Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Molecular characterization and expression of CD96 in red seabream (Pagrus major)

  • Won-Sik Woo (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Kwang-Min Choi (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Min-Soo Joo (East Sea Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Gyoungsik Kang (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Kyung-Ho Kim (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Ha-Jeong Son (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Min-Young Sohn (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Do-Hyung Kim (Department of Aquatic Life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Chan-Il Park (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University)
  • Received : 2022.11.04
  • Accepted : 2022.12.08
  • Published : 2023.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

CD96 is a membrane-bound receptor discovered in humans in 1992 that is mainly present in natural killer cells and T cells derived from haematopoietic cells and performs immune functions. Based on the sequence of CD96 obtained from red seabream (Pagrus major), phylogenetic analysis with other species, infections of normal fish, Streptococcus iniae and red sea bream iridovirus (RSIV), and expression analysis was conducted using real-time polymerase chain reaction. Phylogenetic analysis showed the highest homology with Sparus aurata, and multiple sequence analysis confirmed the conservation of major domains between different fish species. Normal fish high expression results were confirmed in the head kidney, and spleen, which are the haematopoietic organs of the fish. High expression levels were confirmed in the gills, liver, spleen, and kidney on day three after RSIV infection. After S. iniae infection, high expression was confirmed in the gills and liver on day one, and high expression was confirmed in the spleen from 12 hours. These results show that PmCD96 functions as an immune gene in P. major and is considered a basic research case for CD96 in fish's hematopoietic organ immune system.

Keywords

Acknowledgement

This research was supported by Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (20200470, Development of Electrinic illustrated book for ornamental fish).

References

  1. Blake SJ, Stannard K, Liu J, Allen S, Yong MCR, Mittal D, et al. Suppression of metastases using a new lymphocyte checkpoint target for cancer immunotherapy. Cancer Discov. 2016;6:446-59. https://doi.org/10.1158/2159-8290.CD-15-0944
  2. Bork P, Holm L, Sander C. The immunoglobulin fold: structural classification, sequence patterns and common core. J Mol Biol. 1994;242:309-20. https://doi.org/10.1016/S0022-2836(84)71582-8
  3. Brooks J, Fleischmann-Mundt B, Woller N, Niemann J, Ribback S, Peters K, et al. Perioperative, spatiotemporally coordinated activation of T and NK cells prevents recurrence of pancreatic cancer. Cancer Res. 2018;78:475-88. https://doi.org/10.1158/0008-5472.CAN-17-2415
  4. Chan CJ, Martinet L, Gilfillan S, Souza-Fonseca-Guimaraes F, Chow MT, Town L, et al. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat Immunol. 15:2014;431-8. https://doi.org/10.1038/ni.2850
  5. Daeron M, Jaeger S, Du Pasquier L, Vivier E. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol Rev. 2008;224:11-43. https://doi.org/10.1111/j.1600-065X.2008.00666.x
  6. Du Pasquier L, Zucchetti I, De Santis R. Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol Rev. 2004;198:233-48. https://doi.org/10.1111/j.0105-2896.2004.00122.x
  7. El Aamri F, Real F, Acosta F, Bravo J, Roman L, Deniz S, et al. Differential innate immune response of European seabass (Dicentrarchus labrax) against Streptococcus iniae. Fish Shellfish Immunol. 2015;46:436-41. https://doi.org/10.1016/j.fsi.2015.05.054
  8. Eriksson EM, Keh CE, Deeks SG, Martin JN, Hecht FM, Nixon DF. Differential expression of CD96 surface molecule represents CD8+ T cells with dissimilar effector function during HIV-1 infection. PLOS ONE. 2012;7:e51696.
  9. Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol. 2004;172:3994-8. https://doi.org/10.4049/jimmunol.172.7.3994
  10. Georgiev H, Ravens I, Papadogianni G, Halle S, Malissen B, Loots GG, et al. Coming of age: CD96 emerges as modulator of immune responses. Front Immunol. 2018;9:1072.
  11. Hwang SD, Shim SH, Kwon MG, Chae YS, Shim WJ, Jung JH, et al. Molecular cloning and expression analysis of two lipopolysaccharide-induced TNF-α factors (LITAFs) from rock bream, Oplegnathus fasciatus. Fish Shellfish Immunol. 2014;36:467-74. https://doi.org/10.1016/j.fsi.2013.12.023
  12. Johnston RJ, Comps-Agrar L, Hackney J, Yu X, Huseni M, Yang Y, et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8+ T cell effector function. Cancer Cell. 2014;26:923-37. https://doi.org/10.1016/j.ccell.2014.10.018
  13. Kurtulus S, Sakuishi K, Ngiow SF, Joller N, Tan DJ, Teng MWL, et al. TIGIT predominantly regulates the immune response via regulatory T cells. J Clin Invest. 2015;125:4053-62. https://doi.org/10.1172/JCI81187
  14. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  15. Neil Barclay A. Membrane proteins with immunoglobulin-like domains-a master superfamily of interaction molecules. Semin Immunol. 2003;15:215-23. https://doi.org/10.1016/S1044-5323(03)00047-2
  16. Pulsford A, Tomlinson MG, Lemaire-Gony S, Glynn PJ. Development and immunocompetence of juvenile flounder Platichthys flesus, L. Fish Shellfish Immunol. 1994;4:63-78. https://doi.org/10.1006/fsim.1994.1006
  17. Scapigliati G, Fausto AM, Picchietti S. Fish lymphocytes: an evolutionary equivalent of mammalian innate-like lymphocytes? Front Immunol. 2018;9:971.
  18. Seth S, Maier MK, Qiu Q, Ravens I, Kremmer E, Forster R, et al. The murine pan T cell marker CD96 is an adhesion receptor for CD155 and nectin-1. Biochem Biophys Res Commun. 2007;364:959-65. https://doi.org/10.1016/j.bbrc.2007.10.102
  19. Sinclair NRSTC, Chan PL. Relationship between antibody-mediated immunosuppression and tolerance induction. Nature. 1971;234:104-5. https://doi.org/10.1038/234104a0
  20. Wang PL, O'Farrell S, Clayberger C, Krensky AM. Identification and molecular cloning of tactile. A novel human T cell activation antigen that is a member of the Ig gene superfamily. J Immunol. 1992;148:2600-8. https://doi.org/10.4049/jimmunol.148.8.2600
  21. Williams AF, Barclay AN. The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol. 1988;6:381-405. https://doi.org/10.1146/annurev.iy.06.040188.002121
  22. Xie C, Wang Z, Li Y, Wu F, Xia H, Lu Y, et al. Molecular characterization and expression of CD96 in Nile tilapia (Oreochromis niloticus) in response to different pathogens stimulus. Aquacult Rep. 2021;20:100705.