Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection
2013
Castro , Dona Maria Rosario (INRA , Jouy-En-Josas (France). UR 0892 Unité de recherche Virologie et Immunologie Moléculaires) | Jouneau , Luc (INRA , Jouy-En-Josas (France). UR 0892 Unité de recherche Virologie et Immunologie Moléculaires) | Pham , Hang-Phuong (Université de Paris - 6Centre National de la Recherche Scientifique, ParisParis(France). UMR 7211, ‘‘Integrative Immunology’’ TeamUMR 7211, ‘‘Immunology, Immunopathology, Immunotherapy’’) | Bouchez , Olivier (INRA , Auzeville (France). UMR 0444 Laboratoire de Génétique Cellulaire) | Giudicelli , Véronique (Université de Montpellier 2, Montpellier(France). IMGT, the International ImMunoGeneTics Information System, Laboratoire d’ImmunoGénétique Moléculaire LIGM, IGH, UPR CNRS 1142) | Lefranc , Marie-Paule (Université de Montpellier 2, Montpellier(France). The International ImMunoGeneTics Information System, Laboratoire d’ImmunoGénétique Moléculaire LIGM, IGH, UPR CNRS 1142) | Quillet , Edwige (INRA , Jouy-En-Josas (France). UMR 1313 Génétique Animale et Biologie Intégrative) | Benmansour , Abdenour (INRA , Jouy-En-Josas (France). UR 0892 Unité de recherche Virologie et Immunologie Moléculaires) | Cazals , Frédéric (Institut National de Recherche en Informatique et en Automatique, Sophia Antipolis(France). Algorithms-Biology-Structure) | Six , Adrien (Université de Paris - 6Centre National de la Recherche Scientifique, ParisParis(France). UMR 7211, ‘‘Integrative Immunology’’ TeamUMR 7211, ‘‘Immunology, Immunopathology, Immunotherapy’) | Fillatreau , Simon (Leibniz Institute, Berlin(Allemagne). Deutsches RheumaForschungszentrum) | Sunyer , Oriol (University of Pennsylvania, Philadelphia(Etats-Unis). Department of Pathobiology, School of Veterinary Medicine) | Boudinot , Pierre(auteur de correspondance) (INRA , Jouy-En-Josas (France). UR 0892 Unité de recherche Virologie et Immunologie Moléculaires)
Upon infection, B-lymphocytes expressing antibodies specific for the intruding pathogen develop clonal responses triggered by pathogen recognition via the B-cell receptor. The constant region of antibodies produced by such responding clones dictates their functional properties. In teleost fish, the clonal structure of B-cell responses and the respective contribution of the three isotypes IgM, IgD and IgT remain unknown. The expression of IgM and IgT are mutually exclusive, leading to the existence of two B-cell subsets expressing either both IgM and IgD or only IgT. Here, we undertook a comprehensive analysis of the variable heavy chain (VH) domain repertoires of the IgM, IgD and IgT in spleen of homozygous isogenic rainbow trout (Onchorhynchus mykiss) before, and after challenge with a rhabdovirus, the Viral Hemorrhagic Septicemia Virus (VHSV), using CDR3-length spectratyping and pyrosequencing of immunoglobulin (Ig) transcripts. In healthy fish, we observed distinct repertoires for IgM, IgD and IgT, respectively, with a few amplified μ and τ junctions, suggesting the presence of IgM- and IgT-secreting cells in the spleen. In infected animals, we detected complex and highly diverse IgM responses involving all VH subgroups, and dominated by a few large public and private clones. A lower number of robust clonal responses involving only a few VH were detected for the mucosal IgT, indicating that both IgM(+) and IgT(+) spleen B cells responded to systemic infection but at different degrees. In contrast, the IgD response to the infection was faint. Although fish IgD and IgT present different structural features and evolutionary origin compared to mammalian IgD and IgA, respectively, their implication in the B-cell response evokes these mouse and human counterparts. Thus, it appears that the general properties of antibody responses were already in place in common ancestors of fish and mammals, and were globally conserved during evolution with possible functional convergences.
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