Helicases in Antiviral Immunity: Dual Properties as Sensors and Effectors

Trends in Biochemical Sciences

Volumn 40, Issue 10, 2015, Pages 576-585

  Ahmad, Sadeem ^a,b   Hur, Sun ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Antiviral immunity; Dicer; Dicer like helicase; Helicase; MDA5; RIG I

Indexed keywords

CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; DICER; DICER RELATED RNA HELICASE 1; DICER RELATED RNA HELICASE 3; DOUBLE STRANDED RNA; HELICASE; INTERFERON STIMULATED GENE FACTOR 3; MELANOMA DIFFERENTIATION ASSOCIATED GENE 5; PROTEIN KINASE R; RECA PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; DEAD BOX PROTEIN; RIBONUCLEASE III;

AMINO TERMINAL SEQUENCE; ANTIVIRAL IMMUNITY; BIOGENESIS; CAENORHABDITIS ELEGANS; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; COMPLEX FORMATION; EFFECTOR CELL; ENDOSOME; GENE SILENCING; INNATE IMMUNITY; MICROORGANISM DETECTION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; RNA BINDING; RNA INTERFERENCE; SIGNAL DETECTION; UPREGULATION; VIRUS GENOME; VIRUS IMMUNITY; VIRUS INFECTION; ANIMAL; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DEAD-BOX RNA HELICASES; HUMANS; IMMUNITY, INNATE; RIBONUCLEASE III; SIGNAL TRANSDUCTION; VIRUS DISEASES;

EID: 84942097640     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.08.001     Document Type: Review

References (91)

1. Wilson G.G. Organization of restriction-modification systems. Nucleic Acids Res. 1991, 19:2539-2566.
2. Linder P., Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 2011, 12:505-516.
3. Bleichert F., Baserga S.J. The long unwinding road of RNA helicases. Mol. Cell 2007, 27:339-352.
4. Putnam A.A., Jankowsky E. DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim. Biophys. Acta 2013, 1829:884-893.
5. Pyle A.M. RNA helicases and remodeling proteins. Curr. Opin. Chem. Biol. 2011, 15:636-642.
6. Luo D., et al. Duplex RNA activated ATPases (DRAs): platforms for RNA sensing, signaling and processing. RNA Biol. 2013, 10:111-120.
7. Sato S., et al. The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 2015, 42:123-132.
8. Weber M., et al. Influenza virus adaptation PB2-627K modulates nucleocapsid inhibition by the pathogen sensor RIG-I. Cell Host Microbe 2015, 17:309-319.
9. Yao H., et al. ATP-Dependent effector-like functions of RIG-I-like receptors. Mol. Cell 2015, 58:541-548.
10. Ding S.W. RNA-based antiviral immunity. Nat. Rev. Immunol. 2010, 10:632-644.
11. Zhang Z., et al. DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cell. Immunity 2011, 34:866-878.
12. Zhang Z., et al. DHX9 pairs with IPS-1 to sense double-stranded RNA in myeloid dendritic cells. J. Immunol. 2011, 187:4501-4508.
13. Moy R.H., et al. Stem-loop recognition by DDX17 facilitates miRNA processing and antiviral defense. Cell 2014, 158:764-777.
14. Yoneyama M., Fujita T. Recognition of viral nucleic acids in innate immunity. Rev. Med. Virol. 2010, 20:4-22.
15. Kang D.C., et al. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:637-642.
16. Yoneyama M., et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5:730-737.
17. Andrejeva J., et al. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-promoter. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17264-17269.
18. Ramos H.J., Gale M. RIG-I like receptors and their signaling crosstalk in the regulation of antiviral immunity. Curr. Opin. Virol. 2011, 1:167-176.
19. Wu B., Hur S. How RIG-I like receptors activate MAVS. Curr. Opin. Virol. 2015, 12:91-98.
20. Nishino T., et al. Crystal structure and functional implications of Pyrococcus furiosus hef helicase domain involved in branched DNA processing. Structure 2005, 13:143-153.
21. Jiang F., et al. Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 2011, 479:423-427.
22. Vela A., et al. The thermodynamic basis for viral RNA detection by the RIG-I innate immune sensor. J. Biol. Chem. 2012, 287:42564-42573.
23. Kowalinski E., et al. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011, 147:423-435.
24. Luo D., et al. Structural insights into RNA recognition by RIG-I. Cell 2011, 147:409-422.
25. Wu B., et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 2013, 152:276-289.
26. Berke I.C., et al. MDA5 assembles into a polar helical filament on dsRNA. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18437-18441.
27. Peisley A., et al. Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:21010-21015.
28. Wang Y., et al. Structural and functional insights into 5'-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat. Struct. Mol. Biol. 2010, 17:781-787.
29. Lu C., et al. The structural basis of 5' triphosphate double-stranded RNA recognition by RIG-I C-terminal domain. Structure 2010, 18:1032-1043.
30. Schlee M., et al. Recognition of 5' triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 2009, 31:25-34.
31. Goubau D., et al. Antiviral immunity via RIG-I-mediated recognition of RNA bearing 5'-diphosphates. Nature 2014, 514:372-375.
32. Peisley A., et al. Kinetic mechanism for viral dsRNA length discrimination by MDA5 filament. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E3340-E3349.
33. del Toro Duany Y., et al. MDA5-filament, dynamics and disease. Curr. Opin. Virol. 2015, 12:20-25.
34. Zeng W., et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.
35. Myong S., et al. Cytosolic viral sensor RIG-I is a 5'-triphosphate-dependent translocase on double-stranded RNA. Science 2009, 323:1070-1074.
36. Peisley A., et al. RIG-I forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Mol. Cell 2013, 51:573-583.
37. Patel J.R., et al. ATPase-driven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon. EMBO Rep. 2013, 14:780-787.
38. Kohlway A., et al. Defining the functional determinants for RNA surveillance by RIG-I. EMBO Rep. 2013, 14:772-779.
39. Peisley A., et al. Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature 2014, 509:110-114.
40. Luo D., et al. Visualizing the determinants of viral RNA recognition by innate immune sensor RIG-I. Structure 2012, 20:1983-1988.
41. Bamming D., Horvath C.M. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I, and LGP2. J. Biol. Chem. 2009, 284:9700-9712.
42. Rice G.I., et al. Gain-of-function mutations in IFIH1 cause a spectrum of human disease phenotypes associated with upregulated type I interferon signaling. Nat. Genet. 2014, 46:503-509.
43. Schoggins J.W., et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
44. Yoneyama M., et al. Shared and unique functions of the DExD/H-Box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175:2851-2858.
45. Rothenfusser S., et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 2005, 175:5260-5268.
46. Saito T., et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:582-587.
47. Venkataraman T., et al. Loss of DExD/H Box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 2007, 178:6444-6455.
48. Komuro A., Horvath C.M. RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J. Virol. 2006, 80:12332-12342.
49. Childs K.S., et al. LGP2 plays a critical role in sensitizing mda-5 to activation by double-stranded RNA. PLoS ONE 2013, 8:e64202.
50. Satoh T., et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1512-1517.
51. Bruns A.M., et al. ATP hydrolysis enhances RNA recognition and antiviral signal transduction by the innate immune sensor, laboratory of genetics and physiology 2 (LGP2). J. Biol. Chem. 2013, 288:938-946.
52. Bruns A.M., et al. The innate immune sensor LGP2 activates antiviral signaling by regulating MDA5-RNA interaction and filament assembly. Mol. Cell 2014, 55:771-781.
53. + T cell survival and fitness. Immunity 2012, 37:235-248.
54. Lau P.W., et al. The molecular architecture of human Dicer. Nat. Struct. Mol. Biol. 2012, 19:436-440.
55. Maillard P.V., et al. Antiviral RNA interference in mammalian cells. Science 2013, 342:235-238.
56. Li Y., et al. RNA interference functions as an antiviral immunity mechanism in mammals. Science 2013, 342:231-234.
57. Seo G.J., et al. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 2013, 14:435-445.
58. Morel J.B., et al. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 2002, 14:629-639.
59. van Rij R.P., et al. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 2006, 20:2985-2995.
60. Lu R., et al. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 2005, 436:1040-1043.
61. Wilkins C., et al. RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 2005, 436:1044-1047.
62. Deddouche S., et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat. Immunol. 2008, 9:1425-1432.
63. Paradkar P.N., et al. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PLoS Negl. Trop. Dis. 2014, 8:e2823.
64. Fire A., et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
65. Winston W.M., et al. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 2002, 295:2456-2459.
66. Attarzadeh-Yazdi G., et al. Cell-to-cell spread of the RNA interference response suppresses Semliki Forest Virus (SFV) infection of mosquito cell cultures and cannot be antagonized by SFV. J. Virol. 2009, 83:5735-5748.
67. Ding S-W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
68. Diaz-Pendon J.A., et al. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 2007, 19:2053-2063.
69. Deleris A., et al. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 2006, 313:68-71.
70. Lee Y.S., et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
71. Galiana-Arnoux D., et al. Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat. Immunol. 2006, 7:590-597.
72. Wang X.H., et al. RNA interference directs innate immunity against viruses in adult Drosophila. Science 2006, 312:452-454.
73. Paradkar P.N., et al. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18915-18920.
74. Nykanen A., et al. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 2001, 107:309-321.
75. Berstein E., et al. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
76. Cenik E.S., et al. Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driven ribonuclease. Mol. Cell 2011, 42:172-184.
77. Welker N.C., et al. Dicer's helicase domain discriminates dsRNA termini to promote an altered reaction mode. Mol. Cell 2011, 41:589-599.
78. Sinha N.K., et al. Drosophila Dicer-2 cleavage is mediated by helicase- and dsRNA termini-dependent states that are modulated by Loquacious-PD. Mol. Cell 2015, 58:406-417.
79. Ketting R.F., et al. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 2001, 15:2654-2659.
80. Colmenares S.U., et al. Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol. Cell 2007, 27:449-461.
81. Ma E., et al. Autoinhibition of human dicer by its internal helicase domain. J. Mol. Biol. 2008, 380:237-243.
82. Flemr M., et al. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 2013, 155:807-816.
83. Sawh A.N., Duchaine T.F. A truncated form of dicer tilts the balance of RNA interference pathways. Cell Rep. 2013, 4:454-463.
84. Sarkies P., Miska E.A. RNAi pathways in the recognition of foreign RNA: antiviral responses and host-parasite interactions in nematodes. Biochem. Soc. Trans. 2013, 41:876-880.
85. Pak J., Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 2007, 315:241-244.
86. Sijen T., et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 2001, 107:465-476.
87. Tabara H., et al. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 2002, 109:861-871.
88. Guo X., et al. Homologous RIG-I-like helicase proteins direct RNAi-mediated antiviral immunity in C. elegans by distinct mechanisms. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16085-16090.
89. Ashe A., et al. A deletion polymorphism in the Caenorhabditis elegans RIG-I homolog disables viral RNA dicing and antiviral immunity. Elife 2013, 2:e00994.
90. Gu W., et al. Distinct Argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol. Cell 2009, 36:231-244.
91. Fitzgerald M.E., et al. Dicer-related helicase 3 forms an obligate dimer for recognizing 22G-RNA. Nucleic Acids Res. 2014, 42:3919-3930.