Oas1b-dependent immune transcriptional profiles of west nile virus infection in the collaborative cross

G3: Genes, Genomes, Genetics

Volumn 7, Issue 6, 2017, Pages 1665-1682

  Green, Richard ^a   Wilkins, Courtney ^a   Thomas, Sunil ^a   Sekine, Aimee ^a   Hendrick, Duncan M ^a   Voss, Kathleen ^a   Ireton, Renee C ^a   Mooney, Michael ^b   Go, Jennifer T ^a   Choonoo, Gabrielle ^b   Jeng, Sophia ^b   de Villena, Fernando Pardo Manuel ^c,d   Ferris, Martin T ^c   McWeeney, Shannon ^b   Gale, Michael ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Flavivirus; Innate immunity; MPP; Multi parent Advanced Generation Inter Cross (MAGIC); Multiparental populations; Oas; Viral infection

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; OAS1B PROTEIN, MOUSE; TRANSCRIPTOME;

ALLELISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMOSOME 5; CONTROLLED STUDY; FOUNDER EFFECT; GENE DOSAGE; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENETIC TRANSCRIPTION; HAPLOTYPE; INNATE IMMUNITY; MOUSE; NONHUMAN; QUANTITATIVE TRAIT LOCUS; VIROGENESIS; VIRUS INFECTION; VIRUS TRANSCRIPTION; WEST NILE VIRUS; ANIMAL; DISEASE MODEL; DISEASE PREDISPOSITION; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; IMMUNOMODULATION; MALE; VIROLOGY; WEST NILE FEVER;

2',5'-OLIGOADENYLATE SYNTHETASE; ANIMALS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; IMMUNOMODULATION; MALE; MICE; QUANTITATIVE TRAIT LOCI; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; WEST NILE FEVER; WEST NILE VIRUS;

EID: 85020295478     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.117.041624     Document Type: Article

References (61)

1. Bigham, A. W., K. J. Buckingham, S. Husain, M. J. Emond, K. M. Bofferding et al., 2011 Host genetic risk factors for West Nile virus infection and disease progression. PLoS One 6(9): e24745
2. Boon, A. C., J. deBeauchamp, A. Hollmann, J. Luke, M. Kotb et al., 2009 Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J. Virol. 83(20): 10417-10426
3. Bottomly, D., B. Wilmot, and S. K. McWeeney 2014 Oligomask: a framework for assessing and removing the effect of genetic variants on microarray probes. R J. 6(1): 159-163
4. Brinton, M. A., and A. A. Perelygin, 2003 Genetic resistance to flaviviruses. Adv. Virus Res. 60: 43-85
5. Cartmell, T., S. Poole, A. V. Turnbull, N. J. Rothwell, and G. N. Luheshi, 2000 Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J. Physiol. 526(Pt. 3): 653-661
6. Choi, U. Y., J. S. Kang, Y. S. Hwang, and Y. J. Kim, 2015 Oligoadenylate synthase-like (OASL) proteins: dual functions and associations with diseases. Exp. Mol. Med. 47: e144
7. Courtney, S. C., H. Di, B. M. Stockman, H. Liu, S. V. Scherbik et al., 2012 Identification of novel host cell binding partners of Oas1b, the protein conferring resistance to flavivirus-induced disease in mice. J. Virol. 86: 7953-7963
8. Cuevas, R. A., A. Ghosh, C. Wallerath, V. Hornung, C. B. Coyne et al., 2016 MOV10 provides antiviral activity against RNA viruses by enhancing RIG-I-MAVS-independent IFN induction. J. Immunol. 9: 3877-3886
9. Daffis, S., M. S. Suthar, M. Gale, Jr, and M. S. Diamond, 2009 Measure and countermeasure: type I IFN (IFN-alpha/beta) antiviral response against West Nile virus. J. Innate Immun. 5: 435-445
10. Drappier, M., and T. Michiels, 2015 Inhibition of the OAS/RNase L pathway by viruses. Curr. Opin. Virol. 15: 19-26
11. Elbahesh, H., B. K. Jha, R. H. Silverman, S. V. Scherbik, and M. A. Brinton, 2011 The Flvr-encoded murine oligoadenylate synthetase 1b (Oas1b) suppresses 2-5A synthesis in intact cells. Virology 409(2): 262-270
12. Elkhateeb, E., H. T. Tag-El-Din-Hassan, N. Sasaki, D. Torigoe, M. Morimatsu et al., 2016 The role of mouse 29,59-oligoadenylate synthetase 1 paralogs. Infect. Genet. Evol. 45: 393-401
13. Engelhardt, O. G., E. Ullrich, G. Kochs, and O. Haller, 2001 Interferon induced antiviral Mx1 GTPase is associated with components of the SUMO-1 system and promyelocytic leukemia protein nuclear bodies. Exp. Cell Res. 271: 286-295
14. Errett, J. S., M. S. Suthar, A. McMillan, M. S. Diamond, and M. Gale, Jr., 2013 The essential, nonredundant roles of RIG-I and MDA5 in detecting and controlling West Nile virus infection. J. Virol. 87(21): 11416-11425
15. Ferguson, W., S. Dvora, J. Gallo, A. Orth, and S. Boissinot, 2008 Long-term balancing selection at the west nile virus resistance gene, Oas1b, maintains transspecific polymorphisms in the house mouse. Mol. Biol. Evol. 8: 1609-1618
16. Ferris, M. T., and M. Heise, 2014 Quantitative genetics in the study of virus-induced disease. Adv. Virus Res. 88: 193-225
17. Ferris, M. T., D. L. Aylor, D. Bottomly, A. C. Whitmore, L. D. Aicher et al., 2013 Modeling host genetic regulation of influenza pathogenesis in the collaborative cross. PLoS Pathog. 2: e1003196
18. Flammer, J. R., J. Dobrovolna, M. A. Kennedy, Y. Chinenov, C. K. Glass et al., 2010 The type I interferon signaling pathway is a target for glucocorticoid inhibition. Mol. Cell. Biol. 19: 4564-4574
19. Fredericksen, B. L., 2014 The neuroimmune response to West Nile virus. J. Neurovirol. 2: 113-121
20. Gatti, D. M., K. L. Svenson, A. Shabalin, L. Y. Wu, W. Valdar et al., 2014 Quantitative trait locus mapping methods for diversity outbred mice. G3 4(9): 1623-1633
21. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling et al., 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80
22. Graham, J. B., S. Thomas, J. Swarts, A. A. McMillan, M. T. Ferris et al., 2015 Genetic diversity in the collaborative cross model recapitulates human West Nile virus disease outcomes. MBio 6(3): e00493-e00515
23. Graham, J. B., J. L. Swarts, C. Wilkins, S. Thomas,R.Green et al., 2016 A mouse model of chronic West Nile virus disease. PLoS Pathog. 12(11): e1005996
24. Gralinski, L. E., M. T. Ferris, D. L. Aylor, A. C. Whitmore, R. Green et al., 2015 Genome wide identification of SARS-CoV susceptibility loci using the collaborative cross. PLoS Genet. 11(10): e1005504
25. Gralinski, L., V. Menachery, A. Morgan, A. Totura, A. Beall et al., 2017 Allelic variation in mouse Ticam2 contributes to SARS-CoV pathogenesis. G3 (Bethesda) 7: 1653-1663
26. Green,R., C. Wilkins, S. Thomas,A. Sekine, R. C. Ireton et al., 2016a Identifying protective host gene expression signatures within the spleen during West Nile virus infection in the collaborative cross model. Genom. Data 10: 114-117
27. Green, R., C. Wilkins, S. Thomas, A. Sekine, R. C. Ireton et al., 2016b Transcriptional profiles of WNV neurovirulence in a genetically diverse collaborative cross population. Genom. Data 10: 137-140
28. Iraqi, F.A., M. Mahajne, Y. Salaymah, H. Sandovski, H. Tayem et al. Collaborative Cross Consortium, 2012 The genome architecture of the collaborative cross mouse genetic reference population. Genetics 190(2): 389-401
29. Jang, I. K., J. Zhang, and H. Gu, 2009 Grb2, a simple adapter with complex roles in lymphocyte development, function, and signaling. Immunol. Rev. 232(1): 150-159
30. Kajaste-Rudnitski, A., T. Mashimo, M. P. Frenkiel, J. L. Guénet, M. Lucas et al., 2006 The 29,59-oligoadenylate synthetase 1b is a potent inhibitor of West Nile virus replication inside infected cells. J. Biol. Chem. 281(8): 4624-4637
31. Keane, T. M., L. Goodstadt, P. Danecek, M. A. White, K. Wong et al., 2011 Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477(7364): 289-294
32. Krämer, A., J. Green, J. Pollard, and S. Tugendreich, 2014 Causal analysis approaches in ingenuity pathway analysis. Bioinformatics 4: 1-8
33. Kristiansen, H., H. H. Gad, S. Eskildsen-Larsen, P. Despres, and R. Hartmann, 2011 The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities. J. Interferon Cytokine Res. 1: 41-47
34. Lazear, H. M., and M. S. Diamond, 2015 New insights into innate immune restriction of West Nile virus infection. Curr. Opin. Virol. 11: 1-6
35. Lazear, H. M., A. Lancaster, C. Wilkins, M. S. Suthar, A. Huang et al., 2013 IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog. 1: e1003118
36. Lee, M. S., B. Kim, G. T. Oh, and Y. J. Kim, 2013 OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7. Nat. Immunol. 4: 346-355
37. Li, H., C. Leo, J. Zhu, X. Wu, J. O'Neil et al., 2000 Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol. Cell. Biol. 20: 1784-1796
38. Li, Y., S. Banerjee, Y. Wang, S. A. Goldstein et al., 2016 Activation of RNase L is dependent on OAS3 expression during infection with diverse human viruses. Proc. Natl. Acad. Sci. USA. Feb 23(8): 2241-2246
39. Loo, Y. M., and M. Gale, Jr., 2008 Unveiling viral enablers. Nat. Biotechnol. 10: 1093-1094
40. Loo, Y. M., and M. Gale, Jr., 2011 Immune signaling by RIG-I-like receptors. Immunity 34(5): 680-692
41. Loraine, A. E., I. C. Blakley, S. Jagadeesan, J. Harper, G. Miller et al., 2015 Analysis and visualization of RNA-Seq expression data using RStudio, bioconductor, and integrated genome browser. Methods Mol. Biol. 1284: 481-501
42. Malathi, K., B. Dong, M. Gale, Jr., and R. H. Silverman, 2007 Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature. 448: 816-819
43. Mashimo, T., M. Lucas, D. Simon-Chazottes, M. P. Frenkiel, X. Montagutelli et al., 2002 A nonsense mutation in the gene encoding 29-59-oligoadenylate synthetase/L1 isoform is associated with West Nile virus susceptibility in laboratory mice. Proc. Natl. Acad. Sci. USA 99(17): 11311-11316
44. Mashima, R., K. Saeki, D. Aki, Y. Minoda, H. Takaki et al., 2005 FLN29, a novel interferon-and LPS-inducible gene acting as a negative regulator of toll-like receptor signaling. J. Biol. Chem. 280(50): 41289-41297
45. Morgan, A. P., C. P. Fu, C. Y. Kao, C. E. Welsh et al., 2015 The Mouse Universal Genotyping Array: From Substrains to Subspecies. G3 (Bethesda). 2015 12: 263-279
46. Morgan, A. P., D. M. Gatti, T. M. Keane, R. J. Galante, A. I. Pack et al., 2017 Structural variation shapes the landscape of recombination in mouse. Genetics 206: 603-619
47. Neri, F., A. Zippo, A. Krepelova, A. Cherubini, M. Rocchigiani et al., 2012 Myc regulates the transcription of the PRC2 gene to control the expression of developmental genes in embryonic stem cells. Mol. Cell. Biol. 32(4): 840-851
48. Oreper, D. G., Y. Cai, L. M. Tarantino, F. Pardo-Manuel de Villena, and W. Valdar, 2017 Inbred strain variant database (ISVDB): a repository for probabilistically informed sequence differences among the collaborative cross strains and their founders. G3 (Bethesda) 7: 1623-1630
49. Perelygin, A. A., S. V. Scherbik, I. B. Zhulin, B. M. Stockman, Y. Li et al., 2002 Positional cloning of the murine flavivirus resistance gene. Proc. Natl. Acad. Sci. USA 99(14): 9322-9327
50. Perlman, R., W. P. Schiemann, M. W. Brooks, H. F. Lodish, and R. A. Weinberg, 2001 TGF-beta-induced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation. Nat. Cell Biol. 3: 708-714
51. Rasmussen, A. L., A. Okumura, M. T. Ferris, R. Green, F. Feldmann et al., 2014 Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance. Science 346(6212): 987-991
52. Scherbik, S. V., J. M. Paranjape, B. M. Stockman, R. H. Silverman, and M. A. Brinton, 2006 RNase L plays a role in the antiviral response to West Nile virus. J. Virol. 80(6): 2987-2999
53. Shaffer, A. L., A. Rosenwald, E. M. Hurt, J. M. Giltnane, L. T. Lam et al., 2001 Signatures of the immune response. Immunity. 15: 375-385
54. Shaw, T., and P. Martin, 2009 Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep. 8: 881-886
55. Shorter, J. R., F. Odet, D. L. Aylor, W. Pan, C.-Y. Kao et al., 2017 Male infertility is responsible for nearly half of the extinction observed in the Collaborative Cross. Genetics 206: 557-572
56. Siddiqui, M. A., and K. Malathi, 2012 RNase L induces autophagy via c-Jun N-terminal kinase and double-stranded RNA-dependent protein kinase signaling pathways. J. Biol. Chem. 287: 43651-43664
57. Smyth, G.K., 2004 Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article3
58. Srivastava, A., A. P. Morgan, M. Najarian, V. K. Sarsani, J. S. Sigmon et al., 2017 The genomes of the collaborative cross. Genetics 206: 537-556
59. Suthar, M. S., D. Y. Ma, S. Thomas, J. M. Lund, N. Zhang et al., 2010 IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog. 6(2): e1000757
60. Suthar, M. S., M. S. Diamond, and M. Gale, Jr., 2013 West Nile virus infection and immunity. Nat. Rev. Microbiol. 2: 115-128
61. Yang, H., J. R.Wang, J. P. Didion, R. J. Buus, T. A. Bell et al., 2011 Subspecific origin and haplotype diversity in the laboratory mouse. Nat. Genet. 43(7): 648-655