Immunology of Fish

Innate immunity provides some form of defence against pathogens in all multicellular organisms but with cartilaginous and bony fish, although the lowest group of jawed vertebrates, the addition of a classic adaptive immune response becomes apparent. This provides the refinements of specificity for antigen recognition and memory. The T- and B lymphocytes are the effector leucocytes, acquiring their antigen-specific receptors (immunoglobulin for B cells and T-cell receptor for T cells) in the anterior kidney (bone marrow being absent) and thymus. The B cells are responsible for the production of antibodies that function as different immunoglobulin classes, whereas subsets of T lymphocytes are capable of killing target cells or helping with B- and other T-cell functions. Knowledge of these mechanisms is important for the use and design of vaccines, now so essential for the aquaculture industry, whereas studies of fish immunology contribute to the understanding of the evolution of adaptive immunity.

Key concepts:

  • Fish possess innate and adaptive immune responses, with classical adaptive immunity present only in jawed vertebrates.
  • Adaptive immunity allows memory of prior exposure to foreign molecules (antigens), so that on subsequent contact protective mechanisms are more rapidly mobilized: the basis of vaccination.
  • Lymphocytes mediate adaptive immunity and have surface receptors that recognize antigens, initiating the production of circulating antibodies and the activation of cell-mediated responses.
  • The functions of the immune system are similar in fish and mammals although there are differences due to the aquatic physiology and ectothermic nature of fish that provide evolutionary interest.
  • Leucocyte–antigen interactions take place in immune sites, such as the kidneys, spleen, gills and intestine. Bone marrow and lymph nodes are lacking.
  • Knowledge of fish immunology is proving essential for the development of vaccines for the expanding aquaculture industry.

Keywords: fish; haematopoiesis; immunology; inflammation; vaccines

Figure 1. Gene organization of the IgM heavy chain seen in (a) cartilaginous fish and (b) bony fish.
close
 References
    Alder MN, Herrin BR, Sadlonova A et al. (2008) Antibody responses of variable lymphocyte receptors in the lamprey. Nature Immunology 9: 319–327.
    Beetz S, Diekhoff D and Steiner LA (2007) Characterization of terminal deoxynucleotidyl transferase and polymerase in zebrafish. Immunogenetics 59: 735–744.
    Chang C-I, Zhang Y-A, Zou J, Nie P and Secombes CJ (2006) Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Antimicrobial Agents and Chemotherapy 50: 185–195.
    Chang M, Nie P, Collet B, Secombes CJ and Zou J (2009) Identification of an additional two-cysteine containing type I interferon in rainbow trout Oncorhynchus mykiss provides evidence of a major gene duplication event within this gene family in teleosts. Immunogenetics 61: 315–325.
    Charlemagne J (1997) Phylogeny of the T-cell receptor. Developmental and Comparative Immunology 21: 85–86.
    Chaves-Pozo E, Pelegrín P, García-Castillo J et al. (2004) Acidophilic granulocytes of the marine fish gilthead seabream (Sparus aurata L.) produce interleukin-1 following infection with Vibrio anguillarum. Cell and Tissue Research 316: 189–195.
    Cole AM, Weis P and Diamond G (1997) Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. Journal of Biological Chemistry 272: 12008–12013.
    Corripio-Miyar Y, Zou J, Richmond H and Secombes CJ (2009) Identification of interleukin-22 in gadoids and examination of its expression level in vaccinated fish. Molecular Immunology 46: 2098–2106.
    Danilova N, Bussmann J, Jekosch K and Steiner LA (2005) The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nature Immunology 6: 295–302.
    Dooley H and Flajnik MF (2006) Antibody repertoire development in cartilaginous fish. Developmental and Comparative Immunology 30: 43–56.
    Falco A, Chico V, Marroqui L et al. (2008) Expression and antiviral activity of a -defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences. Molecular Immunology 45: 757–765.
    Gong Y-F, Xiang L-X and Shao J-Z (2009) CD154-CD40 interactions are essential for thymus-dependent antibody production in zebrafish: insights into the origin of costimulatory pathway in helper T cell-regulated adaptive immunity in early vertebrates. Journal of Immunology 182: 7749–7762.
    Guo P, Hirano M, Herrin BR et al. (2009) Dual nature of the adaptive immune system in lampreys. Nature 459: 796–801.
    Hanington PC, Tam J, Katzenback BA et al. (2009) Development of macrophages of cyprinid fish. Developmental and Comparative Immunology 33: 411–429.
    Hansen JD, Landis ED and Phillips RB (2005) Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. Proceedings of the National Academy of Sciences of the USA 102: 6919–6924.
    Håstein T, Gudding R and Evensen Ø (2005) Bacterial vaccines for fish – an update of the current situation worldwide. In: Midtlng P (ed.) Progress in Fish Vaccinology: Developments in Biologicals 121: 55–74.
    Haugarvoli E, Bjerkå I, Nowak BF, Hordvik I and Koppang EO (2008) Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon. Journal of Anatomy 213: 202–209.
    Hikima J, Hirono I and Aoki T (1997) Characterization and expression of c-type lysozyme cDNA from Japanese flounder (Paralichthys olivaceus). Molecular Marine Biology and Biotechnology 6: 339–344.
    Knight J, Stet RJM and Secombes CJ (1998) Modulation of MHC class II expression in rainbow trout Oncorhynchus mykiss macrophages by TNF and LPS. Fish & Shellfish Immunology 8: 545–553.
    Langenau DM and Zon LI (2005) The zebrafish: a new model of T-cell and thymic development. Nature Reviews 5: 307–317.
    Li J, Barreda DR, Zhang Y-A et al. (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nature Immunology 7: 1116–1124.
    Liongue C, Hall CJ, O'Connell BA, Crosier P and Ward AC (2009) Zebrafish granulocyte colony-stimulating factor receptor signalling promotes myelopoiesis and myeloid cell migration. Blood 113: 2535–2546.
    Liu Y, Chang MX, Wu SC and Nie P (2009) Characterization of C-C chemokine receptor subfamily in teleost fish. Molecular Immunology 46: 498–504.
    Maier VH, Dorn KV, Gudmundsdottir BK and Gudmundsson GH (2008) Characterisation of cathelicidin gene family members in divergent fish species. Molecular Immunology 45: 3723–3730.
    Martin SAM, Zou J, Houlihan DF and Secombes CJ (2007) Directional responses following recombinant cytokine stimulation of rainbow trout (Oncorhynchus mykiss) RTS-11 macrophage cells as revealed by transcriptome profiling. BMC Genomics 8: 150.
    Mulero I, Noga EJ, Meseguer J, Garcia-Ayala A and Mulero V (2008) The antimicrobial peptides piscidins are stored in the granules of professional phagocytic granulytes of fish and are delivered to the bacteria-containing phagosome upon phagocytosis. Developmental and Comparative Immunology 32: 1531–1538.
    Mulero I, Sepulcre MP, Meseguer J, Garcia-Ayala A and Mulero V (2007) Histamine is stored in mast cells of most evolutionary advanced fish and regulates the fish inflammatory response. Proceedings of the National Academy of Sciences of the USA 104: 19434–19439.
    Niethammer P, Grabher C, Look AT and Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459: 996–999.
    Nomiyama H, Hieshima K, Osada N et al. (2008) Extensive expansion and diversification of the chemokine gene family in zebrafish: identification of a novel chemokine subfamily CX. BMC Genomics 9: 222.
    Østergaard AE, Martin SAM, Wang T, Stet RJM and Secombes CJ (2009) Rainbow trout (Oncorhynchus mykiss) possess multiple novel immunoglobulin-like transcripts containing either an ITAM or ITIMs. Developmental and Comparative Immunology 33: 525–532.
    Pancer Z, Saha NR, Kasamatsu J et al. (2005) Variable lymphocyte receptors in hagfish. Proceedings of the National Academy of Sciences of the USA 102: 9224–9229.
    Roach JC, Glusman G, Rowen L et al. (2005) The evolution of vertebrate Toll-like receptors. Proceedings of the National Academy of Sciences of the USA 102: 9577–9582.
    Robertsen B (2008) Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish & Shellfish Immunology 25: 351–357.
    Schorpp M, Bialecki M, Diekhoff D et al. (2006) Conserved functions of Ikaros in vertebrate lymphocyte development: genetic evidence for distinct larval and adult phases of T cell development and two lineages of B cells in zebrafish. Journal of Immunology 177: 2463–2476.
    Shen L, Stuge TB, Zhou H et al. (2002) Channel catfish cytotoxic cells: a mini-review. Developmental and Comparative Immunology 26: 141–149.
    Sun B, Robertsen B, Wang Z and Liu B (2009) Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Developmental and Comparative Immunology 33: 547–558.
    Utke K, Bergmann S, Lorenzen N et al. (2007) Cell-mediated cytotoxicity in rainbow trout, Oncorhynchus mykiss, infected with viral haemorrhagic septicaemia virus. Fish & Shellfish Immunology 22: 182–196.
    Utke K, Kock H, Schuetze H et al. (2008) Cell-mediated immune responses in rainbow trout after DNA immunization against viral hemorrhagic septicaemia virus. Developmental and Comparative Immunology 32: 239–252.
    Wang T, Hanington PC, Belosevic M and Secombes CJ (2008) Two macrophage colony-stimulating factor genes exist in fish that differ in gene organization and are differentially expressed. Journal of Immunology 181: 3310–3322.
    Wang T, Ward M, Grabowski P and Secombes CJ (2001) Molecular cloning, gene organization and expression of rainbow trout (Oncorhynchus mykiss) inducible nitric oxide synthase (iNOS) gene. Biochemical Journal 358: 747–755.
    Wilson M, Bengten E, Miller NW et al. (1997) A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proceedings of the National Academy of Sciences of the USA 94: 4593–4597.
    Yazawa R, Cooper GA, Beetz-Sargent M et al. (2008a) Functional adaptive diversity of the Atlantic salmon T-cell receptor gamma locus. Molecular Immunology 45: 2150–2157.
    Yazawa R, Cooper GA, Hunt P et al. (2008b) Striking antigen recognition diversity in the Atlantic salmon T-cell receptor / locus. Developmental and Comparative Immunlogy 32: 204–212.
    Yoder JA (2009) Form, function and phylogenetics of NITRs in bony fish. Developmental and Comparative Immunolgy 33: 135–144.
    Zhang Y-A, Hikima J-I, Li J et al. (2009) Conservation of structural and functional features in a primordial CD80/86 molecule from rainbow trout (Oncorhynchus mykiss), a primitive teleost fish. Journal of Immunology 183: 83–96.
    Zhou H, Stuge TB, Miller NW et al. (2001) Heterogeneity of channel catfish CTL with respect to target recognition and cytotoxic mechanisms employed. Journal of Immunology 167: 1325–1332.
    Zou J, Mercier C, Koussounadis A and Secombes CJ (2007) Discovery of multiple beta-defensin like homologues in teleost fish. Molecular Immunology 44: 638–647.
    Zwollo P, Cole S, Bromage E and Kaattari S (2005) B cell heterogeneity in the teleost kidney: evidence for a maturation gradient from anterior to posterior kidney. Journal of Immunology 174: 6608–6616.
 Further Reading
    Alvarez-Pellitero P (2008) Fish immunity and parasite infections: from innate immunity to immune prophylactic prospects. Veterinary Immunology and Immunopathology 126: 171–198.
    Bajoghli B, Aghaallaei N, Hess I et al. (2009) Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138: 186–197.
    Bird S, Zou J and Secombes CJ (2006) Advances in fish cytokine biology gives clues to the evolution of a complex network. Current Pharmaceutical Design 12: 3051–3069.
    Hsu E, Pulham N, Rumfelt LL and Flajnik MF (2006) The plasticity of immunoglobulin gene systems in evolution. Immunological Reviews 210: 8–26.
    Koppang EO, Fischer U, Satoh M and Jirillo E (2007) Inflammation in fish as seen from a morphological point of view with a special reference to the vascular compartment. Current Pharmaceutical Design 13: 3649–3655.
    Pancer Z and Cooper MD (2006) The evolution of adaptive immunity. Annual Review of Immunology 24: 497–518.
    Rombout JHWM, Huttenhuis HBT, Picchietti S and Scapigliati G (2005) Phylogeny and ontogeny of fish leucocytes. Fish & Shellfish Immunology 19: 441–455.
    Stavnezer J and Amemiya CT (2004) Evolution of isotype switching. Seminars in Immunology 16: 257–275.
    book Zaccone G, Meseguer J and Garcia-Ayala A (eds) (2009) Fish Defenses, vol. 1, 390pp. Enfield, NH: Science Publishers.
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Fletcher, Thelma C, and Secombes, Christopher J(Feb 2010) Immunology of Fish. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000520.pub2]