Activation of RNase L is dependent on OAS3 expression during infection with diverse human viruses

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 8, 2016, Pages 2241-2246

  Li, Yize ^a   Banerjee, Shuvojit ^b   Wang, Yuyan ^a,c   Goldstein, Stephen A ^a   Dong, Beihua ^b   Gaughan, Christina ^b   Silverman, Robert H ^b   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c FUDAN UNIVERSITY   (China)

Author keywords

2 5A; Antiviral response; Oligoadenylate synthetase 3; Ribonuclease L; Type I interferon

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; CRISPR ASSOCIATED PROTEIN; OAS3 PROTEIN; RIBONUCLEASE L; UNCLASSIFIED DRUG; 2',5'-OLIGOADENYLATE SYNTHETASE 2, HUMAN; 2-5A-DEPENDENT RIBONUCLEASE; OAS1 PROTEIN, HUMAN; OAS3 PROTEIN, HUMAN; RIBONUCLEASE; RIBOSOME RNA; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; CELL LYSATE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DNA VIRUS; ENCEPHALOMYOCARDITIS VIRUS; ENZYME ACTIVATION; GENE EXPRESSION; GENETIC TRANSFECTION; INFLUENZA VIRUS; LA CROSSE VIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA VIRUS; SINDBIS VIRUS; STABLE EXPRESSION; VACCINIA VIRUS; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION; WEST NILE VIRUS; WILD TYPE; ALPHAVIRUS INFECTION; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL LINE; CRISPR CAS SYSTEM; GENE INACTIVATION; GENETICS; HUMAN; INFLUENZA; METABOLISM; VACCINIA; WEST NILE FEVER;

2',5'-OLIGOADENYLATE SYNTHETASE; ALPHAVIRUS INFECTIONS; CELL LINE; CRISPR-CAS SYSTEMS; ENDORIBONUCLEASES; ENZYME ACTIVATION; GENE KNOCKOUT TECHNIQUES; HUMANS; INFLUENZA, HUMAN; MODELS, BIOLOGICAL; RNA, RIBOSOMAL; RNA, VIRAL; SINDBIS VIRUS; VACCINIA; VIRUS DISEASES; WEST NILE FEVER;

EID: 84959253492     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1519657113     Document Type: Article

References (49)

1. Silverman RH (2007) Viral encounters with 2', 5'-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81(23):12720-12729.
2. Kristiansen H, Gad HH, Eskildsen-Larsen S, Despres P, Hartmann R (2011) The oligoadenylate synthetase family: An ancient protein family with multiple antiviral activities. J Interferon Cytokine Res 31(1):41-47.
3. Ibsen MS, et al. (2015) Structural and functional analysis reveals that human OASL binds dsRNA to enhance RIG-I signaling. Nucleic Acids Res 43(10):5236-5248.
4. Hornung V, Hartmann R, Ablasser A, Hopfner KP (2014) OAS proteins and cGAS: Unifying concepts in sensing and responding to cytosolic nucleic acids. Nat Rev Immunol 14(8):521-528.
5. Silverman RH, Weiss SR (2014) Viral phosphodiesterases that antagonize double-stranded RNA signaling to RNase L by degrading 2-5A. J Interferon Cytokine Res 34(6):455-463.
6. Drappier M, Michiels T (2015) Inhibition of the OAS/RNase L pathway by viruses. Curr Opin Virol 15:19-26.
7. Lee MS, Kim B, Oh GT, Kim YJ (2013) OASL1 inhibits translation of the type I interferon- regulating transcription factor IRF7. Nat Immunol 14(4):346-355.
8. Zhu J, et al. (2014) Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity 40(6):936-948.
9. Lim JK, et al. (2009) Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog 5(2):e1000321.
10. Mandal S, Abebe F, Chaudhary J (2011) 2'-5' oligoadenylate synthetase 1 polymorphism is associated with prostate cancer. Cancer 117(24):5509-5518.
11. Field LL, et al. (2005) OAS1 splice site polymorphism controlling antiviral enzyme activity influences susceptibility to type 1 diabetes. Diabetes 54(5):1588-1591.
12. Fedetz M, et al. (2006) OAS1 gene haplotype confers susceptibility to multiple sclerosis. Tissue Antigens 68(5):446-449.
13. Qi LS, et al. (2013) Repurposing CRISPR as an RNA-guided platform for sequencespecific control of gene expression. Cell 152(5):1173-1183.
14. Shalem O, et al. (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343(6166):84-87.
15. Silverman RH, Skehel JJ, James TC, Wreschner DH, Kerr IM (1983) rRNA cleavage as an index of ppp(A2'p)nA activity in interferon-treated encephalomyocarditis virusinfected cells. J Virol 46(3):1051-1055.
16. Schroeder A, et al. (2006) The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3.
17. Thakur CS, Xu Z, Wang Z, Novince Z, Silverman RH (2005) A convenient and sensitive fluorescence resonance energy transfer assay for RNase L and 2', 5' oligoadenylates. Methods Mol Med 116:103-113.
18. Min JY, Krug RM (2006) The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2'-5' oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci USA 103(18):7100-7105.
19. Cooper DA, et al. (2015) RNase L targets distinct sites in influenza A virus RNAs. J Virol 89(5):2764-2776.
20. García-Sastre A, et al. (1998) Influenza A virus lacking the NS1 gene replicates in interferon- deficient systems. Virology 252(2):324-330.
21. Beattie E, et al. (1995) Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J Virol 69(1):499-505.
22. Xiang Y, et al. (2002) Blockade of interferon induction and action by the E3L doublestranded RNA binding proteins of vaccinia virus. J Virol 76(10):5251-5259.
23. Kjær KH, et al. (2014) Mitochondrial localization of the OAS1 p46 isoform associated with a common single nucleotide polymorphism. BMC Cell Biol 15:33.
24. Rasheed S, Nelson-Rees WA, Toth EM, Arnstein P, Gardner MB (1974) Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33(4):1027-1033.
25. Donovan J, Whitney G, Rath S, Korennykh A (2015) Structural mechanism of sensing long dsRNA via a noncatalytic domain in human oligoadenylate synthetase 3. Proc Natl Acad Sci USA 112(13):3949-3954.
26. Lin RJ, et al. (2009) Distinct antiviral roles for human 2', 5'-oligoadenylate synthetase family members against dengue virus infection. J Immunol 183(12):8035-8043.
27. Zheng S, et al. (2015) Porcine 2', 5'-oligoadenylate synthetases inhibit Japanese encephalitis virus replication in vitro. J Med Virol, 10.1002/jmv.24397.
28. Bréhin AC, et al. (2009) The large form of human 2', 5'-Oligoadenylate Synthetase (OAS3) exerts antiviral effect against Chikungunya virus. Virology 384(1):216-222.
29. Wells JA, Swyryd EA, Stark GR (1984) An improved method for purifying 2', 5'-oligoadenylate synthetases. J Biol Chem 259(2):1363-1370.
30. Zhao L, et al. (2013) Cell-type-specific activation of the oligoadenylate synthetase- RNase L pathway by a murine coronavirus. J Virol 87(15):8408-8418.
31. Ibsen MS, et al. (2014) The 2'-5'-oligoadenylate synthetase 3 enzyme potently synthesizes the 2'-5'-oligoadenylates required for RNase L activation. J Virol 88(24):14222-14231.
32. Donovan J, Dufner M, Korennykh A (2013) Structural basis for cytosolic doublestranded RNA surveillance by human oligoadenylate synthetase 1. Proc Natl Acad Sci USA 110(5):1652-1657.
33. Ilson DH, Torrence PF, Vilcek J (1986) Two molecular weight forms of human 2', 5'-oligoadenylate synthetase have different activation requirements. J Interferon Res 6(1):5-12.
34. Zhou A, et al. (1997) Interferon action and apoptosis are defective in mice devoid of 2', 5'-oligoadenylate-dependent RNase L. EMBO J 16(21):6355-6363.
35. Castelli JC, et al. (1998) The role of 2'-5' oligoadenylate-activated ribonuclease L in apoptosis. Cell Death Differ 5(4):313-320.
36. Huang H, et al. (2014) Dimeric structure of pseudokinase RNase L bound to 2-5A reveals a basis for interferon-induced antiviral activity. Mol Cell 53(2):221-234.
37. Gack MU, et al. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5(5):439-449.
38. Hall RA, Scherret JH, Mackenzie JS (2001) Kunjin virus: An Australian variant of West Nile? Ann N Y Acad Sci 951:153-160.
39. Frolova EI, et al. (2002) Roles of nonstructural protein nsP2 and Alpha/Beta interferons in determining the outcome of Sindbis virus infection. J Virol 76(22):11254-11264.
40. Oleszak EL, Leibowitz JL, Rodriguez M (1988) Isolation and characterization of two plaque size variants of Theiler's murine encephalomyelitis virus (DA strain). J Gen Virol 69(Pt 9):2413-2418.
41. Hoskins JM, Sanders FK (1957) Propagation of mouse encephalomyocarditis virus in ascites tumour cells maintained in vitro. Br J Exp Pathol 38(3):268-272.
42. Basler CF, et al. (2003) The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J Virol 77(14):7945-7956.
43. Thompson WH, Kalfayan B, Anslow RO (1965) Isolation of California Encephalitis Group Virus from a Fatal Human Illness. Am J Epidemiol 81:245-253.
44. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77(8):4911-4927.
45. Dong B, Silverman RH (1995) 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J Biol Chem 270(8):4133-4137.
46. Wang T, Wei JJ, Sabatini DM, Lander ES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343(6166):80-84.
47. Ran FA, et al. (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8(11):2281-2308.
48. Elbahesh H, Jha BK, Silverman RH, Scherbik SV, Brinton MA (2011) The Flvr-encoded murine oligoadenylate synthetase 1b (Oas1b) suppresses 2-5A synthesis in intact cells. Virology 409(2):262-270.
49. Zhao L, et al. (2012) Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 11(6):607-616.