Innate and adaptive immunity in teleost fish: A review

Veterinarni Medicina

Volumn 56, Issue 10, 2011, Pages 486-503

  Uribe, C ^a   Folch, H ^a   Enriquez, R ^a   Moran, Gabriel ^a  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

Fish; Immune response; Immunomodulators

Indexed keywords

TELEOSTEI; VERTEBRATA;

EID: 84855725332     PISSN: 03758427     EISSN: None     Source Type: Journal    
DOI: 10.17221/3294-VETMED     Document Type: Review

References (175)

1. 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
2. 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
3. Alexander JB, Ingram GA (1992): Noncellular nonspecific defense mechanisms of fish. Annual Review of Fish Disease 2, 249-279
4. 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
5. Anderson DP (1992): Immunostimulants, adjuvants and vaccine carriers in fish: applications to aquaculture. Annual Review of Fish Disease 2, 281-307
6. Aranishi F, Nakane M (1997): Epidermal proteases of the Japanese eel. Fish Physiology and Biochemistry 16, 471-478
7. 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
8. 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
9. Armstrong PB, Quigley JP (1999): α-2-Macroglobulin: an evolutionarily conserved arm of the innate immune system. Developmental and Comparative Immunology 23, 375-390
10. 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
11. Bayne CJ, Gerwick L (2001): The acute phase response and innate immunity of fish. Developmental and Comparative Immunology 25, 725-743
12. Birkemo GA, Luders T, Andersen O, Nes IF, Nissen-Meyer J (2003): Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Journal of Biochemistry, Molecular Biology and Biophysics 1646, 207-215
13. Blazer VS (1991): Piscine macrophage function and nutritional influences: A review. Journal of Aquatic Animal Health 3, 77-86
14. Boes M (2000): Role of natural and immune IgM antibodies in immune responses. Molecular Immunology 37, 1141-1149
15. Boshra H, Li J, Sunyer JO(2006): Recent advances on the complement system of teleost fish. Fish and Shellfish Immunology 20, 239-262
16. 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
17. Bowden TJ (2008): Modulation of the immune system of fish by their environment. Fish and Shellfish Immunology 25, 373-383
18. 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
19. Bowden TJ, Cook P, Rombout JHWM (2005): Development and function of the thymus in teleosts. Fish and Shellfish Immunology 19, 413-427
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. Cook MT, Hayball PJ, Birdseye L, Bagley C, Nowak BF, Hayball JD (2003): Isolation and partial characterization of a pentraxin-like protein with complement-fixing activity from snapper (Pagrus auratus, Sparidae) serum. Developmental and Comparative Immunology 27, 579-588
28. 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
29. Cosgrove M (1998): Nucleotides. Nutrition 14, 748-751
30. Dalmo RA (2005): Ontogeny of the fish immune system. Fish and Shellfish Immunology 19, 395-396
31. 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
32. Dalmo RA, Bogwald J (2008): β-glucans as conductors of immune symphonies. Fish and Shellfish Immunology 25, 384-396
33. 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
34. 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
35. 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
36. 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
37. 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
38. 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
39. Di Luzio NR (1985): Update on the immunomodulating activities of glucans. Seminars in Immunopathology 8, 387-400
40. Dinarello CA (1997): Interleukin-1. Cytokine Growth Factor Review 8, 253-265
41. 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
42. 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
43. 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
44. Ellis AE (2001): Innate host defence mechanism of fish against viruses and bacteria. Developmental and Comparative Immunology 25, 827-839
45. 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
46. Evans D, Jaso-Friedmann L (1992): Nonspecific cytotoxic cells as effectors of immunity in fish. Annual Review of Fish Disease 2, 109
47. Faisal M, Ahmed G, Peters II, Cooper EL (1989): Natural citotoxicity of tilapia leukocytes. Disease of Aquatic Organims 7, 17-22
48. 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
49. 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
50. Fuller R (1989): Probiotic in man and animals. Journal of Applied Bacteriology 66, 365-378
51. Gatesoupe FJ (1999): The use of probiotics in aquaculture. Aquaculture 180, 147-165
52. Gil A (2002): Modulation of the immune response mediated by dietary nucleotides. European Journal of Clinical Nutrition 56, S1-S4
53. 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
54. 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
55. Hanington PC, Wang T, Secombes CJ, Belosevic M (2007): Growth factors of lower vertebrates: characterization of goldfish (Carassius auratus L.) macrophage colony-stimulating factor-1. Journal of Biological Chemistry 282, 31865-31872
56. 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
57. 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
58. 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
59. 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
60. 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
61. Hibiya T (ed.) (1994): An Atlas of Fish Histology. Normal and Pathological Features. Gustav Fischer Verlag, Stuttgart, Germany. 5-125
62. 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
63. Holland MC, Lambris JD (2002):. The complement system of teleosts. Fish and Shellfish Immunology 12, 399-420
64. Hoover GJ, El-MowafiA, 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
65. 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
66. Ingram GA (1980): Substances involved in the natural resistance of fish to infection a review. Journal of Fish Biology 16, 23-60
67. 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
68. Jenkins JA, Ourth DD (1993): Opsonic effect of the alternative complement pathway on channel catfish peripheral blood phagocytes. Veterinary Immunology Immunopathology 39, 447-459
69. 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
70. 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
71. 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
72. 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
73. 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
74. 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
75. 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
76. 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
77. 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
78. 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
79. 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
80. 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
81. 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
82. 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
83. 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
84. 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
85. Lie O, Evensen O, Sorensen A, Froysadal E (1989): Study on lysozyme activity in some fish species. Disease of Aquatic Organism 6, 1-5
86. 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
87. Lorenzen N, LaPatra SE (1999): Immunity to rhabdovirus in rainbow trout: the antibody response. Fish and Shellfish Immunology 9, 345-360
88. 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
89. Lund V, Olafsen JA (1998): A comparative study of pentraxin-like proteins in different fish species. Developmental and Comparative Immunology 22, 185-194
90. 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
91. Maier VH, Dorn KV, Gudmundsdottir BK, Gudmundsson GH (2008): Characterisation of cathelicidin gene family members in divergent fish species. Molecular Immunology 45, 3723-3730
92. Magnadottir B (2006): Innate immunity of fish (overview). Fish and Shellfish Immunology 20, 137-151
93. Magnadottir B (2010): Immunological control of fish diseases. Journal of Marine Biotechnology 12, 361-379
94. 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
95. 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
96. 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
97. 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
98. 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
99. Matsushita M, Endo Y, Nonaka M, Fujita T (1998): Complement-related serine proteases in tunicates and vertebrates. Current Opinion in Immunology 10, 29-35
100. 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
101. McKinney EC, Achmale MC (1994): Damselfish with neurofibromatosis exhibit cytotoxicity in toward tumor targets. Developmental and Comparative Immunology 18, 305-313
102. Morrison RN, Nowak B (2002): The antibody response of teleost fish. Seminars in Avian and Exotic Pet Medicine 11, 46-54
103. 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
104. 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
105. 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
106. 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
107. 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
108. Navarro J, Ruiz-Bravo A, Jimenez-Varela M, Gil A (1996): Modulation of antibody-forming cell and mitogen-driven lymphoproliferative responses by dietary nucleotides in mice. Immunology Letters 53, 141-145
109. Nikoskelainen S, Lehtinen J, Lilius EM (2002): Bacteriolytic activity of rainbow trout (Oncorhynchus mykiss) complement. Developmental and Comparative Immunology 26, 797-804
110. 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
111. 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
112. 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
113. 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
114. 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
115. 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
116. Ramadan A, AfifiNA, 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
117. 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
118. 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
119. Robertsen B (2006): The interferon system of teleost fish. Fish and Shellfish Immunology 20, 172-191
120. 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
121. 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
122. 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
123. Rombout JH, Huttenhuis HBT, Picchietti S, Scapigliati S (2005): Phylogeny and ontogeny of fish leucocites. Fish and Shellfish Immunology 19, 441-455
124. 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
125. Rudolph FB (1994): The biochemistry and physiology of nucleotides. Journal of Nutrition 124, 124S-127S
126. Sakai DK (1992): Repertoire of complement in immunological defense mechanisms of fish. Annual Review of Fish Disease 2, 223-247
127. 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
128. Samuel CE (2001): Antiviral actions of interferons. Clinical Microbiology Review 14, 778-809
129. 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
130. 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
131. 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
132. Saurabh S, Sahoo PK (2008): Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Research 39, 223-239
133. Savan R, Sakai M (2006): Genomics of fish cytokines. Comparative Biochemistry and Physiology D 1, 9-101
134. 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
135. 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
136. Secombes CJ (2008): Will advances in fish immunology change vaccination strategies? Fish and Shellfish Immunology 25, 409-416
137. Secombes CJ, Fletcher TC (1992): The role of phagocytes in the protective mechanisms of fish. Annual Review of Fish Disease 2, 53-71
138. 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
139. Shephard KL (1994): Functions for fish mucus. Reviews in Fish Biology Fisheries 4, 401-429
140. 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
141. 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
142. 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
143. 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
144. 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
145. 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
146. Suzumura E, Kurata O, Okamoto N, Ykeda Y (1994): Characteristics of natural killer cells in carp. Fish Pathology 29, 199-203
147. 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
148. 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
149. 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
150. 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
151. 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
152. 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
153. Trede NS, Zapata A, Zon LI (2001): Fishing for lymphoid genes. Trends in Immunology 22, 302-307
154. 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
155. 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
156. Wang YB (2007): Effect of probiotics on growth performance and digestive enzyme activity of the shrimp Penaeus vannamei. Aquaculture 269, 259-264
157. 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
158. 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
159. Wang YB, Li JR, Lin J (2008): Probiotics in aquaculture: challenges and outlook. Aquaculture 281, 1-4
160. Watts M, Munday BL, Burke CM (2001): Immune responses of teleost fish. Australian Veterinary Journal 79, 570-574
161. Whittington RJ, Munday BL, Akhlaghi M, ReddacliffGL, 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
162. Whyte SK (2007): The innate immune response of finfish e A review of current knowledge. Fish and Shellfish Immunology 23, 1127-1151
163. Wilson MR, Warr GW (1992): Fish immunoglobulins and the genes that encode them. Annual Review of Fish Disease 2, 201-221
164. 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
165. Willett C, Cortes, A Zuasti A, Zapata A. (1999): Early hematopoiesis and developing lymphoid organs in the zebrafish. Developmental Dynamics 214, 323-336
166. 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
167. 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
168. 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
169. Yano T, Matsuyama H, Mangindaan REP (1991): Polysaccharide induced protection of carp Cyprinus carpio against bacterial infection. Journal of Fish Disease 14, 577-582
170. 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
171. 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
172. 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
173. 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
174. 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
175. 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