The ATP-dependent RNA helicase DDX3X modulates herpes simplex virus 1 gene expression

Journal of Virology

Volumn 91, Issue 8, 2017, Pages

  Khadivjam, Bita ^a   Stegen, Camille ^a   Hogue Racine, Marc Aurèle ^a   El Bilali, Nabil ^a   Döhner, Katinka ^b   Sodeik, Beate ^b   Lippé, Roger ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

DDX3X; DNA virus; Helicase; Herpes; Herpes simplex virus; Host pathogen interaction; Host pathogen interactions; Interferon; RNA virus; Transcriptional regulation; Translational control

Indexed keywords

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ATP DEPENDENT RNA HELICASE DDX3X; BETA INTERFERON; UNCLASSIFIED DRUG; DDX3X PROTEIN, HUMAN; DEAD BOX PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME LOCALIZATION; GENE DUPLICATION; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; NONHUMAN; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; VIRION; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 85016550937     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02411-16     Document Type: Article

References (35)

1. Ditton HJ, Zimmer J, Kamp C, Rajpert-De Meyts E, Vogt PH. 2004. The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control. Hum Mol Genet 13: 2333-2341. https://doi.org/10.1093/hmg/ddh240.
2. Sharma D, Jankowsky E. 2014. The Ded1/DDX3 subfamily of DEAD-box RNA helicases. Crit Rev Biochem Mol Biol 49:343-360. https://doi.org/10.3109/10409238.2014.931339.
3. 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. https://doi.org/10.1128/JVI.01517-07.
4. 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. https://doi.org/10.1073/pnas.0704894104.
5. Ko C, Lee S, Windisch MP, Ryu WS. 2014. DDX3 DEAD-box RNA helicase is a host factor that restricts hepatitis B virus replication at the transcriptional level. J Virol 88:13689-13698. https://doi.org/10.1128/JVI.02035-14.
6. Vashist S, Urena L, Chaudhry Y, Goodfellow I. 2012. Identification of RNA-protein interaction networks involved in the norovirus life cycle. J Virol 86:11977-11990. https://doi.org/10.1128/JVI.00432-12.
7. Chahar HS, Chen S, Manjunath N. 2013. P-body components LSM1, GW182, DDX3, DDX6 and XRN1 are recruited to WNV replication sites and positively regulate viral replication. Virology 436:1-7. https://doi.org/10.1016/j.virol.2012.09.041.
8. Yedavalli VS, Neuveut C, Chi YH, Kleiman L, Jeang KT. 2004. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119:381-392. https://doi.org/10.1016/j.cell.2004.09.029.
9. Wang H, Kim S, Ryu WS. 2009. DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. J Virol 83:5815-5824. https://doi.org/10.1128/JVI.00011-09.
10. Soulat D, Burckstummer T, Westermayer S, Goncalves A, Bauch A, Stefanovic A, Hantschel O, Bennett KL, Decker T, Superti-Furga G. 2008. The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J 27:2135-2146. https://doi.org/10.1038/emboj.2008.126.
11. Gu L, Fullam A, Brennan R, Schroder M. 2013. Human DEAD box helicase 3 couples IκB kinase epsilon to interferon regulatory factor 3 activation. Mol Cell Biol 33:2004-2015. https://doi.org/10.1128/MCB.01603-12.
12. Wang H, Ryu WS. 2010. Hepatitis B virus polymerase blocks pattern recognition receptor signaling via interaction with DDX3: implications for immune evasion. PLoS Pathog 6:e1000986. https://doi.org/10.1371/journal.ppat.1000986.
13. 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. https://doi.org/10.1038/emboj.2008.143.
14. Pellett PE, Roizman B. 2007. The family Herpesviridae: a brief introduction, p 2479-2500. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
15. Weir JP. 2001. Regulation of herpes simplex virus gene expression. Gene 271:117-130. https://doi.org/10.1016/S0378-1119(01)00512-1.
16. Loret S, Guay G, Lippé R. 2008. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol 82:8605-8618. https://doi.org/10.1128/JVI.00904-08.
17. Loret S, Lippé R. 2012. Biochemical analysis of infected cell polypeptide (ICP)0, ICP4, UL7 and UL23 incorporated into extracellular herpes simplex virus type 1 virions. J Gen Virol 93:624-634. https://doi.org/10.1099/vir.0.039776-0.
18. Everett RD. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770. https://doi.org/10.1002/1521-1878(200008)22:8761::AID-BIES103.0.CO;2-A.
19. Watson RJ, Clements JB. 1980. A herpes simplex virus type 1 function continuously required for early and late virus RNA synthesis. Nature 285:329-330. https://doi.org/10.1038/285329a0.
20. Yang WC, Devi-Rao GV, Ghazal P, Wagner EK, Triezenberg SJ. 2002. General and specific alterations in programming of global viral gene expression during infection by VP16 activation-deficient mutants of herpes simplex virus type 1. J Virol 76:12758-12774. https://doi.org/10.1128/JVI.76.24.12758-12774.2002.
21. Stegen C, Yakova Y, Henaff D, Nadjar J, Duron J, Lippé R. 2013. Analysis of virion-incorporated host proteins required for herpes simplex virus type 1 infection through a RNA interference screen. PLoS One 8:e53276. https://doi.org/10.1371/journal.pone.0053276.
22. Sekiguchi T, Iida H, Fukumura J, Nishimoto T. 2004. Human DDX3Y, the Y-encoded isoform of RNA helicase DDX3, rescues a hamster temperature-sensitive ET24 mutant cell line with a DDX3X mutation. Exp Cell Res 300:213-222. https://doi.org/10.1016/j.yexcr.2004.07.005.
23. Desai P, Person S. 1998. Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J Virol 72:7563-7568.
24. Soto-Rifo R, Ohlmann T. 2013. The role of the DEAD-box RNA helicase DDX3 in mRNA metabolism. Wiley Interdiscip Rev RNA 4:369-385. https://doi.org/10.1002/wrna.1165.
25. Pene V, Li Q, Sodroski C, Hsu CS, Liang TJ. 2015. Dynamic interaction of stress granules, DDX3X, and IKK-α mediates multiple functions in hepatitis C virus infection. J Virol 89:5462-5477. https://doi.org/10.1128/JVI.03197-14.
26. Nagel CH, Pohlmann A, Sodeik B. 2014. Construction and characterization of bacterial artificial chromosomes (BACs) containing herpes simplex virus full-length genomes. Methods Mol Biol 1144:43-62. https://doi.org/10.1007/978-1-4939-0428-0_4.
27. 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. https://doi.org/10.1038/sj.onc.1210687.
28. Wren JD, Conway T. 2006. Meta-analysis of published transcriptional and translational fold changes reveals a preference for low-fold inductions. OMICS 10:15-27. https://doi.org/10.1089/omi.2006.10.15.
29. Lippé R. 2012. Deciphering novel host-herpesvirus interactions by virion proteomics. Front Microbiol 3:181. https://doi.org/10.3389/fmicb.2012.00181.
30. Chao CH, Chen CM, Cheng PL, Shih JW, Tsou AP, Lee YH. 2006. DDX3, a DEAD box RNA helicase with tumor growth-suppressive property and transcriptional regulation activity of the p21waf1/cip1 promoter, is a candidate tumor suppressor. Cancer Res 66:6579-6588. https://doi.org/10.1158/0008-5472.CAN-05-2415.
31. Pomerantz JL, Baltimore D. 1999. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18:6694-6704. https://doi.org/10.1093/emboj/18.23.6694.
32. Paladino P, Mossman KL. 2009. Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response. J Interferon Cytokine Res 29:599-607. https://doi.org/10.1089/jir.2009.0074.
33. Schroder M. 2011. Viruses and the human DEAD-box helicase DDX3: inhibition or exploitation? Biochem Soc Trans 39:679-683. https://doi.org/10.1042/BST0390679.
34. Turcotte S, Letellier J, Lippé R. 2005. Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J Virol 79:8847-8860. https://doi.org/10.1128/JVI.79.14.8847-8860.2005.
35. 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. https://doi.org/10.1099/vir.0.015909-0.