Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Immunomodulatory properties of enzymatic extract of Stichopus japonicus on murine splenocytes

  • Mihindukulasooriya, Suyama Prasansali (Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University) ;
  • Kim, Bohyung (Department of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University) ;
  • Dinh, Duong Thi Thuy (Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University) ;
  • Herath, Kalahe Hewage Iresha Nadeeka Madushani (Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University) ;
  • Cho, Jinhee (Department of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University) ;
  • Kim, Hyo Jin (Department of Food Bioengineering, Jeju National University) ;
  • Yang, Jiwon (Department of Animal Biotechnology, Faculty of Biotechnology, Jeju National University) ;
  • Jee, Youngheun (Interdisciplinary Graduate Program in Advanced Convergence Technology & Science, Jeju National University)
  • Received : 2021.06.10
  • Accepted : 2021.08.08
  • Published : 2021.08.31
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Abstract

Red sea cucumber Stichopus japonicus is an invertebrate animal inhabiting in coasts of Korea, China, and Japan. They are traditionally used for food and medicine and well known for their distinctive biologically and pharmacologically important compounds. We investigated the effect of amyloglucosidase (AMG) enzymatic extracts of S. japonicus (AESJ) on the proliferation and cytokine secretion of murine splenocytes stimulated with concanavalin A (Con A). AESJ enhanced the proliferation of splenocytes and the production of IL-2 (Th1 cytokine), IL-1β (Th1 promoting cytokine), and IL-4, IL-10 (Th2 type cytokines) when treated alone. However, under Con A stimulation, AESJ suppressed the proliferation of splenocytes, attenuated the secretion of IL-2, IL-4, IL-10, and enhanced IL-1β secretion. These results suggest that AESJ exhibits immunomodulatory effect by moderating the proliferation of splenocytes and the secretion of IL-2, IL-1β, IL-4, and IL-10 differently depending on the absence and presence of Con A stimulation. These data evidence the immunomodulatory potential of AESJ, which can be further developed into a functional food mediating homeostasis.

Keywords

Acknowledgement

The authors wish to thank Dr. T.H. Chung for the editorial assistance.

References

  1. Abood WN, Fahmi I, Abdulla MA, Ismail S. Immunomodulatory effect of an isolated fraction from Tinospora crispa on intracellular expression of INF-γ, IL-6 and IL-8. BMC Complement Altern Med. 2014;14:205. https://doi.org/10.1186/1472-6882-14-205
  2. Adeoyo OR, Pletschke BI, Dames JF. Purification and characterization of an amyloglucosidase from an ericoid mycorrhizal fungus (Leohumicola incrustata). AMB Express. 2018;8:154. https://doi.org/10.1186/s13568-018-0685-1
  3. Affan A, Heo SJ, Jeon YJ, Lee JB. Optimal growth conditions and antioxidative activities of Cylindrotheca closterium (Bacillariophyceae). J Phycol. 2009;45:1405-15. https://doi.org/10.1111/j.1529-8817.2009.00763.x
  4. Azam S, Jakaria M, Kim IS, Kim J, Haque ME, Choi DK. Regulation of toll-like receptor (TLR) signaling pathway by polyphenols in the treatment of age-linked neurodegenerative diseases: focus on TLR4 signaling. Front Immunol. 2019;10:1000. https://doi.org/10.3389/fimmu.2019.01000
  5. Benlhassan-Chahour K, Penit C, Dioszeghy V, Vasseur F, Janvier G, Riviere Y, et al. Kinetics of lymphocyte proliferation during primary immune response in macaques infected with pathogenic simian immunodeficiency virus SIV-mac251: preliminary report of the effect of early antiviral therapy. J Virol. 2003;77:12479-93. https://doi.org/10.1128/JVI.77.23.12479-12493.2003
  6. Bordbar S, Anwar F, Saari N. High-value components and bioactives from sea cucumbers for functional foods: a review. Mar Drugs. 2011;9:1761-805. https://doi.org/10.3390/md9101761
  7. Cameron AR, Nelson J, Forman HJ. Depolarization and increased conductance precede superoxide release by concanavalin A-stimulated rat alveolar macrophages. Proc Natl Acad Sci USA. 1983;80:3726-8. https://doi.org/10.1073/pnas.80.12.3726
  8. Cao RA, Surayot U, You S. Structural characterization of immunostimulating protein-sulfated fucan complex extracted from the body wall of a sea cucumber, Stichopus japonicus. Int J Biol Macromol. 2017;99:539-48. https://doi.org/10.1016/j.ijbiomac.2017.03.026
  9. Cho J, Bing SJ, Kim A, Lee NH, Byeon SH, Kim GO, et al. Beetroot (Beta vulgaris) rescues mice from γ-ray irradiation by accelerating hematopoiesis and curtailing immunosuppression. Pharm Biol. 2017;55:306-16. https://doi.org/10.1080/13880209.2016.1237976
  10. Chung EY, Liu J, Homma Y, Zhang Y, Brendolan A, Saggese M, et al. Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity. 2007;27:P952-64. https://doi.org/10.1016/j.immuni.2007.11.014
  11. Da Silva TA, de Souza MA, Cecilio NT, Roque-Barreira MC. Activation of spleen cells by ArtinM may account for its immunomodulatory properties. Cell Tissue Res. 2014;357:719-30. https://doi.org/10.1007/s00441-014-1879-8
  12. Doskocil I, Havlik J, Verlotta R, Tauchen J, Vesela L, Macakova K, et al. In vitro immunomodulatory activity, cytotoxicity and chemistry of some central European polypores. Pharm Biol. 2016;54:2369-76. https://doi.org/10.3109/13880209.2016.1156708
  13. Duan X, Zhang M, Mujumdar AS, Wang S. Microwave freeze drying of sea cucumber (Stichopus japonicus). J Food Eng. 2010;96:491-7. https://doi.org/10.1016/j.jfoodeng.2009.08.031
  14. Gomez-Gil E, Franco A, Madrid M, Vazquez-Marin B, Gacto M, Fernandez-Breis J, et al. Quorum sensing and stress-activated MAPK signaling repress yeast to hypha transition in the fission yeast Schizosaccharomyces japonicus. PLOS Genet. 2019;15:e1008192. https://doi.org/10.1371/journal.pgen.1008192
  15. Han L, Meng M, Guo M, Cheng D, Shi L, Wang X, et al. Immunomodulatory activity of a water-soluble polysaccharide obtained from highland barley on immunosuppressive mice models. Food Funct. 2019;10:304-14. https://doi.org/10.1039/C8FO01991F
  16. Heo SJ, Park EJ, Lee KW, Jeon YJ. Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol. 2005;96:1613-23. https://doi.org/10.1016/j.biortech.2004.07.013
  17. Herath KHINM, Cho J, Kim A, Kim HS, Han EJ, Kim HJ, et al. Differential modulation of immune response and cytokine profiles of Sargassum horneri ethanol extract in murine spleen with or without Concanavalin A stimulation. Biomed Pharmacother. 2019;110:930-42. https://doi.org/10.1016/j.biopha.2018.12.001
  18. Herath KM, Lee JH, Cho J, Kim A, Shin SM, Kim B, et al. Immunostimulatory effect of pepsin enzymatic extract from Porphyra yezoensis on murine splenocytes. J Sci Food Agric. 2018;98:3400-8. https://doi.org/10.1002/jsfa.8851
  19. Himaya SWA, Ryu B, Qian ZJ, Kim SK. Sea cucumber, Stichopus japonicus ethyl acetate fraction modulates the lipopolysaccharide induced iNOS and COX-2 via MAPK signaling pathway in murine macrophages. Environ Toxicol Pharmacol. 2010;30:68-75. https://doi.org/10.1016/j.etap.2010.03.019
  20. Khotimchenko Y. Pharmacological potential of sea cucumbers. Int J Mol Sci. 2018;19:1342. https://doi.org/10.3390/ijms19051342
  21. Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8:223-46.
  22. Ko SC, Lee JK, Byun HG, Lee SC, Jeon YJ. Purification and characterization of angiotensin I-converting enzyme inhibitory peptide from enzymatic hydrolysates of Styela clava flesh tissue. Process Biochem. 2012;47:34-40. https://doi.org/10.1016/j.procbio.2011.10.005
  23. Lacy P, Stow JL. Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood. 2011;118:9-18. https://doi.org/10.1182/blood-2010-08-265892
  24. Lei HY, Chang CP. Lectin of Concanavalin A as an anti-hepatoma therapeutic agent. J Biomed Sci. 2009;16:10. https://doi.org/10.1186/1423-0127-16-10
  25. Malek TR. The main function of IL-2 is to promote the development of T regulatory cells. J Leukoc Biol. 2003;74:961-5. https://doi.org/10.1189/jlb.0603272
  26. Moudgil KD, Choubey D. Cytokines in autoimmunity: role in induction, regulation, and treatment. J Interferon Cytokine Res. 2011;31:695-703. https://doi.org/10.1089/jir.2011.0065
  27. Oh GW, Ko SC, Lee DH, Heo SJ, Jung WK. Biological activities and biomedical potential of sea cucumber (Stichopus japonicus): a review. Fish Aquatic Sci. 2017;20:28. https://doi.org/10.1186/s41240-017-0071-y
  28. Ortuno-Sahagun D, Zanker K, Rawat AKS, Kaveri SV, Hegde P. Natural immunomodulators. J Immunol Res. 2017;2017:7529408.
  29. Puddu P, Carollo M, Pietraforte I, Spadaro F, Tombesi M, Ramoni C, et al. IL-2 induces expression and secretion of IFN-γ in murine peritoneal macrophages. J Leukoc Biol. 2005;78:686-95. https://doi.org/10.1189/jlb.0105035
  30. Romagnani S. T-cell subsets (Th1 versus Th2). Ann Allergy Asthma Immunol. 2000;85:9-18. https://doi.org/10.1016/S1081-1206(10)62426-X
  31. Sass G, Heinlein S, Agli A, Bang R, Schumann J, Tiegs G. Cytokine expression in three mouse models of experimental hepatitis. Cytokine. 2002;19:115-20. https://doi.org/10.1006/cyto.2002.1948
  32. Song Y, Jin SJ, Cui LH, Ji XJ, Yang FG. Immunomodulatory effect of Stichopus japonicus acid mucopolysaccharide on experimental hepatocellular carcinoma in rats. Molecules. 2013;18:7179-93. https://doi.org/10.3390/molecules18067179
  33. Steen-Louws C, Hartgring SAY, Popov-Celeketic J, Lopes AP, de Smet MBM, Eijkelkamp N, et al. IL4-10 fusion protein: a novel immunoregulatory drug combining activities of interleukin 4 and interleukin 10. Clin Exp Immunol. 2019;195:1-9. https://doi.org/10.1111/cei.13224
  34. Taiyeb-Ali TB, Zainuddin SLA, Swaminathan D, Yaacob H. Efficacy of 'Gamadent' toothpaste on the healing of gingival tissues: a preliminary report. J Oral Sci. 2003;45:153-9. https://doi.org/10.2334/josnusd.45.153
  35. Wargasetia TL, Widodo. Mechanisms of cancer cell killing by sea cucumber-derived compounds. Invest New Drugs. 2017;35:820-6. https://doi.org/10.1007/s10637-017-0505-5
  36. Wijesinghe WAJP, Jeon YJ. Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia. 2012;83:6-12. https://doi.org/10.1016/j.fitote.2011.10.016
  37. Wluka A, Olszewski WL. Innate and adaptive processes in the spleen. Ann Transplant. 2006;11:22-9.
  38. Yan J, Ma Y, Zhao F, Gu W, Jiao Y. Identification of immunomodulatory signatures induced by American ginseng in murine immune cells. Evid Based Complement Alternat Med. 2013;2013:972814.
  39. Yang WC, Hwang YS, Chen YY, Liu CL, Shen CN, Hong WH, et al. Interleukin-4 supports the suppressive immune responses elicited by regulatory T cells. Front Immunol. 2017;8:1508. https://doi.org/10.3389/fimmu.2017.01508
  40. Ye J, Shen C, Huang Y, Zhang X, Xiao M. Anti-fatigue activity of sea cucumber peptides prepared from Stichopus japonicus in an endurance swimming rat model. J Sci Food Agric. 2017;97:4548-56. https://doi.org/10.1002/jsfa.8322
  41. Zhou X, Dong Q, Kan X, Peng L, Xu X, Fang Y, et al. Immunomodulatory activity of a novel polysaccharide from Lonicera japonica in immunosuppressed mice induced by cyclophosphamide. PLOS ONE. 2018;13:e0204152. https://doi.org/10.1371/journal.pone.0204152
  42. Zhu J, Paul WE. Heterogeneity and plasticity of T helper cells. Cell Res. 2010;20:4-12. https://doi.org/10.1038/cr.2009.138