Skip to main content
Log in

Characterization and expression analysis of B Cell receptor accessory molecule CD79 gene in humphead snapper (Lutjanus sanguineus)

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

CD79, a key component of the B cell antigen receptor complex, is composed of CD79α(Igα) and CD79β(Igβ) encoded by mb-1 and B29 respectively, and plays an important role in B cell signaling. In this study, we isolated and characterized mb-1 and B29 from humphead snapper (Lutjanus sanguineus). Their tissue distribution and expression profiles after stimulations in vitro and in vivo were also investigated. The humphead snapper mb-1 and B29 contain open reading frames of 684 bp and 606 bp, encoding 227 amino acids and 201 amino acids, respectively. Both CD79α and CD79β possess signal peptide, extracellular Ig domain, transmembrane region and immunoreceptor tyrosine kinase activation motif (ITAM). Mb-1 is highly expressed in lymphoid organs (thymus, posterior kidney and spleen) and mucosal-associated lymphoid tissues (gill and intestine), while B29 is mainly detected in posterior kidney, spleen, gill and skin. Furthermore, transcription of mb-1 and B29 in head kidney leucocytes was up-regulated following lipopolysaccharide (LPS), pokeweed mitogen (PWM), and polyinosinic-polycytidylic acid (PolyI:C) stimulation, respectively, and their expression level in anterior kidney and spleen was also increased after challenged with formalin-inactived Vibrio harveyi. These results indicated that humphead snapper CD79 molecule might play an important role in immune response to pathogen infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Braun, D., Caramalho, I., and Demengeot, J., 2002. IFN-a/ß enhances BCR-dependent B cell responses. International Immunology, 14(4): 411–419.

    Article  Google Scholar 

  • Burkhardt, A. L., Costa, T., Misulovin, Z., Stealy, B., Bolen, J. B., and Nußsenzweig, M. C., 1994. Iga and Igß are functionally homologous to the signaling proteins of the T-cell receptor. Molecular and Cellular Biology, 14(2): 1095–1103.

    Article  Google Scholar 

  • Cai, S. H., Huang, Y. C., Lu, Y. S., Wu, Z. H., Wang, B., Tang, J. F., and Jian, J. C., 2013. Expression and immunogenicity analysis of accessory colonization factor A from Vibrio alginolyticus strain HY9901. Fish and Shellfish Immunology, 34(2): 454–462.

    Article  Google Scholar 

  • Chu, P. G., and Arber, D. A., 2001. CD79: A review. Applied Immunohistochemistry and Molecular Morphology, 9(2): 97–106.

    Google Scholar 

  • Darawiroj, D., Kondo, H., Hirono, I., and Aoki, T., 2008. Immune-related gene expression profiling of yellowtail (Seriola quinqueradiata) kidney cells stimulated with ConA and LPS using microarray analysis. Fish and Shellfish Immunology, 24(2): 260–266.

    Article  Google Scholar 

  • DeFranco, A. L., 1993. Structure and function of the B cell antigen receptor. Annual Review of Cell and Developmental Biology, 9: 377–410.

    Article  Google Scholar 

  • Duncan, L., Webster, K., Gupta, V., Nair, S., and Deane, E., 2010. Molecular characterisation of the CD79a and CD79b subunits of the B cell receptor complex in the gray shorttailed opossum (Monodelphis domestica) and tammar wallaby (Macropus eugenii): Delayed B cell immunocompetence in marsupial neonates. Veterinary Immunology and Immunopathology, 136 (3-4): 235–247.

    Article  Google Scholar 

  • Dylke, J., Lopes, J., Dang-Lawson, M., Machtaler, S., and Matsuuchi, L., 2007. Role of the extracellular and transmembrane domain of Ig-a/ß in assembly of the B cell antigen receptor (BCR). Immunology Letters, 112(1): 47–57.

    Article  Google Scholar 

  • Ferrari, S., Lougaris, V., Caraffi, S., Zuntini, R., Yang, J., Soresina, A., Meini, A., Cazzola, G., Roßsi, C., Reth, M., and Plebani, A., 2007. Mutations of the Igß gene cause agammaglobulinemia in man. The Journal of Exprimental Medicine, 204(9): 2047–2051.

    Article  Google Scholar 

  • Grøntvedt, R. N., and Espelid, S., 2003. Immunoglobulin producing cells in the spotted wolffish (Anarhichas minor Olafsen): Localization in adults and during juvenile development. Developmental and Comparative Immunology, 27 (6-7): 569–578.

    Article  Google Scholar 

  • Guselnikov, S. V., Bell, A., Najakshin, A. M., Robert, J., and Taranin, A. V., 2003. Signaling FcR and TCR subunit homologs in the amphibian Xenopus laevis. Developmental and Comparative Immunology, 27(8): 727–733.

    Article  Google Scholar 

  • Ha, H. J., Kubagawa, H., and Burrows, P. D., 1992. Molecular cloning and expression pattern of a human gene homologous to the murine mb-1 gene. The Journal of Immunology, 148(5): 526–1531.

    Google Scholar 

  • Halaby, D. M., and Mornon, J. P., 1998. The immunoglobulin superfamily: An insight on its tissular, species, and functional diversity. Journal of Molecular Evolution, 46(4): 389–400.

    Article  Google Scholar 

  • Hermanson, G. G., Eisenberg, D., Kincade, P. W., and Wall, R., 1988. B29: A member of the immunoglobulin gene superfamily exclusively expressed on B-lineage cells. Proceedings of the National Academy of Sciences, 85(18): 6890–6894.

    Article  Google Scholar 

  • Herren, B., and Burrows, P. D., 2002. B cell-restricted human mb-1 gene: Expression, function, and lineage infidelity. Immunological Research, 26 (1-3): 35–43.

    Article  Google Scholar 

  • Hombach, J., Tsubata, T., Leclercq, L., Stappert, H., and Reth, M., 1990. Molecular-components of the B-cell antigen receptor complex of the IgM class. Nature, 343(6260): 760–762.

    Article  Google Scholar 

  • Kabak, S., Skaggs, B. J., Gold, M. R., Affolter, M., West, K. L., Foster, M. S., Siemasko, K., Chan, A. C., Aebersold, R., and Clark, M. R., 2002. The direct recruitment of BLNK to immunoglobulin a couples the B-cell antigen receptor to distal signaling pathways. Molecular and Cellular Biology, 22(8): 2524–235.

    Article  Google Scholar 

  • Kaloff, C. R., and Haas, I. G., 1995. Coordination of immunoglobulin chain folding and immunoglobulin chain assembly is essential for the formation of functional IgG. Immunity, 2(6): 629–637.

    Article  Google Scholar 

  • Katsukura, H., Murakami, R., Chijiiwa, Y., Otsuka, A., Tanaka, M., Nakashima, K., and Ono, M., 2001. Structure of the ß-chain (B29) gene of the chicken B-cell receptor and conserved collinearity with genes for potential skeletal muscle sodium channel and growth hormone. Immunogenetics, 53(9): 770–775.

    Article  Google Scholar 

  • Kehrer, S. R., Hannan, C. M., and Raison, R. L., 1998. Identification of a subpopulation of leucocytes from the rainbow trout (Oncorhynchus mykiss) responsive to pokeweed mitogen. Fish and Shellfish Immunology, 8(6): 477–487.

    Article  Google Scholar 

  • Keightley, R. G., Cooper, M. D., and Lawton, A. R., 1976. The T cell dependence of B cell differentiation induced by pokeweed mitogen. The Journal of Immunology, 117: 1538–1544.

    Google Scholar 

  • Kraus, M., Pao, L. I., Reichlin, A., Hu, Y., Canono, B., Cambier, J. C., Nußsenzweig, M. C., and Rajewsky, K., 2001. Interference with immunoglobulin (Ig)a immunoreceptor tyrosinebased activation motif (ITAM) phosphorylation modulates or blocks B cell development, depending on the availability of an Igß cytoplasmic tail. The Journal of Experimental Medicine, 194(4): 455–469.

    Article  Google Scholar 

  • Lee, S. J., Kim, S. J., Park, C. G., Park, J., Kim, J. H., and Chun, T., 2008. Molecular cloning and expression analysis of pig CD79a. Veterinary Immunology and Immunopathology, 125 (3-4): 368–374.

    Article  Google Scholar 

  • Li, R., Wang, T., Bird, S., Zou, J., Dooley, H., and Secombes, C. J., 2013. B cell receptor accessory molecule CD79a: Characterisation and expression analysis in a cartilaginous fish, the spiny dogfish (Squalus acanthias). Fish and Shellfish Immunology, 34(6): 1404–1415.

    Article  Google Scholar 

  • Livak, K. J., and Schmittgen, T. D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT Method. Methods, 25(4): 402–408.

    Article  Google Scholar 

  • Luger, D., Yang, Y. A., Raviv, A., Weinberg, D., Banerjee, S., Lee, M. J., Trepel, J., Yang, L., and Wakefield, L. M., 2013. Expression of the B-cell receptor component CD79a on immature myeloid cells contributes to their tumor promoting effects. PLoS One, 8 (10): e76115.

    Article  Google Scholar 

  • Minegishi, Y., Coustan-Smith, E., Rapalus, L., Ersoy, F., Campana, D., and Conley, M. E., 1999. Mutations in Iga (CD79a) result in a complete block in B-cell development. The Journal of Clinical Investigation, 104(8): 1115–1121.

    Article  Google Scholar 

  • Patel, S., Sørhus, E., Fiksdal, I. U., Espedal, P. G., Bergh, O., Rødseth, O. M., Morton, H. C., and Nerland, A. H., 2009. Ontogeny of lymphoid organs and development of IgMbearing cells in Atlantic halibut (Hippoglossus hippoglossus L.). Fish and Shellfish Immunology, 26(3): 385–395.

    Article  Google Scholar 

  • Patterson, H. C., Kraus, M., Kim, Y. M., Ploegh, H., and Rajewsky, K., 2006. The B cell receptor promotes B cell activation and proliferation through a non-ITAM tyrosine in the Iga cytoplasmic domain. Immunity, 25(1): 55–65.

    Article  Google Scholar 

  • Pike, K. A., Iacampo, S., Friedmann, J. E., and Ratcliffe, M. J., 2004. The cytoplasmic domain of Iga is necessary and sufficient to support efficient early B cell development. Journal of Immunol, 72(4): 2210–2218.

    Article  Google Scholar 

  • Reth, M., 1989. Antigen receptor tail clue. Nature, 338(6214): 383–384.

    Article  Google Scholar 

  • Reth, M., 1992. Antigen receptors on B lymphocytes. Annual Review of Immunology, 10: 97–121.

    Article  Google Scholar 

  • Reth, M., 1995. The B-cell antigen receptor complex and coreceptors. Immunology Today, 16(7): 310–313.

    Article  Google Scholar 

  • Sahoo, M., Edholm, E. S., Stafford, J. L., Bengtén, E., Miller, N. W., and Wilson, M., 2008. B cell receptor accessory molecules in the channel catfish, Ictalurus punctatus. Development and Comparative Immunology, 32(11): 1385–1397.

    Article  Google Scholar 

  • Sakaguchi, N., Kashiwamura, S., Kimoto, M., Thalmann, P., and Melchers, F., 1988. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-1ike properties. The EMBO Journal, 7(11): 3457–3464.

    Google Scholar 

  • Sakai, M., Kono, T., and Savan, R., 2005. Identification of expressed genes in carp (Cyprinus carpio) head kidney cells after in vitro treatment with immunostimulants. Journal of Developmental Biology (Basel), 121: 45–51.

    Google Scholar 

  • Sanchez, M., Misulovin, Z., Burkhardt, A. L., Mahajan, S., Costa, T., Franke, R., Bolen, J. B., and Nußsenzweig, M., 1993. Signal transduction by immunoglobulin is mediated through Iga and Igß. The Journal of Experimental Medicine, 178(3): 1049–1055.

    Article  Google Scholar 

  • Schrder, M. B., Flao, E., and Pilstrm, L., 1998. Localisation of Ig heavy chain mRNA positive cells in Atlantic cod (Gadus morhuabL.) tissues identified by in situ hybridization. Fish and Shellfish Immunology, 8(1): 45–50.

    Google Scholar 

  • Siegers, G. M., Yang, J., Duerr, C. U., Nielsen, P. J., Reth, M., and Schamel, W. W., 2006. Identification of disulfide bonds in the Ig-a/Ig-ß component of the B cell antigen receptor using the Drosophila S2 cell reconstitution system. International Immunology, 18(9): 1385–1396.

    Article  Google Scholar 

  • Swanson, C. L., Wilson, T. J., Strauch, P., Colonna, M., Pelanda, R., and Torres, R. M., 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. The Journal of Experimental Medicine, 207(7): 1485–5000.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30(12): 2725–2729.

    Article  Google Scholar 

  • Taniguchi, T., and Takaoka, A., 2002. The interferon-a/ß system in antiviral responses: A multimodal machinery of gene regulation by the IRF family of transcription factors. Current Opinion in Immunology, 14(1): 111–116.

    Article  Google Scholar 

  • Thompson, A. A., Do, H. N., Saxon, A., and Wall, R., 1999. Widespread B29 (CD79b) gene defects and loss of expression in chronic lymphocytic leukemia. Leukemia & Lymphoma, 32 (5-6): 561–569

    Google Scholar 

  • Van Noesel, C. J., Van Lier, R. A., Cordell, J. L., Tse, A. G., Van Schijndel, G. M., de Vries, E. F., Mason, D. Y., and Borst, J., 1991. The membrane IgM-associated heterodimer on human B cells is a newly defined B cell antigen that contains the protein product of the mb-1 gene. The Jouranl of Immunology, 146(11): 3881–3888.

    Google Scholar 

  • Wang, H., Diamond, R. A., and Rothenberg, E. V., 1998. Croßslineage expression of Igß(B29) in thymocytes: Positive and negative gene regulation to establish T cell identity. Proceedings of the National Academy of Sciences, 95(12): 6831–6836.

    Article  Google Scholar 

  • Wang, P. C., Huang, J. P., Tsai, M. A., Cheng, S. Y., Tsai, S. S., Chen, S. D., Chen, S. P., Chiu, S. H., Liaw, L. L., Chang, L. T., and Chen, S. C., 2005). Systemic infection of Kudoa lutjanus n. sp. (Myxozoa: Myxosporea) in red snapper Lutjanus erythropterus from Taiwan. Disease of Aquatic Organisms, 67 (1-2): 115–124.

    Article  Google Scholar 

  • Williams, A. F., and Barclay, A. N., 1988. The immunoglobulin superfamily-domains for cell surface recognition. Annual Review of Immunology, 6: 381–405.

    Article  Google Scholar 

  • Youn, H. Y., Goitsuka, R., Kato, H., Mason, D. Y., Watari, T., Tsujimoto, H., and Hasegawa, A., 1996. Molecular cloning of bovine mb-1 cDNA. Veterinary Immunology and Immunopathology, 52(3): 191–200.

    Article  Google Scholar 

  • Zhang, X. Z., Wu, Z. H., Yang, S. P., Pang, H. Y., Jian, J. C., and Lu, Y. S., 2011. Expression pattern of heat-shock cognate 70 gene of humphead snapper, Lutjanus sanguineus (Cuvier), infected by Vibrio harveyi. Journal of Fish Disease, 34(10): 719–729.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zaohe Wu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, Y., Yan, X., Cai, S. et al. Characterization and expression analysis of B Cell receptor accessory molecule CD79 gene in humphead snapper (Lutjanus sanguineus). J. Ocean Univ. China 15, 318–326 (2016). https://doi.org/10.1007/s11802-016-2816-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-016-2816-0

Keywords

Navigation