Genetic resistance to rhabdovirus infection in teleost fish is paralleled to the derived cell resistance status

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Verrier, Eloi R ^a,b,c   Langevin, Christelle ^a   Tohry, Corinne ^a   Houel, Armel ^a   Ducrocq, Vincent ^b   Benmansour, Abdenour ^a   Quillet, Edwige ^b   Boudinot, Pierre ^a  

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

^b UMR1313 GÉNÉTIQUE ANIMALE ET BIOLOGIE INTÉGRATIVE   (France)

^c AGROPARISTECH   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ANIMAL CELL; ARTICLE; CELL LINE; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; DOUBLED HAPLOID LINE; FIBROBLAST CULTURE; GENETIC RESISTANCE; HAPLOTYPE; HEREDITY; HOST RESISTANCE; INFECTION RESISTANCE; INFECTION SENSITIVITY; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; INFECTIOUS PANCREATIC NECROSIS VIRUS; INFECTIOUS SALMON ANEMIA VIRUS; INNATE IMMUNITY; MOLECULAR CLONING; NONHUMAN; ORTHOMYXOVIRUS; RAINBOW TROUT; RHABDOVIRUS INFECTION; TELEOST; VIRAL HEMORRHAGIC SEPTICEMIA VIRUS; VIROGENESIS; ANIMAL; FISH; FISH DISEASE; GENETICS; METABOLISM; VIROLOGY;

BIRNAVIRIDAE; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; INFECTIOUS PANCREATIC NECROSIS VIRUS; INFECTIOUS SALMON ANEMIA VIRUS; ONCORHYNCHUS MYKISS; ORTHOMYXOVIRIDAE; RHABDOVIRIDAE; TELEOSTEI; VIRAL HEMORRHAGIC SEPTICEMIA VIRUS;

ANIMALS; CELL LINE; DISEASE SUSCEPTIBILITY; FISH DISEASES; FISHES; INTERFERONS; RHABDOVIRIDAE INFECTIONS;

EID: 84859706288     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033935     Document Type: Article

References (75)

1. Alcais A, Abel L, Casanova JL, (2009) Human genetics of infectious diseases: between proof of principle and paradigm. J Clin Invest 119: 2506-2514.
2. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, et al. (1996) Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 273: 1856-1862.
3. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, et al. (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86: 367-377.
4. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, et al. (1996) Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382: 722-725.
5. Brown KE, Hibbs JR, Gallinella G, Anderson SM, Lehman ED, et al. (1994) Resistance to parvovirus B19 infection due to lack of virus receptor (erythrocyte P antigen). N Engl J Med 330: 1192-1196.
6. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, et al. (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med 9: 548-553.
7. Bruton OC, (1962) A decade with agammaglobulinemia. J Pediatr 60: 672-676.
8. Fischer A, Le Deist F, Hacein-Bey-Abina S, Andre-Schmutz I, Basile Gde S, et al. (2005) Severe combined immunodeficiency. A model disease for molecular immunology and therapy. Immunol Rev 203: 98-109.
9. Rigaud S, Fondaneche MC, Lambert N, Pasquier B, Mateo V, et al. (2006) XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 444: 110-114.
10. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, et al. (2004) The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427: 848-853.
11. Goff SP, (2004) Retrovirus restriction factors. Mol Cell 16: 849-859.
12. Abel L, Casanova JL, (2000) Genetic predisposition to clinical tuberculosis: bridging the gap between simple and complex inheritance. Am J Hum Genet 67: 274-277.
13. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, et al. (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317: 944-947.
14. Cole RK, (1968) Studies on genetic resistance to Marek's disease. Avian Dis 12: 9-28.
15. Hanson MP, van Zandy JN, Law GR, (1967) Differences in susceptibility to Marek s diseasein chickens carrying two different B locus blood alleles. Poult Sci 46: 1268.
16. Fuji K, Kobayashi K, Hasegawa O, Coimbra M, Sakamoto T, et al. (2006) Identification of a single major genetic locus controlling the resistance to lymphocystis disease in Japanese flounder (Paralichthys olivaceus). Aquaculture 254: 203-210.
17. Dorson M, Quillet E, Hollebecq MG, Torhy C, Chevassus B, (1995) Selection of rainbow trout resistant to viral haemorrhagic septicaemia virus and transmission of resistance by gynogenesis. Vet Res 26: 361-368.
18. Slierendrecht WJ, Olesen NJ, Juul-Madsen HR, Lorenzen N, Henryon M, et al. (2001) Rainbow trout offspring with different resistance to viral haemorrhagic septicaemia. Fish Shellfish Immunol 11: 155-167.
19. Biacchesi S, Le Berre M, Le Guillou S, Benmansour A, Bremont M, et al. (2007) Fish genotype significantly influences susceptibility of juvenile rainbow trout, Oncorhynchus mykiss (Walbaum), to waterborne infection with infectious salmon anaemia virus. J Fish Dis 30: 631-636.
20. Purcell MK, Lapatra SE, Woodson JC, Kurath G, Winton JR, (2010) Early viral replication and induced or constitutive immunity in rainbow trout families with differential resistance to Infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol 28: 98-105.
21. Quillet E, Dorson M, Le Guillou S, Benmansour A, Boudinot P, (2007) Wide range of susceptibility to rhabdoviruses in homozygous clones of rainbow trout. Fish Shellfish Immunol 22: 510-519.
22. Norris A, Foyle L, Ratcliff J, (2008) Heritability of mortality in response to a natural pancreas disease (SPDV) challenge in Atlantic salmon, Salmo salar L., post-smolts on a West of Ireland sea site. J Fish Dis 31: 913-920.
23. Kjoglum S, Larsen S, Bakke HG, Grimholt U, (2006) How specific MHC class I and class II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 21: 431-441.
24. Guy DR, Bishop SC, Brotherstone S, Hamilton A, Roberts RJ, et al. (2006) Analysis of the incidence of infectious pancreatic necrosis mortality in pedigreed Atlantic salmon, Salmo salar L., populations. J Fish Dis 29: 637-647.
25. Shapira Y, Magen Y, Zak T, Kotler M, Hulata G, et al. (2005) Differential resistance to Koi herpesvirus (KHV)/carp interstitial nephritis and gill necrosis virus (CNGV) among common carp (Cyprinus carpio) strains and crossbreds. Aquaculture 245: 1-11.
26. Ødegård J, Olesen I, Dixon P, Zsigmond J, Nielsen H-M, et al. (2010) Genetic analysis of common carp (Cyprinus carpio) strains. II: Resistance to koi herpesvirus and Aeromonas hydrophila and their relationship with pond survival. Aquaculture 304: 7-13.
27. Kirpichnikov V, Ilyasov J, Shart L, Vikhman A, Ganchenko A, et al. (1993) Selection of Krasnodar common carp (Cyprinus carpio L.) for resistance to dropsy: principal results and prospects. Aquaculture 111: 7-20.
28. Overgard AC, Nerland AH, Patel S, (2010) Evaluation of potential reference genes for real time RT-PCR studies in Atlantic halibut (Hippoglossus Hippoglossus L.); during development, in tissues of healthy and NNV-injected fish, and in anterior kidney leucocytes. BMC Mol Biol 11: 36.
29. Houston RD, Gheyas A, Hamilton A, Guy DR, Tinch AE, et al. (2008) Detection and confirmation of a major QTL affecting resistance to infectious pancreatic necrosis (IPN) in Atlantic salmon (Salmo salar). Dev Biol (Basel) 132: 199-204.
30. Li J, Boroevich KA, Koop BF, Davidson WS, (2011) Comparative genomics identifies candidate genes for infectious salmon anemia (ISA) resistance in Atlantic salmon (Salmo salar). Mar Biotechnol (NY) 13: 232-241.
31. Ozaki A, Sakamoto T, Khoo S, Nakamura K, Coimbra M, et al. (2001) Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Molecular Genetics and Genomics 265: 23-31.
32. Moen T, Baranski M, Sonesson AK, Kjoglum S, (2009) Confirmation and fine-mapping of a major QTL for resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar): population-level associations between markers and trait. BMC Genomics 10: 368.
33. Palti Y, Parsons J, Thorgaard G, (1999) Identification of candidate DNA marquers associated with IHN virus resistance in backcrosses of rainbow (Oncorhynchus mykiss) and cutthroat trout (O. clarki). Aquaculture 173: 81-94.
34. Boudinot P, Boubekeur S, Benmansour A, (2001) Rhabdovirus infection induces public and private T cell responses in teleost fish. J Immunol 167: 6202-6209.
35. Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, et al. (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics 55: 561-569.
36. Hansen JD, Strassburger P, Thorgaard GH, Young WP, Du Pasquier L, (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163: 774-786.
37. Koop BF, von Schalburg KR, Leong J, Walker N, Lieph R, et al. (2008) A salmonid EST genomic study: genes, duplications, phylogeny and microarrays. BMC Genomics 9: 545.
38. Basurco B, Benmansour A, (1995) Distant strains of the fish rhabdovirus VHSV maintain a sixth functional cistron which codes for a nonstructural protein of unknown function. Virology 212: 741-745.
39. Benmansour A, Paubert G, Bernard J, de Kinkelin P, (1994) The polymerase-associated protein (M1) and the matrix protein (M2) from a virulent and an avirulent strain of viral hemorrhagic septicemia virus (VHSV), a fish rhabdovirus. Virology 198: 602-612.
40. Bernard J, Lecocq-Xhonneux F, Rossius M, Thiry ME, de Kinkelin P, (1990) Cloning and sequencing the messenger RNA of the N gene of viral haemorrhagic septicaemia virus. J Gen Virol 71 (Pt 8): 1669-1674.
41. Thiry M, Lecoq-Xhonneux F, Dheur I, Renard A, de Kinkelin P, (1991) Sequence of a cDNA carrying the glycoprotein gene and part of the matrix protein M2 gene of viral haemorrhagic scepticaemia virus, a fish rhabdovirus. Biochim Biophys Acta 1090: 345-347.
42. Chiou PP, Kim CH, Ormonde P, Leong JA, (2000) Infectious hematopoietic necrosis virus matrix protein inhibits host-directed gene expression and induces morphological changes of apoptosis in cell cultures. J Virol 74: 7619-7627.
43. Biacchesi S, LeBerre M, Lamoureux A, Louise Y, Lauret E, et al. (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.
44. Chang M, Collet B, Nie P, Lester K, Campbell S, et al. (2011) Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in Rainbow trout (Oncorhynchus mykiss). J Virol 85: 8403-8412.
45. Lauksund S, Svingerud T, Bergan V, Robertsen B, (2009) Atlantic salmon IPS-1 mediates induction of IFNa1 and activation of NF-kappaB and localizes to mitochondria. Dev Comp Immunol 33: 1196-1204.
46. Robertsen B, (2006) The interferon system of teleost fish. Fish Shellfish Immunol 20: 172-191.
47. Hamming OJ, Lutfalla G, Levraud JP, Hartmann R, (2011) Crystal structure of Zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates. J Virol 85: 8181-8187.
48. Verrier ER, Langevin C, Benmansour A, Boudinot P, (2011) Early antiviral response and virus-induced genes in fish. Dev Comp Immunol 35: 1204-1214.
49. Altmann SM, Mellon MT, Distel DL, Kim CH, (2003) Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77: 1992-2002.
50. Lutfalla G, Roest Crollius H, Stange-Thomann N, Jaillon O, Mogensen K, et al. (2003) Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish. BMC Genomics 4: 29.
51. Levraud JP, Boudinot P, Colin I, Benmansour A, Peyrieras N, et al. (2007) Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J Immunol 178: 4385-4394.
52. Aggad D, Mazel M, Boudinot P, Mogensen KE, Hamming OJ, et al. (2009) The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J Immunol 183: 3924-3931.
53. Oshiumi H, Matsuo A, Matsumoto M, Seya T, (2008) Pan-vertebrate toll-like receptors during evolution. Curr Genomics 9: 488-493.
54. Matsuo A, Oshiumi H, Tsujita T, Mitani H, Kasai H, et al. (2008) Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses. J Immunol 181: 3474-3485.
55. Robertsen B, (2008) Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish Shellfish Immunol 25: 351-357.
56. Boudinot P, Blanco M, de Kinkelin P, Benmansour A, (1998) Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology 249: 297-306.
57. Le Berre M, de Kinkelin P, Metzger A, (1977) Identification sérologique des Rhabdovirus de Salmonidés. Bull Off It Epizoot 87: 391-393.
58. Wolf K, (1988) Infectious pancreatic necrosis. Fish viruses and fish viral diseases New York Cornell University Press pp. 115-157.
59. Quillet E, Dorson M, Aubard G, Torhy C, (2001) In vitro viral haemorrhagic septicaemia virus replication in excised fins of rainbow trout: correlation with resistance to waterborne challenge and genetic variation. Dis Aquat Organ 45: 171-182.
60. Ducrocq V, Sölkner J, Mészáros G, (2010) Survival Kit V6- a Software Package for Survival Analysis (ID232). 9th World Congress on Genetics Applied to Livestock Production (WCGALP) Leipzig, Germany.
61. Cox D, (1972) Regression models and life table. J Royal Stat Soc 34: 187-220.
62. Jorgensen HB, Sorensen P, Cooper GA, Lorenzen E, Lorenzen N, et al. (2011) General and family-specific gene expression responses to viral hemorrhagic septicaemia virus infection in rainbow trout (Oncorhynchus mykiss). Mol Immunol 48: 1046-1058.
63. Lorenzen N, Lorenzen E, Einer-Jensen K, Heppell J, Wu T, et al. (1998) Protective immunity to VHS in Rainbow trout (Oncorhyncus mykiss). Fish Shellfish Immunol 8: 261-270.
64. Purcell MK, Marjara IS, Batts W, Kurath G, Hansen JD, (2011) Transcriptome analysis of rainbow trout infected with high and low virulence strains of infectious hematopoietic necrosis virus. Fish Shellfish Immunol 30: 84-93.
65. Harmache A, LeBerre M, Droineau S, Giovannini M, Bremont M, (2006) Bioluminescence imaging of live infected salmonids reveals that the fin bases are the major portal of entry for Novirhabdovirus. J Virol 80: 3655-3659.
66. Zou J, Tafalla C, Truckle J, Secombes CJ, (2007) Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179: 3859-3871.
67. Lopez-Munoz A, Roca FJ, Meseguer J, Mulero V, (2009) New insights into the evolution of IFNs: zebrafish group II IFNs induce a rapid and transient expression of IFN-dependent genes and display powerful antiviral activities. J Immunol 182: 3440-3449.
68. Trobridge GD, Leong JA, (1995) Characterization of a rainbow trout Mx gene. J Interferon Cytokine Res 15: 691-702.
69. Trobridge GD, Chiou PP, Leong JA, (1997) Cloning of the rainbow trout (Oncorhynchus mykiss) Mx2 and Mx3 cDNAs and characterization of trout Mx protein expression in salmon cells. J Virol 71: 5304-5311.
70. O'Farrell C, Vaghefi N, Cantonnet M, Buteau B, Boudinot P, et al. (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.
71. Boudinot P, Massin P, Blanco M, Riffault S, Benmansour A, (1999) 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 73: 1846-1852.
72. van der Aa LM, Levraud JP, Yahmi M, Lauret E, Briolat V, et al. (2009) A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biol 7: 7.
73. Boudinot P, Salhi S, Blanco M, Benmansour A, (2001) Viral haemorrhagic septicaemia virus induces vig-2, a new interferon-responsive gene in rainbow trout. Fish Shellfish Immunol 11: 383-397.
74. Sun B, Robertsen B, Wang Z, Liu B, (2009) Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev Comp Immunol 33: 547-558.
75. Bearzotti M, Delmas B, Lamoureux A, Loustau AM, Chilmonczyk S, et al. (1999) Fish rhabdovirus cell entry is mediated by fibronectin. J Virol 73: 7703-7709.