/10.1007/978-1-4615-1291-2_10
  136. Smith, L. C., Azumi, K. and Nonaka, M. (1999) Complement systems in invertebrate. The ancient alternative and lectin pathways. Immunopharmacology 42, 107-120 https://doi.org/10.1016/S0162-3109(99)00009-0
  137. Soderhall, K., Bangyeekhun, E., Mayo, S. and Soderhall, K. (2003) Hemocyte production and maturation in an invertebrate animal: proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus. Dev. Comp. Immunol. 27, 661-672 https://doi.org/10.1016/S0145-305X(03)00039-9
  138. Soderhall, K., Corenius, L. and Johansson, M. (1996) The prophenoloxidase activating system in invertebrates; in New Directions in Invertebrate Immunology, Soderhall, K., Iwanaga, S. and Vasta, G. R. (eds.), pp. 229-254, SOS Publication, Fair Haven, USA
  139. Soderhall, K., Johnasson, M. and Cerenius, L. (1994) Pattern recognition in invertebrates: The $\beta$-1,3-glucan binding proteins; in Phylogenetic Perspectives in Immunity: The Insect Host Defense, Hoffmann, J. A., Janeway, C. A. and Natori, S. (eds.), pp. 97-104, R. G. Landes Co., Austin, USA
  140. Suetake, T., Tsuda, S., Kawabata, S., Miura, K., Iwanaga, S., Hikichi, K. Nitta, K. and Kawano, K. (2000) Chitin-binding proteins in invertebrates and plants comprise a common chitinbinding structural motif. J. Biol. Chem. 275, 17929-17932 https://doi.org/10.1074/jbc.C000184200
  141. Sugumaran, M. (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res. 15, 2-9 https://doi.org/10.1034/j.1600-0749.2002.00056.x
  142. Takahashi, H., Azumi, K. and Yokosawa, H. (1995) A novel membrane glycoprotein involved in ascidian hemocyte aggregation and phagocytosis. Eur. J. Biochem. 233, 778-783 https://doi.org/10.1111/j.1432-1033.1995.778_3.x
  143. Takaki, Y., Seki, N., Kawabata, S., Iwanaga, S. and Muta, T. (2002) Duplicated binding sites for (1$\rightarrow$ 3)-beta-D-glucan in the horseshoe crab coagulation factor G: Implications for a molecular basis of the pattern recognition in innate immunity. J. Biol. Chem. 277, 14281-14287 https://doi.org/10.1074/jbc.M200177200
  144. Tamura, H., Tanaka, S., Oda, T., Uemura, Y., Aketagawa, J. and Hashimoto, Y. (1996) Purification and characterization of a (1- 3)-$\beta$-D-glucan binding protein from horseshoe crab (Tachypleus tridentatus) amoebocytes. Carbohyd. Res. 295, 103-116
  145. Tan, N. S., Ho, B. and Ding, J. L. (2000) High-affinity LPS binding domain(s) in recombinant factor C of a horseshoe crab neutralizes LPS-induced lethality. FASEB J. 14, 859-870
  146. Tan, N. S., Ng, M. L., Yau, Y. H., Chong, P. K., Ho, B. and Ding, J. L. (2000) Definition of endotoxin binding sites in horseshoe crab factor C recombinant sushi proteins and neutralization of endotoxin by sushi peptides. FASEB J. 14, 1801-1813 https://doi.org/10.1096/fj.99-0866com
  147. Tanaka, S. and Iwanaga, S. (1993) Limulus test for detecting bacterial endotoxins. Methods Enzymol. 223, 358-364 https://doi.org/10.1016/0076-6879(93)23057-T
  148. Theopold, U., Li, D. Schefer, C. and Schmidt, O. (2002) The coagulation of insect hemolymph. CMLS Cell. Mol. Life Sci. 59, 363-372 https://doi.org/10.1007/s00018-002-8428-4
  149. Theopold, U., Schmidt, O., Soderhall, K. and Dushay, M. S. (2004) Coagulation in arthropods: defense, wound closure and healing. Trends Immunol. 25, 289-294 https://doi.org/10.1016/j.it.2004.03.004
  150. Tokunaga, F. and Iwanaga, S. (1993) Horseshoe crab transglutaminase. Methods Enzymol. 223, 378-388 https://doi.org/10.1016/0076-6879(93)23059-V
  151. Tzou, P., De Gregorio, E. and Lemaitre, B. (2002) How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr. Opin. Microbiol. 5, 102-110 https://doi.org/10.1016/S1369-5274(02)00294-1
  152. Underhill, D. M. and Orinsky, A. (2002) Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14, 103- 110 https://doi.org/10.1016/S0952-7915(01)00304-1
  153. Vasta, G. R., Quesenbery, M. S., Ahmed, H, and O'Leary, N. (1999) Lectins from tunicates: Structure-function relationships in innate immunity. Adv. Exp. Med. Biol. 484, 275-287
  154. Wang, R., Lee, S. Y., Cerenius, L. and Soderhall, K. (2001) Properties of the prophenoloxidase activating enzyme of the freshwater crayfish, Pacifastacus leniusculus. Eur. J. Biochem. 268, 895-902 https://doi.org/10.1046/j.1432-1327.2001.01945.x
  155. Waterfield, N. R., Wren, B. W. and Ffrench-Constant, R. H. (2004) Invertebrates as a source of emerging human pathogens. Nat. Rev. Microbiol. 2, 833-841 https://doi.org/10.1038/nrmicro1008
  156. Xin, J. I., Azumi, K., Sasaki, M. and Nonaka, M. (1997) Ancient origin of the complement lectin pathway revealed by molecular cloning of mannan binding protein-associated serine protease from a urochordate, the Japanese ascidian, Halocynthia roretzi. Proc. Natl. Acad. Sci. USA 94, 6340-6345 https://doi.org/10.1073/pnas.94.12.6340
  157. Yoshida, H., Kinoshita, K. and Ashida, M. (1996) Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 271, 13854-13860 https://doi.org/10.1074/jbc.271.23.13854
  158. Yu, X. Q., Gan, H. and Kanost, M. R. (1999) Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenoloxidase. Insect Biochem. Mol. Biol. 29, 585-597 https://doi.org/10.1016/S0965-1748(99)00036-3
  159. Zhang, R., Cho, H. Y., Kim, H. S., Ma, Y. G., Osaki, T., Kawabata, S., Soderhall, K. and Lee, B. L. (2003) Characterization and properties of a 1,3-beta-D-glucan pattern recognition protein of Tenebrio molitor larvae that is specifically degraded by serine protease during prophenoloxidase activation. J. Biol. Chem. 278, 42072-42079 https://doi.org/10.1074/jbc.M307475200
  160. Zhu, Y., Thangamani, S., Ho, B. and Ding, J. L. (2005) The ancient origin of the complement system. EMBO J. 24, 383- 394 https://doi.org/10.1038/sj.emboj.7600533

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  35. Hemolymph biochemical parameters reference intervals and total hemocyte counts of narrow clawed crayfish Astacus leptodactylus (Eschscholtz, 1823) vol.24, 2013, https://doi.org/10.1016/j.ecolind.2012.07.002
  36. Two variants of selenium-dependent glutathione peroxidase from the disk abalone Haliotis discus discus: Molecular characterization and immune responses to bacterial and viral stresses vol.45, pp.2, 2015, https://doi.org/10.1016/j.fsi.2015.05.028
  37. Behavioural and immunological responses to an immune challenge in Octopus vulgaris vol.122, 2013, https://doi.org/10.1016/j.physbeh.2013.08.029
  38. Proteome ofAedes aegyptiin response to infection and coinfection with microsporidian parasites vol.2, pp.4, 2012, https://doi.org/10.1002/ece3.199
  39. Transcriptome analysis of eyestalk and hemocytes in the ridgetail white prawn Exopalaemon carinicauda: assembly, Annotation and Marker Discovery vol.42, pp.1, 2015, https://doi.org/10.1007/s11033-014-3749-6
  40. Chemical and structural defensive external strategies in six sabellid worms (Annelida) vol.35, pp.1, 2014, https://doi.org/10.1111/maec.12053
  41. Discovery of immune molecules and their crucial functions in shrimp immunity vol.34, pp.4, 2013, https://doi.org/10.1016/j.fsi.2012.09.021
  42. Effects of niacin on Staphylococcus aureus internalization into bovine mammary epithelial cells by modulating NF-κB activation vol.71-72, 2014, https://doi.org/10.1016/j.micpath.2014.03.005
  43. Cytologic Diagnosis of Diseases of Invertebrates vol.10, pp.1, 2007, https://doi.org/10.1016/j.cvex.2006.11.003
  44. Expression of Manduca sexta serine proteinase homolog precursors in insect cells and their proteolytic activation vol.38, pp.1, 2008, https://doi.org/10.1016/j.ibmb.2007.09.011
  45. Expression and localization of MCsialec, a sialic acid-specific lectin in the marine bivalve Manila clam, Ruditapes philppinarum vol.33, pp.11, 2010, https://doi.org/10.1111/j.1365-2761.2010.01195.x
  46. Characterization of a prophenoloxidase from hemocytes of the shrimp Litopenaeus vannamei that is down-regulated by white spot syndrome virus vol.25, pp.1-2, 2008, https://doi.org/10.1016/j.fsi.2007.12.002
  47. Comparative Overview of Toll-Like Receptors in Lower Animals vol.27, pp.2, 2010, https://doi.org/10.2108/zsj.27.154
  48. First insights into the biochemistry of Sabella spallanzanii (Annelida: Polychaeta) mucus: a potentially unexplored resource for applicative purposes vol.91, pp.01, 2011, https://doi.org/10.1017/S0025315410001013
  49. cDNA cloning, characterization and expression analysis of peroxiredoxin 5 gene in the ridgetail white prawn Exopalaemon carinicauda vol.40, pp.12, 2013, https://doi.org/10.1007/s11033-013-2702-4
  50. Caspase-11: arming the guards against bacterial infection vol.265, pp.1, 2015, https://doi.org/10.1111/imr.12292
  51. Hemolymph clotting in crustaceans: Implications for neuropeptide extraction from invertebrate hemolymph vol.27, pp.3, 2006, https://doi.org/10.1016/j.peptides.2005.08.027
  52. PmLT, a C-type lectin specific to hepatopancreas is involved in the innate defense of the shrimp Penaeus monodon vol.99, pp.3, 2008, https://doi.org/10.1016/j.jip.2008.08.003
  53. Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization vol.211, pp.4, 2006, https://doi.org/10.1016/j.imbio.2005.10.015
  54. Mapping the peptide and protein immune response in the larvae of the fleshflySarcophaga bullata vol.14, pp.6, 2008, https://doi.org/10.1002/psc.967
  55. Molecular responses during cadmium-induced stress in Daphnia magna: Integration of differential gene expression with higher-level effects vol.83, pp.3, 2007, https://doi.org/10.1016/j.aquatox.2007.04.010
  56. Gene expression responses of white shrimp (Litopenaeus vannamei) infected with necrotizing hepatopancreatitis bacterium vol.420-421, 2014, https://doi.org/10.1016/j.aquaculture.2013.10.042
  57. Host defence peptides from invertebrates – emerging antimicrobial strategies vol.211, pp.4, 2006, https://doi.org/10.1016/j.imbio.2005.10.017
  58. Antimicrobial activity in the tick Rhipicephalus (Boophilus) microplus eggs: Cellular localization and temporal expression of microplusin during oogenesis and embryogenesis vol.33, pp.8, 2009, https://doi.org/10.1016/j.dci.2009.02.009
  59. Three novel clade B serine protease inhibitors from disk abalone, Haliotis discus discus: Molecular perspectives and responses to immune challenges and tissue injury vol.45, pp.2, 2015, https://doi.org/10.1016/j.fsi.2015.04.020
  60. Digital gene expression analysis in hemocytes of the white shrimp Litopenaeus vannamei in response to low salinity stress vol.42, pp.2, 2015, https://doi.org/10.1016/j.fsi.2014.11.020
  61. Identification of immunological expressed sequence tags in the mealworm beetle Tenebrio molitor vol.58, pp.12, 2012, https://doi.org/10.1016/j.jinsphys.2012.09.009
  62. Prophenoloxidase activating enzyme-III from giant freshwater prawn Macrobrachium rosenbergii: characterization, expression and specific enzyme activity vol.39, pp.2, 2012, https://doi.org/10.1007/s11033-011-0872-5
  63. Enzyme activity demonstrates multiple pathways of innate immunity in Indo-Pacific anthozoans vol.279, pp.1743, 2012, https://doi.org/10.1098/rspb.2011.2487
  64. Flow Cytometric Characterization of Freshwater Crayfish Hemocytes for the Examination of Physiological Status in Wild and Captive Animals vol.21, pp.3, 2009, https://doi.org/10.1577/H09-003.1
  65. Differentially enhanced gene expression in hemocytes from Macrobrachium rosenbergii challenged in vivo with lipopolysaccharide vol.100, pp.1, 2009, https://doi.org/10.1016/j.jip.2008.09.005
  66. Bacterial diseases of crabs: A review vol.106, pp.1, 2011, https://doi.org/10.1016/j.jip.2010.09.018
  67. Identification of immune response-related genes in the Chinese oak silkworm, Antheraea pernyi by suppression subtractive hybridization vol.114, pp.3, 2013, https://doi.org/10.1016/j.jip.2013.09.004
  68. Kazal-type serine proteinase inhibitors from the black tiger shrimp Penaeus monodon and the inhibitory activities of SPIPm4 and 5 vol.27, pp.2, 2009, https://doi.org/10.1016/j.fsi.2009.05.014
  69. Laccase-like activity in the hemolymph of Venerupis philippinarum: Characterization and kinetic properties vol.35, pp.6, 2013, https://doi.org/10.1016/j.fsi.2013.09.009
  70. Molecular cloning, characterization, and expression analysis of two different types of lectins from the oriental river prawn, Macrobrachium nipponense vol.45, pp.2, 2015, https://doi.org/10.1016/j.fsi.2015.04.022
  71. Domain inhibitory and bacteriostatic activities of the five-domain Kazal-type serine proteinase inhibitor from black tiger shrimp Penaeus monodon vol.33, pp.4, 2009, https://doi.org/10.1016/j.dci.2008.09.009
  72. Purification and characterization of a β-glucan binding protein from the haemolymph of freshwater prawnMacrobrachium rosenbergii vol.46, pp.1, 2015, https://doi.org/10.1111/are.12160
  73. Comparative proteomic profiles of the hepatopancreas inFenneropenaeus chinensisresponse to hypoxic stress vol.9, pp.12, 2009, https://doi.org/10.1002/pmic.200800518
  74. IrAM—An α2-macroglobulin from the hard tick Ixodes ricinus: Characterization and function in phagocytosis of a potential pathogen Chryseobacterium indologenes vol.33, pp.4, 2009, https://doi.org/10.1016/j.dci.2008.09.011
  75. Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans vol.213, pp.3-4, 2008, https://doi.org/10.1016/j.imbio.2007.12.004
  76. A farnesoic acid O-methyltransferase (FAMeT) from Exopalaemon carinicauda is responsive to Vibrio anguillarum and WSSV challenge vol.19, pp.3, 2014, https://doi.org/10.1007/s12192-013-0464-5
  77. Differential induction of HSP-70 expression in response to IHHNV in white shrimp Litopenaeus vannamei naturally co-infected with IHHNV and IMNV vol.4, pp.1, 2012, https://doi.org/10.1186/2008-6970-4-17
  78. Identification and expression analysis of a novel defense gene fromActias selene vol.49, pp.3-4, 2015, https://doi.org/10.1080/00305316.2015.1081648
  79. Screening of Protease Inhibitory Activity in Aqueous Extracts of Marine Invertebrates from Cuban Coast vol.07, pp.04, 2016, https://doi.org/10.4236/ajac.2016.74030
  80. Variation in Resistance to the Invasive Crayfish Plague and Immune Defence in the Native Noble Crayfish vol.51, pp.4, 2014, https://doi.org/10.5735/086.051.0403
  81. Potential relationship among three antioxidant enzymes in eliminating hydrogen peroxide in penaeid shrimp vol.17, pp.4, 2012, https://doi.org/10.1007/s12192-011-0317-z
  82. Eicosanoids mediate sHSP 20.8 gene response to biotic stress in larvae of the Chinese oak silkworm Antheraea pernyi vol.562, pp.1, 2015, https://doi.org/10.1016/j.gene.2014.12.035
  83. Exploring the mechanisms of action of human secretory RNase 3 and RNase 7 againstCandida albicans vol.5, pp.5, 2016, https://doi.org/10.1002/mbo3.373
  84. Isolation and partial characterisation of four novel plasma lectins from the American lobster Homarus americanus vol.33, pp.2, 2009, https://doi.org/10.1016/j.dci.2008.08.007
  85. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution vol.32, pp.5, 2008, https://doi.org/10.1111/j.1574-6976.2008.00123.x
  86. Inflammatory caspases are innate immune receptors for intracellular LPS 2014, https://doi.org/10.1038/nature13683
  87. Two prophenoloxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon vol.33, pp.2, 2009, https://doi.org/10.1016/j.dci.2008.09.003
  88. Identification of outer membrane protein ompR from rickettsia-like organism and induction of immune response in Crassostrea ariakensis vol.45, pp.11, 2008, https://doi.org/10.1016/j.molimm.2008.02.026
  89. The evolution of virulence of West Nile virus in a mosquito vector: implications for arbovirus adaptation and evolution vol.13, pp.1, 2013, https://doi.org/10.1186/1471-2148-13-71
  90. Identification and characterization of a serine protease inhibitor Esserpin from the Chinese mitten crab Eriocheir sinensis vol.34, pp.6, 2013, https://doi.org/10.1016/j.fsi.2013.03.371
  91. Molecular cloning and expression of a C-type lectin-like protein from orange-spotted grouperEpinephelus coioides vol.84, pp.2, 2014, https://doi.org/10.1111/jfb.12296
  92. A transcriptomic analysis of the response of the arctic pteropod Limacina helicina to carbon dioxide-driven seawater acidification vol.38, pp.10, 2015, https://doi.org/10.1007/s00300-015-1738-4
  93. A novel C-type lectin is involved in the innate immunity of Macrobrachium nipponense vol.50, 2016, https://doi.org/10.1016/j.fsi.2016.01.026
  94. Effect of high water temperature on mortality, immune response and viral replication of WSSV-infected Marsupenaeus japonicus juveniles and adults vol.305, pp.1-4, 2010, https://doi.org/10.1016/j.aquaculture.2010.04.024
  95. PmSERPIN3 from black tiger shrimp Penaeus monodon is capable of controlling the proPO system vol.41, pp.2, 2013, https://doi.org/10.1016/j.dci.2013.04.022
  96. The Effects of Defoliation-Induced Delayed Changes in Silver Birch Foliar Chemistry on Gypsy Moth Fitness, Immune Response, and Resistance to Baculovirus Infection vol.38, pp.3, 2012, https://doi.org/10.1007/s10886-012-0090-1
  97. The staphylococcal surface-glycopolymer wall teichoic acid (WTA) is crucial for complement activation and immunological defense against Staphylococcus aureus infection vol.221, pp.10, 2016, https://doi.org/10.1016/j.imbio.2016.06.003
  98. Plasmodium falciparum GPI toxin: A common foe for man and mosquito vol.114, pp.3, 2010, https://doi.org/10.1016/j.actatropica.2009.06.003
  99. A Review of the Culture and Diseases of Redclaw CrayfishCherax quadricarinatus(Von Martens 1868) vol.44, pp.1, 2013, https://doi.org/10.1111/jwas.12011
  100. Protease IV, a quorum sensing-dependent protease ofPseudomonas aeruginosamodulates insect innate immunity vol.94, pp.6, 2014, https://doi.org/10.1111/mmi.12830
  101. Comparative genomic study of arachnid immune systems indicates loss of beta-1,3-glucanase-related proteins and the immune deficiency pathway vol.29, pp.2, 2016, https://doi.org/10.1111/jeb.12780
  102. Molecular cloning and characterization of the lipopolysaccharide and β-1,3-glucan binding protein from red claw crayfish, Cherax quadricarinatus vol.441, 2015, https://doi.org/10.1016/j.aquaculture.2015.02.011
  103. Molecular mechanisms of the shrimp clotting system vol.34, pp.4, 2013, https://doi.org/10.1016/j.fsi.2012.09.018
  104. Recent advances in researches on the innate immunity of shrimp in China vol.39, pp.1-2, 2013, https://doi.org/10.1016/j.dci.2012.03.016
  105. Purification and characterization of an N-acetylglucosamine specific lectin from marine bivalve Macoma birmanica vol.27, pp.1, 2009, https://doi.org/10.1016/j.fsi.2008.11.001
  106. Fusarium solani species complex associated with carapace lesions and branchitis in captive American horseshoe crabs Limulus polyphemus vol.109, pp.3, 2014, https://doi.org/10.3354/dao02764
  107. Transcriptome Analysis Revealed Changes of Multiple Genes Involved in Haliotis discus hannai Innate Immunity during Vibrio parahemolyticus Infection vol.11, pp.4, 2016, https://doi.org/10.1371/journal.pone.0153474
  108. Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera vol.16, pp.1, 2015, https://doi.org/10.1186/s12864-015-1776-x
  109. Identification and expression of immune genes in the flat oyster Ostrea edulis in response to bonamiosis vol.492, pp.1, 2012, https://doi.org/10.1016/j.gene.2011.11.001
  110. Platelets in inflammation and infection vol.26, pp.4, 2015, https://doi.org/10.3109/09537104.2015.1010441
  111. Immunocompetence of Galleria mellonella: Sex- and stage-specific differences and the physiological cost of mounting an immune response during metamorphosis vol.53, pp.2, 2007, https://doi.org/10.1016/j.jinsphys.2006.11.003
  112. Immune response of Litopenaeus vannamei after infection with Vibrio harveyi vol.406-407, 2013, https://doi.org/10.1016/j.aquaculture.2013.05.010
  113. Cloning, characterization and expression analysis of the gene for a putative lipopolysaccharide-induced TNF-α factor of the Pacific oyster, Crassostrea gigas vol.24, pp.1, 2008, https://doi.org/10.1016/j.fsi.2007.07.003
  114. The effects of hypoxia and pH on phenoloxidase activity in the Atlantic blue crab, Callinectes sapidus vol.144, pp.2, 2006, https://doi.org/10.1016/j.cbpa.2006.02.042
  115. Molecular cloning and expression of a C-type lectin gene from Venerupis philippinarum vol.41, pp.1, 2014, https://doi.org/10.1007/s11033-013-2846-2
  116. Immunomodulatory properties of shellfish derivatives associated with human health vol.6, pp.31, 2016, https://doi.org/10.1039/C5RA26375A
  117. Effect of temperature on biochemical and cellular properties of captive Limulus polyphemus vol.334-337, 2012, https://doi.org/10.1016/j.aquaculture.2011.12.029
  118. Quantitative gene expression and in situ localization of scygonadin potentially associated with reproductive immunity in tissues of male and female mud crabs, Scylla paramamosain vol.31, pp.2, 2011, https://doi.org/10.1016/j.fsi.2011.05.009
  119. PI3K-AKT signaling pathway is involved in hypoxia/thermal-induced immunosuppression of small abalone Haliotis diversicolor vol.59, 2016, https://doi.org/10.1016/j.fsi.2016.11.011
  120. Protein expression profiling in the gill of Litopenaeus vannamei(Boone, 1931) naturally infected with white spot syndrome virus vol.88, pp.7-8, 2015, https://doi.org/10.1163/15685403-00003446
  121. On the influence of diffusion on the competition between bacteria and innate immune system of invertebrates vol.59, pp.2, 2010, https://doi.org/10.1007/s11587-010-0078-5
  122. Molecular characterization and expression analysis of IκB from Haliotis discus discus vol.34, pp.6, 2013, https://doi.org/10.1016/j.fsi.2013.02.017
  123. Molecular cloning and expression analysis of a hemolin-like molecule from Antheraea pernyi vol.26, pp.1, 2015, https://doi.org/10.1016/j.intimp.2015.03.010
  124. cDNA cloning and structural characterization of a lectin from the mussel Crenomytilus grayanus with a unique amino acid sequence and antibacterial activity vol.35, pp.4, 2013, https://doi.org/10.1016/j.fsi.2013.07.011
  125. Comparative Transcriptome Analysis Reveals Sex-Biased Gene Expression in Juvenile Chinese Mitten Crab Eriocheir sinensis vol.10, pp.7, 2015, https://doi.org/10.1371/journal.pone.0133068
  126. Functional genomics of the evolution of increased resistance to parasitism in Drosophila vol.20, pp.5, 2011, https://doi.org/10.1111/j.1365-294X.2010.04911.x
  127. Crosstalk between the two systems, blood coagulation and complement vol.22, pp.4, 2011, https://doi.org/10.2491/jjsth.22.171
  128. Antibacterial activity in vivo and in vitro in the hemolymph of Galleria mellonella infected with Pseudomonas aeruginosa vol.152, pp.2, 2009, https://doi.org/10.1016/j.cbpb.2008.10.008
  129. Differential immune response in the hard clam (mercenaria mercenaria) against bacteria and the protistan pathogen QPX (quahog parasite unknown) vol.32, pp.6, 2012, https://doi.org/10.1016/j.fsi.2012.03.018
  130. Leishmanolysin-like Molecules in Herpetomonas samuelpessoai Mediate Hydrolysis of Protein Substrates and Interaction with Insect vol.161, pp.4, 2010, https://doi.org/10.1016/j.protis.2010.02.001
  131. The cytosolic manganese superoxide dismutase cDNA in swimming crab Portunus trituberculatus: Molecular cloning, characterization and expression vol.309, pp.1-4, 2010, https://doi.org/10.1016/j.aquaculture.2010.09.008
  132. The Macromolecular Assembly of Pathogen-Recognition Receptors is Impelled by Serine Proteases, via Their Complement Control Protein Modules vol.377, pp.3, 2008, https://doi.org/10.1016/j.jmb.2008.01.045
  133. Non-canonical activation of inflammatory caspases by cytosolic LPS in innate immunity vol.32, 2015, https://doi.org/10.1016/j.coi.2015.01.007
  134. High Molecular Weight Lectin Isolated from the Mucus of the Giant African SnailAchatina fulica vol.75, pp.1, 2011, https://doi.org/10.1271/bbb.100389
  135. Platelets: bridging hemostasis, inflammation, and immunity vol.35, pp.3, 2013, https://doi.org/10.1111/ijlh.12084
  136. Shrimp Molecular Responses to Viral Pathogens vol.13, pp.4, 2011, https://doi.org/10.1007/s10126-010-9287-x
  137. Identification, cloning, characterization and recombinant expression of an anti-lipopolysaccharide factor from the hemocytes of Indian mud crab, Scylla serrata vol.27, pp.2, 2009, https://doi.org/10.1016/j.fsi.2009.05.009
  138. Oxidative modification of von Willebrand factor by neutrophil oxidants inhibits its cleavage by ADAMTS13 vol.115, pp.3, 2010, https://doi.org/10.1182/blood-2009-03-213967
  139. Molecular cloning and characterization of the lipopolysaccharide and β-1,3-glucan binding protein from oriental river prawn, Macrobrachium nipponense vol.41, pp.6, 2014, https://doi.org/10.1007/s11033-014-3261-z
  140. Molecular characterization and expression analysis of extracellular copper–zinc superoxide dismutase gene from swimming crab Portunus trituberculatus vol.38, pp.3, 2011, https://doi.org/10.1007/s11033-010-0337-2
  141. Physiological and immune responses of zhikong scallop Chlamys farreri to the acute viral necrobiotic virus infection vol.29, pp.1, 2010, https://doi.org/10.1016/j.fsi.2010.02.019
  142. Microarray expression profiling of Spodoptera litura in response to oxidative stress vol.77, pp.3, 2011, https://doi.org/10.1002/arch.20431
  143. Solanum nigrum enhancement of the immune response and disease resistance of tiger shrimp, Penaeus monodon against Vibrio harveyi vol.318, pp.1-2, 2011, https://doi.org/10.1016/j.aquaculture.2011.05.024
  144. The responsive expression of a chitinase gene in the ridgetail white prawn Exopalaemon carinicauda against Vibrio anguillarum and WSSV challenge vol.19, pp.4, 2014, https://doi.org/10.1007/s12192-013-0488-x
  145. Growth and immune response of Chinese mitten crab (Eriocheir sinensis) fed diets containing different lipid sources vol.47, pp.6, 2016, https://doi.org/10.1111/are.12654
  146. The development of Angiostrongylus vasorum (Baillet, 1866) in the freshwater snail Pomacea canaliculata (Lamarck, 1822) vol.89, pp.06, 2015, https://doi.org/10.1017/S0022149X14000856
  147. Innate immune response in the hemolymph of an ascidian, Halocynthia roretzi, showing soft tunic syndrome, using label-free quantitative proteomics vol.35, pp.8, 2011, https://doi.org/10.1016/j.dci.2011.01.011
  148. Molecular cloning, characterization and expression of a C-type lectin cDNA in Chinese mitten crab, Eriocheir sinensis vol.31, pp.2, 2011, https://doi.org/10.1016/j.fsi.2011.06.001
  149. Multifunctional role of β-1, 3 glucan binding protein purified from the haemocytes of blue swimmer crab Portunus pelagicus and in vitro antibacterial activity of its reaction product vol.48, 2016, https://doi.org/10.1016/j.fsi.2015.11.023
  150. Purification and characterization of a novel salivary antimicrobial peptide from the tick, Ixodes scapularis vol.390, pp.3, 2009, https://doi.org/10.1016/j.bbrc.2009.09.127
  151. Reappraisal of the Serum (1→3)‐β‐D‐Glucan Assay for the Diagnosis of Invasive Fungal Infections—A Study Based on Autopsy Cases from 6 Years vol.46, pp.12, 2008, https://doi.org/10.1086/588295
  152. Association of CfLGBP gene polymorphism with disease susceptibility/resistance of Zhikong scallop (Chlamys farreri) to Listonella anguillarum vol.32, pp.6, 2012, https://doi.org/10.1016/j.fsi.2012.03.017
  153. Particularity and universality of a putative Gram-negative bacteria-binding protein (GNBP) gene from amphioxus (Branchiostoma belcheri): Insights into the function and evolution of GNBP vol.33, pp.4, 2012, https://doi.org/10.1016/j.fsi.2012.07.016
  154. Three-dimensional structure and ligand-binding site of carp fishelectin (FEL) vol.71, pp.5, 2015, https://doi.org/10.1107/S1399004715004174
  155. Transcriptome-wide analysis of microRNAs in Branchiostoma belcheri upon Vibrio parahemolyticus infection vol.74, 2017, https://doi.org/10.1016/j.dci.2017.05.002
  156. Effect of dietary copper on the growth performance, non-specific immunity and resistance to Aeromonas hydrophila of juvenile Chinese mitten crab, Eriocheir sinensis vol.34, pp.5, 2013, https://doi.org/10.1016/j.fsi.2013.01.021
  157. Expression of candidate genes related to metabolism, immunity and cellular stress during massive mortality in the American oyster Crassostrea virginica larvae in relation to biochemical and physiological parameters vol.499, pp.1, 2012, https://doi.org/10.1016/j.gene.2012.02.021
  158. Gene silencing of a prophenoloxidase activating enzyme in the shrimp, Penaeus monodon, increases susceptibility to Vibrio harveyi infection vol.33, pp.7, 2009, https://doi.org/10.1016/j.dci.2009.01.006
  159. Clearance of Vibrio campbellii injected into the hemolymph of Callinectes sapidus, the Atlantic blue crab: The effects of prior exposure to bacteria and environmental hypoxia vol.25, pp.6, 2008, https://doi.org/10.1016/j.fsi.2008.02.009
  160. Geographical variation in parasitism shapes larval immune function in a phytophagous insect vol.100, pp.12, 2013, https://doi.org/10.1007/s00114-013-1119-1
  161. Proteomic approach for acute-phase proteins of hemolymph and muscles in Scylla serrata challenged by a pathogenic bacterium vol.1, pp.3, 2006, https://doi.org/10.1007/s11515-006-0031-x
  162. The expression pattern of scygonadin during the ontogenesis of Scylla paramamosain predicting its potential role in reproductive immunity vol.35, pp.10, 2011, https://doi.org/10.1016/j.dci.2011.03.028
  163. The development of antimicrobial peptides as an approach to prevention of antibiotic resistance vol.26, pp.3, 2015, https://doi.org/10.1097/MRM.0000000000000032
  164. Alterations of pattern in immune response and vitellogenesis during induced ovarian development by unilateral and bilateral ablation in Litopenaeus vannamei vol.79, pp.6, 2013, https://doi.org/10.1007/s12562-013-0652-3
  165. The spider hemolymph clot proteome reveals high concentrations of hemocyanin and von Willebrand factor-like proteins vol.1864, pp.2, 2016, https://doi.org/10.1016/j.bbapap.2015.11.004
  166. Gene expression patterns in response to pathogen challenge and interaction with hemolin suggest that the Yippee protein of Antheraea pernyi is involved in the innate immune response vol.138, 2016, https://doi.org/10.1016/j.jip.2016.05.010
  167. C-reactive protein collaborates with plasma lectins to boost immune response against bacteria vol.26, pp.14, 2007, https://doi.org/10.1038/sj.emboj.7601762
  168. Coagulation and innate immune responses: can we view them separately? vol.114, pp.12, 2009, https://doi.org/10.1182/blood-2009-05-199208
  169. The first serine protease inhibitor from Lasiodora sp. (Araneae: Theraphosidae) hemocytes vol.46, pp.12, 2011, https://doi.org/10.1016/j.procbio.2011.09.012
  170. Molecular cloning and characterization of a cytoplasmic manganese superoxide dismutase and a mitochondrial manganese superoxide dismutase from Chinese mitten crab Eriocheir sinensis vol.47, pp.1, 2015, https://doi.org/10.1016/j.fsi.2015.09.035
  171. Differential expression of serine protease inhibitors 1 and 2 in Crassostrea corteziensis and C. virginica infected with Perkinsus marinus vol.112, pp.3, 2015, https://doi.org/10.3354/dao02808
  172. Expression profiles of selenium dependent glutathione peroxidase and glutathione S-transferase from Exopalaemon carinicauda in response to Vibrio anguillarum and WSSV challenge vol.35, pp.3, 2013, https://doi.org/10.1016/j.fsi.2013.05.016
  173. Molecular Characterization and Expression Analysis of a Toll-like receptor 2/6 gene from Abalone (Haliotis discus hannai) vol.31, pp.3, 2015, https://doi.org/10.9710/kjm.2015.31.3.233
  174. HGA-2, a novel galactoside-binding lectin from the sea cucumber Holothuria grisea binds to bacterial cells vol.64, 2014, https://doi.org/10.1016/j.ijbiomac.2013.12.035
  175. Expression and characterization of two STAT isoforms from Sf9 cells vol.32, pp.7, 2008, https://doi.org/10.1016/j.dci.2007.12.001
  176. IrFC – An Ixodes ricinus injury-responsive molecule related to Limulus Factor C vol.46, pp.2, 2014, https://doi.org/10.1016/j.dci.2014.05.016
  177. Phenoloxidase activity in the hemolymph of the spiny lobster Panulirus argus vol.23, pp.6, 2007, https://doi.org/10.1016/j.fsi.2007.04.001
  178. Molecular cloning of a C-type lectin (LvLT) from the shrimp Litopenaeus vannamei: Early gene down-regulation after WSSV infection vol.23, pp.2, 2007, https://doi.org/10.1016/j.fsi.2006.12.005
  179. The study on biodefence of fish and shellfish vol.73, pp.3, 2007, https://doi.org/10.2331/suisan.73.400
  180. Molecular characterization and expression of a novel big defensin (Sb-BDef1) from ark shell, Scapharca broughtonii vol.33, pp.5, 2012, https://doi.org/10.1016/j.fsi.2012.09.008
  181. Agglutinin-mediated phagocytosis-associated generation of superoxide anion and nitric oxide by the hemocytes of the giant freshwater prawn Macrobrachium rosenbergii vol.24, pp.3, 2008, https://doi.org/10.1016/j.fsi.2007.12.005
  182. Immune benefits from alternative host plants could maintain polyphagy in a phytophagous insect vol.177, pp.2, 2015, https://doi.org/10.1007/s00442-014-3097-1
  183. Purification, characterization and induction of a C-type lectin in the freshwater planarian Dugesia japonica vol.7, pp.2, 2012, https://doi.org/10.2478/s11535-012-0014-7
  184. The solution structure of horseshoe crab antimicrobial peptide tachystatin B with an inhibitory cystine-knot motif vol.13, pp.4, 2007, https://doi.org/10.1002/psc.846
  185. Identification and functional characterization of TNF receptor associated factor 3 in the sea cucumber Apostichopus japonicus vol.59, 2016, https://doi.org/10.1016/j.dci.2016.01.021
  186. Prophenoloxidase system and its role in shrimp immune responses against major pathogens vol.34, pp.4, 2013, https://doi.org/10.1016/j.fsi.2012.08.019
  187. Molecular characterization, immune responsive expression and functional analysis of QM, a putative tumor suppressor gene from the Pacific white shrimp, Litopenaeus vannamei vol.37, pp.1, 2014, https://doi.org/10.1016/j.fsi.2014.01.005
  188. Ciona intestinalis interleukin 17-like genes expression is upregulated by LPS challenge vol.48, pp.1, 2015, https://doi.org/10.1016/j.dci.2014.09.014
  189. Innate immune response and gene expression ofScylla paramamosainunderVibrio parahaemolyticusinfection vol.46, pp.2, 2015, https://doi.org/10.1111/are.12194
  190. Identification of a C-type lectin with antiviral and antibacterial activity from pacific white shrimp Litopenaeus vannamei vol.46, pp.2, 2014, https://doi.org/10.1016/j.dci.2014.04.014
  191. Studies on the role of protein kinase A in humoral immune response of Galleria mellonella larvae vol.52, pp.7, 2006, https://doi.org/10.1016/j.jinsphys.2006.04.002
  192. The influence of Pseudomonas aeruginosa secreted virulence factors on hemocyte-mediated immune response of Galleria mellonella vol.65, pp.2, 2010, https://doi.org/10.2478/v10067-011-0012-6
  193. Towards an integrated network of coral immune mechanisms vol.279, pp.1745, 2012, https://doi.org/10.1098/rspb.2012.1477
  194. Mass mortality and slow recovery of Diadema antillarum: Could compromised immunity be a factor? vol.161, pp.5, 2014, https://doi.org/10.1007/s00227-013-2382-6
  195. Hemolymph coagulation and phenoloxidase activity inUca tangeriinduced byEscherichia coliendotoxin vol.13, pp.3, 2016, https://doi.org/10.3109/1547691X.2015.1096983
  196. Evidence of Antibacterial Activities in Peptide Fractions Originating from Snow Crab (Chionoecetes opilio) By-Products vol.2, pp.3, 2010, https://doi.org/10.1007/s12602-010-9043-6
  197. Healthier or bigger? Trade-off mediating male dimorphism in the black scavenger fly Sepsis thoracica (Diptera: Sepsidae) vol.42, pp.4, 2017, https://doi.org/10.1111/een.12413
  198. A lectin with antifungal activity from the mussel Crenomytilus grayanus vol.42, pp.2, 2015, https://doi.org/10.1016/j.fsi.2014.11.036
  199. A novel siglec (CgSiglec-1) from the Pacific oyster (Crassostrea gigas) with broad recognition spectrum and inhibitory activity to apoptosis, phagocytosis and cytokine release vol.61, 2016, https://doi.org/10.1016/j.dci.2016.03.026
  200. Effects of white spot syndrome virus infection and role of immune polysaccharides of juvenile Cherax quadricarinatus vol.437, 2015, https://doi.org/10.1016/j.aquaculture.2014.11.013
  201. Prospect for lectins in arthropods vol.77, pp.3, 2010, https://doi.org/10.1080/11250003.2010.492794
  202. Natural occurrence ofBacillus thuringiensisandBacillus cereusin eukaryotic organisms: a case for symbiosis vol.18, pp.3, 2008, https://doi.org/10.1080/09583150801942334
  203. Screening of genes regulated by relish in Chinese shrimp Fenneropenaeus chinensis vol.41, pp.2, 2013, https://doi.org/10.1016/j.dci.2013.06.003
  204. Inference of the Oxidative Stress Network in Anopheles stephensi upon Plasmodium Infection vol.9, pp.12, 2014, https://doi.org/10.1371/journal.pone.0114461
  205. Kinetic Properties of Hexameric Tyrosinase from the Crustacean Palinurus elephas vol.84, pp.3, 2008, https://doi.org/10.1111/j.1751-1097.2008.00349.x
  206. Discoidin I from Dictyostelium discoideum and Interactions with Oligosaccharides: Specificity, Affinity, Crystal Structures, and Comparison with Discoidin II vol.400, pp.3, 2010, https://doi.org/10.1016/j.jmb.2010.05.042
  207. Mosquito midguts and malaria: cell biology, compartmentalization and immunology vol.28, pp.4, 2006, https://doi.org/10.1111/j.1365-3024.2006.00804.x
  208. Senescence in immune priming and attractiveness in a beetle vol.25, pp.7, 2012, https://doi.org/10.1111/j.1420-9101.2012.02516.x
  209. Proteolytic cascades and their involvement in invertebrate immunity vol.35, pp.10, 2010, https://doi.org/10.1016/j.tibs.2010.04.006
  210. Molecular cloning, expression analysis and characterization of peroxiredoxin during WSSV infection in shrimp Fenneropenaeus indicus vol.109, pp.1, 2012, https://doi.org/10.1016/j.jip.2011.09.006
  211. FLOW-CYTOMETRIC CHARACTERIZATION OF THE CELL-SURFACE GLYCANS OF SYMBIOTIC DINOFLAGELLATES (SYMBIODINIUM SPP.)1 vol.46, pp.3, 2010, https://doi.org/10.1111/j.1529-8817.2010.00819.x
  212. A cDNA Cloning of a Novel Alpha-Class Tyrosinase ofPinctada fucata: Its Expression Analysis and Characterization of the Expressed Protein vol.2014, 2014, https://doi.org/10.1155/2014/780549
  213. An fMLP receptor is involved in activation of phagocytosis by hemocytes from specific insect species vol.33, pp.6, 2009, https://doi.org/10.1016/j.dci.2008.12.006
  214. Cuticle laccase of the silkworm, Bombyx mori: Purification, gene identification and presence of its inactive precursor in the cuticle. vol.39, pp.4, 2009, https://doi.org/10.1016/j.ibmb.2008.12.005
  215. Molecular cloning and tissue-specific expression of a five-kazal domain serine proteinase inhibitor from crayfish Procambarus clarkii hemocytes vol.321, pp.1-2, 2011, https://doi.org/10.1016/j.aquaculture.2011.08.031
  216. A smaller particle size improved the oral bioavailability of monkey head mushroom, Hericium erinaceum, powder resulting in enhancement of the immune response and disease resistance of white shrimp, Litopenaeus vannamei vol.30, pp.6, 2011, https://doi.org/10.1016/j.fsi.2011.03.012
  217. Essential function of transglutaminase and clotting protein in shrimp immunity vol.45, pp.5, 2008, https://doi.org/10.1016/j.molimm.2007.09.016
  218. Difference between hemocyanin subunits from shrimp Penaeus japonicus in anti-WSSV defense vol.32, pp.7, 2008, https://doi.org/10.1016/j.dci.2007.11.010
  219. Molecular cloning and expression analysis of Relish gene from the ridgetail white prawn Exopalaemon carinicauda vol.81, pp.4, 2015, https://doi.org/10.1007/s12562-015-0898-z
  220. Cloning and characterization of a sialic acid binding lectins (SABL) from Manila clam Venerupis philippinarum vol.30, pp.4-5, 2011, https://doi.org/10.1016/j.fsi.2011.02.022
  221. cDNA cloning, characterization and expression analysis of catalase in swimming crab Portunus trituberculatus vol.39, pp.12, 2012, https://doi.org/10.1007/s11033-012-1826-2
  222. A C1q domain containing protein from Crassostrea gigas serves as pattern recognition receptor and opsonin with high binding affinity to LPS vol.45, pp.2, 2015, https://doi.org/10.1016/j.fsi.2015.05.021
  223. l-Type lectin from the kuruma shrimp Marsupenaeus japonicus promotes hemocyte phagocytosis vol.44, pp.2, 2014, https://doi.org/10.1016/j.dci.2014.01.016
  224. Distinct regulation patterns of the two prophenoloxidase activating enzymes corresponding to bacteria challenge and their compensatory over expression feature in white shrimp (Litopenaeus vannamei) vol.39, pp.2, 2014, https://doi.org/10.1016/j.fsi.2014.04.026
  225. Identification of the gene encoding pro-phenoloxidase A3in the fruitfly,Drosophila melanogaster vol.18, pp.2, 2009, https://doi.org/10.1111/j.1365-2583.2008.00858.x
  226. A clip domain serine proteinase plays a role in antibacterial defense but is not required for prophenoloxidase activation in shrimp vol.34, pp.2, 2010, https://doi.org/10.1016/j.dci.2009.09.004
  227. Next-Generation Sequencing and the Crustacean Immune System: The Need for Alternatives in Immune Gene Annotation vol.56, pp.6, 2016, https://doi.org/10.1093/icb/icw023
  228. First Insights into the Subterranean Crustacean Bathynellacea Transcriptome: Transcriptionally Reduced Opsin Repertoire and Evidence of Conserved Homeostasis Regulatory Mechanisms vol.12, pp.1, 2017, https://doi.org/10.1371/journal.pone.0170424
  229. Structure-activity relationships of the intramolecular disulfide bonds in coprisin, a defensin from the dung beetle vol.47, pp.11, 2014, https://doi.org/10.5483/BMBRep.2014.47.11.262
  230. Multiplex immune-related genes expression analysis response to bacterial challenge in mud crab, Scylla paramamosain vol.34, pp.2, 2013, https://doi.org/10.1016/j.fsi.2012.11.029
  231. Genotoxic effects of the water-soluble fraction of heavy oil in the brackish/freshwater amphipod Quadrivisio aff. lutzi (Gammaridea) as assessed using the comet assay vol.22, pp.4, 2013, https://doi.org/10.1007/s10646-013-1055-z
  232. Switch between tyrosinase and catecholoxidase activity of scorpion hemocyanin by allosteric effectors vol.582, pp.5, 2008, https://doi.org/10.1016/j.febslet.2008.01.056
  233. Purification and characterization of a novel peptide with inhibitory effects on colitis induced mice by dextran sulfate sodium from enzymatic hydrolysates of Crassostrea gigas vol.33, pp.4, 2012, https://doi.org/10.1016/j.fsi.2012.08.017
  234. Intromission Induces and Insemination Reduces Female Immune Response in the Medfly vol.23, pp.2, 2010, https://doi.org/10.1007/s10905-010-9203-2
  235. Effect of Relative Humidity on Entomopathogens Infection and Antioxidant Responses of the Beet Armyworm,Spodoptera exigua(Hübner) vol.22, pp.3, 2014, https://doi.org/10.4001/003.022.0310
  236. The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab) vol.32, pp.4, 2012, https://doi.org/10.1016/j.fsi.2012.01.003
  237. Phagocytic activity of Limulus polyphemus amebocytes in vitro vol.111, pp.3, 2012, https://doi.org/10.1016/j.jip.2012.08.002
  238. Tyrosinase causes the blue shade of an abnormal pearl vol.77, pp.3, 2011, https://doi.org/10.1093/mollus/eyr013
  239. Ctenidins: antimicrobial glycine-rich peptides from the hemocytes of the spider Cupiennius salei vol.67, pp.16, 2010, https://doi.org/10.1007/s00018-010-0364-0
  240. Concholepas hemocyanin biosynthesis takes place in the hepatopancreas, with hemocytes being involved in its metabolism vol.342, pp.3, 2010, https://doi.org/10.1007/s00441-010-1057-6
  241. Morphofunctional characterization and antibacterial activity of haemocytes fromOctopus vulgaris vol.49, pp.21-24, 2015, https://doi.org/10.1080/00222933.2013.826830
  242. Synergism between mutational meltdown and Red Queen in parthenogenetic biotypes of the freshwater planarianSchmidtea polychroa vol.116, pp.2, 2007, https://doi.org/10.1111/j.0030-1299.2007.15388.x
  243. Oxidative stress response of the black tiger shrimp Penaeus monodon to Vibrio parahaemolyticus challenge vol.46, pp.2, 2015, https://doi.org/10.1016/j.fsi.2015.06.032
  244. Effects of diets with fermented duckweed (Lemna sp.) on growth performance and gene expression in the Pacific white shrimp, Litopenaeus vannamei vol.23, pp.2, 2015, https://doi.org/10.1007/s10499-014-9835-x
  245. Host plant variation plastically impacts different traits of the immune system of a phytophagous insect vol.25, pp.6, 2011, https://doi.org/10.1111/j.1365-2435.2011.01911.x
  246. Identification, sequence characterization and expression analysis of the arginine kinase gene in response to laminarin challenge from the Oriental land snail, Nesiohelix samarangae vol.29, pp.3, 2013, https://doi.org/10.9710/kjm.2013.29.3.171
  247. Novel Insights into Antiviral Gene Regulation of Red Swamp Crayfish, Procambarus clarkii, Infected with White Spot Syndrome Virus vol.8, pp.11, 2017, https://doi.org/10.3390/genes8110320
  248. Novel approach to study gastropod-mediated innate immune reactions against metastrongyloid parasites vol.117, pp.4, 2018, https://doi.org/10.1007/s00436-018-5803-0
  249. Mutagenesis Studies and Structure-function Relationships for GalNAc/Gal-Specific Lectin from the Sea Mussel Crenomytilus grayanus vol.16, pp.12, 2018, https://doi.org/10.3390/md16120471
  250. Environmental stress tolerance and immune response for the small abalone hybrids pp.1573-143X, 2018, https://doi.org/10.1007/s10499-018-0310-y
  251. C-Type Lectin-20 Interacts with ALP1 Receptor to Reduce Cry Toxicity in Aedes aegypti vol.10, pp.10, 2018, https://doi.org/10.3390/toxins10100390
  252. Innate Immune Memory in Invertebrate Metazoans: A Critical Appraisal vol.9, pp.1664-3224, 2018, https://doi.org/10.3389/fimmu.2018.01915
  253. Identification and expression analysis of a TLR11 family gene in the sea urchin Strongylocentrotus intermedius vol.70, pp.5, 2018, https://doi.org/10.1007/s00251-017-1035-1