What really rigs up RIG-I?

Journal of Innate Immunity

Volumn 8, Issue 5, 2016, Pages 429-436

  Barik, Sailen ^a  

^a CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

5 ? Triphosphate; Leader read through transcript; Pathogen associated molecular patterns; Retinoic acid inducible gene 1; Viral RNAs

Indexed keywords

GENOMIC RNA; LEADER READ THROUGH RNA; LEADER RNA; MESSENGER RNA; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN;

INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA STRUCTURE; RNA VIRUS; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; VIRUS; VIRUS INFECTION;

ANIMALS; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMUNITY, INNATE; RECEPTORS, PATTERN RECOGNITION; RNA, VIRAL; VIRUS DISEASES; VIRUSES;

EID: 84979021427     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000447947     Document Type: Review

References (78)

1. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5: 730-737
2. 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. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105
3. Kell AM, Gale M Jr. RIG-I in RNA virus recognition. Virology 2015; 479-480: 110-121
4. Yoneyama M, Onomoto K, Jogi M, Akaboshi T, Fujita T. Viral RNA detection by RIG-I-like receptors. Curr Opin Immunol 2015; 32: 48-53
5. Wang Y, Ludwig J, Schuberth C, Goldeck M, Schlee M, Li H, Juranek S, Sheng G, Micura R, Tuschl T, Hartmann G, Patel DJ. Structural and functional insights into 5 ' -ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat Struc Mol Biol 2010; 17: 781-787
6. Jiang F, Ramanathan A, Miller MT, Tang G-Q, Gale M, Patel SS, Marcotrigiano J. Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 2011; 479: 423-427
7. Civril F, Bennett M, Moldt M, Deimling T, Witte G, Schiesser S, Carell T, Hopfner KP. The RIG-I ATPase domain structure reveals insights into ATP-dependent antiviral signalling. EMBO Rep 2011; 12: 1127-1134
8. Kowalinski E, Lunardi T, McCarthy AA, Louber J, Brunel J, Grigorov B, Gerlier D, Cusack S. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011; 147: 423-435
9. Beckham SA, Brouwer J, Roth A, Wang D, Sadler AJ, John M, Jahn-Hofmann K, Williams BR, Wilce JA, Wilce MC. Conformational rearrangements of RIG-I receptor on formation of a multiprotein:dsRNA assembly. Nucleic Acids Res 2013; 41: 3436-3445
10. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-988
11. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437: 1167-1172
12. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. VISA is an adapter protein required for virus-Triggered IFN-β signaling. Mol Cell 2005; 19: 727-740
13. Sadler AJ, Williams BRG: Interferon-inducible antiviral effectors. Nat Rev Immunol 2008; 8: 559-568
14. Zinzula L, Tramontano E. Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: hide, mask, hit. Antiviral Res 2013; 100: 615-635
15. Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, Gerlier D. Cytosolic 5 ' -Triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2007; 2:e279
16. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G: 5 ' -Triphosphate RNA is the ligand for RIG-I. Science 2006; 314: 994-997
17. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. RIG-Imediated antiviral responses to single-stranded RNA bearing 5 ' -phosphates. Science 2006; 314: 997-1001
18. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, Barchet W, Coch C, Janke M, Mihailovic A, Wardle G, Juranek S, Kato H, Kawai T, Poeck H, Fitzgerald KA, Takeuchi O, Akira S, Tuschl T, Latz E, Ludwig J, Hartmann G. Recognition of 5 ' triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negativestrand virus. Immunity 2009; 31: 25-34
19. Cazenave C, Uhlenbeck OC. RNA templatedirected RNA synthesis by T7 RNA polymerase. Proc Natl Acad Sci USA 1994; 91: 6972-6976
20. Schlee M, Hartmann G. The chase for the RIG-I ligand - recent advances. Mol Ther 2010; 18: 1254-1262
21. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-Transcribed RNA intermediate. Nat Immunol 2009; 10: 1065-1072
22. Goldeck M, Schlee M, Hartmann G, Hornung V. Enzymatic synthesis and purification of a defined RIG-I ligand. Methods Mol Biol 2014; 1169: 15-25
23. Marques JT, Devosse T, Wang D, Zamanian- Daryoush M, Serbinowski P, Hartmann R, Fujita T, Behlke MA, Williams BR: A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 2006; 24: 559-565
24. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. Length-dependent recognition of double-stranded ribonucleic acids by RIG-I and MDA-5. J Exp Med 2008; 205: 1601-1610
25. Schmidt A, Schwerd T, Hamm W, Hellmuth JC, Cui S, Wenzel M, Hoffmann FS, Michallet MC, Besch R, Hopfner KP, Endres S, Rothenfusser S: 5 ' -Triphosphate RNA requires basepaired structures to activate antiviral signaling via RIG-I. Proc Natl Acad Sci USA 2009; 106: 12067-12072
26. Baum A, Sachidanandam R, Garcia-Sastre A. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci USA 2010; 107: 16303-16308
27. Banerjee AK, Barik S, De BP. Gene expression of nonsegmented negative strand RNA viruses. Pharmacol Ther 1991; 51: 47-70
28. Cowton VM, McGivern DR, Fearns R. Unravelling the complexities of respiratory syncytial virus RNA synthesis. J Gen Virol 2006; 87: 1805-1821
29. Li T, Pattnaik AK. Overlapping signals for transcription and replication at the 3 ' terminus of the vesicular stomatitis virus genome. J Virol 1999; 73: 444-452
30. Cowton VM, Fearns R. Evidence that the respiratory syncytial virus polymerase is recruited to nucleotides 1-11 at the 3 ' end of the nucleocapsid and can scan to access internal signals. J Virol 2005; 79: 11311-11322
31. Fearns R, Peeples ME, Collins PL. Mapping the transcription and replication promoters of respiratory syncytial virus. J Virol 2002; 76: 1663-1672
32. Kuo L, Fearns R, Collins PL. Analysis of the gene start and gene end signals of human respiratory syncytial virus: quasi-Templated initiation at position 1 of the encoded mRNA. J Virol 1997; 71: 4944-4953
33. Harmon SB, Megaw AG, Wertz GW. RNA sequences involved in transcriptional termination of respiratory syncytial virus. J Virol 2001; 75: 36-44
34. Barik S. Transcription of human respiratory syncytial virus genome RNA in vitro: requirement of cellular factor(s). J Virol 1992; 66: 6813-6818
35. Wertz GM, Howard MB, Davis N, Patton J. The switch from transcription to replication of a negative-strand RNA virus. Cold Spring Harb Symp Quant Biol 1987; 52: 367-371
36. Harouaka D, Wertz GW. Second-site mutations selected in transcriptional regulatory sequences compensate for engineered mutations in the vesicular stomatitis virus nucleocapsid protein. J Virol 2012; 86: 11266-11275
37. Albertini AA, Wernimont AK, Muziol T, Ravelli RB, Clapier CR, Schoehn G, Weissenhorn W, Ruigrok RW. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 2006; 313: 360-363
38. Green TJ, Zhang X, Wertz GW, Luo M. Structure of the vesicular stomatitis virus nucleoprotein- RNA complex. Science 2006; 313: 357-360
39. Schoehn G, Mavrakis M, Albertini A, Wade R, Hoenger A, Ruigrok RW. The 12A structure of trypsin-Treated measles virus N-RNA. J Mol Biol 2004; 339: 301-312
40. tenOever BR, Servant MJ, Grandvaux N, Lin R, Hiscott J. Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J Virol 2002; 76: 3659-3669
41. Weber M, Gawanbacht A, Habjan M, Rang A, Borner C, Schmidt AM, Veitinger S, Jacob R, Devignot S, Kochs G, Garcia-Sastre A, Weber F. Incoming RNA virus nucleocapsids containing a 5 ' -Triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 2013; 13: 336-346
42. Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P. Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci USA 1987; 84: 8140-8144
43. Killip MJ, Smith M, Jackson D, Randall RE. Activation of the interferon induction cascade by influenza A viruses requires viral RNA synthesis and nuclear export. J Virol 2014; 88: 3942-3952
44. Lopez CB. Defective viral genomes: critical danger signals of viral infections. J Virol 2014; 88: 8720-8723
45. Fuller FJ, Marcus PI. Interferon induction by viruses. IV. Sindbis virus: early passage defective- interfering particles induce interferon. J Gen Virol 1980; 48: 63-73
46. Strahle L, Garcin D, Kolakofsky D. Sendai virus defective-interfering genomes and the activation of interferon-β. Virology 2006; 351: 101-111
47. Runge S, Sparrer KM, Lassig C, Hembach K, Baum A, Garcia-Sastre A, Soding J, Conzelmann KK, Hopfner KP. In vivo ligands of MDA5 and RIG-I in measles virus-infected cells. PLoS Pathog 2014; 10:e1004081
48. Colonno RJ, Banerjee AK. Complete nucleotide sequence of the leader RNA synthesized in vitro by vesicular stomatitis virus. Cell 1978; 15: 93-101
49. Leppert M, Rittenhouse L, Perrault J, Summers DF, Kolakofsky D. Plus and minus strand leader RNAs in negative strand virusinfected cells. Cell 1979; 18: 735-747
50. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M Jr. Innate immunity induced by composition- dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008; 454: 523-527
51. Bitko V, Musiyenko A, Bayfield MA, Maraia RJ, Barik S. Cellular La protein shields nonsegmented negative-strand RNA viral leader RNA from RIG-I and enhances virus growth by diverse mechanisms. J Virol 2008; 82: 7977-7987
52. Blumberg BM, Kolakofsky D. Intracellular vesicular stomatitis virus leader RNAs are found in nucleocapsid structures. J Virol 1981; 40: 568-576
53. Oh SW, Onomoto K, Wakimoto M, Onoguchi K, Ishidate F, Fujiwara T, Yoneyama M, Kato H, Fujita T. Leader-containing uncapped viral transcript activates RIG-I in antiviral stress granules. PLoS Pathog 2016; 12:e1005444
54. Ray-Soni A, Bellecourt MJ, Landick R. Mechanisms of bacterial transcription termination: all good things must end. Annu Rev Biochem 2016; 85: 319-347
55. Baltimore D, Huang AS, Stampfer M. Ribonucleic acid synthesis of vesicular stomatitis virus, II. An RNA polymerase in the virion. Proc Natl Acad Sci USA 1970; 66: 572-576
56. Kuo L, Fearns R, Collins PL. The structurally diverse intergenic regions of respiratory syncytial virus do not modulate sequential transcription by a dicistronic minigenome. J Virol 1996; 70: 6143-6150
57. Jin H, Cheng X, Traina-Dorge VL, Park HJ, Zhou H, Soike K, Kemble G. Evaluation of recombinant respiratory syncytial virus gene deletion mutants in African green monkeys for their potential as live attenuated vaccine candidates. Vaccine 2003; 21: 3647-3652
58. Maraia RJ, Intine RV. Recognition of nascent RNA by the human La antigen: conserved and divergent features of structure and function. Mol Cell Biol 2001; 21: 367-379
59. Tremaglio CZ, Noton SL, Deflube LR, Fearns R. Respiratory syncytial virus polymerase can initiate transcription from position 3 of the leader promoter. J Virol 2013; 87: 3196-3207
60. Poch O, Sauvaget I, Delarue M, Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 1989; 8: 3867-3874
61. Cartee TL, Megaw AG, Oomens AG, Wertz GW. Identification of a single amino acid change in the human respiratory syncytial virus L protein that affects transcriptional termination. J Virol 2003; 77: 7352-7360
62. Li ML, Weng KF, Shih SR, Brewer G. The evolving world of small RNAs from RNA viruses. Wiley Interdiscip Rev RNA DOI: 10.1002/wrna.1351
63. Hussain M, Asgari S. MicroRNA-like viral small RNA from Dengue virus 2 autoregulates its replication in mosquito cells. Proc Natl Acad Sci USA 2014; 111: 2746-2751
64. Kincaid RP, Sullivan CS. Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathog 2012; 8:e1003018
65. Parameswaran P, Sklan E, Wilkins C, Burgon T, Samuel MA, Lu R, Ansel KM, Heissmeyer V, Einav S, Jackson W, Doukas T, Paranjape S, Polacek C, dos Santos FB, Jalili R, Babrzadeh F, Gharizadeh B, Grimm D, Kay M, Koike S, Sarnow P, Ronaghi M, Ding SW, Harris E, Chow M, Diamond MS, Kirkegaard K, Glenn JS, Fire AZ. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog 2010; 6:e1000764
66. Umbach JL, Yen HL, Poon LL, Cullen BR. Influenza A virus expresses high levels of an unusual class of small viral leader RNAs in infected cells. MBio 2010; 1:e00204-e00210
67. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, Jung JU, Hopfner KP, Ha T. Cytosolic viral sensor RIG-I is a 5 ' -Triphosphatedependent translocase on double-stranded RNA. Science 2009; 323: 1070-1074
68. Peisley A, Wu B, Yao H, Walz T, Hur S. RIGI forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Mol Cell 2013; 51: 573-583
69. Patel JR, Jain A, Chou YY, Baum A, Ha T, Garcia-Sastre A. ATPase-driven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon. EMBO Rep 2013; 14: 780-787
70. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007; 446: 916-920
71. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, Grishin NV, Chen ZJ. Ubiquitin induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 2012; 36: 959-973
72. Zeng W, Sun L, Jiang X, Chen X, Hou F, Adhikari A, Xu M, Chen ZJ. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010; 141: 315-330
73. Peisley A, Wu B, Xu H, Chen ZJ, Hur S. Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature 2014; 509: 110-114
74. Kuniyoshi K, Takeuchi O, Pandey S, Satoh T, Iwasaki H, Akira S, Kawai T. Pivotal role of RNA-binding E3 ubiquitin ligase MEX3C in RIG-I-mediated antiviral innate immunity. Proc Natl Acad Sci USA 2014; 111: 5646-5651
75. Sun Z, Ren H, Liu Y, Teeling JL, Gu J. Phosphorylation of RIG-I by casein kinase II inhibits its antiviral response. J Virol 2011; 85: 1036-1047
76. Nistal-Villan E, Gack MU, Martinez-Delgado G, Maharaj NP, Inn KS, Yang H, Wang R, Aggarwal AK, Jung JU, Garcia-Sastre A. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-β production. J Biol Chem 2010; 285: 20252-20261
77. Gack MU, Nistal-Villan E, Inn KS, Garcia- Sastre A, Jung JU. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J Virol 2010; 84: 3220-3229
78. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 2013; 38: 437-449