DOI QR코드

DOI QR Code

Bioactivity-Guided Fraction from Viscera of Abalone, Haliotis discus hannai Suppresses Cellular Basophils Activation and Anaphylaxis in Mice

  • Kap Seong Choi (Department of Food Science and Technology, Sunchon National University) ;
  • Tai-Sun Shin (Division of Food and Nutrition, Chonnam National University) ;
  • Ginnae Ahn (Department of Marine Bio-Food Sciences, Chonnam National University) ;
  • Shin Hye Kim (Division of Food and Nutrition, Chonnam National University) ;
  • Jiyeon Chun (Department of Food Science and Technology, Sunchon National University) ;
  • Mina Lee (College of Pharmacy and Research Institute of Life and Pharmaceutical Sciences, Sunchon National University) ;
  • Dae Heon Kim (Department of Biomedical Science, Sunchon National University) ;
  • Han-Gil Choi (Faculty of Biological Science and Institute for Environmental Science, Wonkwang University) ;
  • Kyung-Dong Lee (Department of Companion animal industry, College of Health & Welfare, Dongshin University) ;
  • Sun-Yup Shim (Department of Food Science and Technology, Sunchon National University)
  • Received : 2023.10.11
  • Accepted : 2023.11.08
  • Published : 2024.02.28

Abstract

Basophils and mast cells are specialized effector cells in allergic reactions. Haliotis discus hannai (abalone), is valuable seafood. Abalone male viscera, which has a brownish color and has not been previously reported to show anti-allergic activities, was extracted with acetone. Six different acetone/hexane fractions (0, 10, 20, 30, 40, and 100%) were obtained using a silica column via β-hexosaminidase release inhibitory activity-guided selection in phorbol myristate acetate and a calcium ionophore, A23187 (PMACI)-induced human basophils, KU812F cells. The 40% acetone/hexane fraction (A40) exhibited the strongest inhibition of PMACI-induced-β-hexosaminidase release. This fraction dose-dependently inhibited reactive oxygen species (ROS) production and calcium mobilization without cytotoxicity. Western blot analysis revealed that A40 down-regulated PMACI-induced MAPK (ERK 1/2, p-38, and JNK) phosphorylation, and the NF-κB translocation from the cytosol to membrane. Moreover, A40 inhibited PMACI-induced interleukin (IL)-1β, IL-6, and IL-8 production. Anti-allergic activities of A40 were confirmed based on inhibitory effects on IL-4 and tumor necrosis factor alpha (TNF-α) production in compound (com) 48/80-induced rat basophilic leukemia (RBL)-2H3 cells. A40 inhibited β-hexosaminidase release and cytokine production such as IL-4 and TNF-α produced by com 48/80-stimulated RBL-2H3 cells. Furthermore, it's fraction attenuated the IgE/DNP-induced passive cutaneous anaphylaxis (PCA) reaction in the ears of BALB/c mice. Our results suggest that abalone contains the active fraction, A40 is a potent therapeutic and functional material to treat allergic diseases.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2020R1A2C1013664).

References

  1. Gershwin LJ. 2015. Comparative immunology of allergic responses. Annu. Rev. Anim. Biosci. 3: 327-346. https://doi.org/10.1146/annurev-animal-022114-110930
  2. Jimenez-Andrade GY, Ibarra-Sanchez A, Gonzalez D, Lamas M, GonzalezEspinosa C. 2013. Immunoglobulin E induces VEGF production in mast cells and potentiates their pro-tumorigenic actions through a Fyn kinase-dependent mechanism. J. Hematol. Oncol. 6: 56.
  3. Galli SJ, Tsai M, Piliponsky AM. 2008. The development of allergic inflammation. Nature 454: 445-454. https://doi.org/10.1038/nature07204
  4. Stone KD, Prussin C, Metclafe DD. 2010. IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 125: S73-S80. https://doi.org/10.1016/j.jaci.2009.11.017
  5. Shao-heng HE, Zhang H, Zeng X, Chen D, Yang P. 2013. Mast cells and basophils are essential for allergies: mechanisms of allergic inflammation and a proposed procedure for diagnosis. Acta Pharmacol. Sin. 34: 1270-1283. https://doi.org/10.1038/aps.2013.88
  6. Galli SJ, Gordon JR,Wershil BK. 1991. Cytokine production by mast cells and basophils. Curr. Opin. Immunol. 3: 865-872. https://doi.org/10.1016/S0952-7915(05)80005-6
  7. Valent P, Hartmann K, Bonadonna P, Niedoszytko M, Triggiani M, Arock M, Brockow K. 2022. Mast cell activation syndromes: collegium internationale allergologicum update 2022. J. Allergy Clin. Immunol. 183: 693-705. https://doi.org/10.1159/000524532
  8. Ngoc PL, Gold DR, Tzianabos AO, Weiss ST, Celedon JC. 2005. Cytokines, allergy, and asthma. Curr. Opin. Allergy Clin. Immunol. 5: 161-166. https://doi.org/10.1097/01.all.0000162309.97480.45
  9. Finkel T. 2011. Signal transduction by reactive oxygen species. J. Cell Biol. 194: 7-15. https://doi.org/10.1083/jcb.201102095
  10. Swindle EJ, Hunt JA, Coleman JW. 2002. A comparison of reactive oxygen species generation by rat peritoneal macrophages and mast cells using the highly sensitive real-time chemiluminescent probe pholasin: inhibition of antigen-induced mast cell degranulation by macrophage derived hydrogen peroxide. J. Immunol. 169: 5866-5873. https://doi.org/10.4049/jimmunol.169.10.5866
  11. Morris G, Gevezova M, Sarafian V, Maes M. 2022. Redox regulation of the immune response. Cell. Mol. Immunol. 19: 1079-1101. https://doi.org/10.1038/s41423-022-00902-0
  12. Berridge MJ. 1993. Inositol trisphosphate and calcium signaling. Nature 361: 315-325. https://doi.org/10.1038/361315a0
  13. Whitmarsh AJ. 2007. Regulation of gene transcription by mitogen-activated protein kinase signaling pathways. Biochim. Biophys. Acta 1773: 1285-1298. https://doi.org/10.1016/j.bbamcr.2006.11.011
  14. Yeung YT, Aziz F, Guerrero-Castilla A, Arguelles S. 2018. Signaling pathways in inflammation and anti-inflammatory therapies. Curr. Pharm. Des. 24: 1449-1484. https://doi.org/10.2174/1381612824666180327165604
  15. Zhao H, Wu L, Yan G, Chen Y, Zhou M, Wu Y, et al. 2021. Inflammation and tumor progression: signaling pathways and targeted intervention. Signal Transduct. Target. Ther. 6: 263
  16. Zhou DA, Ma DD, Zhao J, Wan XL, Tong L, Song S, et al. 2016. Simultaneous recovery of protein and polysaccharide from abalone (Haliotis discus hannai Ino) gonad using enzymatic hydrolysis method. J. Food Process. Preserv. 40: 119-130. https://doi.org/10.1111/jfpp.12589
  17. Guo S, Wang J, He C, Wei H, Ma Y, Xiong H. 2020. Preparation and antioxidant activities of polysaccharides obtained from abalone viscera by combination of enzymolysis and multiple separation methods. J. Food Sci. 85: 4260-4270. https://doi.org/10.1111/1750-3841.15520
  18. Gong F, Chen MF, Chen J, Li C, Zhou C, Hong P, et al. 2019. Boiled abalone byproduct peptide exhibits anti-tumor activity in HT1080 Cells and HUVECs by suppressing the metastasis and angiogenesis in Vitro. J. Agric. Food Chem. 67: 8855-8867. https://doi.org/10.1021/acs.jafc.9b03005
  19. Suleria HAR, Masci PP, Gobe GC, Osborne SA. 2017. Therapeutic potential of abalone and status of bioactive molecules: a comprehensive review. Crit. Rev. Food Sci. Nutr. 57: 1742-1748. https://doi.org/10.1080/10408398.2015.1031726
  20. Shin TS, Choi KS, Chun J, Kho KH, Son SA, Shim SY. 2022. Antiinflammatory effects of abalone (Haliotis discus hannai) viscera via inhibition of ROS production in LPS-stimulated RAW264.7 cells. Microbiol. Biotechnol. Lett. 50: 22-30. https://doi.org/10.48022/mbl.2109.09005
  21. Choi KS, Shin TS, Chun JY, Ahn G, Han EJ, Kim MJ, et al. 2022. Sargahydroquinoic acid isolated from Sargassum serratifolium as inhibitor of cellular basophils activation and passive cutaneous anaphylaxis in mice. Int. Immunopharmacol. 105: 108567.
  22. Evans H, Killoran KE, Mitre E. 2014. Measuring local anaphylaxis in mice. J. Vis. Exp. 92: e52005-e52005. https://doi.org/10.3791/52005-v
  23. Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordan RP, Paul WE. 1989. Mast cell lines produce lymphokines in response to crosslinkage of Fc epsilon RI or to calcium ionophores. Nature 339: 64-67. https://doi.org/10.1038/339064a0
  24. Kaur G, Sharma A, Bhatnagar A. 2021. Role of oxidative stress in pathophysiology of rheumatoid arthritis: insights into NRF2-KEAP1 signalling. Autoimmunity 54: 385-397. https://doi.org/10.1080/08916934.2021.1963959
  25. Gilfillan AM, Rivera J. 2009. The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228: 149-169. https://doi.org/10.1111/j.1600-065X.2008.00742.x
  26. Siraganian RP, Castro RO, Barbu EA, Zhang J. 2010. Mast cell signaling: the role of protein tyrosine kinase syk, its activation and screening methods for new pathway participants. FEBS Lett. 584: 4933-4940. https://doi.org/10.1016/j.febslet.2010.08.006
  27. Geldman A, Pallen CJ. 2014. Protein tyrosine phosphatases in mast cell signaling. Methods Mol. Biol. 1220: 269-286. https://doi.org/10.1007/978-1-4939-1568-2_17
  28. Sibilano R, Frossi B, Pucillo CE. 2014. Mast cell activation: a complex interplay of positive and negative signaling pathways. Eur. J. Immunol. 44: 2558-2566. https://doi.org/10.1002/eji.201444546
  29. Nigrovic PA, Binstadt BA, Monach PA. 2007. Mast cells contribute to initiation of autoantibody-mediated arthritis via IL-1. Proc. Natl. Acad. Sci. USA 104: 2325-2330. https://doi.org/10.1073/pnas.0610852103
  30. Lype J, Odermatt A, Bachmann S, Coeudevez M, Fux M. 2021. IL-1β promotes immunoregulatory responses in human blood basophils. Allergy 76: 2017-2029. https://doi.org/10.1111/all.14760
  31. Galli SJ, Gaudenzio N, Tsai M. 2020. Mast cells in inflammation and disease: recent progress and ongoing concerns. Annu. Rev. Immunol. 38: 49-77. https://doi.org/10.1146/annurev-immunol-071719-094903
  32. Metcalfe DD, Peavy RD, Gilfillan AM. 2009. Mechanisms of mast cell signaling in anaphylaxis. J. Allergy Clin. Immunol. 124: 639-946.  https://doi.org/10.1016/j.jaci.2009.08.035