Genomic survey of early responses to viruses in Atlantic salmon, Salmo salar L.

Molecular Immunology

Volumn 49, Issue 1-2, 2011, Pages 163-174

  Krasnov, Aleksei ^a   Timmerhaus, Gerrit ^a,b   Schiøtz, Berit Lyng ^a   Torgersen, Jacob ^a   Afanasyev, Sergey ^a,c   Iliev, Dimitar ^d   Jørgensen, Jorunn ^d   Takle, Harald ^a,e   Jørgensen, Sven Martin ^a  

^a NOFIMA   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^d UNIVERSITY OF TROMSØ   (Norway)

^e AVS Chile SA Casilla 300 ^*  (Chile)

Author keywords

Atlantic salmon; Immune cytochemistry; Immunogenomics; Oligonucleotide microarray; Virus

Indexed keywords

ALPHA INTERFERON; BACTERIAL DNA; CHEMOKINE RECEPTOR CCR10; DOUBLE STRANDED RNA; GIG1 PROTEIN; GIG2 PROTEIN; PROTEIN; PROTEOME; RETINOIC ACID INDUCIBLE PROTEIN I; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; ATLANTIC SALMON; CARDIOMYOPATHY; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC MARKER; GENETIC VARIABILITY; HEART; IMMUNOFLUORESCENCE TEST; LEUKOCYTE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; TELEOST; VIRUS GENE; VIRUS INFECTION; VIRUS LOAD; VIRUS RESPONSIVE GENE;

ANIMALS; BASE SEQUENCE; FISH DISEASES; FISH PROTEINS; GENE EXPRESSION PROFILING; GENOME; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMO SALAR; VIRUS DISEASES;

BACTERIA (MICROORGANISMS); CYPRINIDAE; MAMMALIA; SALMO SALAR; SALMONIDAE; TELEOSTEI; TETRAPODA; VERTEBRATA;

EID: 82455179451     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.08.007     Document Type: Article

References (49)

1. Amin A.B., Trasti J. Endomyocarditis in Atlantic salmon in Norwegian sea farms. Bull. Eur. Assoc. Fish. Pathol. 1988, 8:70-71.
2. Biacchesi S., LeBerre M., Lamoureux A., Louise Y., Lauret E., Boudinot P., Brémont M. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol. 2009, 83:7815-7827.
3. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
4. Chawla-Sarkar M., Lindner D.J., Liu Y.F., Williams B.R., Sen G.C., Silverman R.H., Borden E.C. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003, 8:237-249.
5. Chin K.C., Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:15125-15130.
6. da Silva R.P., Platt N., de Villiers J.S., Gordon S. Membrane molecules and macrophage endocytosis: scavenger receptor and macrosialin as markers of plasma-membrane and vacuolar functions. Biochem. Soc. Trans. 1996, 24:220-224.
7. Du Pasquier L. Fish 'n' TRIMs. J. Biol. 2009, 8:50.
8. Ghazal P., González Armas J.C., García-Ramírez J.J., Kurz S., Angulo A. Viruses: hostages to the cell. Virology 2000, 275:233-237.
9. Haugland O., Mikalsen A.B., Nilsen P., Lindmo K., Thu B.J., Eliassen T.M., Roos N., Rode M., Evensen O. Cardiomyopathy syndrome of Atlantic salmon (Salmo salar L.) is caused by a dsRNA virus of the Totiviridae family. J. Virol. 2011, 85:5275-5286.
10. Iliev D.B., Jørgensen S.M., Rode M., Krasnov A., Harneshaug I., Jørgensen J.B. CpG-induced secretion of MHCII-beta and exosomes from salmon (Salmo salar) APCs. Dev. Comp. Immunol. 2010, 34:29-41.
11. Jennings L.K., Crossno J.T., Fox C.F., White M.M., Green C.A. Platelet p24/CD9, a member of the tetraspanin family of proteins. Ann. N.Y. Acad. Sci. 1994, 714:175-184.
12. Jorgensen S.M., Afanasyev S., Krasnov A. Gene expression analyses in Atlantic salmon challenged with infectious salmon anemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 2008, 9:179.
13. Kileng Ø., Brundtland M.I., Robertsen B. Infectious salmon anemia virus is a powerful inducer of key genes of the type I interferon system of Atlantic salmon, but is not inhibited by interferon. Fish Shellfish Immunol. 2007, 23:378-389.
14. Kongtorp R.T., Taksdal T., Lyngøy A. Pathology of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar. Dis. Aquat. Organ. 2004, 59:217-224.
15. Kongtorp R.T., Taksdal T. Studies with experimental transmission of heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L. J. Fish Dis. 2009, 32:253-362.
16. Krasnov A., Timmerhaus G., Afanasyev S., Jørgensen S.M. Development and assessment of oligonucleotide microarrays for Atlantic salmon (Salmo salar L.). Comp. Biochem. Physiol. D: Genomics Proteomics 2011, 6:31-38.
17. López-Muñoz A., Sepulcre M.P., Roca F.J., Figueras A., Meseguer J., Mulero V. Evolutionary conserved pro-inflammatory and antigen presentation functions of zebrafish IFNγ revealed by transcriptomic and functional analysis. Mol. Immunol. 2011, 48:1073-1083.
18. MacMicking J.D. IFN-inducible GTPases and immunity to intracellular pathogens. Trends Immunol. 2004, 25:601-609.
19. Magder S., Neculcea J., Neculcea V., Sladek R. Lipopolysaccharide and TNF-alpha produce very similar changes in gene expression in human endothelial cells. J. Vasc. Res. 2006, 43:447-461.
20. O'Farrell C., Vaghefi N., Cantonnet M., Buteau B., Boudinot P., Benmansour A. Survey of transcript expression in rainbow trout leukocytes reveals a major contribution of interferon-responsive genes in the early response to a rhabdovirus infection. J. Virol. 2002, 76:8040-8049.
21. Ooi E.L., Verjan N., Haraguchi I., Oshima T., Kondo H., Hirono I., Aoki T., Kiyono H., Yuki Y. Innate immunomodulation with recombinant interferon-alpha enhances resistance of rainbow trout (Oncorhynchus mykiss) to infectious hematopoietic necrosis virus. Dev. Comp. Immunol. 2008, 32:1211-1220.
22. Palacios G., Lovoll M., Tengs T., Hornig M., Hutchison S., Hui J., Kongtorp R.T., Savji N., Bussetti A.V., Solovyov A., Kristoffersen A.B., Celone C., Street C., Trifonov V., Hirschberg D.L., Rabadan R., Egholm M., Rimstad E., Lipkin W.I. Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS One 2010, 5:e11487.
23. Parfitt D.A., Michael G.J., Vermeulen E.G., Prodromou N.V., Webb T.R., Gallo J.M., Cheetham M.E., Nicoll W.S., Blatch G.L., Chapple J.P. The ataxia protein sacsin is a functional co-chaperone that protects against polyglutamine-expanded ataxin-1. Hum. Mol. Genet. 2009, 18:1556-1565.
24. Park K., Scott A.L. Cholesterol 25-hydroxylase production by dendritic cells and macrophages is regulated by type I interferons. J. Leukoc. Biol. 2010, 88:1081-1087.
25. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
26. Piron M., Vende P., Cohen J., Poncet D. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 1998, 17:5811-5821.
27. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 2006, 20:172-191.
28. Robertsen B. Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol. 2008, 25:351-357.
29. Røkenes 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.
30. Sabini E., Ort S., Monnerjahn C., Konrad M., Lavie A. Structure of human dCK suggests strategies to improve anticancer and antiviral therapy. Nat. Struct. Biol. 2003, 10:513-519.
31. Sakamoto H., Kinjyo I., Yoshimura A. The janus kinase inhibitor, Jab/SOCS-1, is an interferon-gamma inducible gene and determines the sensitivity to interferons. Leuk. Lymphoma 2000, 38:49-58.
32. Samal B., Sun Y., Stearns G., Xie C., Suggs S., McNiece I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol. Cell. Biol. 1994, 14:1431-1437.
33. Sarkar D., Desalle R., Fisher P.B. Evolution of MDA-5/RIG-I-dependent innate immunity: independent evolution by domain grafting. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17040-17045.
34. Schiøtz B.L., Jorgensen S.M., Rexroad C.R., Gjøen T., Krasnov A. Transcriptomic analysis of responses to infectious salmon anemia virus infection in macrophage-like cells. Virus Res. 2008, 136:65-74.
35. Shin A., Toy T., Rothenfusser S., Robson N., Vorac J., Dauer M., Stuplich M., Endres S., Cebon J., Maraskovsky E., Schnurr M. P2Y receptor signaling regulates phenotype and IFN-alpha secretion of human plasmacytoid dendritic cells. Blood 2008, 111:3062-3069.
36. Schröder M., Bowie A.G. TLR3 in antiviral immunity: key player or bystander?. Trends Immunol. 2005, 26:462-468.
37. Segura-Totten M., Wilson K.L. BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol. 2004, 14:261-266.
38. Skjesol A., Skjæveland I., Elnæs M., Timmerhaus G., Fredriksen B.N., Jørgensen S.M., Krasnov A., Jørgensen J. IPNV with high and low virulence: host immune responses and viral mutations during infection. Virol. J. 2011, 8:396.
39. Stein C., Caccamo M., Laird G., Leptin M. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 2007, 8:R251.
40. Sun B., Robertsen B., Wang Z., Liu B. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 2009, 33:547-558.
41. Tadiso T., Krasnov A., Skugor S., Afanasyev S., Hordvik I., Nilsen F. Gene expression analyses of immune responses in Atlantic salmon during early stages of infection by salmon louse (Lepeophtheirus salmonis) revealed bi-phasic responses coinciding with the copepod-chalimus transition. BMC Genomics 2011, 12:141.
42. van der Aa L.M., Levraud J.P., Yahmi M., Lauret E., Briolat V., Herbomel P., Benmansour A., Boudinot P. A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biol. 2009, 7:7.
43. Verrier, E.R., Langevin, C., Benmansour, A., Boudinot, P. Early antiviral response andvirus-induced genes in fish. Dev. Comp. Immunol., in press.
44. Wagner H. Interactions between bacterial CpG-DNA and TLR9 bridge innate and adaptive immunity. Curr. Opin. Microbiol. 2002, 5:62-99.
45. Workenhe S.T., Hori T.S., Rise M.L., Kibenge M.J., Kibenge F.S. Infectious salmon anaemia virus (ISAV) isolates induce distinct gene expression responses in the Atlantic salmon (Salmo salar) macrophage/dendritic-like cell line TO, assessed using genomic techniques. Mol. Immunol. 2009, 46:2955-2974.
46. Yang C., Su J., Huang T., Zhang R., Peng L. Identification of a retinoic acid-inducible gene I from grass carp (Ctenopharyngodon idella) and expression analysis in vivo and in vitro. Fish Shellfish Immunol. 2011, 30:936-943.
47. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale M., Akira S., Yonehara S., Kato A., Fujita T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175:2851-2858.
48. Zhang Y.B., Gui J.F. Identification of two novel interferon-stimulated genes from cultured CAB cells induced by UV-inactivated grass carp hemorrhage virus. Dis. Aquat. Organ. 2004, 60:1-9.
49. Zou J., Chang M., Nie P., Secombes C.J. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol. Biol. 2009, 9:85.