Mucosal Immunoglobulin IgT at Gilthead Seabream Gill Plays a Predominant Role of Immunity during Vibrio harveyi Infection
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Authors
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Chen Meng-Han
Department of veterinarian, National Taiwan University, Taipei, Taiwan
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Wang Chung Ping
Institute of biochemistry, Academica Sinica, Taiwan
Keywords:
Teleost gill, mucosal, gilthead seabream, V. harveyi infectionAbstract
Teleost gill is considered a mucosal surface and a major site for pathogen entry. This study elucidated the predominant role of IgT, a primitive immunoglobulin classspecialized in mucosal immunity, in the gill of gilthead seabream during V. harveyi infection. Results showed that gill bacteria cells were mainly coated by IgT upon V. harveyi infection. An increase of IgT+ B cells and IgT concentration in gill mucus were also observed. Gilthead seabream devoid of IgT had significant increase of gill bacterial load and became highly susceptible to V. harveyi infection. Taken together, this study demonstrated that IgT plays a predominant role in the antibacterial immunity of gilthead seabream gill.
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References
1. Abós, B., Castro, R., Pignatelli, J., Luque, A., González, L., and Tafalla, C. (2013). Transcriptional heterogeneity of IgM+ cells in rainbow trout (Oncorhynchus mykiss) tissues. PLoS One, 8(12) : e82737. doi:10.1371/journal.pone.0082737
2. Beck, J. M., Young, V. B., and Huffnagle, G. B. (2012). The microbiome of the lung. Transl Res, 160(4) : 258-266. doi:10.1016/j.trsl.2012.02.005
3. Bjørgen, H., and Koppang, E. O. (2021). Anatomy of teleost fish immune structures and organs. Immunogenetics, 73(1) : 53-63. doi:10.1007/s00251-020-01196-0
4. Buonocore, F., Scapigliati, G., Pallavicini, A., and Gerdol, M. (2020). Identification of an IgD/IgT chimera in the European sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol, 105 : 224-232. doi:10.1016/j.fsi.2020.07.041
5. Castro, R., Bromage, E., Abós, B., Pignatelli, J., González Granja, A., Luque, A., and Tafalla, C. (2014). CCR7 is mainly expressed in teleost gills, where it defines an IgD+IgM- B lymphocyte subset. J Immunol, 192(3) : 1257-1266. doi:10.4049/jimmunol.1302471
6. Castro, R., Jouneau, L., Pham, H. P., Bouchez, O., Giudicelli, V., Lefranc, M. P., and Boudinot, P. (2013). Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection. PLoS Pathog, 9(1) : e1003098. doi:10.1371/journal.ppat.1003098
7. Chieng, C. C. Y., Daud, H. M., Yusoff, F. M., Thompson, K. D., and Abdullah, M. (2020). Mucosal responses of brown-marbled grouper Epinephelus fuscoguttatus (Forsskål, 1775) following intraperitoneal infection with Vibrio harveyi. J Fish Dis, 43(10) : 1249-1258. doi:10.1111/jfd.13222
8. dos Santos, N. M., Taverne-Thiele, J. J., Barnes, A. C., van Muiswinkel, W. B., Ellis, A. E., and Rombout, J. H. (2001). The gill is a major organ for antibody secreting cell production following direct immersion of sea bass (Dicentrarchus labrax, L.) in a Photobacterium damselae ssp. piscicida bacterin: an ontogenetic study. Fish Shellfish Immunol, 11(1) : 65-74. doi:10.1006/fsim.2000.0295
9. Fernandez, C., Mascolo, D., Monaghan, S. J., Baily, J. L., Chalmers, L., Paladini, G., and Fridman, S. (2019). Methacarn preserves mucus integrity and improves visualization of amoebae in gills of Atlantic salmon (Salmo salar L.). J Fish Dis, 42(6) : 883-894. doi:10.1111/jfd.12988
10. Fu, Q., Wei, Z., Chen, Y., Xie, J., Zhang, X., He, T., and Chen, X. (2021). Development of monoclonal antibody against IgT of a perciform fish, large yellow croaker (Larimichthys crocea) and characterization of IgT(+) B cells. Dev Comp Immunol, 119 : 104027. doi:10.1016/j.dci.2021.104027
11. Giffroy, D., Courtoy, P. J., and Vaerman, J. P. (2001). Polymeric IgA binding to the human pIgR elicits intracellular signalling, but fails to stimulate pIgR-transcytosis. Scand J Immunol, 53(1) : 56-64. doi:10.1046/j.1365-3083.2001.00843.x
12. Gong, H., Wang, Q., Lai, Y., Zhao, C., Sun, C., Chen, Z., and Huang, Z. (2020). Study on Immune Response of Organs of Epinephelus coioides and Carassius auratus After Immersion Vaccination With Inactivated Vibrio harveyi Vaccine. Front Immunol, 11 : 622387. doi:10.3389/fimmu.2020.622387
13. Hamuro, K., Suetake, H., Saha, N. R., Kikuchi, K., and Suzuki, Y. (2007). A teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin. J Immunol, 178(9) : 5682-5689. doi:10.4049/jimmunol.178.9.5682
14. Hansen, J. D., Landis, E. D., and Phillips, R. B. (2005). Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. Proc Natl Acad Sci U S A, 102(19) : 6919-6924. doi:10.1073/pnas.0500027102
15. Ji, J. F., Hu, C. B., Zhang, N., Huang, X., Shao, T., Fan, D. D., and Shao, J. Z. (2021). New Insights into IgZ as a Maternal Transfer Ig Contributing to the Early Defense of Fish against Pathogen Infection. J Immunol, 206(9) : 2001-2014. doi:10.4049/jimmunol.2001197
16. Kong, W. G., Yu, Y. Y., Dong, S., Huang, Z. Y., Ding, L. G., Cao, J. F., and Xu, Z. (2019). Pharyngeal Immunity in Early Vertebrates Provides Functional and Evolutionary Insight into Mucosal Homeostasis. J Immunol, 203(11) : 3054-3067. doi:10.4049/jimmunol.1900863
17. Lin, A. V. (2015). Indirect ELISA. Methods Mol Biol, 1318 : 51-59. doi:10.1007/978-1-4939-2742-5_5
18. Magadán-Mompó, S., Sánchez-Espinel, C., and Gambón-Deza, F. (2011). Immunoglobulin heavy chains in medaka (Oryzias latipes). BMC Evol Biol, 11 : 165. doi:10.1186/1471-2148-11-165
19. Makesh, M., Sudheesh, P. S., and Cain, K. D. (2015). Systemic and mucosal immune response of rainbow trout to immunization with an attenuated Flavobacterium psychrophilum vaccine strain by different routes. Fish Shellfish Immunol, 44(1) : 156-163. doi:10.1016/j.fsi.2015.02.003
20. Parra, D., Korytář, T., Takizawa, F., and Sunyer, J. O. (2016). B cells and their role in the teleost gut. Dev Comp Immunol, 64 : 150-166. doi:10.1016/j.dci.2016.03.013
21. Perše, M., and Večerić-Haler, Ž. (2019). The Role of IgA in the Pathogenesis of IgA Nephropathy. Int J Mol Sci, 20(24) : doi:10.3390/ijms20246199
22. Piazzon, M. C., Galindo-Villegas, J., Pereiro, P., Estensoro, I., Calduch-Giner, J. A., Gómez-Casado, E., and Pérez-Sánchez, J. (2016). Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish. Front Immunol, 7 : 637. doi:10.3389/fimmu.2016.00637
23. Ramirez-Gomez, F., Greene, W., Rego, K., Hansen, J. D., Costa, G., Kataria, P., and Bromage, E. S. (2012). Discovery and characterization of secretory IgD in rainbow trout: secretory IgD is produced through a novel splicing mechanism. J Immunol, 188(3) : 1341-1349. doi:10.4049/jimmunol.1101938
24. Rességuier, J., Dalum, A. S., Pasquier, L. D., Zhang, Y., Koppang, E. O., Boudinot, P., and Wiegertjes, G. F. (2020). Lymphoid Tissue in Teleost Gills: Variations on a Theme. Biology (Basel), 9(6) : doi:10.3390/biology9060127
25. Shen, G. M., Shi, C. Y., Fan, C., Jia, D., Wang, S. Q., Xie, G. S., and Huang, J. (2017). Isolation, identification and pathogenicity of Vibrio harveyi, the causal agent of skin ulcer disease in juvenile hybrid groupers Epinephelus fuscoguttatus × Epinephelus lanceolatus. J Fish Dis, 40(10) : 1351-1362. doi:10.1111/jfd.12609
26. Vazquez, M. I., Catalan-Dibene, J., and Zlotnik, A. (2015). B cells responses and cytokine production are regulated by their immune microenvironment. Cytokine, 74(2) : 318-326. doi:10.1016/j.cyto.2015.02.007
27. Wei, H., and Wang, J. Y. (2021). Role of Polymeric Immunoglobulin Receptor in IgA and IgM Transcytosis. Int J Mol Sci, 22(5). doi:10.3390/ijms22052284
28. Woof, J. M., and Mestecky, J. (2005). Mucosal immunoglobulins. Immunol Rev, 206 : 64-82. doi:10.1111/j.0105-2896.2005.00290.x
29. Xu, H. Y., Dong, F., Zhai, X., Meng, K. F., Han, G. K., Cheng, G. F., and Xu, Z. (2020). Mediation of Mucosal Immunoglobulins in Buccal Cavity of Teleost in Antibacterial Immunity. Front Immunol, 11 : 562795. doi:10.3389/fimmu.2020.562795
30. Xu, Z., Parra, D., Gómez, D., Salinas, I., Zhang, Y. A., von Gersdorff Jørgensen, L., and Sunyer, J. O. (2013). Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proc Natl Acad Sci U S A, 110(32) : 13097-13102. doi:10.1073/pnas.1304319110
31. Xu, Z., Takizawa, F., Casadei, E., Shibasaki, Y., Ding, Y., Sauters, T. J. C., and Sunyer, J. O. (2020). Specialization of mucosal immunoglobulins in pathogen control and microbiota homeostasis occurred early in vertebrate evolution. Sci Immunol, 5(44). doi:10.1126/sciimmunol.aay3254
32. Yu, Y. Y., Kong, W., Yin, Y. X., Dong, F., Huang, Z. Y., Yin, G. M., and Xu, Z. (2018). Mucosal immunoglobulins protect the olfactory organ of teleost fish against parasitic infection. PLoS Pathog, 14(11) : e1007251. doi:10.1371/journal.ppat.1007251
33. Zhang, X. H., He, X., and Austin, B. (2020). Vibrio harveyi: a serious pathogen of fish and invertebrates in mariculture. Mar Life Sci Technol, 1-15. doi:10.1007/s42995-020-00037-z
34. Zhang, X. T., Yu, Y. Y., Xu, H. Y., Huang, Z. Y., Liu, X., Cao, J. F., and Xu, Z. (2021). Prevailing Role of Mucosal Igs and B Cells in Teleost Skin Immune Responses to Bacterial Infection. J Immunol, 206(5) : 1088-1101. doi:10.4049/jimmunol.2001097
35. Zhang, Y. A., Salinas, I., Li, J., Parra, D., Bjork, S., Xu, Z., and Sunyer, J. O. (2010). IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol, 11(9) : 827-835. doi:10.1038/ni.1913
