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Tyrosinase, a new innate humoral immune parameter in large yellow croaker (Pseudosciaena crocea R)

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Abstract

We evaluated the immune response to infection with a pathogen in large yellow croaker (Pseudosciaena crocea Richardson). The fish were given an intraperitoneal (i.p.) injection of Vibrio parahaemolyticus or sterile sea water (control). We collected blood sera from the fish 0.17, 1, 2, 4, 8, 12, or 16 d after injection (dpi). We measured tyrosinase activity and the concentrations of lysozyme, NOS, and antibodies. Serum tyrosinase activity was significantly higher at 0.17 and 4 dpi than in the control group, and peaked at 8 dpi. Lysozyme activity was significantly higher at 2 and 12 dpi than in the control group, but lower at 16 dpi. There is no statistical difference in the level of nitric oxides synthase (NOS) activity or antibodies between the control and injection groups. This is the first report of the tyrosinase activity in the serum of large yellow croaker. Our results indicate that tyrosinase plays an important role in the immediate immune defense against V. parahaemolyticus in large yellow croaker. Tyrosinase is a candidate parameter for investigation of fish innate immune defense.

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References

  • Agius C, Roberts R J. 2003. Melano-macrophage centres and their role in fish pathology. J. Fish Dis., 26: 499–509.

    Article  Google Scholar 

  • Ai Q, Mai K, Zhang L, Tan B, Zhang W, Xu W, Li H. 2007. Effects of dietary β-1, 3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol., 22: 394–402.

    Article  Google Scholar 

  • Alcaide E, Amaro C, Todoli R, Oltra R. 1999. Isolation and characterization of Vibrio parahaemolyticus causing infection in iberian toothcarp Aphanius iberus. Dis. Aquat. Org., 35: 77–80.

    Article  Google Scholar 

  • Alexander J B, Ingram G A. 1992. Non cellular nonspecific defense mechanisms of fish. Annu. Rev. Fish Dis., 2: 249–279.

    Article  Google Scholar 

  • Ashida M. 1971. Purification and characterization of prophenoloxidase from haemolymph of the silkworm Bombyx mori. Arch. Biochem. Biophys., 144: 749–762.

    Article  Google Scholar 

  • Ashida M, Brey P T. 1998. Recent advances on the research of the insect prophenoloxidase cascade. In: Brey P T and Hultmark D. ed. Molecular Mechanisms of Immune Responses in Insects, Chapman and Hall, London. p. 135–172.

    Google Scholar 

  • Barroso J B, Carreras A, Esteban F J, Peinado M A, Martínez-Lara E, Valderrama R, Jiménez A, Rodrigo J, Lupiáñez J A. 2000. Molecular and kinetic characterization and cell type location of inducible nitric oxide synthase in fish. Am. J. Physiol. Regul. Integr. Comp. Physiol., 279: 650–656.

    Google Scholar 

  • Bayne C J, Gerwick L. 2001. The acute phase response and innate immunity of fish. Dev. Comp. Immunol., 25: 725–743.

    Article  Google Scholar 

  • Bilodeau A L, Peterson B C, Bosworth B G. 2006. Response of toll-like receptors, lysozyme, and IGF-I in back-cross hybrid (F1 male (blue × channel) × female channel) catfish challenged with virulent Edwardsiella ictaluri. Fish Shellfish Immunol., 20: 29–39

    Article  Google Scholar 

  • Boes M. 2000. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol., 37: 1 141–1 149.

    Article  Google Scholar 

  • Bohn J. 1999. Are natural antibodies involved in tumour defence? Immunol. Lett., 69: 317–320.

    Article  Google Scholar 

  • Boman H G, Hultmark D. 1987. Cell-free immunity in insects. Annu. Rev. Microbiol., 41: 103–126.

    Article  Google Scholar 

  • Bradford M M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248–254.

    Article  Google Scholar 

  • Bridle A R, Morrison R N, Nowak B F. 2006. The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during amoebic gill disease (AGD). Fish Shellfish Immunol., 20: 346–364.

    Article  Google Scholar 

  • Brivio M F, Pagani M, Restelli S. 2002. Immune suppression of Galleria mellonella (Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Exp. parasitol., 101: 149–156.

    Article  Google Scholar 

  • Cerenius L, Soderhall K. 2004. The prophenoloxidase-activating system in invertebrates. Immunol. Rev., 198: 116–126.

    Article  Google Scholar 

  • Chen X H, Lin K B, Wang X W. 2003. Outbreaks of an iridovirus disease in maricultured large yellow croaker, Larimichthys crocea (Richardson), in China. J. Fish Dis., 26: 615–619.

    Article  Google Scholar 

  • Chow D A, Wang H, Zhang Z. 1999. Natural antibody surveillance of neoplastic and activated cells. Biotecnol. Apl., 16: 18–19.

    Google Scholar 

  • Chun J, McMaster J, Han Y S, Schwartz A, Paskewitz S M. 2000. Two-dimensional gel analysis of haemolymph proteins from Plasmodium-melanizing and non-melanizing strains of Anopheles gambiae. Insect Mol. Biol., 9: 39–45.

    Article  Google Scholar 

  • Clark I A, Rockett K A. 1996. Nitric oxide and parasitic disease. Adv. Parasitol., 37: 1–34..

    Article  Google Scholar 

  • Crosbie P B B, Nowak B F. 2004. Immune responses of barramundi, Lates calcarifer (Bloch), after administration of an experimental Vibrio harveyi bacterin by intraperitoneal injection, anal incubation and immersion. J. Fish Dis., 27: 623–632.

    Article  Google Scholar 

  • Dautremepuits C, Betoulle S, Paris-Palacios S, Vernet G. 2004. Humoral immune factors modulated by copper and chitosan in healthy or parasitised carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Aquat. Toxicol., 68: 325–338.

    Article  Google Scholar 

  • Fange R, Lundblad G, Lind J. 1976. Lysozyme and chitinase in blood and lymphomyeloid tissues of marine fish. Mar. Biol., 36: 277–282.

    Article  Google Scholar 

  • Gonzalez R, Matsiota P, Torchy C, De Kinkelin P, Avrameas S. 1989. Natural anti-TNP antibodies from rainbow trout interfere with viral infection in vitro. Res. Immunol., 140: 675–684.

    Article  Google Scholar 

  • Gonzalez S F, Buchmann K, Nielsen M E. 2007. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: Inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish Shellfish Immunol., 22: 641–650.

    Article  Google Scholar 

  • Gregorio E A, Ratcliffe N A. 1991. The prophenoloxidase system and in vitro interaction of Trypanosoma rangeli with Rhodnius prolixus and Triatoma infestans haemolymph. Parasite Immunol., 13: 551–564.

    Article  Google Scholar 

  • Gross K A, Powell M D, Butler R, Morrison R N, Nowak B F. 2005. Changes in the innate immune response of Atlantic salmon, Salmo salar L., exposed to experimental infection with Neoparamoeba sp. J. Fish Dis., 28: 293–299.

    Article  Google Scholar 

  • Haugarvoll E, Thorsen J, Laane M, Huang Q, Koppang E O. 2006. Melanogenesis and evidence for melanosome transport to the plasma membrane in a CD83+ teleost leukocyte cell line. Pigment Cell Res., 19: 214–225.

    Article  Google Scholar 

  • Hernandez A, Tort L. 2003. Annual variation of complement, lysozyme and haemagglutinin levels in serum of the gilthead seabream Sparus aurata. Fish Shellfish Immunol., 15: 479–481.

    Article  Google Scholar 

  • Horowitz N H, Shen S. 1952. Neurospora tyrosinase. J. Biol. Chem., 197: 513–520.

    Google Scholar 

  • Ingram G A. 1980. Substances involved in the natural resistance of fish to infection. J. Fish Biol., 16: 23–60.

    Article  Google Scholar 

  • Jian J, Wu Z. 2003. Effects of traditional Chinese medicine on nonspecific immunity and disease resistance of large yellow croaker, Pseudosciaena crocea (Richardson). Aquaculture, 218: 1–9.

    Article  Google Scholar 

  • Jolles P, Jolles J. 1984. What’s new in lysozyme research? Always a model system, today as yesterday. Mol. Cell Biochem., 63: 165–189.

    Article  Google Scholar 

  • Kanost M R, Jiang H, Yu X Q. 2004. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev., 198: 97–105.

    Article  Google Scholar 

  • Kim D H, Austin B. 2006. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol., 21: 513–524.

    Article  Google Scholar 

  • Korner A, Pawelek J. 1982. Mammalian tyrosinase catalyzes three reactions in the biosynthesis of melanin. Science, 217: 1 163–1 165.

    Article  Google Scholar 

  • Kumari J, Sahoo P K, Swain T, Sahoo S K, Sahu A K, Mohanty B R. 2006. Seasonal variation in the innate immune parameters of the Asian catfish Clarias batrachus. Aquaculture, 252: 121–127.

    Article  Google Scholar 

  • Li Q L, Chen Q. 2001. Identification of bacterial pathogen and treatment after infection of Pseudosciaena crocea in marine cage culture. Chinese J. Appl. Environ. Biol., 7: 489–493. (in Chinese with English abstract)

    Google Scholar 

  • Liu G, Zheng W, Chen X. 2007. Molecular cloning of proteasome activator PA28-β subunit of large yellow croaker (Pseudosciana crocea) and its coordinated up-regulation with MHC class I γ-chain and β 2-microglobulin in poly I:C-treated fish. Mol. Immunol., 44: 1 190–1 197.

    Google Scholar 

  • Liu P C, Chen Y C, Huang C Y, Lee K K. 2000. Virulence of Vibrio parahaemolyticus isolated from cultured small abalone Haliotis diversicolor supertexta, with withering syndrome. Lett. Appl. Microbial., 31: 433–437.

    Article  Google Scholar 

  • Ma C, Kanost M R. 2000. A β 1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biolog. Chem., 275: 7 505–7 514.

    Google Scholar 

  • Mackintosh J A. 2001. The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J. Theor. Biol., 211: 101–113.

    Article  Google Scholar 

  • Magnadóttir B. 2006, Innate immunity of fish (overview). Fish Shellfish Immunol., 20: 137–151.

    Article  Google Scholar 

  • Magor B G, Magor K E. 2001. Evolution of effectors and receptors of innate immunity. Dev. Comp. Immunol., 25: 651–682.

    Article  Google Scholar 

  • Mao Z, Yu L, You Z, Wei Y, Liu Y. 2007. Cloning, expression and immunogenicity analysis of five outer membrane proteins of Vibrio parahaemolyticus zj2003. Fish Shellfish Immunol., 23: 567–575.

    Article  Google Scholar 

  • Marletta M A, Yoon P S, Iyengar R, Leaf C D, Wishnok J S. 1988. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry, 27: 8 706–8 711.

    Article  Google Scholar 

  • Mavrouli M D, Tsakas S, TheodorouG L, Lampropoulou M, Marmaras V J. 2005. MAP kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochim. Biophys. Acta, 1744: 145–156.

    Article  Google Scholar 

  • Mevorach D, Zhou J L, Song X, Elkon K B. 1998. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med., 188: 387–392.

    Article  Google Scholar 

  • Neumann N F, Belosevic M. 1996. Deactivation of primed respiratory burst response of goldfish macrophages by leukocyte-derived macrophage activating factor(s). Dev. Comp. Immunol., 20: 427–439.

    Article  Google Scholar 

  • Neumann N F, Fagan D, Belosevic M. 1995. Macrophage activating factor(s) secreted by mitogen stimulated goldfish kidney leukocytes synergize with bacterial lipopolysaccharide to induce nitric oxide production in teleost macrophages. Dev. Comp. Immunol., 19: 473–482.

    Article  Google Scholar 

  • Orlow S J. 1995. Melanosomes are specialized members of the lysosomal lineage of organelles. J. Invest. Dermatol., 105: 3–7.

    Article  Google Scholar 

  • Panigrahi A, Kiron V, Kobayashi T, Puangkaew J, Satoh S, Sugita H. 2004. Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet. Immunol. Immunopathol., 102: 379–388.

    Article  Google Scholar 

  • Qian R, Chu W, Mao Z, Zhang C, Wei Y, Yu L. 2007. Expression, characterization and immunogenicity of a major outer membrane protein from Vibrio alginolyticus. Acta Biochim. Biophys. Sin., 39: 194–200.

    Article  Google Scholar 

  • Raposo G, Fevrier B, Stoorvogel W, Marks M S. 2002. Lysosome-related organelles: a view from immunity and pigmentation. Cell Struct.Funct., 27: 443–456.

    Article  Google Scholar 

  • Reid R R, Prodeus A P, Khan W, Hsu T, Rosen F S, Carroll M C. 1997. Endotoxin shock in antibody-deficient mice: unraveling the role of natural antibody and complement in the clearance of lipopolysaccharide. J. Immunol., 159: 970–975.

    Google Scholar 

  • Saeij J P J, Van Muiswinkel W B, Groeneveld A, Wiegertjes G F. 2002. Immune modulation by fish kinetoplastid parasites: a role for nitric oxide. Parasitology, 124: 77–86.

    Article  Google Scholar 

  • Sahoo P K, Pillai B R, Mohanty J, Kumari J, Mohanty S, Mishra B K. 2006. In vivo humoral and cellular reactions, and fate of injected bacteria Aeromonas hydrophila in freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol., 23: 327–340.

    Article  Google Scholar 

  • Schoor W P, Plumb J A. 1994. Induction of nitric oxide synthase in channel catfish Ictalurus punctatus by Edwardsiella ictaluri. Dis. Aquat. Org., 19: 153–155.

    Article  Google Scholar 

  • Sigh J, Lindenstrøm T, Buchmann K. 2004. The parasitic ciliate Ichthyophthirius multifiliis induces expression of immune relevant genes in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis., 27: 409–417.

    Article  Google Scholar 

  • Sinyakov M S, Dror M, Zhevelev H M, Margel S, Avtalion R R. 2002. Natural antibodies and their significance in active immunization and protection against a defined pathogen in fish. Vaccine, 20: 3 668–3 674.

    Article  Google Scholar 

  • Siwicki A K, Anderson D P. 1993. An easy spectrophotometric assay for determining total protein and immunoglobulin levels in fish sera: correlation to fish health. Tech. Fish Immunol., 3: 23–30.

    Google Scholar 

  • Siwicki A K, Morand M, Fuller Jr J, Nissen S, Goryczko K, Ostaszewski P, Kazun K, Głombski E. 2003. Influence of feeding the leucine metabolite β-hydroxy-β-methylbutyrate (HMB) on the non-specific cellular and humoral defence mechanisms of rainbow trout (Oncorhynchus mykiss). J. Appl. Ichthyol., 19: 44–48.

    Article  Google Scholar 

  • Sudheesh P S, Xu H S. 2001. Pathogenicity of Vibrio parahaemolyticus in tiger prawn Penaeus monodon Fabricius: possible role of extracellular proteases. Aquaculture, 196: 37–46.

    Article  Google Scholar 

  • Tafalla C, Coll J, Secombes C J. 2005. Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection. Dev. Comp. Immunol., 29: 615–626.

    Article  Google Scholar 

  • Tort L, Rotllant J, Liarte C, Acerete L, Hernández A, Ceulemans S, Coutteau P, Padros F. 2004. Effects of temperature decrease on feeding rates, immune indicators and histopathological changes of gilthead seabream Sparus aurata fed with an experimental diet. Aquaculture, 229: 55–65.

    Article  Google Scholar 

  • Wang G J, Xie J, Yu D G, Zhu H Y. 2005. Effect of Vibrio parahaemolyticus on nitric oxide synthase activity in serum of Epinephelus coioides. Mar. Fish., 27: 60–63. (in Chinese with English abstract)

    Google Scholar 

  • Wang J, Su Y, Quan C, Ding S, Zhan W. 2001. Genetic diversity of the wild and reared Pseudosciaena crocea. Chin. J. Oceanol. Limnol., 19:152–156.

    Article  Google Scholar 

  • Wang J, Su Y, Yan Q. 2003. A fast and indirect fluorescent antibody assay for the Vibrio in large yellow croaker Pseudosciaena crocea (Richardson). Chin. J. Oceanol. Limnol., 21: 91–96.

    Article  Google Scholar 

  • Wang R, Neumann N F, Shen Q, Belosevic M. 1995. Establishment and characterization of a macrophage cell line from the goldfish. Fish Shellfish Immunol., 5: 329–346.

    Article  Google Scholar 

  • Wilson R, Ratcliffe N A. 2000. Effect of lysozyme on the lectin-mediated phagocytosis of Bacilluscereus by haemocytes of the cockroach, Blaberus discoidalis. J. Insect Physiol., 46: 663–670.

    Article  Google Scholar 

  • Xu B F, Lin N F, Yang J X, Yu F S, Dong C F, Lin T L. 2002. Isolation, identification and pathogenicity analysis of Vibrio parahaemolyticus from Pseudosciaena crocea. Fujian J. of Agricul. Sci., 17: 174–177. (in Chinese with English abstract)

    Google Scholar 

  • Yildirim M, Lim C, Wan P J, Klesius P H. 2003. Growth performance and immune response of channel catfish (Ictalurus punctatus) fed diets containing graded levels of gossypol-acetic acid. Aquaculture, 219: 751–768.

    Article  Google Scholar 

  • Yin G, Jeney G, Racz T, Xu P, Jun X, Jeney Z. 2006. Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on non-specific immune response of tilapia, Oreochromis niloticus. Aquaculture, 253: 39–47.

    Article  Google Scholar 

  • Zhang X B, Huang H L, Zhang L Z, Li Q H, Zhang L Z, Zhang Q. 1994. Measurement of nitric oxide synthase activity and its application. J. Beijing Med. Univ., 26: 173–176. (in Chinese with English abstract)

    Google Scholar 

  • Zheng W, Chen X. 2006a. Cloning and expression analysis of interferon-γ-inducible-lysosomal thiol reductase gene in large yellow croaker (Pseudosciaena crocea). Mol. Immunol., 43: 2 135–2 141.

    Article  Google Scholar 

  • Zheng W, Liu G, Ao J, Chen X. 2006b. Expression analysis of immune-relevant genes in the spleen of large yellow croaker (Pseudosciaena crocea) stimulated with poly I:C. Fish Shellfish Immunol., 21: 414–430.

    Article  Google Scholar 

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Correspondence to Yilei Wang  (王艺磊).

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Supported by the Ministry of Education of China (No. 205079), the Education Department of Fujian Province (No. JA004229), the Sciences and Technology Department of Fujian Province (Nos. 2005N041, 2008N0121) and the Innovation Team Foundation of Jimei University (No. 2008A001)

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Wang, S., Wang, Y., Zhang, Z. et al. Tyrosinase, a new innate humoral immune parameter in large yellow croaker (Pseudosciaena crocea R). Chin. J. Ocean. Limnol. 27, 527–535 (2009). https://doi.org/10.1007/s00343-009-9178-z

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