Differential regulation of cathelicidin in salmon and cod

Fish and Shellfish Immunology

Volumn 35, Issue 2, 2013, Pages 532-538

  Broekman, Daniela C ^a   Gudmundsson, Gudmundur H ^a   Maier, Valerie H ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

Author keywords

AMP; Cathelicidin; Cell culture; Cell signalling; ECP; Gene expression; H; Innate immunity; P.s.; PAMPs; PI3K; TLR

Indexed keywords

GADIFORMES; MAMMALIA; SALMONIDAE; VERTEBRATA;

EID: 84880041179     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.05.005     Document Type: Article

References (78)

1. Maroti G., Kereszt A., Kondorosi E., Mergaert P. Natural roles of antimicrobial peptides in microbes, plants and animals. Res Microbiol 2011, 162:363-374.
2. Boman H.G. Antibacterial peptides: basic facts and emerging concepts. JIntern Med 2003, 254:197-215.
3. Ganz T. The role of antimicrobial peptides in innate immunity. Integr Comp Biol 2003, 43:300-304.
4. Zanetti M. The role of cathelicidins in the innate host defenses of mammals. Curr Issues Mol Biol 2005, 7:179-196.
5. Palffy R., Gardlik R., Behuliak M., Kadasi L., Turna J., Celec P. On the physiology and pathophysiology of antimicrobial peptides. Mol Med 2009, 15:51-59.
6. Lai Y., Gallo R.L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 2009, 30:131-141.
7. Bridle A., Nosworthy E., Polinski M., Nowak B. Evidence of an antimicrobial-immunomodulatory role of Atlantic salmon cathelicidins during infection with Yersinia ruckeri. PLoS One 2011, 6:e23417.
8. Pan C.Y., Wu J.L., Hui C.F., Lin C.H., Chen J.Y. Insights into the antibacterial and immunomodulatory functions of the antimicrobial peptide, epinecidin-1, against Vibrio vulnificus infection in zebrafish. Fish Shellfish Immunol 2011, 31:1019-1025.
9. Jia X., Patrzykat A., Devlin R.H., Ackerman P.A., Iwama G.K., Hancock R.E. Antimicrobial peptides protect coho salmon from Vibrio anguillarum infections. Appl Environ Microbiol 2000, 66:1928-1932.
10. Hsieh J.C., Pan C.Y., Chen J.Y. Tilapia hepcidin (TH)2-3 as a transgene in transgenic fish enhances resistance to Vibrio vulnificus infection and causes variations in immune-related genes after infection by different bacterial species. Fish Shellfish Immunol 2010, 29:430-439.
11. Cunliffe R.N., Mahida Y.R. Expression and regulation of antimicrobial peptides in the gastrointestinal tract. JLeukoc Biol 2004, 75:49-58.
12. Uvell H., Engstrom Y. Amultilayered defense against infection: combinatorial control of insect immune genes. Trends Genet 2007, 23:342-349.
13. Broekman D.C., Frei D.M., Gylfason G.A., Steinarsson A., Jornvall H., Agerberth B., et al. Cod cathelicidin: isolation of the mature peptide, cleavage site characterisation and developmental expression. Dev Comp Immunol 2011, 35:296-303.
14. Chang C.I., Pleguezuelos O., Zhang Y.A., Zou J., Secombes C.J. Identification of a novel cathelicidin gene in the rainbow trout, Oncorhynchus mykiss. Infect Immun 2005, 73:5053-5064.
15. Chang C.I., Zhang Y.A., Zou J., Nie P., Secombes C.J. Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Antimicrobial Agents Chemother 2006, 50:185-195.
16. Lu X.J., Chen J., Huang Z.A., Shi Y.H., Lv J.N. Identification and characterization of a novel cathelicidin from ayu, Plecoglossus altivelis. Fish Shellfish Immunol 2011, 31:52-57.
17. Maier V.H., Schmitt C.N., Gudmundsdottir S., Gudmundsson G.H. Bacterial DNA indicated as an important inducer of fish cathelicidins. Mol Immunol 2008, 45:2352-2358.
18. Solstad T., Larsen A.N., Seppola M., Jorgensen T.O. Identification, cloning and expression analysis of a hepcidin cDNA of the Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol 2008, 25:298-310.
19. Casadei E., Wang T., Zou J., Gonzalez Vecino J.L., Wadsworth S., Secombes C.J. Characterization of three novel beta-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss). Mol Immunol 2009, 46:3358-3366.
20. Yu F.S., Cornicelli M.D., Kovach M.A., Newstead M.W., Zeng X., Kumar A., et al. Flagellin stimulates protective lung mucosal immunity: role of cathelicidin-related antimicrobial peptide. JImmunol 2010, 185:1142-1149.
21. Menzies B.E., Kenoyer A. Staphylococcus aureus infection of epidermal keratinocytes promotes expression of innate antimicrobial peptides. Infect Immun 2005, 73:5241-5244.
22. Weber G., Heilborn J.D., Chamorro Jimenez C.I., Hammarsjo A., Torma H., Stahle M. Vitamin D induces the antimicrobial protein hCAP18 in human skin. JInvest Dermatol 2005, 124:1080-1082.
23. Schwab M., Reynders V., Shastri Y., Loitsch S., Stein J., Schroder O. Role of nuclear hormone receptors in butyrate-mediated up-regulation of the antimicrobial peptide cathelicidin in epithelial colorectal cells. Mol Immunol 2007, 44:2107-2114.
24. D'Aldebert E., Biyeyeme Bi Mve M.J., Mergey M., Wendum D., Firrincieli D., Coilly A., et al. Bile salts control the antimicrobial peptide cathelicidin through nuclear receptors in the human biliary epithelium. Gastroenterology 2009, 136:1435-1443.
25. Termen S., Tollin M., Rodriguez E., Sveinsdottir S.H., Johannesson B., Cederlund A., et al. PU.1 and bacterial metabolites regulate the human gene CAMP encoding antimicrobial peptide LL-37 in colon epithelial cells. Mol Immunol 2008, 45:3947-3955.
26. Steinmann J., Halldorsson S., Agerberth B., Gudmundsson G.H. Phenylbutyrate induces antimicrobial peptide expression. Antimicrobial Agents Chemother 2009, 53:5127-5133.
27. Perron G.G., Zasloff M., Bell G. Experimental evolution of resistance to an antimicrobial peptide. Proc Biol Sci 2006, 273:251-256.
28. Sarker P., Ahmed S., Tiash S., Rekha R.S., Stromberg R., Andersson J., et al. Phenylbutyrate counteracts Shigella mediated downregulation of cathelicidin in rabbit lung and intestinal epithelia: a potential therapeutic strategy. PLoS One 2011, 6:e20637.
29. Raqib R., Sarker P., Bergman P., Ara G., Lindh M., Sack D.A., et al. Improved outcome in shigellosis associated with butyrate induction of an endogenous peptide antibiotic. Proc Natl Acad Sci U S A 2006, 103:9178-9183.
30. Gudmundsson G.H., Bergman P., Andersson J., Raqib R., Agerberth B. Battle and balance at mucosal surfaces - the story of Shigella and antimicrobial peptides. Biochem Biophys Res Commun 2010, 396:116-119.
31. Yang D., Chertov O., Oppenheim J.J. Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). JLeukoc Biol 2001, 69:691-697.
32. Chromek M., Slamova Z., Bergman P., Kovacs L., Podracka L., Ehren I., et al. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 2006, 12:636-641.
33. Nizet V., Ohtake T., Lauth X., Trowbridge J., Rudisill J., Dorschner R.A., et al. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001, 414:454-457.
34. Lee P.H., Ohtake T., Zaiou M., Murakami M., Rudisill J.A., Lin K.H., et al. Expression of an additional cathelicidin antimicrobial peptide protects against bacterial skin infection. Proc Natl Acad Sci U S A 2005, 102:3750-3755.
35. Uzzell T., Stolzenberg E.D., Shinnar A.E., Zasloff M. Hagfish intestinal antimicrobial peptides are ancient cathelicidins. Peptides 2003, 24:1655-1667.
36. Scocchi M., Pallavicini A., Salgaro R., Bociek K., Gennaro R. The salmonid cathelicidins: a gene family with highly varied C-terminal antimicrobial domains. Comp Biochem Physiol B Biochem Mol Biol 2009, 152:376-381.
37. Maier V.H., Dorn K.V., Gudmundsdottir B.K., Gudmundsson G.H. Characterisation of cathelicidin gene family members in divergent fish species. Mol Immunol 2008, 45:3723-3730.
38. Broekman D.C., Zenz A., Gudmundsdottir B.K., Lohner K., Maier V.H., Gudmundsson G.H. Functional characterization of codCath, the mature cathelicidin antimicrobial peptide from Atlantic cod (Gadus morhua). Peptides 2011, 32:2044-2051.
39. Jensen I., Steiro K., Sommer A.I., Mennen S., Johansen A., Sandaker E.K., et al. Establishing a cell line from Atlantic cod as a novel tool for invitro studies. Fish Shellfish Immunol 2013, 34:199-208.
40. Zhang Z., Louboutin J.P., Weiner D.J., Goldberg J.B., Wilson J.M. Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect Immun 2005, 73:7151-7160.
41. Troyer D.L., Reed A., Oberst D., Chengappa M.M. Arapid and simplified protocol for DNA isolation from bacteria. Vet Res Commun 1990, 14:447-451.
42. Marshall O.J. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 2004, 20:2471-2472.
43. Ingerslev H.C., Pettersen E.F., Jakobsen R.A., Petersen C.B., Wergeland H.I. Expression profiling and validation of reference gene candidates in immune relevant tissues and cells from Atlantic salmon (Salmo salar L.). Mol Immunol 2006, 43:1194-1201.
44. Olsvik P.A., Softeland L., Lie K.K. Selection of reference genes for qRT-PCR examination of wild populations of Atlantic cod Gadus morhua. BMC Res Notes 2008, 1:47.
45. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
46. Whyte S.K. The innate immune response of finfish - a review of current knowledge. Fish Shellfish Immunol 2007, 23:1127-1151.
47. Magnadottir B. Innate immunity of fish (overview). Fish Shellfish Immunol 2006, 20:137-151.
48. Tort L., Balasch J.C., Mackenzie S. Fish immune system. A crossroads between innate and adaptive responses. Inmunología 2003, 22:277-286.
49. Star B., Nederbragt A.J., Jentoft S., Grimholt U., Malmstrom M., Gregers T.F., et al. The genome sequence of Atlantic cod reveals a unique immune system. Nature 2011, 477:207-210.
50. Magnadottir B. Immunological control of fish diseases. Mar Biotechnol (NY) 2010, 12:361-379.
51. Feng C.Y., Johnson S.C., Hori T.S., Rise M., Hall J.R., Gamperl A.K., et al. Identification and analysis of differentially expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonas salmonicida. Physiol Genomics 2009, 37:149-163.
52. Cammarata M., Benenati G., Odom E.W., Salerno G., Vizzini A., Vasta G.R., et al. Isolation and characterization of a fish F-type lectin from gilt head bream (Sparus aurata) serum. Biochim Biophys Acta 2007, 1770:150-155.
53. Boshra H., Wang T., Hove-Madsen L., Hansen J., Li J., Matlapudi A., et al. Characterization of a C3a receptor in rainbow trout and Xenopus: the first identification of C3a receptors in nonmammalian species. JImmunol 2005, 175:2427-2437.
54. Sha Z., Abernathy J.W., Wang S., Li P., Kucuktas H., Liu H., et al. NOD-like subfamily of the nucleotide-binding domain and leucine-rich repeat containing family receptors and their expression in channel catfish. Dev Comp Immunol 2009, 33:991-999.
55. Aoki T., Takano T., Santos M.D., Kondo H., Hirono I. Molecular innate immunity in teleost fish: review and future perspectives. Fisheries for global welfare and environment, 5th world fisheries congress 2008 2008, 263-276. TERRAPUB. K. Tsukamoto, T. Kawamura, T. Takeuchi, T.D. Beard, M.J. Kaiser (Eds.).
56. Purcell M.K., Smith K.D., Hood L., Winton J.R., Roach J.C. Conservation of Toll-like receptor signaling pathways in teleost fish. Comp Biochem Physiol Part D Genomics Proteomics 2006, 1:77-88.
57. Palti Y. Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 2011, 35:1263-1272.
58. Coscia M.R., Giacomelli S., Oreste U. Toll-like receptors: an overview from invertebrates to vertebrates. Invertebr Surviv J 2011, 8:210-226.
59. Zhang J., Liu S., Rajendran K.V., Sun L., Zhang Y., Sun F., et al. Pathogen recognition receptors in channel catfish: III Phylogeny and expression analysis of Toll-like receptors. Dev Comp Immunol 2013, 40:185-194.
60. Laing K.J., Purcell M.K., Winton J.R., Hansen J.D. Agenomic view of the NOD-like receptor family in teleost fish: identification of a novel NLR subfamily in zebrafish. BMC Evol Biol 2008, 8:42.
61. Zhao Y., Yang J., Shi J., Gong Y.N., Lu Q., Xu H., et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011, 477:596-600.
62. Shewring D.M., Zou J., Corripio-Miyar Y., Secombes C.J. Analysis of the cathelicidin 1 gene locus in Atlantic cod (Gadus morhua). Mol Immunol 2011, 48:782-787.
63. Jensen I., Larsen R., Robertsen B. An antiviral state induced in Chinook salmon embryo cells (CHSE-214) by transfection with the double-stranded RNA poly I: C. Fish Shellfish Immunol 2002, 13:367-378.
64. Jorgensen J.B., Johansen A., Hegseth M.N., Zou J., Robertsen B., Collet B., et al. Arecombinant CHSE-214 cell line expressing an Mx1 promoter-reporter system responds to both interferon type I and type II from salmonids and represents a versatile tool to study the IFN-system in teleost fish. Fish Shellfish Immunol 2007, 23:1294-1303.
65. Rebl A., Goldammer T., Seyfert H.M. Toll-like receptor signaling in bony fish. Vet Immunol Immunopathol 2010, 134:139-150.
66. Sepulcre M.P., Alcaraz-Perez F., Lopez-Munoz A., Roca F.J., Meseguer J., Cayuela M.L., et al. Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-kappaB activation. JImmunol 2009, 182:1836-1845.
67. Iliev D.B., Roach J.C., Mackenzie S., Planas J.V., Goetz F.W. Endotoxin recognition: in fish or not in fish?. FEBS Lett 2005, 579:6519-6528.
68. Ringo E., Gatesoupe F.-J. Lactic acid bacteria in fish: a review. Aquaculture 1997, 160:177-203.
69. Balcazar J.L., de Blas I., Ruiz-Zarzuela I., Cunningham D., Vendrell D., Muzquiz J.L. The role of probiotics in aquaculture. Vet Microbiol 2006, 114:173-186.
70. Fukao T., Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol 2003, 24:358-363.
71. Yu Y., Nagai S., Wu H., Neish A.S., Koyasu S., Gewirtz A.T. TLR5-mediated phosphoinositide 3-kinase activation negatively regulates flagellin-induced proinflammatory gene expression. JImmunol 2006, 176:6194-6201.
72. Hazeki K., Nigorikawa K., Hazeki O. Role of phosphoinositide 3-kinase in innate immunity. Biol Pharm Bull 2007, 30:1617-1623.
73. Fuentes E.N., Bjornsson B.T., Valdes J.A., Einarsdottir I.E., Lorca B., Alvarez M., et al. IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways invivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. Am J Physiol Regul Integr Comp Physiol 2011, 300:R1532-R1542.
74. Hazeki K., Kinoshita S., Matsumura T., Nigorikawa K., Kubo H., Hazeki O. Opposite effects of wortmannin and 2-(4-morpholinyl)-8-phenyl-1(4H)-benzopyran-4-one hydrochloride on toll-like receptor-mediated nitric oxide production: negative regulation of nuclear factor-{kappa}B by phosphoinositide 3-kinase. Mol Pharmacol 2006, 69:1717-1724.
75. Helms J.B., Rothman J.E. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 1992, 360:352-354.
76. Zieve G.W., Turnbull D., Mullins J.M., McIntosh J.R. Production of large numbers of mitotic mammalian cells by use of the reversible microtubule inhibitor nocodazole. Nocodazole accumulated mitotic cells. Exp Cell Res 1980, 126:397-405.
77. He Y., Xu Y., Zhang C., Gao X., Dykema K.J., Martin K.R., et al. Identification of a lysosomal pathway that modulates glucocorticoid signaling and the inflammatory response. Sci Signal 2011, 4:ra44.
78. Yasuda H., Leelahavanichkul A., Tsunoda S., Dear J.W., Takahashi Y., Ito S., et al. Chloroquine and inhibition of Toll-like receptor 9 protect from sepsis-induced acute kidney injury. Am J Physiol Renal Physiol 2008, 294:F1050-F1058.