Interferon type I and type II responses in an Atlantic salmon (Salmo salar) SHK-1 cell line by the salmon TRAITS/SGP microarray

Physiological Genomics

Volumn 32, Issue 1, 2007, Pages 33-44

  Martin, S A M ^a   Taggart, J B ^b   Seear, P ^d   Bron, J E ^b   Talbot, R ^c   Teale, A J ^b   Sweeney, G E ^d   Hoyheim B ^e   Houlihan, D F ^a   Tocher, D R ^b   Zou, J ^a   Secombes, C J ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF STIRLING   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Fish; Immune; Transcriptome

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; INTERFERON; RECOMBINANT INTERFERON;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; DNA MICROARRAY; GENE EXPRESSION; LEUKOCYTE CULTURE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SALMONID;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; CLONING, MOLECULAR; CYTOKINES; DNA, COMPLEMENTARY; INTERFERON TYPE I; INTERFERON TYPE II; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECOMBINANT PROTEINS; SALMO SALAR;

SALMO SALAR; SALMONIDAE;

EID: 37449010560     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00064.2007     Document Type: Article

References (64)

1. Aparicio S, Chapman J, Stupka E, Putnam N, Chia J, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, Gelpke MDS, Roach J, Oh T, Ho IY, Wong M, Detter C, Verhoef F, Predki P, Tay A, Lucas S, Richardson P, Smith SF, Clark MS, Edwards YJK, Doggett N, Zharkikh A, Tavtigian SV, Pruss D, Barnstead M, Evans C, Baden H, Powell J, Glusman G, Rowen L, Hood L, Tan YH, Elgar G, Hawkins T, Venkatesh B, Rokhsar D, Brenner S. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301-1310, 2002.
2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29, 2000.
3. Bird S, Zou J, Savan R, Kono T, Sakai M, Woo J, Secombes C. Characterisation and expression analysis of an interleukin 6 homologue in the Japanese pufferfish, Fugu rubripes. Dev Comp Immunol 29: 775-789, 2005.
4. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-gamma. Annu Rev Immunol 15: 749-795, 1997.
5. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, Gaasterland T, Glenisson P, Holstege FCP, Kim IF, Markowitz V, Matese JC, Parkinson H, Robinson A, Sarkans U, Schulze-Kremer S, Stewart J, Taylor R, Vilo J, Vingron M. Minimum information about a microarray experiment (MIAME) - toward standards for microarray data. Nat Genet 29: 365-371, 2001.
6. Byon JY, 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 Immunol 18: 135-147, 2005.
7. Collet B, Hovens GCJ, Mazzoni D, Hirono I, Aoki T, Secombes CJ. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2). Dev Comp Immunol 27: 111-126, 2003.
8. Collet B, McDonald C, Secombes CJ. The promoter for the Interferon Regulatory Factor (IRF)-2 in the rainbow trout Oncorhynchus mykiss: cloning and reporter gene activity. Fish Shellfish Immunol 15: 473-477, 2003.
9. Collet B, Secombes CJ. The rainbow trout (Oncorhynchus mykiss) Mx1 promoter - structural and functional characterization. Eur J Biochem 268: 1577-1584, 2001.
10. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676, 2005.
11. Dannevig BH, Brudeseth BE, Gjoen T, Rode M, Wergeland HI, Evensen O, Press CM. Characterisation of a long-term cell line (SHK-1) developed from the head kidney of Atlantic salmon (Salmo salar L). Fish Shellfish Immunol 7: 213-226, 1997.
12. Dao CT, Zhang DE. ISG15: a ubiquitin-like enigma. Front Biosci 10: 2701-2722, 2005.
13. Der SD, Zhou AM, Williams BRG, Silverman RH. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95: 15623-15628, 1998.
14. Ewart KV, Belanger JC, Williams J, Karakach T, Penny S, Tsoi SCM, Richards RC, Douglas SE. Identification of genes differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Dev Comp Immunol 29: 333-347, 2005.
15. Froschauer A, Braasch I, Volff JN. Fish genomes, comparative genomics and vertebrate evolution. Curr Genomics 7: 43-57, 2006.
16. Gjermandsen IM, Justesen J, Martensen PM. The interferon-induced gene ISG12 is regulated by various cytokines as the gene 6-16 in human cell lines. Cytokine 12: 233-238, 2000.
17. Gracey AY, Fraser EJ, Li WZ, Fang YX, Taylor RR, Rogers J, Brass A, Cossins AR. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101: 16970-16975, 2004.
18. Haas AL, Ahrens P, Bright PM, Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J Biol Chem 262: 11315-11323, 1987.
19. Hardie LJ, Laing KJ, Daniels GD, Grabowski PS, Cunningham C, Secombes CJ. Isolation of the first piscine transforming growth factor beta gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus mykiss). Cytokine 10: 555-563, 1998.
20. Inagaki Y, Nemoto T, Kushida M, Meng Y, Higashi K, Ikeda K, Kawada N, Shirasaki F, Takehara K, Sugiyama K, Fujii M, Yamauchi H, Nakao A, de Crombrugghe B, Watanabe T, Okazaki I. Interferon alfa down-regulates collagen gene transcription and suppresses experimental hepatic fibrosis in mice. Hepatology 38: 890-899, 2003.
21. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard R, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, de Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Crollius HR. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957, 2004.
22. Kim KI, Yan M, Malakhova O, Luo JK, Shen MF, Zou WG, de la Torre JC, Zhang DE. Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol Cell Biol 26: 472-479, 2006.
23. Kono T, Zou J, Bird S, Savan R, Sakai M, Secombes CJ. Identification and expression analysis of lymphotoxin-beta like homologues in rainbow trout Oncorhynchus mykiss. Mol Immunol 43: 1390-1401, 2006.
24. Koppang EO, Dannevig BH, Lie O, Ronningen K, Press CM. Expression of Mhc class I and II mRNA in a macrophage-like cell line (SHK-1) derived from Atlantic salmon, Salmo salar L., head kidney. Fish Shellfish Immunol 9: 473-489, 1999.
25. Krasnov A, Koskinen H, Afanasyev S, Molsa H. Transcribed Tcl-like transposons in salmonid fish. BMC Genomics 6: 2005.
26. Laing KJ, Bols N, Secombes CJ. A CXC chemokine sequence isolated from the rainbow trout Oncorhynchus mykiss resembles the closely related interferon-gamma-inducible chemokines CXCL9, CXCL10 and CXCL11. Eur Cytokine Netw 13: 462-473, 2002.
27. Laing KJ, Secombes CJ. Trout CC chemokines: comparison of their sequences and expression patterns. Mol Immunol 41: 793-808, 2004.
28. Luster AD, Ravetch JV. Genomic characterization of a gamma-interferon-inducible gene (Ip-10) and identification of an interferon-inducible hypersensitive site. Mol Cell Biol 7: 3723-3731, 1987.
29. MacKenzie S, Iliev D, Liarte C, Koskinen H, Planas JV, Goetz FW, Molsa H, Krasnov A, Tort L. Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol Immunol 43: 1340-1348, 2006.
30. Martin S, Zou J, Houlihan D, Secombes C. Directional responses following recombinant cytokine stimulation of rainbow trout (Oncorhynchus mykiss) RTS-11 macrophage cells as revealed by transcriptome profiling. BMC Genomics 8: 150, 2007.
31. Martin SAM, Blaney SC, Houlihan DF, Secombes CJ. Transcriptome response following administration of a live bacterial vaccine in Atlantic salmon (Salmo salar). Mol Immunol 43: 1900-1911, 2006.
32. McBeath AJA, Snow M, Secombes CJ, Ellis AE, Collet B. Expression kinetics of interferon and interferon-induced genes in Atlantic salmon (Salmo salar) following infection with infectious pancreatic necrosis virus and infectious salmon anaemia virus. Fish Shellfish Immunol 22: 230-241, 2007.
33. Milev-Milovanovic I, Long S, Wilson M, Bengten E, Miller NW, Chinchar VG. Identification and expression analysis of interferon gamma genes in channel catfish. Immunogenetics 58: 70-80, 2006.
34. Morrison RN, Cooper GA, Koop BF, Rise ML, Bridle AR, Adams MB, Nowak BF. Transcriptome profiling the gills of amoebic gill disease (AGD)-affected Atlantic salmon (Salmo salar L.): a role for tumor suppressor p53 in AGD pathogenesis? Physiol Genomics 26: 15-34, 2006.
35. 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 76: 8040-8049, 2002.
36. Olsvik PA, Lie KK, Jordal AEO, Nilsen TO, Hordvik I. Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol 6: 22, 2005.
37. Osaki M, Tan LJ, Choy BK, Yoshida Y, Cheah KSE, Auron PE, Goldring MB. The TATA-containing core promoter of the type II collagen gene (COL2A1) is the target of interferon-gamma-mediated inhibition in human chondrocytes: requirement for Stat1 alpha, Jak1 and Jak2. Biochem J 369: 103-115, 2003.
38. Osiak A, Utermohlen O, Niendorf S, Horak I, Knobeloch KP. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signalling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol Cell Biol 25: 6338-6345, 2005.
39. Pertea G, Huang XQ, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19: 651-652, 2003.
40. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2001.
41. Platanias LC. Mechanisms of type-I- and type-II-interferon- mediated signalling. Nat Rev Immunol 5: 375-386, 2005.
42. Postlethwait JAA, Force A, Yan YL. The zebrafish genome. In: The Zebrafish: Genetics and Genomics. San Diego, CA: Academic, 1999, p. 149-163.
43. Purcell MK, Nichols KM, Winton JR, Kurath G, Thorgaard GH, Wheeler P, Hansen JD, Herwig RP, Park LK. Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol Immunol 43: 2089-2106, 2006.
44. Quackenbush J. Microarray data normalization and transformation. Nat Genet 32: 496-501, 2002.
45. Ramana CV, Gil MP, Schreiber RD, Stark GR. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol 23: 96-101, 2002.
46. Rise ML, Jones SRM, Brown GD, von Schalburg KR, Davidson WS, Koop BF. Microarray analyses identify molecular biomarkers of Atlantic salmon macrophage and hematopoietic kidney response to Piscirickettsia salmonis infection. Physiol Genomics 20: 21-35, 2004.
47. Rise ML, von Schalburg KR, Brown GD, Mawer MA, Devlin RH, Kuipers N, Busby M, Beetz-Sargent M, Alberto R, Gibbs AR, Hunt P, Shukin R, Zeznik JA, Nelson C, Jones SRM, Smailus DE, Jones SJM, Schein JE, Marra MA, Butterfield YSN, Stott JM, Ng SHS, Davidson WS, Koop BF. Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res 14: 478-490, 2004.
48. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol 20: 172-191, 2006.
49. Robertsen B, Bergan V, Rokenes T, Larsen R, Albuquerque A. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 23: 601-612, 2003.
50. Robertsen B, Trobridge G, Leong JA. Molecular cloning of double-stranded RNA inducible MX genes from Atlantic salmon (Salmo salar L.). Dev Comp Immunol 21: 397-412, 1997.
51. Rokenes TP, 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 44: 950-959, 2007.
52. Sangrador-Vegas A, Lennington JB, Smith TJ. Molecular cloning of an IL-8-like CXC chemokine and tissue factor in rainbow trout (Oncorhynchus mykiss) by use of suppression subtractive hybridization. Cytokine 17: 66-70, 2002.
53. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189, 2004.
54. Secombes C. Isolation of salmonid macrophages and analysis of their killing activity. In: Techniques in Fish Immunology, edited by Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB. Fair Haven, NJ: SOS, 1990, p. 137-154.
55. Takaoka A, Yanai H. Interferon signalling network in innate defence. Cell Microbiol 8: 907-922, 2006.
56. Trobridge GD, Leong JAC. Characterization of a rainbow trout Mx gene. J Interferon Cytokine Res 15: 691-702, 1995.
57. von Schalburg KR, Rise ML, Cooper GA, Brown GD, Gibbs AR, Nelson CC, Davidson WS, Koop BF. Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 6: 126, 2005.
58. Wang TH, Holland JW, Bols N, Secombes CJ. Cloning and expression of the first nonmammalian interleukin-11 gene in rainbow trout Oncorhynchus mykiss. FEBS J 272: 1136-1147, 2005.
59. Young HA, Hardy KJ. Role of interferon-gamma in immune cell regulation. J Leukoc Biol 58: 373-381, 1995.
60. Zhang YB, Gui HF. Identification of two novel interferon- stimulated genes from cultured CAB cells induced by UV-inactivated grass carp hemorrhage virus. Dis Aquatic Organisms 60: 1-9, 2004.
61. Zou J, Carrington A, Collet B, Dijkstra JM, Yoshiura Y, Bols N, Secombes C. Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175: 2484-2494, 2005.
62. Zou J, Cunningham C, Secombes CJ. The rainbow trout Oncorhynchus mykiss interleukin-1 beta gene has a different organization to mammals and undergoes incomplete splicing. Eur J Biochem 259: 901-908, 1999.
63. Zou J, Tafalla C, Truckle J, Secombes C. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179: 3859-3871, 2007.
64. Zou J, Yasutoshi YB, Dijkstra JM, Sakai M, Ototake M, Secombes C. Identification of an interferon gamma homologue in Fugu, Takifugu rubripes. Fish Shellfish Immunol 17: 403-409, 2004.