Transcriptomic analysis of the host response to early stage salmonid alphavirus (SAV-1) infection in Atlantic salmon Salmo salar L.

Fish and Shellfish Immunology

Volumn 32, Issue 5, 2012, Pages 796-807

  Herath, Tharangani K ^a   Bron, James E ^a   Thompson, Kim D ^a   Taggart, John B ^a   Adams, Alexandra ^a   Ireland, Jacqueline H ^a   Richards, Randolph H ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Atlantic salmon; Host response; Salmonid alphavirus 1 (SAV 1); Transcriptomic analysis

Indexed keywords

ALPHAVIRUS; MAMMALIA; SALMO SALAR; SALMONIDAE; TOGAVIRIDAE;

EID: 84858339239     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2012.02.001     Document Type: Article

References (64)

1. Abbas A.K., Lichtman A.H., Pober J.S. Cellular and molecular immunology 2000, W. B Saunders Company, United States of America. 4th ed.
2. Barber G.N. Host defense, virus and apoptosis. Cell Death Differ 2001, 8:113-126.
3. Barry G., Breakwell L., Fragkoudis R., Attarzadeh-Yazdi G., Rodriguez-Andres J., Kohl A., et al. PKR act early in infection to suppress Semliki forest virus production and strongly enhances the type I interferon response. J Gen Virol 2009, 90:1382-1391.
4. Bick M.J., Carroll J.W.N., Gao G.X., Goff S.P., Rice C.M., MacDonald M.R. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J Virol 2003, 77:11555-11562.
5. Boudinot P., Massin P., Blanco M., Riffault S., Benmansour A. Vig-1, a new fish gene induced by the rhabdovirus glycoprotein, has a virus-induced homologue in humans and shares conserved motifs with the MoaA family. J Virol 1999, 73:1846-1852.
6. Boudinot P., Salhi S., Blanco M., Benmansour A. Viral haemorrhagic septicaemia virus induces Vig-2, a new interferon responsive gene in rainbow trout. Fish Shellfish Immun 2001, 11:383-397.
7. Byon J.Y., Ohira T., Hirono I., Aoki T. Use of a cDNA microarray to study immunity against viral hemorrhagic septicemia (VHS) in Japanese flounder (Paralichthys olivaceus) following DNA vaccination. Fish Shellfish Immun 2005, 18:135-147.
8. Cummings C.A., Relman D.A. Using DNA microarrays to study host-microbe interactions. Emerg Infect Dis 2000, 6:513-525.
9. Desvignes L., Quentel C., Lamour F., Le Ven A. Pathogenesis and immune response in Atlantic salmon (Salmo salar L.) parr experimentally infected with salmon pancreas disease virus (SPDV). Fish Shellfish Immun 2002, 12:77-95.
10. Ellis A.E. Innate host defense mechanisms of fish against viruses and bacteria. Dev Com Immun 2001, 25:827-839.
11. Everette H., McFadden G. Apoptosis: an innate immune response to virus infection. Trends Microbiol 1999, 7:160-165.
12. Ferguson H.W. Systemic pathology of fish; a text and atlas of normal tissue in teleosts and their response in disease 2006, Scotian Press, Windsor Avenue, London, UK. 2nd ed.
13. Fischer U., Utke K., Somamoto T., Kollner B., Ototake M., Nakanishi T. Cytotoxic activities of fish leucocytes. Fish Shellfish Immun 2006, 20:209-226.
14. Fringuelli E., Rowley H.M., Wilson J.C., Hunter R., Rodger H., Graham D.A. Phylogenetic analyses and molecular epidemiology of European salmonid alphaviruses (SAV) based on partial E2 and nsP3 gene nucleotide sequences. J Fish Dis 2008, 31:811-823.
15. Gahlawat S.K., Ellis A.E., Collet B. Expression of interferon and interferon - induced genes in Atlantic salmon Salmo salar cell lines SHK-1 and TO following infection with salmon alphavirus SAV. Fish Shellfish Immun 2009, 26:672-675.
16. Graham D.A., Jewhurst V.A., Rowley H.M., McLoughlin M.F., Todd D. A rapid immunoperoxidase-based virus neutralization assay for salmonid alphavirus used for a serological survey in Northern Ireland. J Fish Dis 2003, 26:407-413.
17. Graham D.A., Jewhurst V.A., Rowley H.M., McLoughlin M.F., Rodger H., Todd D. Longitudinal serological surveys of Atlantic salmon, Salmo salar L., using a rapid immunoperoxidase-based neutralization assay for salmonid alphavirus. J Fish Dis 2005, 28:373-379.
18. Graham D., McLoughlin M., Norris A., McPhee J., Matthews D., Foyle L., et al. Virological, serological and histopathological evaluation of fish strain susceptibility to experimental infection with salmonid alphavirus. Res Vet Sci 2005, 78:22.
19. Graham D.A., Taylor C., Rodgers D., Weston J., Khalili M., Ball N., et al. Development and evaluation of a one-step real-time reverse transcription polymerase chain reaction assay for the detection of salmonid alphaviruses in serum and tissues. Dis Aquat Organ 2006, 70:47-54.
20. Haller O., Staeheli P., Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 2007, 89:812-818.
21. Haller O., Stertz S., Kochs G. The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infec 2007, 9:1636-1643.
22. Hampel M., Alonso E., Aparicio I., Bron J.E., Santos J.L., Taggart J.B., et al. Potential physiological effects of pharmaceutical compounds in Atlantic salmon (Salmo salar) implied by transcriptomic analysis. Environ Sci Pollut R 2010, 17:917-933.
23. Hardwick J.M. Apoptosis in viral pathogenesis. Cell Death Differ 2001, 8:109-110.
24. Herath T., Costa J., Thompson K., Adams A., Richards R. Alternative cell lines for the isolation of salmonid Alphavirus-1. Ice Agri Sci 2009, 22:19-27.
25. Hodneland K., Bratland A., Christie K.E., Endresen C., Nylund A. New subtype of salmonid alphavirus (SAV), Togaviridae, from Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss in Norway. Dis Aquat Organ 2005, 66:113-120.
26. Hodneland K., Endresen C. Sensitive and specific detection of Salmonid alphavirus using real-time PCR (TaqMan (R). J Virol Methods 2006, 131:184-192.
27. Houston R.D., Gheyas A., Hamilton A., Guy D.R., Tinch A.E., Taggart J.B., et al. Detection and confirmation of a major QTL affecting resistance to infectious pancreatic necrosis (IPN) in Atlantic Salmon (Salmo salar). Anim Genomics Anim Health 2008, 132:199-204.
28. Jorgensen S.M., Afanasyev S., Krasnov A. Gene expression analyses in Atlantic salmon challenged with infectious salmon anaemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 2008, 9:179. 10.1186/1471-2164-9-179.
29. Korth M.J., Katze M.G. Unlocking the mysteries of virus-host interactions - does functional genomics hold the key?. Microarrays, Immune Responses and Vaccines 2002, 975:160-168.
30. Krasnov A., Koskinen H., Afanasyev S., Molsa H. Transcribed Tcl-like transposons in salmonid fish. BMC Genomics 2005, 6:107. 10.1186/1471-2164-6-107.
31. Leaver M.J., Villeneuve L.A.N., Obach A., Jensen L., Bron J.E., Tocher D.R., et al. Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 2008, 9:299. 10.1186/1471-2164-9-299.
32. Lin O.E., Ohira T., Hirono I., Saito-Taki T., Aoki T. Immunoanalysis of antiviral Mx protein expression in Japanese flounder (Paralichthys olivaceus) cells. Dev Comp Immunol 2005, 29:443-455.
33. MacDonald M.R., Machlin E.S., Albin O.R., Levy D.E. The zinc finger antiviral protein acts synergistically with an interferon-induced factor for maximal activity against Alphaviruses. J Virol 2007, 81:13509-13518.
34. MacKenzie S., Iliev D., Liarte C., Koskinen H., Planas J.V., Goetz F.W., et al. Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol Immunol 2006, 43:1340-1348.
35. Martin S.A.M., Blaney S.C., Houlihan D.F., Secombes C.J. Transcriptome response following administration of a live bacterial vaccine in Atlantic salmon (Salmo salar). Mol Immunol 2006, 43:1900-1911.
36. McLoughlin M., Nelson R., McCormick J.I., Rowley H. Pathology of experimental pancreas disease in freshwater Atlantic salmon parr. J Aquat Anim Health 1995, 7:104-110.
37. McLoughlin M.F., Graham D.A. Alphavirus infections in salmonids - a review. J Fish Dis 2007, 30:511-531.
38. McLoughlin M.F., Nelson R.T., Rowley H.M., Cox D.I., Grant A.N. Experimental pancreas disease in Atlantic salmon Salmo salar post-smolts induced by salmon pancreas disease virus (SPDV). Dis Aquat Organ 1996, 26:117-124.
39. McLoughlin M.F., Rowley H.M., Doherty C.E. A serological survey of salmon pancreas disease virus (SPDV) antibodies in farmed Atlantic salmon, Salmo salar L. J Fish Dis 1998, 21:305-307.
40. Medigeshi G.R., Hirsch A.J., Streblow D.N., Nikolich-Zugich J., Nelson J.A. West Nile virus entry requires cholesterol-rich membrane microdomains and is independent of alpha v beta 3 integrin. J Virol 2008, 82:5212-5219.
41. Miller K., Traxler G., Kaukinen K., Li S., Richard J., Ginther N. Salmonid host response to infectious hematopoietic necrosis (IHN) virus: cellular receptors, viral control, and novel pathways of defence. Aquaculture 2007, 272:S217-S237.
42. Ng C.G., Coppens I., Govindarajan D., Pisciotta J., Shulaev V., Griffin D.E. Effect of host cell lipid metabolism on alphavirus replication, virion morphogenesis, and infectivity. Proc Natl Acad Sci USA 2008, 105:6326-16331.
43. Novova B., MacKenzie S., Figueras A. Inflammation and innate immune response against viral infections in marine fish. Curr Pharm Design 2010, 16:4175-4184.
44. Olsvik P.A., Lie A.K., Mykkeltvedt E., Samuelsen O.B., Petersen K., Stavrum A., et al. Pharmacokinetics and transcriptional effects of the anti-salmon lice drug emamectin benzoate in Atlantic salmon (Salmo salar L.). BMC Pharm 2008, 8:8-16.
45. Pavlidis P. Using ANOVA for gene selection from microarray studies of the nervous system. Methods 2003, 31:282-289.
46. Pfaffl M.W. Relative quantification 2006, 63-82. Real Time PCR.Taylor and Francis, New York. M. Dorak (Ed.).
47. ®) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
48. Philstrom L., Bengten E. Immunoglobulin in fish-genes, expression and structure. Fish Shellfish Immun 1996, 6:243-262.
49. Purcell M.K., Smith K.D., Hood L., Winton J., Roach J.C. Conservation of Toll-like receptor signaling pathways in teleost fish. Com Biochem Phys D 2006, 1:77-88.
50. Rise M.L., Jones S.R.M., Brown G.D., von Schalburg K.R., Davidson W.S., Koop B.F. Microarray analyses identify molecular biomarkers of Atlantic salmon macrophage and hematopoietic kidney response to Piscirickettsia salmonis infection. Physiol Genomics 2004, 20:21-35.
51. Rise M.L., von Schalburg K.R., Brown G.D., Mawer M.A., Devlin R.H., Kuipers N., et al. Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res 2006, 14:478-490.
52. Roberts R.J. Fish pathology 2003, W.B. Saunders Limited, United States of America. 3th Edition.
53. Rokenes T.P., Larsen R., Robertsen B. Atlantic salmon ISG15: expression and conjugation to cellular proteins in response to interferon, double-stranded RNA and virus infections. Mol Immunol 2007, 44:950-959.
54. Segura-Totten M., Wilson K.L. BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol 2004, 14:261-266.
55. Strauss J.H., Strauss E.G. The alphaviruses - gene-expression, replication, and evolution. Microbiol Rev 1994, 58:491-562.
56. Susuki T., Susuki Y. Virus infection and lipid raft. Biol Pharm Bull 2006, 29:1538-1541.
57. Taggart J.B., Bron J.E., Martin S.A.M., Seear P.J., Hoyheim B., Talbot R., et al. A description of the origins, design and performance of the TRAITS-SGP Atlantic salmon Salmo salar L. cDNA microarray. J Fish Biol 2008, 72:2071-2094.
58. Taksdal T., Olsen A.B., Bjerkas I., Hjortaas M.J., Dannevig B.H., Graham D.A., et al. Pancreas disease in farmed Atlantic salmon, Salmo salar L., and rainbow trout, Oncorhynchus mykiss (Walbaum), in Norway. J Fish Dis 2007, 30:545-558.
59. Taylor L.A., Carthy C.M., Yang D.C., Saad K., Wong D., Schreiner G., et al. Host gene regulation during coxsackievirus B3 infection in mice - assessment by microarrays. Circ Rese 2008, 87:328-334.
60. Verrier E.R., Langevin C., Benmansour A., Boudinot P. Early antiviral response and virus-induced genes in fish. Dev. Comp. Immuno 2011, 35:1204-1214.
61. Wengler G., Koschinski A., Wengler G., Dreyer F. Entry of alphaviruses at the plasma membrane converts the viral surface proteins into an ion-permeable pore that can be detected by electrophysiological analyses of whole-cell membrane currents. J Gen Virol 2003, 84:173-181.
62. Xu C., Guo T.C., Mutoloki S., Haugland S., Marjara I.S. Alpha interferon and not gamma interferon inhibits salmonid alphavirus 3 replication in vitro. J Virol 2011, 84:8903-8912.
63. Young N.D., Cooper G.A., Nowak B.F., Koop B.F., Morrison R.N. Coordinated down-regulation of the antigen processing machinery in the gills of amoebic gill disease-affected Atlantic salmon (Salmo salar L.). Mol Immunol 2008, 45:2581-2597.
64. Zhang Y.G., Burke C.W., Rayman K.D., Klimstra W.B. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J Virol 2007, 81:11246-11255.