Paramyxovirus V proteins interact with the RIG-I/TRIM25 regulatory complex and inhibit RIG-I signaling

Journal of Virology

Volumn 92, Issue 6, 2018, Pages

  Sánchez Aparicio, Maria T ^a   Feinman, Leighland J ^a   García Sastre, Adolfo ^a   Shaw, Megan L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Innate immunity; Interferons; Paramyxovirus; RIG I

Indexed keywords

CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; PROTEIN TRIM25; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; SPROUTY PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN V; DDX58 PROTEIN, HUMAN; MULTIENZYME COMPLEX; TRANSCRIPTION FACTOR; TRIM25 PROTEIN, HUMAN; TRIPARTITE MOTIF PROTEIN; UBIQUITIN PROTEIN LIGASE; V PROTEIN, PARAMYXOVIRUS; VIRAL PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; INHIBITION KINETICS; INNATE IMMUNITY; MEASLES VIRUS; NONHUMAN; PARAMYXOVIRIDAE; PARAMYXOVIRINAE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SENDAI VIRUS; SIGNAL TRANSDUCTION; UBIQUITINATION; A-549 CELL LINE; ANIMAL; DOG; GENETICS; HELA CELL LINE; HUMAN; MDCK CELL LINE; METABOLISM; PARAMYXOVIRUS INFECTION; PHYSIOLOGY; VIRUS REPLICATION;

A549 CELLS; ANIMALS; DEAD BOX PROTEIN 58; DOGS; HELA CELLS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MULTIENZYME COMPLEXES; PARAMYXOVIRIDAE; PARAMYXOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRIPARTITE MOTIF PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85042473241     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01960-17     Document Type: Article

References (60)

1. Epstein JH, Rahman SA, Pulliam JRC, Hassan SS, Halpin K, Smith CS, Jamaluddin AA, Chua KB, Field HE, Hyatt A, Lam SK, Dobson A, Daszak P. 2008. The emergence of Nipah virus in Malaysia: the role of Pteropus bats as hosts and agricultural expansion as a key factor for zoonotic spillover. Int J Infect Dis 12:e46. https://doi.org/10.1016/j.ijid.2008.05.007
2. Lo MK, Rota PA. 2008. The emergence of Nipah virus, a highly pathogenic paramyxovirus. J Clin Virol 43:396-400. https://doi.org/10.1016/j .jcv.2008.08.007
3. Eaton BT, Broder CC, Middleton D, Wang LF. 2006. Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4:23-35. https://doi .org/10.1038/nrmicro1323
4. Goodbourn S, Randall RE. 2009. The regulation of type I interferon production by paramyxoviruses. J Interferon Cytokine Res 29:539-547. https://doi.org/10.1089/jir.2009.0071
5. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, Goodbourn S, Randall RE. 2004. The V proteins of paramyxoviruses bind the IFNinducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101:17264-17269. https://doi.org/ 10.1073/pnas.0407639101
6. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730-737. https://doi.org/10.1038/ni1087
7. Kawai T, Akira S. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143:1-20. https://doi.org/10.1196/annals.1443.020
8. Seth RB, Sun L, Chen ZJ. 2006. Antiviral innate immunity pathways. Cell Res 16:141-147. https://doi.org/10.1038/sj.cr.7310019
9. Wilkins C, Gale M, Jr. 2010. Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22:41-47. https://doi.org/10.1016/j.coi.2009.12.003
10. Gotoh B, Komatsu T, Takeuchi K, Yokoo J. 2002. Paramyxovirus strategies for evading the interferon response. Rev Med Virol 12:337-357. https:// doi.org/10.1002/rmv.357
11. Ramachandran A, Horvath CM. 2009. Paramyxovirus disruption of interferon signal transduction: STATus report. J Interferon Cytokine Res 29: 531-537. https://doi.org/10.1089/jir.2009.0070
12. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K, Foy E, Loo YM, Gale M, Jr, Akira S, Yonehara S, Kato A, Fujita T. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175:2851-2858. https://doi.org/10.4049/jimmunol.175.5.2851
13. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105. https://doi.org/10.1038/nature04734
14. Ikegame S, Takeda M, Ohno S, Nakatsu Y, Nakanishi Y, Yanagi Y. 2010. Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/beta interferon in measles virus-infected human cells. J Virol 84:372-379. https://doi.org/10.1128/JVI.01690-09
15. Yoneyama M, Fujita T. 2009. RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 227:54-65. https://doi.org/10.1111/j .1600-065X.2008.00727.x
16. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol Rev 227:75-86. https://doi.org/10.1111/j.1600-065X.2008.00737.x
17. Satoh T, Kato H, Kumagai Y, Yoneyama M, Sato S, Matsushita K, Tsujimura T, Fujita T, Akira S, Takeuchi O. 2010. LGP2 is a positive regulator of RIG-Iand MDA5-mediated antiviral responses. Proc Natl Acad Sci U S A 107: 1512-1517. https://doi.org/10.1073/pnas.0912986107
18. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172. https://doi.org/10.1038/nature04193
19. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122:669-682. https://doi.org/10.1016/j.cell.2005.08.012
20. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 6:981-988. https://doi.org/10 .1038/ni1243
21. Rothenfusser S, Goutagny N, DiPerna G, Gong M, Monks BG, Schoenemeyer A, Yamamoto M, Akira S, Fitzgerald KA. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J Immunol 175:5260-5268. https://doi.org/10 .4049/jimmunol.175.8.5260
22. Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, Gerlier D. 2007. Cytosolic 5=-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2:e279. https://doi.org/10.1371/journal.pone.0000279
23. Habjan M, Andersson I, Klingstrom J, Schumann M, Martin A, Zimmermann P, Wagner V, Pichlmair A, Schneider U, Muhlberger E, Mirazimi A, Weber F. 2008. Processing of genome 5= termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS One 3:e2032. https://doi.org/10.1371/journal.pone.0002032
24. Baum A, Sachidanandam R, García-Sastre A. 2010. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci U S A 107:16303-16308. https://doi.org/ 10.1073/pnas.1005077107
25. Baum A, García-Sastre A. 2011. Differential recognition of viral RNA by RIG-I. Virulence 2:166-169. https://doi.org/10.4161/viru.2.2.15481
26. Luthra P, Sun D, Silverman RH, He B. 2011. Activation of IFN-γ [sic] expression by a viral mRNA through RNase L and MDA5. Proc Natl Acad Sci U S A 108:2118-2123. https://doi.org/10.1073/pnas.1012409108
27. Childs K, Stock N, Ross C, Andrejeva J, Hilton L, Skinner M, Randall R, Goodbourn S. 2007. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359:190-200. https://doi.org/10 .1016/j.virol.2006.09.023
28. Parisien JP, Bamming D, Komuro A, Ramachandran A, Rodriguez JJ, Barber G, Wojahn RD, Horvath CM. 2009. A shared interface mediates paramyxovirus interference with antiviral RNA helicases MDA5 and LGP2. J Virol 83:7252-7260. https://doi.org/10.1128/JVI.00153-09
29. Childs KS, Andrejeva J, Randall RE, Goodbourn S. 2009. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J Virol 83:1465-1473. https://doi.org/10.1128/JVI.01768-08
30. Ramachandran A, Horvath CM. 2010. Dissociation of paramyxovirus interferon evasion activities: universal and virus-specific requirements for conserved V protein amino acids in MDA5 interference. J Virol 84:11152-11163. https://doi.org/10.1128/JVI.01375-10
31. Motz C, Schuhmann KM, Kirchhofer A, Moldt M, Witte G, Conzelmann KK, Hopfner KP. 2013. Paramyxovirus V proteins disrupt the fold of the RNA sensor MDA5 to inhibit antiviral signaling. Science 339:690-693. https:// doi.org/10.1126/science.1230949
32. Davis ME, Wang MK, Rennick LJ, Full F, Gableske S, Mesman AW, Gringhuis SI, Geijtenbeek TB, Duprex WP, Gack MU. 2014. Antagonism of the phosphatase PP1 by the measles virus V protein is required for innate immune escape of MDA5. Cell Host Microbe 16:19-30. https://doi.org/ 10.1016/j.chom.2014.06.007
33. Sakaguchi T, Irie T, Kuwayama M, Ueno T, Yoshida A, Kawabata R. 2011. Analysis of interaction of Sendai virus V protein and melanoma differentiation-associated gene 5. Microbiol Immunol 55:760-767. https://doi.org/10.1111/j.1348-0421.2011.00379.x
34. Childs K, Randall R, Goodbourn S. 2012. Paramyxovirus V proteins interact with the RNA helicase LGP2 to inhibit RIG-I-dependent interferon induction. J Virol 86:3411-3421. https://doi.org/10.1128/JVI.06405-11
35. Rodriguez KR, Horvath CM. 2014. Paramyxovirus V protein interaction with the antiviral sensor LGP2 disrupts MDA5 signaling enhancement but is not relevant to LGP2-mediated RLR signaling inhibition. J Virol 88:8180-8188. https://doi.org/10.1128/JVI.00737-14
36. Nistal-Villán E, Gack MU, Martinez-Delgado G, Maharaj NP, Inn KS, Yang H, Wang R, Aggarwal AK, Jung JU, García-Sastre A. 2010. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-beta production. J Biol Chem 285:20252-20261. https://doi.org/10.1074/jbc.M109.089912
37. Gack MU, Nistal-Villán E, Inn KS, García-Sastre A, Jung JU. 2010. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J Virol 84:3220-3229. https://doi.org/10.1128/JVI.02241-09
38. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU. 2013. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38:437-449. https://doi.org/10.1016/j.immuni.2012.11.018
39. Loo YM, Gale M, Jr. 2011. Immune signaling by RIG-I-like receptors. Immunity 34:680-692. https://doi.org/10.1016/j.immuni.2011.05.003
40. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916-920. https://doi.org/10.1038/nature05732
41. Zeng W, Sun L, Jiang X, Chen X, Hou F, Adhikari A, Xu M, Chen ZJ. 2010. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141:315-330. https://doi.org/10.1016/j.cell.2010.03.029
42. Patel JR, Jain A, Chou YY, Baum A, Ha T, García-Sastre A. 2013. ATPasedriven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon. EMBO Rep 14:780-787. https://doi.org/10.1038/embor .2013.102
43. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, Grishin NV, Chen ZJ. 2012. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36: 959-973. https://doi.org/10.1016/j.immuni.2012.03.022
44. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, Farzan M, Inoue S, Jung JU, García-Sastre A. 2009. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5:439-449. https://doi.org/10.1016/j .chom.2009.04.006
45. Beaty SM, Park A, Won ST, Hong P, Lyons M, Vigant F, Freiberg AN, tenOever BR, Duprex WP, Lee B. 2017. Efficient and robust Paramyxoviridae reverse genetics systems. mSphere 2:e00376-16. https://doi.org/ 10.1128/mSphere.00376-16
46. Sánchez-Aparicio MT, Ayllon J, Leo-Macias A, Wolff T, García-Sastre A. 2017. Subcellular localizations of RIG-I, TRIM25, and MAVS complexes. J Virol 91:e01155-16. https://doi.org/10.1128/JVI.01155-16
47. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, Chignard M, Si-Tahar M. 2007. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 178:3368-3372. https://doi.org/10.4049/ jimmunol.178.6.3368
48. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, García-Sastre A, Katze MG, Gale M, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82: 335-345. https://doi.org/10.1128/JVI.01080-07
49. Shaw ML, Cárdenas WB, Zamarin D, Palese P, Basler CF. 2005. Nuclear localization of the Nipah virus W protein allows for inhibition of both virus-and Toll-like receptor 3-triggered signaling pathways. J Virol 79:6078-6088. https://doi.org/10.1128/JVI.79.10.6078-6088.2005
50. Ciancanelli MJ, Volchkova VA, Shaw ML, Volchkov VE, Basler CF. 2009. Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism. J Virol 83:7828-7841. https://doi.org/10.1128/JVI.02610-08
51. Hu Y, Li W, Gao T, Cui Y, Jin Y, Li P, Ma Q, Liu X, Cao C. 2017. The severe acute respiratory syndrome coronavirus nucleocapsid inhibits type I interferon production by interfering with TRIM25-mediated RIG-I ubiquitination. J Virol 91:e02143-16. https://doi.org/10.1128/JVI.02143-16
52. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108: 193-199. https://doi.org/10.1016/0378-1119(91)90434-D
53. Shaw ML, García-Sastre A, Palese P, Basler CF. 2004. Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J Virol 78:5633-5641. https://doi.org/10.1128/JVI.78.11.5633-5641.2004
54. Cárdenas WB, Loo YM, Gale M, Jr, Hartman AL, Kimberlin CR, Martinez-Sobrido L, Saphire EO, Basler CF. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J Virol 80:5168-5178. https://doi.org/10 .1128/JVI.02199-05
55. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cárdenas WB, Yount JS, Moran TM, Basler CF, Komuro A, Horvath CM, Xavier R, Ting AT. 2008. The tumour suppressor CYLD is a negative regulator of RIG-Imediated antiviral response. EMBO Rep 9:930-936. https://doi.org/10 .1038/embor.2008.136
56. Mibayashi M, Martinez-Sobrido L, Loo YM, Cárdenas WB, Gale M, Jr, García-Sastre A. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81:514-524. https://doi.org/10.1128/JVI.01265-06
57. Rajsbaum R, Albrecht RA, Wang MK, Maharaj NP, Versteeg GA, Nistal-Villán E, García-Sastre A, Gack MU. 2012. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog 8:e1003059. https://doi.org/10.1371/journal.ppat.1003059
58. Donald HB, Isaacs A. 1954. Counts of influenza virus particles. J Gen Microbiol 10:457-464. https://doi.org/10.1099/00221287-10-3-457
59. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R. 2007. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72-83. https://doi.org/10 .1016/j.virol.2006.09.049
60. Kulkarni S, Volchkova V, Basler CF, Palese P, Volchkov VE, Shaw ML. 2009. Nipah virus edits its P gene at high frequency to express the V and W proteins. J Virol 83:3982-3987. https://doi.org/10.1128/JVI.02599-08