Epidermal mucus, a major determinant in fish health: a review

Document Type: Review article

Authors

1 Department of Biotechnology, College of Engineering and Technology, Biju Patnaik University of Technology, Bhubaneswar, Odisha-751003, India

2 Ph.D. Student, Network of Excellence for Functional Biomaterials, National University of Ireland, Galway, Ireland

3 Department of Biotechnology, North Orissa University, Baripada, Odisha-757003, India

Abstract

Fish epidermal mucus contains innate immune components, secreted by globlet cells that provide the primary defence against different pathogenic microbes and act as a barrier between fish and its immediate niche. The major function of mucus includes entrapment and sloughing of microbes. The mucus also contains many factors such as antimicrobial peptides (AMPs), lysozymes, lectins, proteases, etc that provide innate immunity. The AMPs secreted by epidermal mucus cells displayed antimicrobial activity against a variety of pathogens. Besides, mucosal lysozyme was found to produce significant bacteriolytic action whereas different proteases found in skin mucus of fish can kill the pathogens by cleaving its protein or by activating immunological mechanisms. Lectins are also mucosal agglutinins that play a diverse role in innate immunity like opsonization, activation of complement, etc. Epidermal mucus in fish thus provides an innate and fast acting protection which is non-specific and is found to be relatively temperature independent. The aim of the present review is to provide a broad overview of the different components of epidermal mucus including AMPs, proteases, lysozymes as well as their mode of action on pathogens.

Keywords


Alexander, JB and Ingram, GA (1992). Non-cellular non-specific defense mechanisms of fish. A Rev. Fish. Dis., 2: 249-279.
Al Hassen, JM; Thomson, M; Summers, B and Cradle, RS (1986). Purification and properties of a hemagglutination factor from Arabian Gulf catfish (Arius thalassinus) epidermal secretion. Comp. Biochem. Physiol. B., 85: 31-39.
Aranishi, F (1999). Possible role for cathepsins B and L in bacteriolysis by Japanese eel skin. Fish Shellfish Immunol., 8: 61-64.
Aranishi, F (2000). High sensitivity of skin cathepsins L and B of European eel (Anguilla anguilla) to thermal stress. Aquaculture. 182: 209-213.
Aranishi, F; Mano, N and Hirose, H (1998). Fluorescence localization of epidermal cathepsins L and B in the Japanese eel. Fish Physiol. Biochem., 19: 205-209.
Aranishi, F and Nakane, M (1997). Epidermal proteases of the Japanese eel. Fish Physiol. Biochem., 16: 471-478.
Arasu, A; Kumaresan, V; Sathyamoorthi, A; Palanisamy, R; Prabha, N; Bhatt, P; Roy, A; Thirumalai, MK; Gnanam, AJ; Pasupuleti, M; Marimuthu, K and Arockiaraj, J (2013). Fish lily type lectin-1 contains β-prism 2 architecture: immunological characterization. Mol. Immunol., 56: 497-506.
Arockiaraj, J; Gnanam, AJ; Dhanaraj, M; Ranganath, G; Milton, J; Singh, A; Saravanan, M; Marimuthu, K and Subha, B (2012). Crustin, a WAP domain containing antimicrobial peptide from freshwater prawn Macro-brachium rosenbergii: immune characterization. Fish Shellfish Immunol., 34: 109-118.
Arockiaraj, J; Kumaresan, V; Bhatt, P; Palanisamy, R; Gnanam, AJ; Pasupuleti, M; Kasi, M and Chaurasia, MK (2014). A novel single-domain peptide; anti-LPS factor from prawn: synthesis of peptide; antimicrobial properties and complete molecular characterization. Peptides. 53: 79-88.
Balasubramanian, S and Gunasekaran, G (2015). Fatty acids and amino acids composition in skin epidermal mucus of selected fresh water fish Mugil cephalus. World J. Pharm. Pharm. Sci., 4: 1275-1287.
Beintema, JJ and Terwisscha van Scheltinga, AC (1996), Plant lysozymes. In: Jolles, P (Ed.), Lysozymes: model enzymes in biochemistry and Biology. (Illustrated Edn.), Birkhauser, Basel, Switzerland. PP: 75-86.
Bergsson, G; Agerberth, B; Jornvall, H and Gudmundsson, GH (2005). Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). FEBS. J., 272: 4960-4969.
Birkemo, GA; Luders, T; Andersen, O; Nes, IF and Nissen-Meyer, J (2003). Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Biochimic. Biophys. Acta. 1646: 207-215.
Boshra, H; Li, J and Sunyer, JO (2006). Recent advances on the complement system in teleost fish. Fish Shellfish Immunol., 20: 239-262.
Bridle, A; Nosworthy, E; Polinski, M and Nowak, B (2011). Evidence of an antimicrobial immune-modulatory role of Atlantic salmon cathelicidins during infection with Yersiniar uckeri. Plos One. 6: e23417.
Browne, MJ; Feng, CY; Booth, V and Rise, ML (2011). Characterization and expression studies of Gaduscidin-1 and Gaduscidin-2; paralogous antimicrobial peptidelike transcripts from Atlantic cod (Gadus morhua). Dev. Comp. Immunol., 35: 399-408.
Casadei, E; Wang, T; Zou, J; Gonzalez Vecino, JL; Wadsworth, S and Secombes, CJ (2009). Characteriza-tion of three novel β-defensin antimicrobial peptides in Rainbow trout (Oncorhynchus mykiss). Mol. Immunol., 46: 3358-3366.
Cha, GH; Liu, Y; Peng, T; Huang, MZ; Xie, CY; Xiao, YC and Wang, WN (2015). Molecular cloning; expression of a galectin gene in Pacific white shrimp Litopenaeus vannamei and the antibacterial activity of its recombinant protein. Mol. Immunol., 67: 325-340.
Chang, CI; Zhang, YA; Zou, J; Nie, P and Secombes, CJ (2006). Two cathelicidin genes are present in both Rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Antimicrob. Agents. Ch., 50: 185-195.
Cho, JH; Park, IY; Kim, HS; Kim, MS and Kim SC (2002a). Matrix metalloprotease 2 is involved in the regulation of the antimicrobial peptide parasin I production in catfish skin mucosa. FEBS. Lett., 531: 459-463.
Cho, JH; Park, IY; Kim, HS; Lee, WT; Kim, MS and Kim, SC (2002b). Cathepsin D produces antimicrobial peptide parasin I from histone H2A in the skin mucosa of fish. FASEB. J., 16: 429-431.
Cordero, H; Brinchmann, MF; Cuesta, A; Meseguer, J and Esteban, MA (2015). Skin mucus proteome map of European sea bass (Dicentrarchus labrax). Proteomics. 15: 4007-4020.
Das, SK; Samal, J and Dash, S (2013). Antimicrobial activity of skin mucus of fishes: a review. In: Thatoi, HN and Mishra, BB (Eds.), Advances in biotechnology. (1st Edn.), USA, Studium Press. PP: 491-506.
Dash, S; Das, SK; Samal, J; Ojha, PK; Patra, JK and Thatoi, H (2011). Dose dependence specific and non-specific immune responses of Indian major carp (L. rohita Ham) to intraperitoneal injection of formalin killed Aeromonas hydrophila whole cell vaccine. Vet. Res. Commun., 35: 541-552.
Dash, S; Samal, J and Thatoi, H (2014). A comparative study on innate immunity parameters in the epidermal mucus of Indian major carps. Aquacult. Int., 22: 411-421.
Dash, S; Swain, P; Swain, MM; Nayak, SK; Behura, A; Nanda, PK and Mishra, BK (2008). Investigation on infectious dropsy of Indian major carps. Asian Fish. Sci., 21: 377-384.
Denis, M; Palatty, PD; Bai, NR and Suriya, SJ (2003). Purification and characterization of a sialic acid specific lectin from the hemolymph of the freshwater crab Paratelphusa jacquemontii. Eur. J. Biochem., 270: 4348-4355.
DiConza, JJ (1970). Some characteristics of natural haemagglutinins found in serum and mucus of the catfish; Tachysurus australis. Aust. J. Exp. Biol. Med. Sci., 48: 515-523.
Douglas, SE; Gallant, JW; Gong, Z and Hew, C (2001). Cloning and developmental expression of a family of pleurocidin-like antimicrobial peptides from winter flounder; Pleuronectes americanus (Walbaum). Dev. Comp. Immunol., 25: 137-147.
Easy, RH and Ross, NW (2009). Changes in Atlantic salmon (Salmo salar) epidermal mucus protein composition profiles following infection with sea lice (Lepeophtheirus salmonis). Comp. Biochem. Physiol. Part D., 4: 159-167.
Ekman, DR; Skelton, DM; Davis, JM; Villeneuve, DL; Cavallin, JE; Schroeder, AK; Jensen, M; Ankley, GT and Collette, TW (2015). Metabolite profiling of fish skin mucus: a novel approach for minimally-invasive environmental exposure monitoring and surveillance. Environ. Sci. Technol., 49: 3091-3100.
Ellis, AE (2001). Innate host defense mechanisms of fish against viruses and bacteria. Dev. Comp. Immunol., 25: 827-839.
Esteban, MA (2012). An overview of the immunological defenses in fish skin. ISRN. Immunol., 2012: 1-30 (Article ID 853470).
Falco, A; Chico, V; Marroqui, L; Perez, L; Coll, JM and Estepa, A (2008). Expression and antiviral activity of a β-defensin like peptide identified in the Rainbow trout (Oncorhynchus mykiss) EST sequences. Mol. Immunol., 45: 757-765.
Fan, C; Wang, J; Zhang, X and Song, J (2015). Functional C1q is present in the skin mucus of Siberian sturgeon (Acipenser baerii). Int. Zool., 9: 1-3.
Fast, MD; Sims, DE; Burka, JF; Mustafa, A and Ross, NW (2002). Skin morphology and humoral non-specific defence parameters of mucus and plasma in Rainbow trout; coho and Atlantic salmon. Comp. Biochem. Phys., 132: 645-657.
Fastrez, J (1996). Phage lysozymes. In: Jolles, P (Ed.), Lysozymes: model enzymes in biochemistryand biology. (Illustrated Edn.), Birkhauser, Basel, Switzerland. PP: 35-64.
Fasulo, S; Tagliafierro, G; Contini, S; Ainis, L; Ricca, MB; Yanaihara, N and Zaccone, G (1993). Ectopic expression of bioactive peptides and serotonin in sacciform gland cells of teleost skin. Arch. Histol. Cytol., 56: 117-125.
Fernandes, JM; Molle, G; Kemp, GD and Smith, VJ (2004). Isolation and characterisation of oncorhyncin II; a histone H1-derived antimicrobial peptide from skin secretions of Rainbow trout; Oncorhynchus mykiss. Dev. Comp. Immunol., 28: 127-138.
Fernandes, JMO; Ruangsri, J and Kiron, V (2010). Atlantic cod piscidin and its diversification through positive selection. Plos One. 5: e9501.
Fernandes, JMO and Smith, VJ (2002). A novel antimicrobial function for a ribosomal peptide from Rainbow trout skin. Biochem. Biophys. Res. Commun., 296: 167-171.
Firth, KJ; Johnson, SC and Ross, NW (2000). Characteriza-tion of proteases in the skin mucus of Atlantic salmon (Salmo salar) infected with the salmon louse (Lepeophtheirus salmonis) and in whole-body louse homogenate. J. Parasitol., 86: 1199-1205.
Gewurz, H; Zhang, XH and Lint, TF (1995). Structure and function of the pentraxines. Curr. Opin. Immunol., 7: 54-64.
Guardiola, FA; Alberto, C; Arizcun, M; Meseguer, J and Esteban, MA (2014). Comparative skin mucus and serum humoral defence mechanisms in the teleost gilthead seabream (Sparus aurata). Fish Shellfish Immunol., 36: 545-551.
Hancock, REW (1997). Peptide antibiotics. Lancet., 349: 418-422.
Hancock, REW and Scott, MG (2000). The role of antimicrobial peptides in animal defense. Proc. Natl. Acad. Sci. USA., 97: 8856-8861.
Hartley, BS (1960). Proteolytic enzymes. Annu. Rev. Biochem., 29: 45-72.
Iger, Y and Abraham, M (1990). The process of skin healing in experimentally wounded carp. J. Fish. Biol., 36: 421-437.
Iger, Y and Abraham, M (1997). Rodlet cells in the epidermis of fish exposed to stressors. Tissue. Cell., 29: 431-438.
Ingram, GI (1980). Substances involved in the natural resistance of fish to infection-a review. J. Fish. Biol. 16: 23-60.
Irwin, DM; Yu, M and Wen, Y (1996). Isolation and characterization of vertebrate lysozyme genes. In: Jolles, P (Ed.), Lysozymes: model enzymes in biochemistry and biology. (Illustrated Edn.), Birkhauser, Basel, Switzerland. PP: 225-241.
Itami, T; Takihara, A; Nagano, Y; Suetsuna, K; Mitsutani, A; Takesue, K and Takahashi, Y (1992). Purification and characterization of lysozyme from ayu skin mucus. Nippon. Suisan. Gakkaishi., 58: 1937-1954.
Kamiya, H and Shimizu, Y (1980). Purification and characterization of agglutinins from mucous of windowpane flounder Lophopsetta maculata. Biochim. Biophys. Acta. 622: 171-178.
Kennedy, J; Baker, P and Piper, C (2009). Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar. Biotech., 11: 384-396.
Lauth, X; Shike, H; Burns, JC; Westerman, ME; Ostland, VE; Carlberg, JM; van Oslt, JC; Nizet, V; Taylor, SW; Shimizu, C and Bullet, P (2002). Discovery and characterization of two isoforms of moronecidin; a novel antimicrobial peptide from Hybrid striped bass. J. Biol. Chem., 277: 5030-5039.
Lee-Huang, S; Huang, PL; Sun, Y; Kung, HF; Blithe, DL and Chen, HC (1999). Lysozyme and RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. Proc. Natl. Acad. Sci., 96: 2678-2681.
Leon-Sicairos, N; Lopez-Soto, F; Reyes-Lopez, M; Godínez-Vargas, D; Ordaz-Pichardo, C and de la Garza, M (2006). Amoebicidal activity of milk; apo-lactoferrin; sIgA and lysozyme. Clin. Med. Res., 4: 106-113.
Luders, T; Birkemo, GA; Nissen-Meyer, J; Andersen, O and Nes, IF (2005). Proline conformation-dependent antimicrobial activity of a proline-rich histone h1 n-terminal peptide fragment isolated from the skin mucus of Atlantic salmon. Antimicrob. Agents., 49: 2399-2406.
Lund, V and Olafsen, JA (1998). A comparative study of pentraxin-like proteins in different fish species. Dev. Comp. Immunol., 22: 185-194.
Magnadottir, B; Lange, S; Gudmundsdottir, S; Bogwald, J and Dalmo, RA (2005). Ontogeny of humoral immune parameters in fish. Fish Shellfish Immunol., 19: 429-439.
Maier, VH; Dorn, KV; Gudmundsdottir, BK and Gudmundsson, GH (2008). Characterisation of cathelicidin gene family members in divergent fish species. Mol. Immunol., 45: 3723-3730.
Masso-Silva, JA and Diamond, G (2014). Antimicrobial peptides from fish. Pharmaceuticals. 7: 265-310.
Matsushita, M; Matsushita, A; Endo, Y; Nakata, M; Kojima, N; Mizuochi, T and Fujita, T (2004). Origin of the classical complement pathway: lamprey orthologue of mammalian C1q acts as a lectin. Proc. Nat. Acad. Sci. USA., 101: 10127-10131.
Matsuzaki, K; Sugishita, KI and Miyajima, K (1999). Interactions of an antimicrobial peptide; magainin 2; with lipopolysaccharide-containing liposomes as a model for outer membranes of Gram-negative bacteria. FEBS. Lett., 449: 221-224.
Mercy, PD and Ravindranath, MH (1993). Purification and characterisation of N glycolylneuraminic acid specific lectin from Scylla serrata. Eur. J. Biochem., 215: 697-704.
Morrissey, JH (1998). Coagulation factor X. In: Barret, AJ; Rawlings, ND and Woessner, JF (Eds.), Handbook of proteolytic enzymes. (1st Edn.), London, UK, Academic Press. PP: 163-167.
Nam, BH; Moon, JY and Kim, YO (2010). Multiple β-defensin isoforms identified in early developmental stages of the teleost Paralichthys olivaceus. Fish Shellfish Immunol., 28: 267-274.
Nauta, AJ; Daha, MR; Kooten, C and Roos, A (2003). Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends. Immunol., 24: 148-154.
Nigam, AK; Kumari, U; Mittal, S and Mittal, AK (2012). Comparative analysis of innate immune parameters of the skin mucous secretions from certain freshwater teleosts; inhabiting different ecological niches. Fish. Physiol. Biochem., 38: 1245-1256.
Nonaka, M and Miyazawa, S (2002). Evolution of the initiating enzymes of the complement system. Genome. Biol., 3: reviews1001.1-reviews1001.5.
Oren, Z and Shai, Y (1986). A class of highly potent antibacterial peptides derived from pardaxin; a pore-forming peptide isolated from Moses sole fish Pardachirus marmoratus. Eur. J. Biochem., 237: 303-310.
Ourth, DD; Ratts, VD and Parker, NC (1991). Bacterial complement activity and concentrations of immunoglobulin M; tranferrin and proteins at different ages of Channel catfish. J. Aquat. Anim. Health. 3: 274-280.
Palaksha, KJ; Shin, GW; Kim, YR and Jung, TS (2008). Evaluation of nonspecific immune components from the skin mucus of olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol., 24: 479-488.
Park, CB; Kim, MS and Kim, SC (1996). A novel antimicrobial peptide from Bufo bufo gargarizans. Biochem. Biophys. Res. Commun., 218: 408-413.
Park, CH; Valore, EV; Waring, AJ and Ganz, T (2001). Hepcidin; a rinary antimicrobial peptide synthesized in the liver. J. Biologi. Chem., 276: 7806-7810.
Peng, KC; Pan, CY; Chou, HN and Chen, JY (2010). Using an improved Tol2 transposon system to produce transgenic zebrafish with epinecidin-1 which enhanced resistance to bacterial infection. Fish Shellfish Immunol., 28: 905-917.
Prager, EM and Jolles, P (1996). Animal lysozymes c and g: an overview. In: Jolles, P (Ed.), Lysozymes: model enzymes in biochemistry and Biology. (Illustrated Edn.), Birkhauser, Basel, Switzerland. PP: 9-31.
Putnam, FW (1975). Transferrin. In: Putnam, FW (Ed.), The plasma proteins. (1st Edn.), New York, Academic Press. PP: 265-316.
Qasba, PK and Kumar, S (1997). Molecular divergence of lysozymes and a-lactalbumin. Crit. Rev. Biochem. Mol. Biol., 32: 255-306.
Quesenberry, MS; Ahmed, H; Elola, MT; O’Leary, N and Vasta, GR (2003). Diverse lectin repertoires in tunicates mediate broad recognition and effector innate immune responses. Integr. Comp. Biol., 43: 323-330.
Rai, AK and Mittal, AK (1983). Histochemical response of alkaline phosphatase activity during the healing of cutaneous wounds in a catfish. Experientia. 39: 520-522.
Rai, AK and Mittal, AK (1991). On the activity of acid phosphatase during skin regeneration in Heteropneustes fossilis. Bull. Life. Sci., 12: 33-39.
Rajan, BJM; Fernandes, CM; Caipang, V; Kiron, JH; Rombout, JH and Brinchmann, MF (2011). Proteome reference map of the skin mucus of Atlantic cod (Gadus morhua) revealing immune competent molecules. Fish Shellfish Immunol., 31: 224-231.
Rakers, S; Lars, N; Dieter, S; Charli, K; Jurgen, S; Kristina, S and Ralf, P (2013). Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology. J. Invest. Dermatol., 133: 1140-1149.
Ramos, F and Smith, AC (1978). The C-reactive protein (CRP) test for the detection of early disease in fishes. Aquaculture. 14: 261-266.
Rose, MC and Voynow, JA (2006). Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev., 86: 245-278.
Ross, NW; Firth, KJ; Wang, A; Burka, JF and Johnson, SC (2000). Changes in hydrolytic enzyme activities of naive Atlantic salmon Salmo salar skin mucus due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation. Dis. Aquat. Org., 41: 43-51.
Roussel, P and Delmotte, P (2004). The diversity of epithelial secreted mucins. Curr. Org. Chem., 8: 413-437.
Ruangsri, J; Fernandes, JMO; Brinchmann, M and Kiron, V (2010). Antimicrobial activity in the tissues of Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol., 28: 879-886.
Salinas, I; Zhang, YA and Sunyer, JO (2011). Mucosal immunoglobulins and B cells of teleost fish. Develop. Comp. Immunol., 35: 1346-1365.
Salles, CMC; De-Simone, SG and Leitao, S (2007). Identification and characterization of proteases from skin mucus of tambacu; a Neotropical Hybrid fish. Fish. Physiol. Biochem., 33: 173-179.
Sanahuja, I and Ibarz, A (2015). Skin mucus proteome of gilthead sea bream: a non-invasive method to screen for welfare indicators. Fish Shellfish Immunol., 46: 426-435.
Shai, Y (1994). Pardaxin: channel formation by a shark repellant peptide from fish. Toxicology. 87: 109-129.
Shai, Y (2002). From innate immunity to de-novo designed antimicrobial peptides. Curr. Pharm. Des., 8: 715-725.
Shen, Y; Zhang, J; Xu, X; Fu, J and Li, J (2012). Expression of complement component C7 and involvement in innate immune responses to bacteria in grass carp. Fish Shellfish Immunol., 33: 448-454.
Shephard, KL (1993). Mucus on the epidermis of fish and its influence on drug delivery. Adv. Drug. Deliv. Rev., 11: 403-417.
Shiomi, K; Igarashi, T; Yokota, H; Nagashima, Y and Ishida, M (2000). Isolation and structures of grammistins, peptide toxins from the skin secretion of the soap fish Grammistes sexlineatus. Toxicon. 38: 91-103.
Shiomi, K; Uematsu, H; Ito, H; Yamanaka, H and Kikuchi, T (1990). Purification and properties of a lectin in the skin mucus of the dragonet Repomucenus richardsonii. Nippon. Suisan. Gakkaishi., 56: 119-123.
Shoemaker, CA; Klesius, PH; Xu, D and Shelby, RA (2005). Overview of the immune system of fish. Aquatic American Conference. New Orleans, LA, USA.
Silphaduang, U and Noga, J (2001). Peptide antibiotics in mast cells of fish. Nature. 414: 268-269.
Smith, VJ and Fernandes, JMO (2009). Non-specific antimicrobial proteins of the innate system. In: Zaccone, G; Meseguer, J; Garcia-Ayala, A and Kapoor, BG (Eds.), Fish defences. Vol. I, Enfield, NH, USA, Science Publishers. PP: 241-275.
Spitzer, RH; Downing, SW; Koch, EA and Kaplan, MA (1976). Hemagglutinins in the mucus of pacific hagfish; Eptatretus stouii. Comp. Biochem. Physiol., 54: 409-411.
Stowell, SRCM; Arthur, R; McBride, O; Berger, N; Razi, J; Heimburg-Molinaro, LC; Rodrigues, JP; Gourdine, AJ; Noll, S; von Gunten, DF; Smith, YA; Knirel, JC; Paulson, JC and Cummings, RD (2014). Microbial glycan microarrays define key features of host-microbial interactions. Nat. Chem. Biol. 10: 470-476.
Subramanian, S; MacKinnon, SL and Ross, NW (2007). A comparative study on innate immune parameters in the epidermal mucus of various fish species. Comp. Biochem. Phys., 148: 256-263.
Sugiyama, N; Araki, M; Ishida, M; Nagashima, Y and Shiomi, K (2005). Further isolation and characterization of grammistins from the skin secretion of the soapfish Grammistes sexlineatus. Toxicon. 45: 595-601.
Sussman, M (1974). Iron and infection. In: Jacobs, A and Worwood, M (Eds.), Iron in biochemistry and medicine. (Illustrated Edn.), London, Academic Press. PP: 669-678.
Swain, P; Dash, S; Sahoo, PK; Routray, P; Sahoo, SK; Gupta, SD; Meher, PK and Sarangi, N (2007). Non-specific immune parameters of brood Indian major carp Labeo rohita and their seasonal variations. Fish Shellfish Immunol., 22: 38-43.
Takashima, F and Hibiya, T (1995). An atlas of fish histology: normal and pathological features. 2nd Edn., Gustav Fischer Verlag, Stuttgart.
Tsutsui, S; Okamoto, M; Ono, M; Suetake, H; Kikuchi, K; Nakamura, O; Suzuki, Y and Watanabe, T (2011). A new type of lectin discovered in a fish; flathead Platycephalus indicus suggests an alternative functional role for mammalian plasma kallikrein. Glycobiology. 21: 1580-1587.
Tsutsui, S; Tasumi, S; Suetake, H and Suzuki, Y (2003). Skin mucus lectin of pufferfish (Fugu rubripes) homlogous to monocotyledonous plant lectin. J. Biol. Chem., 278: 20882-20889.
Tsutsui, S; Yamaguchi, M; Hirasawa, A; Nakamura, O and Watanabe, T (2009). Common skate (Raja kenojei)
secretes pentraxin into the cutaneous secretion: the first skin mucus lectin in cartilaginous fish. J. Biochem., 146: 295-306.
Uzzell, T; Stolzenberg, ED; Shinnar, AE and Zasloff, M (2003). Hagfish intestinal antimicrobial peptides are ancient cathelicidins. Peptides. 24: 1655-1667.
Valdenegro-Vega, VA; Crosbie, P; Bridle, A; Leef, M; Wilson, R and Nowak, BF (2014). Differentially expressed proteins in gill and skin mucus of Atlantic salmon (Salmo salar) affected by amoebic gill disease. Fish Shellfish Immunol., 40: 69-77.
Valero, Y; Elena, CP; Jose, M; Maria, AE and Alberto, C (2013). Biological role of fish antimicrobial peptides. In: Seong, MD and Hak, YI (Eds.), Antimicrobial peptides. (1st Edn.), NY, USA, Nova Science Publishers Inc., PP: 31-60.
Vizioli, J and Salzet, M (2002). Antimicrobial peptides: new weapons to control parasitic infections. Trends. Parasitol., 18: 475-476.
Wang, S; Wang, Y; Ma, J; Ding, Y and Zhang, S (2011). Phosvitin plays a critical role in the immunity of zebrafish embryos via acting as a pattern recognition receptor and an antimicrobial effector. J. Biol. Chem., 286: 22653-22664.
Wu, MH; Maier, E; Benz, R and Hancock, REW (1999). Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochem. US., 38: 7235-7242.
Yin, ZX; He, W; Chen, WJ; Yan, JH; Yang, JN; Chan, SM and He, JG (2006). Cloning, expression and antimicrobial activity of an antimicrobial peptide, epinecidin-1, from the orange-spotted grouper, Epinephelus coioides. Aquaculture. 253: 204-211.
Zaccone, G; Kapoor, BG; Fasulo, S and Ainis, L (2001). Structural, histochemical and functional aspects of the epidermis of fishes. Adv. Mar. Biol., 40: 253-348.
Zhao, JG; Zhou, L and Jin, JY (2009). Antimicrobial activity specific to Gram-negative bacteria and immune modulation mediated NF-κB and Sp1 of a medaka β-defensin. Develop. Comp. Immunol., 33: 624-637.
Zou, J; Mercier, C; Koussounadis, A and Secombes, C (2007). Discovery of multiple beta-defensin like homologues in teleost fish. Mol. Immunol., 44: 638-647.