Probiotics-pathogen interactions elicit differential regulation of cutaneous immune responses in epidermal cells of Atlantic cod Gadus morhua

Fish and Shellfish Immunology

Volumn 36, Issue 1, 2014, Pages 113-119

  Lazado, Carlo C ^a   Caipang, Christopher Marlowe A ^b  

^a NORD UNIVERSITY   (Norway)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Epidermal cell; Mucosal; Pathogen; Probiotics; Skin

Indexed keywords

BACTERIA (MICROORGANISMS); GADUS MORHUA; LISTONELLA ANGUILLARUM;

PEROXIDASE; PROBIOTIC AGENT; RNA;

ANIMAL; ANIMAL DISEASE; APOPTOSIS; ARTICLE; ATLANTIC COD; BACTERIAL SKIN DISEASE; CELL SURVIVAL; CHEMISTRY; EPIDERMIS CELL; EPITHELIUM CELL; FISH DISEASE; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; MUCOSAL; NONPARAMETRIC TEST; PATHOGENESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; VIBRIO; VIBRIOSIS;

EPIDERMAL CELL; MUCOSAL; PATHOGEN; PROBIOTICS; SKIN;

ANIMALS; APOPTOSIS; CELL SURVIVAL; EPITHELIAL CELLS; FISH DISEASES; GADUS MORHUA; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; PEROXIDASE; PROBIOTICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SKIN DISEASES, BACTERIAL; STATISTICS, NONPARAMETRIC; VIBRIO; VIBRIO INFECTIONS;

EID: 84891160683     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.10.017     Document Type: Article

References (43)

1. Esteban M.A. An overview of the immunological defenses in fish skin. ISRN Immunol 2012, 2012:29.
2. Rombout J.H.W.M., Taverne N., van de Kamp M., Taverne-Thiele A.J. Differences in mucus and serum immunoglobulin of carp (Cyprinus carpio L.). Develop Comp Immunol 1993, 17:309-317.
3. Bullock A.M., Roberts R.J. Fish dermatology of marine teleost fish. 1. The normal integument. Oceanogr Mar Biol - Annu Rev 1974, 13:383-411.
4. Fast M.D., Sims D.E., Burka J.F., Mustafa A., Ross N.W. Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comp Biochem Physiol Part A: Mol Integr Physiol 2002, 132:645-657.
5. Chivers D.P., Wisenden B.D., Hindman C.J., Michalak T.A., Kusch R.C., Kaminskyj S.G., et al. Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc Biol Sci/R Soc 2007, 274:2611-2619.
6. Buchman K. Immune mechanisms in fish skin against monogeneans - a model. Folia Parasitol (Praha) 1999, 46:1-9.
7. Kijewska A., Wiecaszek B., Kalamarz-Kubiak H., Szulc J., Sobecka E. Skin structure studies and molecular identification of the Atlantic cod Gadus morhua L. of unique golden pigmentation from the Svalbard Bank. JAppl Ichthyol 2012, 28:60-65.
8. Halbgewachs C.F., Marchant T.A., Kusch R.C., Chivers D.P. Epidermal club cells and the innate immune system of minnows. Biol J Linn Soc 2009, 98:891-897.
9. Kilemade M., Lyons-Alcantara M., Rose T., Fitzgerald R., Mothersill C. Rainbow trout primary epidermal cell proliferation as an indicator of aquatic toxicity: an invitro/invivo exposure comparison. Aquat Toxicol 2002, 60:43-59.
10. Tsutsui S., Yoshino Y., Matsui S., Nakamura O., Muramoto K., Watanabe T. Isolation of epidermal cells and cDNA cloning of TNF decoy receptor 3 of conger eel, Conger myriaster. Fish Shellfish Immunol 2008, 24:366-371.
11. Gildberg A., Mikkelsen H. Effects of supplementing the feed to Atlantic cod(Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum. Aquaculture 1998, 167:103-113.
12. Gildberg A., Mikkelsen H., Sandaker E., Ringø E. Probiotic effect of lactic acid bacteria in the feed on growth and survival of fry of Atlantic cod (Gadus morhua). Asia-Pacific conference on science and management of coastal environment 1997, 279-285. Springer, Netherlands. Y.-S. Wong, N.-Y. Tam (Eds.).
13. Verschuere L., Rombaut G., Sorgeloos P., Verstraete W. Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 2000, 64:655-671.
14. Lauzon H.L., Gudmundsdottir S., Pedersen M.H., Budde B.B., Gudmundsdottir B.K. Isolation of putative probionts from cod rearing environment. Vet Microbiol 2008, 132:328-339.
15. Caipang C.M.A., Brinchmann M.F., Kiron V. Antagonistic activity of bacterial isolates from intestinal microbiota of Atlantic cod, Gadus morhua, and an investigation of their immunomodulatory capabilities. Aquacult Res 2010, 41:249-256.
16. Fjellheim A.J., Klinkenberg G., Skjermo J., Aasen I.M., Vadstein O. Selection of candidate probionts by two different screening strategies from Atlantic cod (Gadus morhua L.) larvae. Vet Microbiol 2010, 144:153-159.
17. Lazado C., Caipang C., Gallage S., Brinchmann M., Kiron V. Responses of Atlantic cod Gadus morhua head kidney leukocytes to phytase produced by gastrointestinal-derived bacteria. Fish Physiol Biochem 2010, 36:883-891.
18. Lazado C.C., Caipang C.M.A., Rajan B., Brinchmann M.F., Kiron V. Characterization of GP21 and GP12: two potential probiotic bacteria isolated from the gastrointestinal tract of Atlantic cod. Probiot Antimicrob Proteins 2010, 2:126-134.
19. Lazado C.C., Caipang C.M.A., Kiron V. Enzymes from the gut bacteria of Atlantic cod, Gadus morhua and their influence on intestinal enzyme activity. Aquacult Nutr 2012, 18:423-431.
20. Lazado C.C., Caipang C.M.A., Brinchmann M.F., Kiron V. Invitro adherence of two candidate probiotics from Atlantic cod and their interference with the adhesion of two pathogenic bacteria. Vet Microbiol 2011, 148:252-259.
21. Lazado C.C., Caipang C.M.A., Gallage S., Brinchmann M.F., Kiron V. Expression profiles of genes associated with immune response and oxidative stress in Atlantic cod, Gadus morhua head kidney leukocytes modulated by live and heat-inactivated intestinal bacteria. Comp Biochem Physiol - B Biochem Mol Biol 2010, 155:249-255.
22. Caipang C.M.A., Lazado C.C., Brinchmann M.F., Rombout J.H.W.M., Kiron V. Differential expression of immune and stress genes in the skin of Atlantic cod (Gadus morhua). Comp Biochem Physiol - Part D: Genomics Proteomics 2011, 6:158-162.
23. Rajan B., Fernandes J.M.O., Caipang C.M.A., Kiron V., Rombout J.H.W.M., Brinchmann M.F. Proteome reference map of the skin mucus of Atlantic cod (Gadus morhua) revealing immune competent molecules. Fish Shellfish Immunol 2011, 31:224-231.
24. Caipang C.M.A., Hynes N., Puangkaew J., Brinchmann M.F., Kiron V. Intraperitoneal vaccination of Atlantic cod, Gadus morhua with heat-killed Listonella anguillarum enhances serum antibacterial activity and expression of immune response genes. Fish Shellfish Immunol 2008, 24:314-322.
25. Quade M.J., Roth J.A. Arapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 1997, 58:239-248.
26. Caipang C.M.A., Brinchmann M.F., Kiron V. Profiling gene expression in the spleen of Atlantic cod, Gadus morhua upon vaccination with Vibrio anguillarum antigen. Comp Biochem Physiol - B Biochem Mol Biol 2009, 153:261-267.
27. Caipang C.M.A., Lazado C.C., Brinchmann M.F., Kiron V. Infection-induced changes in expression of antibacterial and cytokine genes in the gill epithelial cells of Atlantic cod, Gadus morhua during incubation with bacterial pathogens. Comp Biochem Physiol - B Biochem Mol Biol 2010, 156:319-325.
28. Caipang C.M.A., Lazado C.C., Brinchmann M.F., Kiron V. Transcription of selected immune-related genes in spleen cells of cod, Gadus morhua following incubation with alginic acid and β-glucan. JExp Mar Biol Ecol 2012, 416-417:202-207.
29. Olafsdottir S.H., Buchmann K. Dexamethasone treatment affects skin mucous cell density in Gyrodactylus derjavini infected Salmo salar. JHelminthol 2004, 78:87-90.
30. Harris J.E., Hunt S. The fine structure of the epidermis of two species of salmonid fish, the Atlantic salmon (Salmo salar L.) and the brown trout (Salmo trutta L.). Cell Tissue Res 1975, 163:535-543.
31. Easy R.H., Ross N.W. Changes in Atlantic salmon (Salmo salar) epidermal mucusprotein composition profiles following infection with sea lice (Lepeophtheirus salmonis). Comp Biochem Physiol Part D: Genomics Proteomics 2009, 4:159-167.
32. Grassmé H., Jendrossek V., Gulbins E. Molecular mechanisms of bacteria induced apoptosis. Apoptosis 2001, 6:441-445.
33. Sepulcre M.P., Sarropoulou E., Kotoulas G., Meseguer J., Mulero V. Vibrio anguillarum evades the immune response of the bony fish sea bass (Dicentrarchus labrax L.) through the inhibition of leukocyte respiratory burst and down-regulation of apoptotic caspases. Mol Immunol 2007, 44:3751-3757.
34. Swain P., Dash S., Sahoo P.K., Routray P., Sahoo S.K., Gupta S.D., et al. Non-specific immune parameters of brood Indian major carp Labeo rohita and their seasonal variations. Fish Shellfish Immunol 2007, 22:38-43.
35. Levy O. Antimicrobial proteins and peptides: anti-infective molecules of mammalian leukocytes. JLeukoc Biol 2004, 76:909-925.
36. Solstad T., Stenvik J., Jørgensen T.Ø. mRNA expression patterns of the BPI/LBP molecule in the Atlantic cod (Gadus morhua L. Fish Shellfish Immunol 2007, 23:260-271.
37. Ruangsri J., Fernandes J.M.O., Brinchmann M., Kiron V. Antimicrobial activity in the tissues of Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol 2010, 28:879-886.
38. Gonzalez S.F., Buchmann K., Nielsen M.E. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish Shellfish Immunol 2007, 22:641-650.
39. Gonzalez S.F., Huising M.O., Stakauskas R., Forlenza M., Lidy Verburg-van Kemenade B.M., Buchmann K., et al. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: inflammatory responses to injury mimicking infection with ectoparasites. Develop Comp Immunol 2007, 31:244-254.
40. Secombes C.J., Wang T., Hong S., Peddie S., Crampe M., Laing K.J., et al. Cytokines and innate immunity of fish. Develop Comp Immunol 2001, 25:713-723.
41. Seppola M., Robertsen B., Jensen I. The gene structure and expression of the non-specific cytotoxic cell receptor protein (NCCRP-1) in Atlantic cod (Gadus morhua L.). Comp Biochem Physiol - B Biochem Mol Biol 2007, 147:199-208.
42. Wernersson S., Reimer J.M., Poorafshar M., Karlson U., Wermenstam N., Bengtén E., et al. Granzyme-like sequences in bony fish shed light on the emergence of hematopoietic serine proteases during vertebrate evolution. Develop Comp Immunol 2006, 30:901-918.
43. Mohapatra S., Chakraborty T., Kumar V., Deboeck G., Mohanta K.N. Aquaculture and stress management: a review of probiotic intervention. JAnim Physiol Anim Nutr 2013, 97:405-430.