Human DDX3 Interacts with the HIV-1 Tat Protein to Facilitate Viral mRNA Translation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lai, Ming Chih ^a   Wang, Shainn Wei ^a   Cheng, Lie ^a   Tarn, Woan Yuh ^b   Tsai, Shaw Jenq ^a   Sun, H Sunny ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DDX3 PROTEIN; DEAD BOX PROTEIN; MESSENGER RNA; REV PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSLATION REGULATION; VIRUS INHIBITION;

DEAD-BOX RNA HELICASES; GENE KNOCKDOWN TECHNIQUES; GENE PRODUCTS, TAT; HEK293 CELLS; HELA CELLS; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, VIRAL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84879725218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068665     Document Type: Article

References (56)

1. Chao CH, Chen CM, Cheng PL, Shih JW, Tsou AP, et al. (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. doi:10.1158/0008-5472.CAN-05-2415. PubMed: 16818630.
2. Botlagunta M, Vesuna F, Mironchik Y, Raman A, Lisok A, et al. (2008) Oncogenic role of DDX3 in breast cancer biogenesis. Oncogene 27: 3912-3922. doi:10.1038/onc.2008.33. PubMed: 18264132.
3. Kanai Y, Dohmae N, Hirokawa N, (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43: 513-525. doi:10.1016/j.neuron.2004.07.022. PubMed: 15312650.
4. Choi YJ, Lee SG, (2012) The DEAD-box RNA helicase DDX3 interacts with DDX5, co-localizes with it in the cytoplasm during the G2/M phase of the cycle, and affects its shuttling during mRNP export. J Cell Biochem 113: 985-996. doi:10.1002/jcb.23428. PubMed: 22034099.
5. 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. doi:10.1038/sj.onc.1210687. PubMed: 17667941.
6. Lee CS, Dias AP, Jedrychowski M, Patel AH, Hsu JL, et al. (2008) Human DDX3 functions in translation and interacts with the translation initiation factor eIF3. Nucleic Acids Res 36: 4708-4718. doi:10.1093/nar/gkn454. PubMed: 18628297.
7. Lai MC, Lee YH, Tarn WY (2008) The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tip-associated protein and participates in translational control. Mol Biol Cell 19: 3847-3858.
8. Lai MC, Chang WC, Shieh SY, Tarn WY (2010) DDX3 regulates cell growth through translational control of cyclin E1. Mol Cell Biol 30: 5444-5453.
9. Shih JW, Wang WT, Tsai TY, Kuo CY, Li HK, et al. (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. doi:10.1042/BJ20110739. PubMed: 21883093.
10. Tarn WY, Chang TH (2009). The current understanding of Ded 1p/DDX3 homologs from yeast to human. RNA Biol 6: 17-20.
11. Grallert B, Kearsey SE, Lenhard M, Carlson CR, Nurse P, et al. (2000) A fission yeast general translation factor reveals links between protein synthesis and cell cycle controls. J Cell Sci 113(8):: 1447-1458.
12. Cullen BR, (2003) Nuclear mRNA export: insights from virology. Trends Biochem Sci 28: 419-424. doi:10.1016/S0968-0004(03)00142-7. PubMed: 12932730.
13. Dingwall C, Ernberg I, Gait MJ, Green SM, Heaphy S, et al. (1989) Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc Natl Acad Sci U S A 86: 6925-6929. doi:10.1073/pnas.86.18.6925. PubMed: 2476805.
14. Laspia MF, Rice AP, Mathews MB, (1989) HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59: 283-292. doi:10.1016/0092-8674(89)90290-0. PubMed: 2553266.
15. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA, (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92: 451-462. doi:10.1016/S0092-8674(00)80939-3. PubMed: 9491887.
16. 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. doi:10.1016/j.cell.2004.09.029. PubMed: 15507209.
17. Cullen BR, (2005) Human immunodeficiency virus: nuclear RNA export unwound. Nature 433: 26-27. doi:10.1038/433026a. PubMed: 15635396.
18. Ishaq M, Hu J, Wu X, Fu Q, Yang Y, et al. (2008) Knockdown of cellular RNA helicase DDX3 by short hairpin RNAs suppresses HIV-1 viral replication without inducing apoptosis. Mol Biotechnol 39: 231-238. doi:10.1007/s12033-008-9040-0. PubMed: 18259889.
19. Kwong AD, Rao BG, Jeang KT, (2005) Viral and cellular RNA helicases as antiviral targets. Nat Rev Drug Discov 4: 845-853. doi:10.1038/nrd1853. PubMed: 16184083.
20. Garbelli A, Radi M, Falchi F, Beermann S, Zanoli S, et al. (2011) Targeting the human DEAD-box polypeptide 3 (DDX3) RNA helicase as a novel strategy to inhibit viral replication. Curr Med Chem 18: 3015-3027. doi:10.2174/092986711796391688. PubMed: 21651478.
21. Kozak M, (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299: 1-34. doi:10.1016/S0378-1119(02)01056-9. PubMed: 12459250.
22. Babendure JR, Babendure JL, Ding JH, Tsien RY, (2006) Control of mammalian translation by mRNA structure near caps. RNA 12: 851-861. doi:10.1261/rna.2309906. PubMed: 16540693.
23. Ricci EP, Soto Rifo R, Herbreteau CH, Decimo D, Ohlmann T, (2008) Lentiviral RNAs can use different mechanisms for translation initiation. Biochem Soc Trans 36: 690-693. doi:10.1042/BST0360690. PubMed: 18631141.
24. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, et al. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLOS Biol 6: e96. doi:10.1371/journal.pbio.0060096. PubMed: 18447581.
25. Parkin NT, Cohen EA, Darveau A, Rosen C, Haseltine W, et al. (1988) Mutational analysis of the 5' non-coding region of human immunodeficiency virus type 1: effects of secondary structure on translation. EMBO J 7: 2831-2837. PubMed: 3181141.
26. Hilliker A, Gao Z, Jankowsky E, Parker R, (2011) The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol Cell 43: 962-972. doi:10.1016/j.molcel.2011.08.008. PubMed: 21925384.
27. Marsden S, Nardelli M, Linder P, McCarthy JE, (2006) Unwinding single RNA molecules using helicases involved in eukaryotic translation initiation. J Mol Biol 361: 327-335. doi:10.1016/j.jmb.2006.06.016. PubMed: 16828800.
28. Chuang RY, Weaver PL, Liu Z, Chang TH, (1997) Requirement of the DEAD-Box protein ded1p for messenger RNA translation. Science 275: 1468-1471. doi:10.1126/science.275.5305.1468. PubMed: 9045610.
29. de la Cruz J, Iost I, Kressler D, Linder P, (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94: 5201-5206. doi:10.1073/pnas.94.10.5201. PubMed: 9144215.
30. Noueiry AO, Chen J, Ahlquist P, (2000) A mutant allele of essential, general translation initiation factor DED1 selectively inhibits translation of a viral mRNA. Proc Natl Acad Sci U S A 97: 12985-12990. doi:10.1073/pnas.240460897. PubMed: 11069307.
31. Berthelot K, Muldoon M, Rajkowitsch L, Hughes J, McCarthy JE, (2004) Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol Microbiol 51: 987-1001. doi:10.1046/j.1365-2958.2003.03898.x. PubMed: 14763975.
32. Fisher AG, Collalti E, Ratner L, Gallo RC, Wong-Staal F, (1985) A molecular clone of HTLV-III with biological activity. Nature 316: 262-265. doi:10.1038/316262a0. PubMed: 2410792.
33. Arya SK, Guo C, Josephs SF, Wong-Staal F, (1985) Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science 229: 69-73. doi:10.1126/science.2990040. PubMed: 2990040.
34. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR, (1989) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338: 254-257. doi:10.1038/338254a0. PubMed: 2784194.
35. Lykke-Andersen J, Shu MD, Steitz JA, (2001) Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293: 1836-1839. doi:10.1126/science.1062786. PubMed: 11546874.
36. Lai MC, Lin RI, Huang SY, Tsai CW, Tarn WY (2000) A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J Biol Chem 275: 7950-7957.
37. Brasey A, Lopez-Lastra M, Ohlmann T, Beerens N, Berkhout B, et al. (2003) The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle. J Virol 77: 3939-3949. doi:10.1128/JVI.77.7.3939-3949.2003. PubMed: 12634354.
38. Buck CB, Shen X, Egan MA, Pierson TC, Walker CM, et al. (2001) The human immunodeficiency virus type 1 gag gene encodes an internal ribosome entry site. J Virol 75: 181-191. doi:10.1128/JVI.75.1.181-191.2001. PubMed: 11119587.
39. SenGupta DN, Berkhout B, Gatignol A, Zhou AM, Silverman RH, (1990) Direct evidence for translational regulation by leader RNA and Tat protein of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 87: 7492-7496. doi:10.1073/pnas.87.19.7492. PubMed: 2120701.
40. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, et al. (2007) DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 81: 13922-13926. doi:10.1128/JVI.01517-07. PubMed: 17855521.
41. Krishnan V, Zeichner SL, (2004) Alterations in the expression of DEAD-box and other RNA binding proteins during HIV-1 replication. Retrovirology 1: 42. doi:10.1186/1742-4690-1-42. PubMed: 15588285.
42. Fang J, Kubota S, Yang B, Zhou N, Zhang H, et al. (2004) A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev. Virology 330: 471-480. doi:10.1016/j.virol.2004.09.039. PubMed: 15567440.
43. Bolinger C, Sharma A, Singh D, Yu L, Boris-Lawrie K, (2010) RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions. Nucleic Acids Res 38: 1686-1696. doi:10.1093/nar/gkp1075. PubMed: 20007598.
44. Kozak M, (1986) Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci U S A 83: 2850-2854. doi:10.1073/pnas.83.9.2850. PubMed: 3458245.
45. Kozak M, (1989) Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol Cell Biol 9: 5134-5142. PubMed: 2601712.
46. Soto-Rifo R, Rubilar PS, Limousin T, de Breyne S, Décimo D, et al. (2012) DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J 31: 3745-3756. doi:10.1038/emboj.2012.220. PubMed: 22872150.
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. doi:10.1093/nar/gks070. PubMed: 22323517.
48. Liu J, Henao-Mejia J, Liu H, Zhao Y, He JJ, (2011) Translational regulation of HIV-1 replication by HIV-1 Rev cellular cofactors Sam68, eIF5A, hRIP, and DDX3. J Neuroimmune Pharmacol 6: 308-321. doi:10.1007/s11481-011-9265-8. PubMed: 21360055.
49. Berkhout B, Arts K, Abbink TE, (2011) Ribosomal scanning on the 5'-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res 39: 5232-5244. doi:10.1093/nar/gkr113. PubMed: 21393254.
50. Charbonneau J, Gendron K, Ferbeyre G, Brakier-Gingras L, (2012) The 5' UTR of HIV-1 full-length mRNA and the Tat viral protein modulate the programmed-1 ribosomal frameshift that generates HIV-1 enzymes. RNA 18: 519-529. doi:10.1261/rna.030346.111. PubMed: 22286970.
51. Gendron K, Ferbeyre G, Heveker N, Brakier-Gingras L, (2011) The activity of the HIV-1 IRES is stimulated by oxidative stress and controlled by a negative regulatory element. Nucleic Acids Res 39: 902-912. doi:10.1093/nar/gkq885. PubMed: 20935056.
52. Cordin O, Banroques J, Tanner NK, Linder P, (2006) The DEAD-box protein family of RNA helicases. Gene 367: 17-37. doi:10.1016/j.gene.2005.10.019. PubMed: 16337753.
53. Graveley BR, (2000) Sorting out the complexity of SR protein functions. RNA 6: 1197-1211. doi:10.1017/S1355838200000960. PubMed: 10999598.
54. Abrahamyan LG, Chatel-Chaix L, Ajamian L, Milev MP, Monette A, et al. (2010) Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J Cell Sci 123: 369-383. doi:10.1242/jcs.055897. PubMed: 20053637.
55. Charnay N, Ivanyi-Nagy R, Soto-Rifo R, Ohlmann T, López-Lastra M, et al. (2009) Mechanism of HIV-1 Tat RNA translation and its activation by the Tat protein. Retrovirology 6: 74. doi:10.1186/1742-4690-6-S3-P74. PubMed: 19671151.
56. Maniatis T, Reed R, (2002) An extensive network of coupling among gene expression machines. Nature 416: 499-506. doi:10.1038/416499a. PubMed: 11932736.