Contrasted innate responses to two viruses in zebrafish: Insights into the ancestral repertoire of vertebrate IFN-stimulated genes

Journal of Immunology

Volumn 192, Issue 9, 2014, Pages 4328-4341

  Briolat, Valérie ^a,b   Jouneau, Luc ^c   Carvalho, Ralph ^d,g   Palha, Nuno ^a,b,e   Langevin, Christelle ^c   Herbomel, Philippe ^a,b   Schwartz, Olivier ^a,b   Spaink, Herman P ^f   Levraud, Jean Pierre ^a,b   Boudinot, Pierre ^c  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

^d ZF screens ^*  (Netherlands)

^e SORBONNE UNIVERSITÉ   (France)

^f LEIDEN UNIVERSITY   (Netherlands)

^g VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; COMPARATIVE STUDY; CONTROLLED STUDY; FEEDBACK SYSTEM; GENE; GENE EXPRESSION; GENE LOCATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOMICS; IN SITU HYBRIDIZATION; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS INFECTION; INNATE IMMUNITY; INTERFERON STIMULATED GENE; INTESTINE; LARVA; LIVER; MICROARRAY ANALYSIS; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA VIRUS INFECTION; SIGNAL TRANSDUCTION; TAXONOMY; VERTEBRATE; VIRUS CELL INTERACTION; ZEBRA FISH;

ALPHAVIRUS INFECTIONS; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; IN SITU HYBRIDIZATION; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; INTERFERONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RHABDOVIRIDAE INFECTIONS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84899573699     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302611     Document Type: Article

References (56)

1. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon a, b, or g using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95: 15623-15628
2. Schoggins, J. W., S. J. Wilson, M. Panis, M. Y. Murphy, C. T. Jones, P. Bieniasz, and C. M. Rice. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485
3. Sadler, A. J., and B. R. G. Williams. 2008. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8: 559-568
4. Schoggins, J. W., and C. M. Rice. 2011. Interferon-stimulated genes and their antiviral effector functions. Curr. Opin. Virol. 1: 519-525
5. Brass, A. L., I-C. Huang, Y. Benita, S. P. John, M. N. Krishnan, E. M. Feeley, B. J. Ryan, J. L. Weyer, L.Van Der Weyden, E. Fikrig, et al. 2009. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139: 1243-1254
6. Flajnik, M., and L. Du Pasquier. 2013. Evolution of the immune system. In Fundamental Immunology, 7th Ed. W. Paul, ed. Wolters Kluwer and Lippincott Willians & Wilkins, New York, p. 67-128
7. Kanther, M., and J. F. Rawls. 2010. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 22: 10-19
8. Meijer, A. H., and H. P. Spaink. 2011. Host-pathogen interactions made transparent with the zebrafish model. Curr. Drug Targets 12: 1000-1017
9. Tobin, D. M., F. J. Roca, S. F. Oh, R. McFarland, T. W. Vickery, J. P. Ray, D. C. Ko, Y. Zou, N. D. Bang, T. T. H. Chau, et al. 2012. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 148: 434-446
10. Ludwig, M., N. Palha, C. Torhy, V. Briolat, E. Colucci-Guyon, M. Brémont, P. Herbomel, P. Boudinot, and J-P. Levraud. 2011. Whole-body analysis of a viral infection: Vascular endothelium is a primary target of infectious hematopoietic necrosis virus in zebrafish larvae. PLoS Pathog. 7: E1001269
11. Palha, N., F. Guivel-Benhassine, V. Briolat, G. Lutfalla, M. Sourisseau, F. Ellett, C-H. Wang, G. J. Lieschke, P. Herbomel, O. Schwartz, and J-P. Levraud. 2013. Real-time whole-body visualization of Chikungunya virus infection and host interferon response in zebrafish. PLoS Pathog. 9: E1003619
12. Herath, T. K., J. E. Bron, K. D. Thompson, J. B. Taggart, A. Adams, J. H. Ireland, and R. H. Richards. 2012. Transcriptomic analysis of the host response to early stage salmonid alphavirus (SAV-1) infection in Atlantic salmon Salmo salar L. Fish Shellfish Immunol. 32: 796-807
13. Timmerhaus, G., A. Krasnov, P. Nilsen, M. Alarcon, S. Afanasyev, M. Rode, H. Takle, and S. M. Jørgensen. 2011. Transcriptome profiling of immune responses to cardiomyopathy syndrome (CMS) in Atlantic salmon. BMC Genomics 12: 459
14. Huang, Y., X. Huang, Y. Yan, J. Cai, Z. Ouyang, H. Cui, P. Wang, and Q. Qin. 2011. Transcriptome analysis of orange-spotted grouper (Epinephelus coioides) spleen in response to Singapore grouper iridovirus. BMC Genomics 12: 556
15. Lu, M-W., F-H. Ngou, Y-M. Chao, Y-S. Lai, N-Y. Chen, F-Y. Lee, and P. P. Chiou. 2012. Transcriptome characterization and gene expression of Epinephelus spp in endoplasmic reticulum stress-related pathway during betanodavirus infection in vitro. BMC Genomics 13: 651
16. Krasnov, A., ø. Kileng, S. Skugor, S. M. Jørgensen, S. Afanasyev, G. Timmerhaus, A-I. Sommer, and I. Jensen. 2013. Genomic analysis of the host response to nervous necrosis virus in Atlantic cod (Gadus morhua) brain. Mol. Immunol. 54: 443-452
17. Purcell, M. K., I. S. Marjara, W. Batts, G. Kurath, and J. D. Hansen. 2011. Transcriptome analysis of rainbow trout infected with high and low virulence strains of infectious hematopoietic necrosis virus. Fish Shellfish Immunol. 30: 84-93
18. Martin, S. A. M., J. B. Taggart, P. Seear, J. E. Bron, R. Talbot, A. J. Teale, G. E. Sweeney, B. Høyheim, D. F. Houlihan, D. R. Tocher, et al. 2007. Interferon type I and type II responses in an Atlantic salmon (Salmo salar) SHK-1 cell line by the salmon TRAITS/SGP microarray. Physiol. Genomics 32: 33-44
19. Stockhammer, O. W., A. Zakrzewska, Z. Hegedu?s, H. P. Spaink, and A. H. Meijer. 2009. Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection. J. Immunol. 182: 5641-5653
20. Levraud, J-P., E. Colucci-Guyon, M. J. Redd, G. Lutfalla, and P. Herbomel. 2008. In vivo analysis of zebrafish innate immunity. Methods Mol. Biol. 415: 337-363
21. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25
22. Van Soest, J. J., O. W. Stockhammer, A. Ordas, G. V. Bloemberg, H. P. Spaink, and A. H. Meijer. 2011. Comparison of static immersion and intravenous injection systems for exposure of zebrafish embryos to the natural pathogen Edwardsiella tarda. BMC Immunol. 12: 58
23. Lutfalla, G., and G. Uze. 2006. Performing quantitative reverse-transcribed polymerase chain reaction experiments. Methods Enzymol. 410: 386-400
24. Boudinot, P., L. M.Van Der Aa, L. Jouneau, L. Du Pasquier, P. Pontarotti, V. Briolat, A. Benmansour, and J-P. Levraud. 2011. Origin and evolution of TRIM proteins: New insights from the complete TRIM repertoire of zebrafish and pufferfish. PLoS ONE 6: E22022
25. Thisse, C., and B. Thisse. 2008. High-resolution in situ hybridization to wholemount zebrafish embryos. Nat. Protoc. 3: 59-69
26. Aggad, D., M. Mazel, P. Boudinot, K. E. Mogensen, O. J. Hamming, R. Hartmann, S. Kotenko, P. Herbomel, G. Lutfalla, and J-P. Levraud. 2009. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J. Immunol. 183: 3924-3931
27. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739
28. Thisse, B., V. Heyer, A. Lux, V. Alunni, A. Degrave, I. Seiliez, J. Kirchner, J-P. Parkhill, and C. Thisse. 2004. Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol. 77: 505-519
29. Covassin, L., J. D. Amigo, K. Suzuki, V. Teplyuk, J. Straubhaar, and N. D. Lawson. 2006. Global analysis of hematopoietic and vascular endothelial gene expression by tissue specific microarray profiling in zebrafish. Dev. Biol. 299: 551-562
30. Biacchesi, S., M. LeBerre, A. Lamoureux, Y. Louise, E. Lauret, P. Boudinot, and M. Brémont. 2009. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J. Virol. 83: 7815-7827
31. Lauksund, S., T. Svingerud, V. Bergan, and B. Robertsen. 2009. Atlantic salmon IPS-1 mediates induction of IFNa1 and activation of NF-kB and localizes to mitochondria. Dev. Comp. Immunol. 33: 1196-1204
32. Levraud, J-P., P. Boudinot, I. Colin, A. Benmansour, N. Peyrieras, P. Herbomel, and G. Lutfalla. 2007. Identification of the zebrafish IFN receptor: Implications for the origin of the vertebrate IFN system. J. Immunol. 178: 4385-4394
33. Langevin, C., E. Aleksejeva, G. Passoni, N. Palha, J-P. Levraud, and P. Boudinot. 2013. The antiviral innate immune response in fish: Evolution and conservation of the IFN system. J. Mol. Biol. 425: 4904-4920
34. Lyles, D. S. 2000. Cytopathogenesis and inhibition of host gene expression by RNA viruses. Microbiol. Mol. Biol. Rev. 64: 709-724
35. Howe, K., M. D. Clark, C. F. Torroja, J. Torrance, C. Berthelot, M. Muffato, J. E. Collins, S. Humphray, K. McLaren, L. Matthews, et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496: 498-503
36. Moffatt, P., M-H. Gaumond, P. Salois, K. Sellin, M-C. Bessette, E. Godin, P. T. De Oliveira, G. J. Atkins, A. Nanci, and G. Thomas. 2008. Bril: A novel bone-specific modulator of mineralization. J. Bone Miner. Res. 23: 1497-1508
37. Sun, B., B. Robertsen, Z. Wang, and B. Liu. 2009. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 33: 547-558
38. Thoulouze, M. I., E. Bouguyon, C. Carpentier, and M. Brémont. 2004. Essential role of the NV protein of Novirhabdovirus for pathogenicity in rainbow trout. J. Virol. 78: 4098-4107
39. Vidy, A., M. Chelbi-Alix, and D. Blondel. 2005. Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J. Virol. 79: 14411-14420
40. Brzózka, K., S. Finke, and K-K. Conzelmann. 2006. Inhibition of interferon signaling by rabies virus phosphoprotein P: Activation-dependent binding of STAT1 and STAT2. J. Virol. 80: 2675-2683
41. Chelbi-Alix, M. K., A. Vidy, J. El Bougrini, and D. Blondel. 2006. Rabies viral mechanisms to escape the IFN system: The viral protein P interferes with IRF-3, Stat1, and PML nuclear bodies. J. Interferon Cytokine Res. 26: 271-280
42. Choi, M. K., C. H. Moon, M. S. Ko, U. H. Lee, W. J. Cho, S. J. Cha, J. W. Do, G. J. Heo, S. G. Jeong, Y. S. Hahm, et al. 2011. A nuclear localization of the infectious haematopoietic necrosis virus NV protein is necessary for optimal viral growth. PLoS ONE 6: E22362
43. Kim, M. S., and K. H. Kim. 2013. The role of viral hemorrhagic septicemia virus( VHSV) NV gene in TNF-a-and VHSV infection-mediated NF-kB activation. Fish Shellfish Immunol. 34: 1315-1319
44. MacKenzie, S., J. C. Balasch, B. Novoa, L. Ribas, N. Roher, A. Krasnov, and A. Figueras. 2008. Comparative analysis of the acute response of the trout, O. mykiss, head kidney to in vivo challenge with virulent and attenuated infectious hematopoietic necrosis virus and LPS-induced inflammation. BMC Genomics 9: 141
45. Laing, K. J., M. K. Purcell, J. R. Winton, and J. D. Hansen. 2008. A genomic view of the NOD-like receptor family in teleost fish: Identification of a novel NLR subfamily in zebrafish. BMC Evol. Biol. 8: 42
46. Stein, C., M. Caccamo, G. Laird, and M. Leptin. 2007. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 8: R251
47. Van Der Aa, L. M., J-P. Levraud, M. Yahmi, E. Lauret, V. Briolat, P. Herbomel, A. Benmansour, and P. Boudinot. 2009. A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biol. 7: 7
48. O?Farrell, C., N. Vaghefi, M. Cantonnet, B. Buteau, P. Boudinot, and A. Benmansour. 2002. 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
49. Boudinot, P., S. Salhi, M. Blanco, and A. Benmansour. 2001. Viral haemorrhagic septicaemia virus induces vig-2, a new interferon-responsive gene in rainbow trout. Fish Shellfish Immunol. 11: 383-397
50. Kochs, G., and O. Haller. 1999. GTP-bound human MxA protein interacts with the nucleocapsids of Thogoto virus (Orthomyxoviridae). J. Biol. Chem. 274: 4370-4376
51. Pulverer, J. E., U. Rand, S. Lienenklaus, D. Kugel, N. Zietara, G. Kochs, R. Naumann, S. Weiss, P. Staeheli, H. Hauser, and M. Köster. 2010. Temporal and spatial resolution of type I and III interferon responses in vivo. J. Virol. 84: 8626-8638
52. Di Bona, D., M. Cippitelli, C. Fionda, C. Cammà, A. Licata, A. Santoni, and A. Craxò. 2006. Oxidative stress inhibits IFN-a-induced antiviral gene expression by blocking the JAK-STAT pathway. J. Hepatol. 45: 271-279
53. Hall, C. J., R. H. Boyle, J.W. Astin, M. V. Flores, S. H. Oehlers, L. E. Sanderson, F. Ellett, G. J. Lieschke, K. E. Crosier, and P. S. Crosier. 2013. Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating b-oxidation-dependent mitochondrial ROS production. Cell Metab. 18: 265-278
54. Park, M-S., J. Steel, A. Garcéa-Sastre, D. Swayne, and P. Palese. 2006. Engineered viral vaccine constructs with dual specificity: Avian influenza and Newcastle disease. Proc. Natl. Acad. Sci. USA 103: 8203-8208
55. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: The control of NF-kB activity. Annu. Rev. Immunol. 18: 621-663
56. He, H., D. Zhou, W. Fan, X. Fu, J. Zhang, Z. Shen, J. Li, J. Li, and Y. Wu. 2012. Cyclophilin A inhibits rotavirus replication by facilitating host IFN-I production. Biochem. Biophys. Res. Commun. 422: 664-669