Dynamic interaction of stress granules, DDX3X, and IKK-α mediates multiple functions in hepatitis C virus infection

Journal of Virology

Volumn 89, Issue 10, 2015, Pages 5462-5477

  Pène, Véronique ^a   Li, Qisheng ^a   Sodroski, Catherine ^a   Hsu, Ching Sheng ^a   Jake Liang, T ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; I KAPPA B KINASE ALPHA; PROTEIN DDX3X; RNA HELICASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; 3' UNTRANSLATED REGION; CORE PROTEIN; DDX3X PROTEIN, HUMAN; DEAD BOX PROTEIN; I KAPPA B KINASE;

3' UNTRANSLATED REGION; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOPLASM; HEPATITIS C; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SURFACE PROPERTY; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL GRANULE; CELL LINE; GENETICS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HOST PATHOGEN INTERACTION; LIPID METABOLISM; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

HEPATITIS C VIRUS; PENE;

3' UNTRANSLATED REGIONS; CELL LINE; CYTOPLASMIC GRANULES; DEAD-BOX RNA HELICASES; HEPACIVIRUS; HEPATITIS C, CHRONIC; HOST-PATHOGEN INTERACTIONS; HUMANS; I-KAPPA B KINASE; LIPID METABOLISM; MODELS, BIOLOGICAL; VIRAL CORE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84928524897     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03197-14     Document Type: Article

References (58)

1. Heim MH. 2013. Innate immunity and HCV. J Hepatol 58:564-574. http://dx.doi.org/10.1016/j.jhep.2012.10.005.
2. Thimme R, Binder M, Bartenschlager R. 2012. Failure of innate and adaptive immune responses in controlling hepatitis C virus infection. FEMS Microbiol Rev 36:663-683. http://dx.doi.org/10.1111/j.1574-6976.2011.00319.x.
3. Liang TJ. 2013. Current progress in development of hepatitis C virus vaccines. Nat Med 19:869-878. http://dx.doi.org/10.1038/nm.3183.
4. Liang TJ, Ghany MG. 2013. Current and future therapies for hepatitis C virus infection. N Engl J Med 368:1907-1917. http://dx.doi.org/10.1056/NEJMra1213651.
5. McLauchlan J. 2000. Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes. J Viral Hepatitis 7:2-14. http://dx.doi.org/10.1046/j.1365-2893.2000.00201.x.
6. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, Zayas M, Bartenschlager R, Wakita T, Hijikata M, Shimotohno K. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9:1089-1097. http://dx.doi.org/10.1038/ncb1631.
7. Rouillé Y, Helle F, Delgrange D, Roingeard P, Voisset C, Blanchard E, Belouzard S, McKeating J, Patel AH, Maertens G, Wakita T, Wychowski C, Dubuisson J. 2006. Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J Virol 80:2832-2841. http://dx.doi.org/10.1128/JVI.80.6.2832-2841.2006.
8. Abid K, Pazienza V, de Gottardi A, Rubbia-Brandt L, Conne B, Pugnale P, Rossi C, Mangia A, Negro F. 2005. An in vitro model of hepatitis C virus genotype 3a-associated triglycerides accumulation. J Hepatol 42: 744-751. http://dx.doi.org/10.1016/j.jhep.2004.12.034.
9. Boulant S, Douglas MW, Moody L, Budkowska A, Targett-Adams P, McLauchlan J. 2008. Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule-and dynein-dependent manner. Traffic 9:1268-1282. http://dx.doi.org/10.1111/j.1600-0854.2008.00767.x.
10. Rocak S, Linder P. 2004. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5:232-241. http://dx.doi.org/10.1038/nrm1335.
11. Shih JW, Wang WT, Tsai TY, Kuo CY, Li HK, Wu Lee YH. 2012. Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. Biochem J 441:119-129. http://dx.doi.org/10.1042/BJ20110739.
12. Adjibade P, Mazroui R. 2014. Control of mRNA turnover: Implication of cytoplasmic RNA granules. Semin Cell Dev Biol 34:15-23. http://dx.doi.org/10.1016/j.semcdb.2014.05.013.
13. Schroder M. 2010. Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochemical Pharmacol 79:297-306. http://dx.doi.org/10.1016/j.bcp.2009.08.032.
14. Shih JW, Lee YH. 2014. Human DExD/H RNA helicases: Emerging roles in stress survival regulation. Clin Chim Acta 436C:45-58. http://dx.doi.org/10.1016/j.cca.2014.05.003.
15. Oshiumi H, Sakai K, Matsumoto M, Seya T. 2010. DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-betainducing potential. Eur J Immunol 40:940-948. http://dx.doi.org/10.1002/eji.200940203.
16. Schroder M, Baran M, Bowie AG. 2008. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 27:2147-2157. http://dx.doi.org/10.1038/emboj.2008.143.
17. Li C, Ge LL, Li PP, Wang Y, Dai JJ, Sun MX, Huang L, Shen ZQ, Hu XC, Ishag H, Mao X. 2014. Cellular DDX3 regulates Japanese encephalitis virus replication by interacting with viral un-translated regions. Virology 449:70-81. http://dx.doi.org/10.1016/j.virol.2013.11.008.
18. Schroder M. 2011. Viruses and the human DEAD-box helicase DDX3: inhibition or exploitation? Biochem Soc Trans 39:679-683. http://dx.doi.org/10.1042/BST0390679.
19. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, Wakita T, Kato N. 2007. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 81:13922-13926. http://dx.doi.org/10.1128/JVI.01517-07.
20. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, Pfeffer S, Landthaler M, Landgraf P, Kan S, Lindenbach BD, Chien M, Weir DB, Russo JJ, Ju J, Brownstein MJ, Sheridan R, Sander C, Zavolan M, Tuschl T, Rice CM. 2007. Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A 104:12884-12889. http://dx.doi.org/10.1073/pnas.0704894104.
21. Li Q, Pene V, Krishnamurthy S, Cha H, Liang TJ. 2013. Hepatitis C virus infection activates an innate pathway involving IKK-alpha in lipogenesis and viral assembly. Nat Med 19:722-729. http://dx.doi.org/10.1038/nm.3190.
22. Angus AG, Dalrymple D, Boulant S, McGivern DR, Clayton RF, Scott MJ, Adair R, Graham S, Owsianka AM, Targett-Adams P, Li K, Wakita T, McLauchlan J, Lemon SM, Patel AH. 2010. Requirement of cellular DDX3 for hepatitis C virus replication is unrelated to its interaction with the viral core protein. J Gen Virol 91:122-132. http://dx.doi.org/10.1099/vir.0.015909-0.
23. Owsianka AM, Patel AH. 1999. Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257:330-340. http://dx.doi.org/10.1006/viro.1999.9659.
24. Kato T, Matsumura T, Heller T, Saito S, Sapp RK, Murthy K, Wakita T, Liang TJ. 2007. Production of infectious hepatitis C virus of various genotypes in cell cultures. J Virol 81:4405-4411. http://dx.doi.org/10.1128/JVI.02334-06.
25. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Kräusslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796. http://dx.doi.org/10.1038/nm1268.
26. Li Q, Brass AL, Ng A, Hu Z, Xavier RJ, Liang TJ, Elledge SJ. 2009. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc Natl Acad Sci U S A 106:16410-16415. http://dx.doi.org/10.1073/pnas.0907439106.
27. Zhang YY, Zhang BH, Ishii K, Liang TJ. 2010. Novel function of CD81 in controlling hepatitis C virus replication. J Virol 84:3396-3407. http://dx.doi.org/10.1128/JVI.02391-09.
28. Jonas S, Izaurralde E. 2013. The role of disordered protein regions in the assembly of decapping complexes and RNP granules. Genes Dev 27:2628-2641. http://dx.doi.org/10.1101/gad.227843.113.
29. Li Q, Zhang YY, Chiu S, Hu Z, Lan KH, Cha H, Sodroski C, Zhang F, Hsu CS, Thomas E, Liang TJ. 2014. Integrative functional genomics of hepatitis C virus infection identifies host dependencies in complete viral replication cycle. PLoS Pathog 10:e1004163. http://dx.doi.org/10.1371/journal.ppat.1004163.
30. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest JP, Mazur J, Bankhead P, Hiet MS, Kallis S, Alvisi G, Samuel CE, Lohmann V, Kaderali L, Rohr K, Frese M, Stoecklin G, Bartenschlager R. 2012. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12:71-85. http://dx.doi.org/10.1016/j.chom.2012.05.013.
31. Garaigorta U, Heim MH, Boyd B, Wieland S, Chisari FV. 2012. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J Virol 86:11043-11056. http://dx.doi.org/10.1128/JVI.07101-11.
32. Beckham CJ, Parker R. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212. http://dx.doi.org/10.1016/j.chom.2008.03.004.
33. Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem Sci 33:141-150. http://dx.doi.org/10.1016/j.tibs.2007.12.003.
34. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15:5383-5398. http://dx.doi.org/10.1091/mbc.E04-08-0715.
35. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160:823-831. http://dx.doi.org/10.1083/jcb.200212128.
36. White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305. http://dx.doi.org/10.1016/j.chom.2007.08.006.
37. White JP, Lloyd RE. 2012. Regulation of stress granules in virus systems. Trends Microbiol 20:175-183. http://dx.doi.org/10.1016/j.tim.2012.02.001.
38. Smith JA, Schmechel SC, Raghavan A, Abelson M, Reilly C, Katze MG, Kaufman RJ, Bohjanen PR, Schiff LA. 2006. Reovirus induces and benefits from an integrated cellular stress response. J Virol 80:2019-2033. http://dx.doi.org/10.1128/JVI.80.4.2019-2033.2006.
39. Lindquist ME, Lifland AW, Utley TJ, Santangelo PJ, Crowe JE, Jr. 2010. Respiratory syncytial virus induces host RNA stress granules to facilitate viral replication. J Virol 84:12274-12284. http://dx.doi.org/10.1128/JVI.00260-10.
40. Raaben M, Groot Koerkamp MJ, Rottier PJ, de Haan CA. 2007. Mouse hepatitis coronavirus replication induces host translational shutoff and mRNAdecay, with concomitant formation of stress granules and processing bodies. Cell Microbiol 9:2218-2229. http://dx.doi.org/10.1111/j.1462-5822.2007.00951.x.
41. Sola I, Galan C, Mateos-Gomez PA, Palacio L, Zuniga S, Cruz JL, Almazan F, Enjuanes L. 2011. The polypyrimidine tract-binding protein affects coronavirusRNAaccumulation levels and relocalizes viral RNAs to novel cytoplasmic domains different from replication-transcription sites. J Virol 85:5136-5149. http://dx.doi.org/10.1128/JVI.00195-11.
42. Yi Z, Pan T, Wu X, Song W, Wang S, Xu Y, Rice CM, Macdonald MR, Yuan Z. 2011. Hepatitis C virus coopts Ras-GTPase-activating proteinbinding protein 1 for its genome replication. J Virol 85:6996-7004. http://dx.doi.org/10.1128/JVI.00013-11.
43. Ariumi Y, Kuroki M, Kushima Y, Osugi K, Hijikata M, Maki M, Ikeda M, Kato N. 2011. Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J Virol 85:6882-6892. http://dx.doi.org/10.1128/JVI.02418-10.
44. Jones DM, Patel AH, Targett-Adams P, McLauchlan J. 2009. The hepatitis C virus NS4B protein can trans-complement viral RNA replication and modulates production of infectious virus. J Virol 83:2163-2177. http://dx.doi.org/10.1128/JVI.01885-08.
45. Pager CT, Schutz S, Abraham TM, Luo G, Sarnow P. 2013. Modulation of hepatitis C virus RNA abundance and virus release by dispersion of processing bodies and enrichment of stress granules. Virology 435:472-484. http://dx.doi.org/10.1016/j.virol.2012.10.027.
46. Shih JW, Tsai TY, Chao CH, Wu Lee YH. 2008. Candidate tumor suppressor DDX3 RNA helicase specifically represses cap-dependent translation by acting as an eIF4E inhibitory protein. Oncogene 27:700-714. http://dx.doi.org/10.1038/sj.onc.1210687.
47. Geissler R, Golbik RP, Behrens SE. 2012. The DEAD-box helicase DDX3 supports the assembly of functional 80S ribosomes. Nucleic Acids Res 40:4998-5011. http://dx.doi.org/10.1093/nar/gks070.
48. Lai MC, Lee YH, Tarn WY. 2008. The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tipassociated protein and participates in translational control. Mol Biol Cell 19:3847-3858. http://dx.doi.org/10.1091/mbc.E07-12-1264.
49. Lee CS, Dias AP, Jedrychowski M, Patel AH, Hsu JL, Reed R. 2008. Human DDX3 functions in translation and interacts with the translation initiation factor eIF3. Nucleic Acids Res 36:4708-4718. http://dx.doi.org/10.1093/nar/gkn454.
50. Hellen CU, Pestova TV. 1999. Translation of hepatitis C virus RNA. J Viral Hepatitis 6:79-87. http://dx.doi.org/10.1046/j.1365-2893.1999.00150.x.
51. Sun C, Querol-Audi J, Mortimer SA, Arias-Palomo E, Doudna JA, Nogales E, Cate JH. 2013. Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation. Nucleic Acids Res 41:7512-7521. http://dx.doi.org/10.1093/nar/gkt510.
52. Mamiya N, Worman HJ. 1999. Hepatitis C virus core protein binds to a DEADboxRNAhelicase. J Biol Chem 274:15751-15756. http://dx.doi.org/10.1074/jbc.274.22.15751.
53. Gawlik K, Baugh J, Chatterji U, Lim PJ, Bobardt MD, Gallay PA. 2014. HCV core residues critical for infectivity also are involved in core-NS5A complex formation. PLoS One 9:e88866. http://dx.doi.org/10.1371/journal.pone.0088866.
54. Hughes M, Griffin S, Harris M. 2009. Domain III of NS5A contributes to both RNA replication and assembly of hepatitis C virus particles. J Gen Virol 90:1329-1334. http://dx.doi.org/10.1099/vir.0.009332-0.
55. Mousseau G, Kota S, Takahashi V, Frick DN, Strosberg AD. 2011. Dimerization-driven interaction of hepatitis C virus core protein with NS3 helicase. J Gen Virol 92:101-111. http://dx.doi.org/10.1099/vir.0.023325-0.
56. Phan T, Kohlway A, Dimberu P, Pyle AM, Lindenbach BD. 2011. The acidic domain of hepatitis C virus NS4A contributes to RNA replication and virus particle assembly. J Virol 85:1193-1204. http://dx.doi.org/10.1128/JVI.01889-10.
57. Popescu CI, Callens N, Trinel D, Roingeard P, Moradpour D, Descamps V, Duverlie G, Penin F, Heliot L, Rouille Y, Dubuisson J. 2011. NS2 protein of hepatitis C virus interacts with structural and nonstructural proteins towards virus assembly. PLoS Pathog 7:e1001278. http://dx.doi.org/10.1371/journal.ppat.1001278.
58. Wen Y, Cheng Kao C. 2014. The hepatitis C virus core protein can modulate RNA-dependentRNAsynthesis by the 2a polymerase. Virus Res 189C:165-176. http://dx.doi.org/10.1016/j.virusres.2014.05.017.