DOI QR코드

DOI QR Code

The Influence of Challenge on Cathepsin B and D Expression Patterns in the Silkworm Bombyx mori L.

  • Wu, Feng-Yao (Jiangsu University of Science and Technology) ;
  • Zou, Feng-Ming (Jiangsu University of Science and Technology) ;
  • Jia, Jun-Qiang (Sericultural Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Wang, Sheng-Peng (Sericultural Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Guo-Zheng (Sericultural Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Guo, Xi-Jie (Sericultural Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Gui, Zhong-Zheng (Sericultural Research Institute, Chinese Academy of Agricultural Sciences)
  • Received : 2011.06.30
  • Accepted : 2011.09.05
  • Published : 2011.09.30

Abstract

Cathepsins are well-characterized proteases that are ubiquitously expressed in lysosomes. Previous work revealed that $Bombyx$ $mori$ cathepsins B and D are expressed in the fat body and undergo decomposition during larval-pupal metamorphosis. Quantitative RT-PCR was performed to detect cathepsin gene expression at the transcription level when challenged by $B.$ $mori$ nuclear polyhedrosis virus (BmNPV), temperature and hormones (20-hydroxyecdysone (20E) and juvenile hormone analogue (JHA)). mRNAs encoding cathepsins B and D were significantly enhanced after the larvae were infected with BmNPV, and the peak of the induction appeared at 1 day before spinning. This attenuated the inducing effect on cathepsin expression caused by infection. Temperature shock induced cathepsin expression at the later stage of the $5^{th}$ instar, and transcription levels varied with development stage and temperature. Cathepsin B and D mRNA expression in the fat body were significantly induced by JHA at the day before spinning, and with 20E, the expression reached a peak at the last day of the $5^{th}$ instar. Cathepsin B and D mRNA expression exhibited detectable changes post-treatment, without significant differences between or among the hormone concentrations.

Keywords

References

  1. Ahn JE, Zhu-Salzman K (2009) CmCatD, a cathepsin D-like protease has a potential role in insect defens against a phytocystatin. J Insect Physiol 55, 678-685. https://doi.org/10.1016/j.jinsphys.2009.04.016
  2. Attardo GM, Strickler-Dinglasan P, Perkin SAH, Caler E, Bonaldo MF, Soares MB, El-Sayeed N, Aksoy S (2006) Analysis of fat body transcriptome from the adult tsetse fly, Glossina morsitans morsitans. Insect Mol Biol 15, 411-424. https://doi.org/10.1111/j.1365-2583.2006.00649.x
  3. Boldbaatar D, Sikasunge CS, Battsetseg B, Xuan X, Fujisaki K (2006) Molecular cloning and functional characterization of an aspartic protease from the hard tick Haemaphysalis longicornis. Insect Biochem Mol Biol 36, 25-36. https://doi.org/10.1016/j.ibmb.2005.10.003
  4. Brunelle F, Nguyen-Quoc B, Cloutier C, Michaud D (1999) Protein hydrolysis by Colorado potato beetle, Leptinotarsa decemlineata, digestive proteases: the catalytic role of cathepsin D. Arch Insect Biochem Physiol 42, 88-98. https://doi.org/10.1002/(SICI)1520-6327(199909)42:1<88::AID-ARCH9>3.0.CO;2-I
  5. Carnevali O, Mosconi G, Cambi A, Ridolfi S, Zanuy S, Polzonetti- Magni AM (2001) Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos. Aquaculture 202, 249-256. https://doi.org/10.1016/S0044-8486(01)00775-X
  6. Cho WL, Raikhel AS (1992) Cloning of cDNA for mosquito lysosomal aspartic protease-sequence-analysis of an insect lysosomal-enzyme similar to cathepsin D and E. J Biol Chem 267, 21823-21829.
  7. Cho WL, Tsao SM, Hays AR (1999) Mosquito cathepsin Blike protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J Biol Chem 274, 13311-13321. https://doi.org/10.1074/jbc.274.19.13311
  8. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Nat Acad Sci USA 98, 12590-12595. https://doi.org/10.1073/pnas.221458698
  9. Duve C (1983) Lysosomes revisited. Eur J Biochem 137, 391- 397. https://doi.org/10.1111/j.1432-1033.1983.tb07841.x
  10. Fehrenbacher N, Jaattela M (2005) Lysosomes as targets for cancer therapy. Cancer Res 65, 2993-2995. https://doi.org/10.1158/0008-5472.CAN-05-0476
  11. Gui ZZ, Lee KS, Kim BY, Choi YS, Wei YD, Choo YM, Kang PD, Yoon HJ, Kim I, Je YH, Seo SJ, Lee SM, Guo XJ, Sohn HD, Jin BR (2006) Functional role of aspartic proteinase cathepsin D in insect metamorphosis. BMC Dev Biol 6, 49. https://doi.org/10.1186/1471-213X-6-49
  12. Gui ZZ, Hou CX, Liu T, Qin G.X, Li MW, Jin BR (2009) Effects of insect viruses and pesticides on glutathione Stransferase activity and gene expression in Bombyx mori L. J Econ Entomol 102, 1591-1598. https://doi.org/10.1603/029.102.0425
  13. Heidtmann HH, Salge U, Havemann K, Kirschke H, Wiederanders B (1993) Secretion of a latent, acid activatable cathepsin L precursor by human non-small cell lung cancer cell lines. Oncol Res 5, 441-451.
  14. Kurata S, Saito H, Natori S (1992) The 29-kDa hemocyte proteinase dissociates fat body at metamorphosis of Sarcophaga. Dev Biol 153, 115-121. https://doi.org/10.1016/0012-1606(92)90096-Y
  15. Lee KS, Kim BY, Choo YM, Yoon HJ, Kang PD, Woo SD, Sohn HD, Roh JY, Gui ZZ, Je YH, Jin BR (2009) Expression prole of cathepsin B in the fat body of Bombyx mori during metamorphosis. Comp Biochem Physiol B 154, 188-194. https://doi.org/10.1016/j.cbpb.2009.06.002
  16. Metcalf P, Fusek M (1993) Two crystal structures for cathepsin D: the lysosomal targeting signal and active site. EMBO J 12, 1293-1302.
  17. Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos JA, Ploegh H, Peters C, Rudensky AY (1998) Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453. https://doi.org/10.1126/science.280.5362.450
  18. Nakanishi H, Zhang J, Koike M, Nishioku T, Okamoto Y, Kominami E, Figura K, Peters C, Yamamoto K, Saftig P, Uchiyama Y (2001) Involvement of nitric oxide released from microglia-macrophages in pathological changes of cathepsin D-decient mice. J Neurosci 21, 7526-7533.
  19. Rabossi A, Stoka V, Puizdar V, Turk V, Quesada-Allue LA (2004) Novel aspartyl proteinase associated to fat body histolysis during Ceratitis capitata early metamorphosis. Arch Insect Biochem Physiol 57, 51-67. https://doi.org/10.1002/arch.20011
  20. Saftig P, Hetman M, Schmahl W, Weber K, Heine L, Mossmann H, Köster A, Hess B, Evers M, Figura K (1995) Mice decient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J 14, 3599- 3608.
  21. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula. J Mol Med 84, 901-910. https://doi.org/10.1007/s00109-006-0097-6
  22. Serbielle CI, Moreau S, Veillard F, Voldoire E, Annie B, Mannucci MA, Volkoff AN, Drezen JM, Lalmanach G, Huguet E (2009) Identification of parasite-responsive cysteine proteases in Manduca sexta. Biol Chem 390, 493-502.
  23. Shiba H, Uchida D, Kobayashi H, Natori M (2001) Involvement of cathepsin B- and L-Like proteinases in silk gland histolysis during metamorphosis of Bombyx mori. Arch Insect Biochem Physiol 390, 28-34.
  24. Shompole S, Jasmer DP (2001) Cathepsin B-like cysteine proteases confer intestinal cysteine protease activity in Haemonchus contortus. J Biol Chem 276, 2928-2934. https://doi.org/10.1074/jbc.M007321200
  25. Silva CP, Xavier-Filho J (1991) Comparison between the levels of aspartic and cysteine proteinases of the larval midguts of Callosobruchus maculatus (F) and Zabrotes subfasciatus (Boh) (Coleoptera, Bruchidae). Comp Biochem Physiol B 99, 529-533. https://doi.org/10.1016/0305-0491(91)90333-9
  26. Sloane BF, Moin K, Sameni M, Tait LR, Rozhin J, Ziegler G (1994) Membrane association of cathepsin B can be induced by transfection of human breast epithelial cells with c-Harasoncogene. J Cell Sci 107, 373-384.
  27. Snigirevskaya ES, Hays AR, Raikhel AS (1997) Secretory and internalization pathways of mosquito yolk protein precursors. Cell Tissue Res 290, 129-142. https://doi.org/10.1007/s004410050915
  28. Takahashi N, Kurata S, Natori S (1993) Molecular cloning of cDNA for the 29 kDa proteinase participating in decomposition of the larval fat body during metamorphosis of Sarcophaga peregrina (flesh fly). FEBS Lett 334, 153-157. https://doi.org/10.1016/0014-5793(93)81702-2
  29. Tsuji H, Akasaki K (1994) Identification and characterization of lysosomal enzymes involved in the proteolysis of phenobarbital- inducible cytochrome P450. Biol Pharm Bull 17, 568-571. https://doi.org/10.1248/bpb.17.568
  30. Turk B, Turk D, Turk V (2000) Lysosomal cysteine proteases: more than scavengers. Biochim Biophys Acta 1477, 98-111. https://doi.org/10.1016/S0167-4838(99)00263-0
  31. Urbich C, Heeschen C, Aicher A, Sasaki K, Bruhl T, Farhadi MR, Vajkoczy P, Hofmann WK, Peters C, Pennacchio LA, Abolmaali ND, Chavakis E, Reinheckel T, Zeiher AM, Dimmeler S (2005) Cathepsin L is required for endothelial progenitor cell-induced neovascularization. Nat Med 11, 206- 213. https://doi.org/10.1038/nm1182
  32. Xu YS, Kawasaki H (2001) Isolation and expression of cathepsin B cDNA in hemocytes during metamorphosis of Bombyx mori. Comp Biochem Physiol B 130, 393-399. https://doi.org/10.1016/S1096-4959(01)00448-1
  33. Yang XM, Hou LJ, Dong DJ, Shao HL, Wang JX, Zhao XF (2006) Cathepsin B-like proteinase is involved in the decomposition of the adult fat body of Helicoverpa armigera. Arch Insect Biochem Physiol 62, 1-10. https://doi.org/10.1002/arch.20115
  34. Yang XM, Hou LJ, Wang JX, Zhao XF (2007) Expression and function of cathepsin B-like proteinase in larval hemocytes of Helicoverpa armigera during metamorphosis. Arch Insect Biochem Physiol 64, 164-174. https://doi.org/10.1002/arch.20169
  35. Zhong D, Katar M, Linebaugh BE, Sloane BF, Berk RS (2001) Expression of cathepsins B, D and L in mouse corneas infected with Pseudomonas aeruginosa. Eur J Biochem 268, 6408-6416. https://doi.org/10.1046/j.0014-2956.2001.02607.x
  36. Zou FM, Lou DS, Zhu YH, Wang SP, Jin BR, Gui ZZ (2011) Expression profiles of glutatione S-transferase (GST) genes in larval midgut of Bombyx mori exposed to insect hormones. Mol Biol Rep 38, 639-647. https://doi.org/10.1007/s11033-010-0150-y

Cited by

  1. Cathepsins of lepidopteran insects: Aspects and prospects vol.64, 2015, https://doi.org/10.1016/j.ibmb.2015.07.005
  2. Identification and functional analysis of the cathepsin D gene promoter of Bombyx mori vol.41, pp.3, 2014, https://doi.org/10.1007/s11033-013-3009-1
  3. Identification of ecdysone response elements (EcREs) in the Bombyx mori cathepsin D promoter vol.425, pp.1, 2012, https://doi.org/10.1016/j.bbrc.2012.07.068
  4. Core promoter regulates the expression of cathepsin B gene in the fat body of Bombyx mori vol.542, pp.2, 2014, https://doi.org/10.1016/j.gene.2014.03.012
  5. larval fat body destruction pp.09621075, 2018, https://doi.org/10.1111/imb.12511
  6. Transcriptomics reveals specific molecular mechanisms underlying transgenerational immunity in Manduca sexta vol.10, pp.20, 2011, https://doi.org/10.1002/ece3.6764