Vet Med - Czech, 2011, 56(10):486-503 | DOI: 10.17221/3294-VETMED
Innate and adaptive immunity in teleost fish: a review
- 1 Faculty of Veterinary Science, Universidad Austral de Chile, Valdivia, Chile
- 2 Faculty of Medicine, Universidad Austral de Chile, Valdivia, Chile
The immune system of fish is very similar to vertebrates, although there are some important differences. Fish are free-living organisms from the embryonic stage of life in their aquatic environment. They have mechanisms to protect themselves from a wide variety of microorganisms. Consequently, fish rely on their innate immune system for an extended period of time, beginning at the early stages of embryogenesis. The components of the innate immune response are divided into physical, cellular and humoral factors and include humoral and cellular receptor molecules that are soluble in plasma and other body fluids. The lymphoid organs found in fish include the thymus, spleen and kidney. Immunoglobulins are the principal components of the immune response against pathogenic organisms. Immunomodulatory products, including nucleotides, glucans and probiotics, are increasingly used in aquaculture production. The use of these products reduces the need for therapeutic treatments, enhances the effects of vaccines and, in turn, improves the indicators of production. The aim of this review is to provide a review of the immune system in fish, including the ontogeny, mechanisms of unspecific and acquired immunity and the action of some immunomodulators.
Keywords: fish; immune response; immunomodulators
Published: October 31, 2011 Show citation
References
- Acton RT, Weinheimer PF, Hall SJ, Niedermeier W, Shelton E, Bennett JC (1971): Tetrameric immune macroglobulins in three orders of bony fishes. Proceedings of the National Academy of Sciences of the United States of America 68, 107-111.
Go to original source...
Go to PubMed...
- Ai Q, Mai K, Zhang L, Tan B, Zhang W, Xu W, Li H (2007): Effects of dietary [beta]-1, 3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish and Shellfish Immunology 22, 394-402.
- Alexander JB, Ingram GA (1992): Noncellular nonspecific defense mechanisms of fish. Annual Review of Fish Disease 2, 249-279.
- Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A, Mohamed MF (2008): Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish and Shellfish Immunology 25, 128- 136.
- Anderson DP (1992): Immunostimulants, adjuvants and vaccine carriers in fish: applications to aquaculture. Annual Review of Fish Disease 2, 281-307.
- Aranishi F, Nakane M (1997): Epidermal proteases of the Japanese eel. Fish Physiology and Biochemistry 16, 471-478.
- Arkoosh MR, Kaattari SL (1991): Development of immunological memory in rainbow trout (Oncorhynchus mykiss). I. An immunochemical and cellular analysis of the B cell response. Developmental and Comparative Immunology 15, 279-293.
- Arma NR, Hirono I, Aoki T (2004): Characterization of expressed genes in kidney cells of Japanese flounder Paralichthys olivaceus treatment with ConA/PMA and LPS. Fish Pathology 39, 189-196.
- Armstrong PB, Quigley JP (1999): α-2-Macroglobulin: an evolutionarily conserved arm of the innate immune system. Developmental and Comparative Immunology 23, 375-390.
- Ballou CE (1982): Yest cell wall and cell surface. In: Strathern JN, Jones EW, Broach JR (eds.): The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression. Cold Spring Harbor Laboratories, New York, USA. 335-360.
- Bayne CJ, Gerwick L (2001): The acute phase response and innate immunity of fish. Developmental and Comparative Immunology 25, 725-743.
- Birkemo GA, Luders T, Andersen O, Nes IF, NissenMeyer J (2003): Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Journal of Biochemistry, Molecular Biology and Biophysics 1646, 207-215.
- Blazer VS (1991): Piscine macrophage function and nutritional influences: A review. Journal of Aquatic Animal Health 3, 77-86.
- Boes M (2000): Role of natural and immune IgM antibodies in immune responses. Molecular Immunology 37, 1141-1149.
- Boshra H, Li J, Sunyer JO (2006): Recent advances on the complement system of teleost fish. Fish and Shellfish Immunology 20, 239-262.
- Brydges NM, Boulcott P, Ellis T, Braithwaite VA (2009): Quantifying stress responses induced by different handling methods in three species of fish. Applied Animal Behaviour Science 116, 295-301.
- Bowden TJ (2008): Modulation of the immune system of fish by their environment. Fish and Shellfish Immunology 25, 373-383.
- Bowden TJ, Butler R, Bricknell IR, Ellis AE (1997): Serum trypsininhibitory activity in five species of farmed fish. Fish and Shellfish Immunology 7, 377-385.
- Bowden TJ, Cook P, Rombout JHWM (2005): Development and function of the thymus in teleosts. Fish and Shellfish Immunology 19, 413-427.
- Burrells C, William PD, Forno PF (2001a): Dietary nucleotides: a novel supplement in fish feeds. 1. Effects on resistance to diseases in salmonids. Aquaculture 199, 159-169.
- Burrells C, William PD, Southage PJ, Wadsworth SL (2001b): Dietary nucleotides: a novel supplement in fish feeds. 2. Effects on vaccination, salt water transfer, growth rate and physiology of Atlantic salmon. Aquaculture 199, 171-184.
- Cain KD, Jones DR, Raison RL (2000): Characterisation of mucosal and systemic immune responses in rainbow trout (Oncorhynchus mykiss) using surface plasmon resonance. Fish and Shellfish Immunology 10, 651- 666.
- Carver JD, Cox WI, Barness LA (1990): Dietary nucleotide effects upon murine natural killer cell activity and macrophage activation. Journal of Parenteral and Enteral Nutrition 14, 18-22.
- Castillo A, Sanchez C, Dominguez J, Kaattari SL, Villena AJ (1993): Ontogeny of IgM and IgM-bearing cells in rainbow trout. Developmental and Comparative Immunology 17, 419-424.
- Chantanachookhin C, Seikai T, Tanaka M (1991): Comparative study of the ontogeny of the lymphoid organs in three species of marine fish. Aquaculture 99, 143- 155.
- Chinchar VG, Bryan L, Silphadaung U, Noga E, Wade D, Rollins-Smith L (2004): Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 323, 268-275.
- Cook MT, Hayball PJ, Birdseye L, Bagley C, Nowak BF, Hayball JD (2003): Isolation and partial characterization of a pentraxin-like protein with complementfixing activity from snapper (Pagrus auratus, Sparidae) serum. Developmental and Comparative Immunology 27, 579-588.
- Cook MT, Hayball PJ, Nowak BF, Hayball JD (2005): The opsonising activity of a pentraxin-like protein isolated from snapper (Pagrus auratus, Sparidae) serum. Developmental and Comparative Immunology 29, 703-712.
- Cosgrove M (1998): Nucleotides. Nutrition 14, 748-751.
- Dalmo RA (2005): Ontogeny of the fish immune system. Fish and Shellfish Immunology 19, 395-396.
- Dalmin G, Kathiresan K, Purushothaman A (2001): Effect of probiotics on bacterial population and health status of shrimp in culture pond ecosystem. Indian Journal of Experimental Biology 39, 939-942.
- Dalmo RA, Bogwald J (2008): β-glucans as conductors of immune symphonies. Fish and Shellfish Immunology 25, 384-396.
- Danneving BH, Lauve A, McPress LC, Landsverk T (1994): Receptor-mediated endocytosis and phagocytosis by rainbow trout head kidney sinusoidal cells. Fish and Shellfish Immunology 4, 3-18.
- Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L (2002): Real-time visualization of mycobacterium-macrophage interactions leading initiation of granuloma formation in zebrafish embryos. Immunity 17, 693-702.
- De Haas CJ, van Leeuwen EMM, van Bommel T, Verhoef J, van Kessel KPM, van Strijp JAG (2000): Serum amyloid P component bound to Gram-negative bacteria prevents lipopolysaccharide-mediated classical pathway complement activation. Infection and Immunity 68, 1753-1759.
- De Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BRG (2001): Functional classification of interferon-stimulated genes identified using microarrays. Journal of Leukocyte Biology 69, 912-920.
- DeVries ME, Kelvin AA, Xu L, Ran L, Robinson J, Kelvin DJ (2006): Defining the origins and evolution of the chemokine/chemokine receptor system. Journal of Immunology 176, 401-415.
- Dijkstra JM, Kollner B, Aoyagi K, Sawamoto Y, Kuroda A, Ototake M (2003): The rainbow trout classical MHC class I molecule Onmy-UBA) 501 is expressed in similar cell types as mammalian classical MHC class I molecules. Fish and Shellfish Immunology 14, 1-23.
- Di Luzio NR (1985): Update on the immunomodulating activities of glucans. Seminars in Immunopathology 8, 387-400.
- Dinarello CA (1997): Interleukin-1. Cytokine Growth Factor Review 8, 253-265.
- Dos Santos NM, Romano N, de Sousa M, Ellis AE, Rombout JH (2000): Ontogeny of B and T cells in sea bass (Dicentrarchus labrax, L.). Fish and Shellfish Immunology 10, 583-596.
- Elcombe BM, Chang RJ, Taves CJ, Winkelhake JL (1985): Evolution of antibody structure and effector functions: comparative hemolytic activities of monomeric and tetrameric IgM from rainbow trout, Salmo gairdnerii. Comparative Biochemistry and Physiology 80, 697-706.
- Ellingsen T, Strand C, Monsen E, Bogwald J, Dalmo RA (2005): The ontogeny of complement component C3 in the spotted wolfish (Anarhichas minor Olafsen). Fish and Shellfish Immunology 18, 351-358.
- Ellis AE (2001): Innate host defence mechanism of fish against viruses and bacteria. Developmental and Comparative Immunology 25, 827-839.
- Engstad RE, Robertsen B (1995): Effects of structurally different yeast B glucans on immune responses in Atlantic salmon (Salmo salar). Journal of Marine Biotechnology 3, 203-207.
- Evans D, Jaso-Friedmann L (1992): Nonspecific cytotoxic cells as effectors of immunity in fish. Annual Review of Fish Disease 2, 109.
- Faisal M, Ahmed G, Peters II, Cooper EL (1989): Natural citotoxicity of tilapia leukocytes. Disease of Aquatic Organims 7, 17-22.
- Ferguson HW (1989): Systemic Pathology of Fish. A text and atlas comparative tissue response in diseases of teleost. Iowa state University Press. Ames. Iowa, USA. 5-103.
- Fischer U, Utke K, Somamoto T, Kollner B, Ototake M, Nakanishi T (2006): Cytotoxic activities of fish leucocytes. Fish and Shellfish Immunology 20, 209-226.
- Fuller R (1989): Probiotic in man and animals. Journal of Applied Bacteriology 66, 365-378.
- Gatesoupe FJ (1999): The use of probiotics in aquaculture. Aquaculture 180, 147-165.
- Gil A (2002): Modulation of the immune response mediated by dietary nucleotides. European Journal of Clinical Nutrition 56, S1-S4.
- Greenlee AD, Brown RA, Ristlow SS (1991): Nonspecific citotoxic cells of Rainbow trout (Oncorhynchus mykiss) kill Yac-1 targets by both necrotic and apoptotic mechanisms. Developmental and Comparative Immunology 15, 153-164.
- Grinde B, Lie O, Poppe T, Salte R (1988): Species and individual variation in lysozyme activity in fish of interest in aquaculture. Aquaculture 68, 299-304.
- Hanington PC, Wang T, Secombes CJ, Belosevic M (2007): Growth factors of lower vertebrates: characterization of goldfish (Carassius auratus L.) macrophage colonystimulating factor-1. Journal of Biological Chemistry 282, 31865-31872.
- Hardie LJ, Laing KJ, Daniels GD, Grabowski PS, Cunningham C, Secombes CJ (1998): Isolation of the first piscine transforming growth factor β gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus mykiss). Cytokine 10, 555-563.
- Hasegawa S, Nakayasu C, Yoshitomi T, Nakanishi T, Okamoto N (1998): Specific cell-mediated cytotoxicity against an allogeneic target cell line in isogeneic ginbuna crucian carp. Fish and Shellfish Immunology 8, 303-313.
- Hatten F, Fredriksen A, Hordvik I, Endresen C (2001): Presence of IgM in cutaneous mucus, but not in gut mucus of Atlantic salmon, Salmo salar. Serum IgM is rapidly degraded when added to gut mucus. Fish and Shellfish Immunology 11, 257-268.
- Hayward CJ, Bott NJ, Nowak BF (2009): Seasonal epizootics of sea lice, Caligus spp., on southern bluefin tuna, Thunnus maccoyii (Castelnau), in a long-term farming trial. Journal of Fish Disease 32, 101-106.
- Hellio C, Pons AM, Beaupoil C, Bourgougnon N, Gal YL (2002): Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. International Journal of Antimicrobial Agents 20, 214-2199.
- Hibiya T (ed.) (1994): An Atlas of Fish Histology. Normal and Pathological Features. Gustav Fischer Verlag, Stuttgart, Germany. 5-125.
- Hinuma S, Abo T, Kumagai K, Hata M (1980): The potent activity of fresh water fish kidney cells in cell-killing. I. Characterization and species distribution of cytotoxicity. Developmental and Comparative Immunology 4, 653-666.
- Holland MC, Lambris JD (2002): The complement system of teleosts. Fish and Shellfish Immunology 12, 399-420.
- Hoover GJ, El-Mowafi A, Simko E, Kocal TE, Ferguson HW, Hayes MA (1998): Plasma proteins of rainbow trout (Oncorhynchus mykiss) isolated by binding to lipopolysaccharide from Aeromonas salmonicida. Comparative Biochemistry and Physiology 120, 559- 569.
- Huising MO, Stet RJM, Savelkoul HFJ, Verburg-van Kemenade BML (2004): The molecular evolution of the interleukin-1 family of cytokines; IL-18 in teleost fish. Developmental and Comparative Immunology 28, 395-413.
- Ingram GA (1980): Substances involved in the natural resistance of fish to infection a review. Journal of Fish Biology 16, 23-60.
- Jeney G, Anderson DP (1993): Glucan injection or bath exposure given alone or in combination with a bacteria enhance the nonspecific defense mechanisms in rainbow trout (Oncorhynchus mykiss). Aquaculture 116, 315-329.
- Jenkins JA, Ourth DD (1993): Opsonic effect of the alternative complement pathway on channel catfish peripheral blood phagocytes. Veterinary Immunology Immunopathology 39, 447-459.
- Jenkins PG, Wrathmell AB, Harris JE, Pulsford AL (1994): Systemic and mucosal immune response to enterically delivered antigen in Oreochromis mossambicus. Fish and Shellfish Immunology 4, 255-271.
- Jones DR, Hannan CM, Russel-Jones GJ, Raison RL (1999): Selective B cell non-responsiveness in the gut of the rainbow trout (Oncorhynchus mykiss). Aquaculture 172, 29-39.
- Jorgensen JB, Sharp GJ, Secombes CJ, Robertsen B (1993): Effect of yeast cell wall glucan on the bacterial activity of rainbow trout macrophages. Fish and Shellfish Immunology 3, 267-277.
- Jyonouchi, H, Zhang L, Tomita Y (1993): Studies of immunomodulating actions of RNA/nucleotides: RNA/ Nucleotides enhance in vitro immunoglobulin production by human peripheral blood mononuclear cells in response to T-dependent stimuli. Pediatric Research 33, 458-465.
- Kaattari SL (1992): Fish B lymphocytes: Defining their form and function. In: Faisal M, Hetrick FM (eds.): Annual Review of Fish Diseases. Vol. 2. Pergamon, Tarrytown, NY, USA. 161-180.
- Kileng O, Brundtland MI, Robertsen B (2007): Infectious salmon anemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon. Fish and Shellfish Immunology 23, 378-389.
- Kodama H, Matsuoka Y, Tanaka Y, Liu YC, Iwasaki T, Watarai S (2004): Changes of C-reactive protein levels in rainbow trout (Oncorhynchus mykiss) sera after exposure to anti-ectoparasitic chemicals used in aquaculture. Fish and Shellfish Immunology 16, 589-597.
- Kono T, Bird S, Sonoda K, Savan R, Secombes CJ, Sakai M (2008): Characterization and expression analysis of an interleukin-7 homologue in the Japanese pufferfish, Fugu rubripes. FEBS Journal 275, 1213-1226.
- Lam SH, Chua HL, Gong Z, Lam TJ, Sin Y (2004): Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Developmental and Comparative Immunology 28, 9-28.
- Lammens M, Decostere A, Haaesebrouck F (2000): Effects of Flavobaterium psychrophilium strains and their metabolites on the oxidative activity of rainbow trout Oncorhynchus mykiss phagocytes. Disease of Aquatic Organisms 41, 173-179.
- Lange S, Magnadottir B (2003): Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum. Comparative Biochemistry and Physiology, Molecular Biology 136, 99-106.
- Lange SR, Bambir S, Dodds AW, Magnadottir B (2004a): The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.) an immunohistochemical study. Fish and Shellfish Immunology 16, 359-367.
- Lange SR, Bambir S, Dodds AW, Magnadottir B (2004b): An immunohistochemical study on complement component C3 in juvenile Atlantic halibut (Hippoglosus hippoglossus L.). Developmental and Comparative Immunology 28, 593-601.
- Leonardi M, Sandino AM, Klempau A (2003): Effect of a nucleotide-enriched diet on the immune system, plasma cortisol levels and resistance to infectious pancreatic necrosis (IPN) in juvenile rainbow trout (Oncorhynchus mykiss). Bulletin of the European Association of Fish Pathologists 23, 52-59.
- Li P, Lewis DH, Gatlin DM (2004): Dietary oligonucleotide from yeast RNA influences immune responses and resistance of hybrid striped bass (Morone chrysops × M. saxatilis) to Streptococcus iniae infection. Fish and Shellfish Immunology 16, 561-569.
- Li JH, Shao JZ, Xiang LX, Wen Y (2007): Cloning, characterization and expression analysis of pufferfish interleukin-4 cDNA: the first evidence of Th2-type cytokine in fish. Molecular Immunology 44, 2078-2086.
- Lie O, Evensen O, Sorensen A, Froysadal E (1989): Study on lysozyme activity in some fish species. Disease of Aquatic Organism 6, 1-5.
- Liu Y, Iwasaki T, Watarai S, Kodama H (2004): Effect of turpentine oil on C-reactive protein (CRP) production in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 17, 203-210.
- Lorenzen N, LaPatra SE (1999): Immunity to rhabdovirus in rainbow trout: the antibody response. Fish and Shellfish Immunology 9, 345-360.
- Lumsden JS, Ostland VE, Byrne PJ, Ferguson HW (1993): Detection of a distinct gill-surface antibody response following horizontal infection and bath challenge of brook trout Salvelinusfontinalis with Flavobactewium branchiophilum, the causative agent of bacterial gill disease. Disease of Aquatic Organism 16, 21-27.
- Lund V, Olafsen JA (1998): A comparative study of pentraxin-like proteins in different fish species. Developmental and Comparative Immunology 22, 185-194.
- Ma CW, Cho YS, Oh KH (2009): Removal of pathogenic bacteria and nitrogens by Lactobacillus spp. JK-8 and JK-11. Aquaculture 287, 266-270.
- Maier VH, Dorn KV, Gudmundsdottir BK, Gudmundsson GH (2008): Characterisation of cathelicidin gene family members in divergent fish species. Molecular Immunology 45, 3723-3730.
- Magnadottir B (2006): Innate immunity of fish (overview). Fish and Shellfish Immunology 20, 137-151.
- Magnadottir B (2010): Immunological control of fish diseases. Journal of Marine Biotechnology 12, 361-379.
- Magnadottir B, Jonsdottir H, Helgason S, Bjornsson B, Jorgensen TO, Pilstrom L (1999): Humoral immune parameters in Atlantic cod (Gadus morhua L.). II. The effects of size and gender under different environmental conditions. Comparative Biochemistry and Physiology 122B, 181-188.
- Magnadottir B, Jonsdottir H, Helgason S, Bjornsson B, Jorgensen TO, Pilstrom L (2001): Immuneparameters of immunised cod (Gadus morhua L). Fish and Shellfish Immunology 10, 75-89.
- Magnadottir B, Lange S, Gudmundsdottir S, Bogwald J, Dalmo RA (2005): Ontogeny of humoral immune parameters in fish. Fish and Shellfish Immunology 19, 429-439.
- Manning MJ, Nakanishi T (1996): Cellular defenses. In: Iwama GK, Nakanishi T (eds.): Fish Fisiology. XV. The fish immune system. Academic press. London, England. 159-205.
- Mathew JA, Guo YX, Goh KP, Chan J, Verburg van Kemenade BM, Kwang J (2002): Characterisation of a monoclonal antibody to carp IL-1beta and the development of a sensitive capture ELISA. Fish and Shellfish Immunology 13, 85-95.
- Matsushita M, Endo Y, Nonaka M, Fujita T (1998): Complement-related serine proteases in tunicates and vertebrates. Current Opinion in Immunology 10, 29-35.
- Matsuyama H, Yano T, Yamakawa T, Nakao M (1992): Opsonic effect of the third complement component (C3) of carp (Cyprinus carpio) on phagocytosis by neutrophils. Fish and Shellfish Immunology 2, 69-78.
- McKinney EC, Achmale MC (1994): Damselfish with neurofibromatosis exhibit cytotoxicity in toward tumor targets. Developmental and Comparative Immunology 18, 305-313.
- Morrison RN, Nowak B (2002): The antibody response of teleost fish. Seminars in Avian and Exotic Pet Medicine 11, 46-54.
- Mulero V, Meseguer J (1998): Functional characterisation of a macrophage-activating factor produced by leucocytes of gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology 8, 143-156.
- Mulero I, Garcia Ayala A, Meseguer J, Mulero V (2007): Maternal transfer of immunity and ontogeny of autologous immunocompetence of fish: A mini review. Aquaculture 268, 244-250.
- Nakanishi T. (1986): Seasonal changes in the humoral immune response and the lymphoid tissues of the marine teleost, Sebastiscus marmoratus. Veterinary Immunology and Immunopathology 12, 213-221.
- Nascimento DS, do Vale A, Toma's AM, Zou J, Secombes CJ, dos Santos NMS (2007): Cloning, promoter analysis and expression in response to bacterial exposure of sea bass (Dicentrarchus labrax L.) interleukin-12 p40 and p35 subunits. Molecular Immunology 44, 2277-2791.
- Nauta AJ, Daha M, van Kooten C, Roos A (2003): Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends in Immunology 24, 148-154.
- Navarro J, Ruiz-Bravo A, Jimenez-Varela M, Gil A (1996): Modulation of antibody-forming cell and mitogendriven lymphoproliferative responses by dietary nucleotides in mice. Immunology Letters 53, 141-145.
- Nikoskelainen S, Lehtinen J, Lilius EM (2002): Bacteriolytic activity of rainbow trout (Oncorhynchus mykiss) complement. Developmental and Comparative Immunology 26, 797-804.
- Olesen NJ, Jorgensen PEV (1986): Quantification of serum immunoglobulin in rainbow trout Salmo gairdneri under various environmental conditions. Disease of Aquatic Organism 1, 183-189.
- Ooi EL, Verjan N, Hirono I, Nochi T, Kondo H, Aoki T, Kiyono H, Yuki Y. (2008): Biological characterisation of a recombinant Atlantic salmon type I interferon synthesized in Escherichia coli. Fish and Shellfish Immunology 24, 506-513.
- Panigrahi A, Kiron V, Puangkaew J, Kobayashi T, Satoh S, Sugita H (2005): The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout Oncorhynchus mykiss. Aquaculture 243, 241-254.
- Petrie-Hanson L, Ainsworth AJ (2000): Differential cytochemical staining characteristics of channel catfish leukocytes identify cell populations in lymphoid organs. Veterinary Immunology and Immunopathology 73, 129-144.
- Pinto RD, Nascimento DS, Reis MIR, do Vale A, dos Santos NMS (2006): Molecular characterization, 3D modelling and expression analysis of sea bass (Dicentrarchus labrax) interleukin-10. Molecular Immunology 44, 2066-2075.
- Press CM, Dannevig BH, Landsverk T (1994): Immune and enzyme histochemical phenotypes of lymphoid and nonlymphoid cells within the spleen and head kidney of Atlantic salmon (Salmo salar L.). Fish and Shellfish Immunology 4, 79-93.
- Ramadan A, Afifi NA, Moustafa M, Samy AM (1994): The effect of ascogen on the immune response of tilapia fish to Aeromonas hydrophila vaccine. Fish and Shellfish Immunology 5, 159-165.
- Ramsay JM, Feist GW, Varga ZM, Westerfield M, Kent ML, Schreck CB (2009): Whole-body cortisol response of zebrafish to acute net handling stress. Aquaculture 297, 157-162.
- Razquin BE, Castillo A, Lopez-Fierro P, Alvarez F, Zapata A, Villena A (1990): Ontogeny of IgM-producing cells in the lymphoid organs of rainbow trout, Salmo gardnieri Richardson: an immunological and enzyme-histochemical study. Journal of Fish Biology 36, 159-173.
- Robertsen B (2006): The interferon system of teleost fish. Fish and Shellfish Immunology 20, 172-191.
- Rokenes TP, Larsen R, Robertsen B (2007): Atlantic salmon ISG15: expression and conjugation to cellular proteins in response to interferon, double-stranded RNA and virus infections. Molecular Immunology 44, 950-959.
- Rombout JH, Blok LJ, Lamers CHJ (1986): Immunization of carp (Cyprinus carpio) with a Vibrio anguillarum bacterin: Indications for a common mucosal immune system. Developmental and Comparative Immunology 10, 341-351.
- Rombout JH, Taverne N, van de Kamp M, Taverne-Thiele AJ (1993): Differences in mucus and serum immunoglobulin of carp (Cyprinus carpio L.). Developmental and Comparative Immunology 17, 309-317.
- Rombout JH, Huttenhuis HBT, Picchietti S, Scapigliati S (2005): Phylogeny and ontogeny of fish leucocites. Fish and Shellfish Immunology 19, 441-455.
- Rorstad G, Aasjord PM, Robertsen B (1993): Adjuvant effect of a yeast glucan in vaccines against furunculosis in Atlantic salmon (Salmo salar). Fish and Shellfish Immunology 3, 179-190.
- Rudolph FB (1994): The biochemistry and physiology of nucleotides. Journal of Nutrition 124, 124S-127S.
- Sakai DK (1992): Repertoire of complement in immunological defense mechanisms of fish. Annual Review of Fish Disease 2, 223-247.
- Sakai M, Taniguchi K, Mamoto K, Ogawa H, Tabata M (2001): Immunostimulant effects of nucleotide isolated from yeast RNA on carp, Cyprinus carpio L. Journal of Fish Disease 24, 433-438.
- Samuel CE (2001): Antiviral actions of interferons. Clinical Microbiology Review 14, 778-809.
- Sanchez C, Babin M, Tomillo J, Ubeira FM, Dominguez J (1993): Quantification of low levels of rainbow trout immunoglobulin by enzyme immunoassay using two monoclonal antibodies. Veterinary Immunology and Immunopathology 36, 65-74.
- Sanchez C, Alvarez A, Castillo A, Zapata A, Villena A, Dominguez J (1995): Two different subpopulations of Ig-bearing cells in lymphoid organs of rainbow trout. Developmental and Comparative Immunology 19, 79-86.
- Sangrador-Vegas A, Martin SA, O'Dea PG, Smith TJ (2000): Cloning and characterization of the rainbow trout (Oncorhynchus mykiss) type II interleukin-1 receptor cDNA. European Journal of Biochemistry 267, 7031-703.
- Saurabh S, Sahoo PK (2008): Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Research 39, 223-239.
- Savan R, Sakai M (2006): Genomics of fish cytokines. Comparative Biochemistry and Physiology D 1, 9-101.
- Scapigliati G, Chausson F, Cooper EL, Scalia D, M Mazzini (1997): Qualitative and quantitative analysis of serum immunoglobulins of four Antarctic fish species. Polar Biology 18, 209-213.
- Schroder MB, Villena AJ, Jorgensen TO (1998): Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L.). Developmental and Comparative Immunology 22, 507-517.
- Secombes CJ (2008): Will advances in fish immunology change vaccination strategies? Fish and Shellfish Immunology 25, 409-416.
- Secombes CJ, Fletcher TC (1992): The role of phagocytes in the protective mechanisms of fish. Annual Review of Fish Disease 2, 53-71.
- Shen L, Stuge TB, Zhou H, Khayat M, Barker KS, Quiniou SM, Wilson M, Bengten E, Chinchar VG, Clem LW, Miller NW (2002): Channel catfish cytotoxic cells: a mini-review. Developmental and Comparative Immunology 26, 141-149.
- Shephard KL (1994): Functions for fish mucus. Reviews in Fish Biology Fisheries 4, 401-429.
- Sherwood ER, Williams DL, McName RB, Jones EL, Browder IW, Di Luzio NR (1987): Enhancement of interleukin 2 production by soluble glucan. Journal of Immunopharmacology 9, 261-267.
- Siwicki AK, Anderson DP, Rumsey GL (1994): Dietary intake of immunostimulants by rainbow trout affects non specific immunity and protects against furunculosis. Veterinary Immunology and Immunopathology 41, 125-139.
- Stafford JL, Belosevic M (2003): Transferrin and the innate immune response of fish: identification of a novel mechanism of macrophage activation. Developmental and Comparative Immunology 27, 539-554.
- Subramaniam S, Stansberg C, Olsen L, Zou J, Secombes CJ, Cunningham C (2002): Cloning of a Salmo salar interleukin-1 receptor-like cDNA. Developmental and Comparative Immunology 26, 415-431.
- Subramanian S, Mackinnon SL, Ross NW (2007): A comparative study on innate immune parameters in the epidermalmucus of various fish species. Comparative Biochemistry and Physiology B 148, 256-263.
- Subramanian S, Ross NW, Mackinnon SL (2008): Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comparative Biochemistry and Physiology B 150, 85-92.
- Suzumura E, Kurata O, Okamoto N, Ykeda Y (1994): Characteristics of natural killer cells in carp. Fish Pathology 29, 199-203.
- Suzumoto BK, Schreck CB, Mclntyre JD (1997): Relative resistances of three transferrin genotypes of coho salmon (Oncorhynchus kisutch) and their hematological responses to bacterial kidney disease. Journal of the Fisheries Research Board of Canada 34, 1-8.
- Sveinbjornsson B, Olsen R, Paulsen S (1996): Immunocytochemical localization of lysozyme in intestinal eosinophilic granule cells (EGCs) of Atlantic salmon, Salmo salar L. Journal of Fish Disease 19, 349-355.
- Szalai AJ, Norcum MT, Bly JE, Clem LW (1992): Isolation of an acute-phase and phosphorylcholine-reactive pentraxin from channel catfish (Ictalurus punctatus). Comparative Biochemistry and Physiology B 102, 535-543.
- Szalai AJ, Bly JE, Clem LW (1994): Changes in serum concentrations of channel catfish (Ictalurus punctatus) phosphorylcholine-reactive protein (PRP) in response to inflammatory agents, low temperature-shock and infection by the fungus Saprolegnia sp. Fish and Shellfish Immunology 4, 323-336.
- Tafalla C, Figueras A, Novoa B (2001): Viral hemorrhagic septicemia virus alters turbot Scophthalmus maximus macrophage nitric oxide production. Disease of Aquatic Organism 47, 101-107.
- Tatner MF, Manning MJ (1983): The ontogeny of cellular immunity in the rainbow trout, Salmo gairdneri Richardson, in relation to the stage of development of the lymphoid organs. Developmental and Comparative Immunology 7, 69-75.
- Trede NS, Zapata A, Zon LI (2001): Fishing for lymphoid genes. Trends in Immunology 22, 302-307.
- Uchida D, Hirose H, Chang PK, Aranishi F, Hirayabu E, Mano N, Mitsuya T, Prayitno SB, Natori M (2000): Characterization of Japanese eel immunoglobulin M and its level in serum. Comparative Biochemestry and Physiology B 127, 525-532.
- Vilain C, Wetzel MC, Du Pasquier L, Charlemagne J (1984): Structural and functional analysis of spontaneous antinitrophenyl antibodies in three cyprinid fish species: carp (Cyrinus carpio), goldfish (Carassius auratus) and tench (Tinca tinca). Developmental and Comparative Immunology 8, 611-622.
- Wang YB (2007): Effect of probiotics on growth performance and digestive enzyme activity of the shrimp Penaeus vannamei. Aquaculture 269, 259-264.
- Wang YB, Xu ZR (2006): Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Animal Feed Science and Technology 127, 283-292.
- Wang T, Holland J, Bols N, Secombes CJ (2007): Molecular and functional characterisation of interleukin-15 in rainbow trout Oncorhynchus mykiss: a potent inducer of interferon-gamma expression in spleen leucocytes. Journal of Immunology 179, 1475-1488.
- Wang YB, Li JR, Lin J (2008): Probiotics in aquaculture: challenges and outlook. Aquaculture 281, 1-4.
- Watts M, Munday BL, Burke CM (2001): Immune responses of teleost fish. Australian Veterinary Journal 79, 570-574.
- Whittington RJ, Munday BL, Akhlaghi M, Reddacliff GL, Carson J (1994): Humoral and peritoneal cell responses of rainbow trout (Oncorhynchus mykiss) to ovalbumin, Vibrio anguillarum and Freund's complete adjuvant following intraperitoneal and bath immunisation. Fish and Shellfish Immunology 4, 475-488.
- Whyte SK (2007): The innate immune response of finfish e A review of current knowledge. Fish and Shellfish Immunology 23, 1127-1151.
- Wilson MR, Warr GW (1992): Fish immunoglobulins and the genes that encode them. Annual Review of Fish Disease 2, 201-221.
- Wilson MR, Bengten E, Miller N, Clem LW, Du Pasquier L, Warr GW (1997): A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proceedings of the National Academy of Sciences of the United States of America 94, 4593-4597.
- Willett C, Cortes, A Zuasti A, Zapata A. (1999): Early hematopoiesis and developing lymphoid organs in the zebrafish. Developmental Dynamics 214, 323-336.
- Withler RE, Evelyn TP (1990): Genetic variation in resistance to bacterial kidney disease within and between two strains of coho salmon from British Columbia. Transactions of the American Fisheries Society 119, 1003-1009.
- Wu Y, Wang S, Peng X (2003): Serum acute phase response (APR)-related proteome of loach to trauma. Fish and Shellfish Immunology 16, 381-389.
- Yano T (1996): The nonspecific immune system: Humoral defence. In: Iwama G, Nakanishi T (eds.): The Fish Immune System: Organism, Pathogen and Environment. Academic Press, San Diego. 105-157.
- Yano T, Matsuyama H, Mangindaan REP (1991): Polysaccharide induced protection of carp Cyprinus carpio against bacterial infection. Journal of Fish Disease 14, 577-582.
- Yin Z, Lam TL, Sin YM (1997): Cytokine-mediated antimicrobial immune response of catfish, Clarias gariepinus, as a defence against Aeromonas hydrophila. Fish and Shellfish Immunology 7, 93-104.
- Yoshiura Y, Kiryu I, Fujiwara A, Suetake H, Suzuki Y, Nakanishi T (2003): Identification and characterization of Fugu orthologues of mammalian interleukin-12 subunits. Immunogenetics 55, 296-306.
- Zapata A, Diez B, Cejalvo T, Gutierrez-De Frias C, Cortes A (2006): Ontogeny of the immune system of fish. Fish and Shellfish Immunology 20, 126-136.
- Zou J, Clarke M, Secombes CJ (2003): Characterisation, expression and promoter analysis of an interleukin 10 homologue in the puffer fish, Fugu rubripes. Immunogenetics 55, 325-335.
- Zou J, Bird S, Truckle J, Bols N, Horne M, Secombes CJ (2004): Identification and expression analysis of an IL-18 homologue and its alternatively spliced form in rainbow trout Oncorhynchus mykiss. European Journal of Biochemistry 271, 1913-1923.
- Zou J, Tafalla C, Truckle J, Secombes CJ (2007): Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. Journal of Immunology 179, 3859-3871.
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.