Multiple functions of DDX3 RNA helicase in gene regulation, tumorigenesis, and viral infection

Frontiers in Genetics

Volumn 5, Issue DEC, 2014, Pages

  Ariumi, Yasuo ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

Author keywords

DDX3; HCV; HIV 1; Innate immunity; RNA helicases; Stress granules; Translation; Tumor suppressor

Indexed keywords

DEAD BOX PROTEIN; ENVELOPE PROTEIN; INITIATION FACTOR; MICRORNA; VIRUS PROTEIN;

APOPTOSIS; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE REGULATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOKINE PRODUCTION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; INNATE IMMUNITY; LIFE CYCLE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; VIRUS INFECTION; VIRUS REPLICATION;

HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; POXVIRIDAE;

EID: 84917741267     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00423     Document Type: Review

References (121)

1. Akira, S., and Takeda, K. (2004). Toll-like receptor signaling. Nat. Rev. Immunol. 4, 499-511. doi: 10.1038/nri1391
2. Andrejeva, J., Child, K. S., Young, D. F., Carlos, T. S., Stocks, N., Goodbourn, S.,et al. (2004). The V protein 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. 101, 17264-17269. doi: 10.1073/pnas.0407639101
3. Angus, A. G., Dalrymple, D., Boulant, S., McGivern, D. R., Clayton, R. F., Scott, M. J.,et al. (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. doi: 10.1099/vir.0.015909-0
4. Ariumi, Y., Kuroki, M., Abe, K., Dansako, H., Ikeda, M., Wakita, T.,et al. (2007). DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J. Virol. 81, 13922-139226. doi: 10.1128/JVI.01517-07
5. Ariumi, Y., Kuroki, M., Kushima, Y., Osugi, K., Hijikata, M., Maki, M.,et al. (2011a). Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J. Virol. 85, 6882-6892. doi: 10.1128/JVI02418-10
6. Ariumi, Y., Kuroki, M., Maki, M., Ikeda, M., Dansako, H., Wakita, T.,et al. (2011b). The ESCRT system is required for hepatitis C virus production. PLoS ONE 6:e14517. doi: 10.1371/journal.pone.0014517
7. Ariumi, Y., Serhan, F., Turelli, P., Telenti, A., and Trono, D. (2006). The integrase interactor 1 (INI1) proteins facilitate Tat-mediated human immunodeficiency virus type 1 transcription. Retrovirology 3, 47. doi: 10.1186/1742-4690-3-47
8. Beckham, C. J., and Parker, R. (2008). P bodies, stress granules, and viral life cycle. Cell Host Microbe 3, 206-212. doi: 10.1016/j.chom.2008.03.004
9. Berkhout, B., Silverman, R. H., and Jeang, K. T. (1989). Tat trans-activates the human immunodeficiency virus through a nascent RNA target. Cell 59, 273-282. doi: 10.1016/0092-8674(89)90289-4
10. Botlagunta, M., Krishnamachary, B., Vesuna, F., Winnard, P. T. Jr., Bol, G. M., Patel, A. H.,et al. (2011). Expression of DDX3 is directly modulated by hypoxia inducible factor-1 alpha in breast epithelial cells. PLoS ONE 6:e17563. doi: 10.1371/journal.pone.0017563
11. Botlagunta, M., Vesuna, F., Mironchik, Y., Raman, A., Lisok, A., Winnard, P. Jr.,et al. (2008). Oncogenic role of DDX3 in breast cancer biogenesis. Oncogene 27, 3912-3922. doi: 10.1038/onc.2008.33
12. Chahar, H. S., Chen, S., and 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. doi: 10.1016/j.virol.2012.09.041
13. Chang, P. C., Chi, C. W., Chau, G. Y., Li, F. Y., Tsai, Y. H., Wu, J. C.,et al. (2006). DDX3, a DEAD box RNA helicase, is deregulated in hepatitis virus-associated hepatocellular carcinoma and is involved in cell growth control. Oncogene 25, 1991-2003. doi: 10.1038/sj.onc.1209239
14. Chang, T. C., and Liu, W. S. (2010). The molecular evolution of PL10 homologs. BMC Evol. Biol. 10:127. doi: 10.1186/1471-2148-10-127
15. Chao, C. H., Chen, C. M., Cheng, P. L., Shih, J. W., Tsou, A. P., and Lee, Y. H. (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
16. Chen, H. H., Yu, H. I., Cho, W. C., and Tarn, W. Y. (2014). DDX3 modulates cell adhesion and mobility and cancer cell metastasis via Rac1-mediated signaling pathway. Oncogene doi: 10.1038/onc.2014.190 [Epub ahead of print].
17. Choi, Y. J., and Lee, S. G. (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
18. Cochrane, A. W., McNally, M. T., and Mouland, A. J. (2006). The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 3, 18. doi: 10.1186/1742-4690-3-18
19. Cordin, O., Banroques, J., Tanner, N. K., and Linder, P. (2006). The DEAD-box protein family of RNA helicases. Gene 367, 17-37. doi: 10.1016/j.gene.2005.10.019
20. Cruciat, C. M., Dolde, C., de Groot, R. E., Ohkawara, B., Reinhard, C., Korswagen, H. C.,et al. (2013). RNA helicase DDX3 is a regulatory subunit of casein kinase 1 in Wnt-ß-catenin signaling. Science 339, 1436-1441. doi: 10.1126/science.1231499
21. Cullen, B. R. (2003). Nuclear mRNA export: insights from virology. Trends Biochem. Sci. 28, 419-424. doi: 10.1016/S0968-0004(03)00142-7
22. DeFilippis, V. R., Alvarado, D., Sali, T., Rothenburg, S., and Früh, K. (2010). Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J. Virol. 84, 585-598. doi: 10.1128/JVI.01748-09
23. Ditton, H. J., Zimmer, J., Kamp, C., Rajpert-De Meyts, E., and Vogt, P. H. (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. doi: 10.1093/hmg/ddh240
24. Fang, J., Kubota, S., Yang, B., Zhou, N., Zhang, H., Godbout, R.,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
25. Foresta, C., Ferlin, A., and More, E. (2000). Deletion and expression analysis of AZFa genes on the human chromosome revealed a major role for DBY in male infertility. Hum. Mol. Genet. 9, 1161-1169. doi: 10.1093/hmg/9.8.1161
26. Fujii, R., Okamoto, M., Aratani, S., Oishi, T., Ohshima, T., Taira, K.,et al. (2001). A role of RNA helicase A in cis-acting transactivation response element-mediated transcriptional regulation of human immunodeficiency virus type 1. J. Biol. Chem. 276, 5445-5451. doi: 10.1074/jbc.M006892200
27. Fukumura, J., Noguchi, E., Sekiguchi, T., and Nishimoto, T. (2003). A temperature-sensitive mutant of the mammalian RNA helicase, DEAD-box isoform, DBX, defective in the transition from G1 to S phase. J. Biochem. 134, 71-82. doi: 10.1093/jb/mvg126
28. Gale, M. Jr., and Foy, E. M. (2005). Evasion of intracellular host defence by hepatitis C virus. Nature 436, 939-945. doi: 10.1038/nature04078
29. Geissler, R., Golbik, R. P., and Behrens, S. E. (2012). The DEAD-box helicase DDX3 supports the assembly of functional 80S ribosomes. Nucleic Acids Res. 40, 4998-5011. doi: 10.1093/nar/gks070
30. Goh, P. Y., Tan, Y. J., Lim, S. P., Tan, Y. H., Lim, S. G., Fuller-Pace, F.,et al. (2004). Cellular RNA helicase p68 relocalization and interaction with the hepatitis C virus (HCV) NS5B protein and the potential role of p68 in HCV RNA replication. J. Virol. 78, 5288-5298. doi: 10.1128/JVI.7810.5288-5298.2004
31. Gu, L., Fullam, A., Brennan, R., and Schröder, M. (2013). Human DEAD box helicase 3 couples I?B kinase e to interferon regulatory factor 3 activation. Mol. Cell. Biol. 33, 2004-2015. doi: 10.1128/MCB.01603-12
32. Hijikata, M., Kato, N., Ootsuyama, Y., Nakagawa, M., and Shimotohno, K. (1991). Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl. Acad. Sci. U.S.A. 88, 5547-5551. doi: 10.1073/pnas.88.13.5547
33. Hijikata, M., Mizushima, H., Tanji, Y., Komoda, Y., Hirowatari, Y., Akagi, T.,et al. (1993). Proteolytic processing and membrane association of putative nonstructural proteins of hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 90, 10773-10777. doi: 10.1073/pnas.90.22.10773
34. Hilliker, A., Gao, Z., Jankowsky, E., and 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
35. Hope, T. J., and Pomerantz, R. J. (1995). The human immunodeficiency virus type 1 Rev protein: a pivotal protein in the viral life cycle. Curr. Top. Microbiol. Immunol. 193, 91-105. doi: 10.1007/978-3-642-78929-8_5
36. Huang, H., Shiffman, M. L., Cheung, R. C., Layden, T. J., Friedman, S., Abar, O. T.,et al. (2006). Identification of two gene variants associated with risk of advanced fibrosis in patients with chronic hepatitis C. Gastroenterology 130, 1679-1687. doi: 10.1053/j.gastro.2006.02.032
37. Ikeda, M., Abe, K., Dansako, H., Nakamura, T., Naka, K, and Kato, N. (2005). Efficient replication of a full-length hepatitis C virus genome, strain O, in cell culture, and development of a luciferase reporter system. Biochem. Biophys. Res. Commun. 329, 1350-1359. doi: 10.1016/j.bbrc.2005.02.138
38. Ishaq, M., Hu, J., Wu, X., Fu, Q., Yang, Y., Liu, Q.,et al. (2008). Knockdown of cellular RNA helicase DDX3 by short hairpin RNAs suppresses HIV-1 replication without inducing apoptosis. Mol. Biotechnol. 39, 231-238. doi: 10.1007/s12033-008-9040-0
39. Jangra, R. K., Yi, M., and Lemon, S. M. (2010). DDX6 (Rck/p54) is required for efficient hepatitis C virus replication but not for internal ribosome entry site-directed translation. J. Virol. 84, 6810-6824. doi: 10.1128/jvi.00397-10
40. Jankowsky, E. (2011). RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36, 19-29. doi: 10.1016/j.tibs.2010.07.008
41. Jeang, K. T., Xiao, H., and Rich, E. A. (1999). Multifaceted activities of the HIV-1 transactivator of transcription, Tat. J. Biol. Chem. 274, 28837-28840. doi: 10.1074/jbc.274.41.28837
42. Jefferson, M., Donaszi-Ivanov, A., Pollen, S., Dalmary, T., Saalbach, G., and Powell, P. P. (2014). Host factors interacting with the pestivirus N terminal protease, Npro are components of the ribonucleoprotein complex. J. Virol. 88, 10340-1053. doi: 10.1128/JVI.00984-14
43. Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M., and Sarnow, P. (2005). Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309, 1577-1581. doi: 10.1126/science.1113329
44. Kalverda, A. P., Thompson, G. S., Vogel, A., Schröder, M., Bowie, A. G., Khan, A. R.,et al. (2009). Poxvirus K7 protein adopts a Bcl-2 fold: biochemical mapping of its interactions with human DEAD box RNA helicase DDX3. J. Mol. Biol. 385, 843-853. doi: 10.1016/j.jmb.2008.09.048
45. Kasim, V., Wu, S., Taira, K., and Miyagishi, M. (2013). Determination of the role of DDX3 a factor involved in mammalian RNAi pathway using an shRNA-expression library. PLoS ONE 8:e59445. doi: 10.1371/journal.pone.0059445
46. Kato, N., Hijikata, M., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S., and Shimotohno, K. (1990). Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc. Natl. Acad. Sci. U.S.A. 87, 9524-9528. doi: 10.1073/pnas.87.24.9524
47. Kato, N., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K.,et al. (2006). Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105. doi: 10.1038/nature04734
48. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H.,et al. (2005). IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6, 981-988. doi: 10.1038/ni1243
49. Kim, Y. S., Lee, S. G., Park, S. H., and Song, K. (2001). Gene structure of the human DDX3 and chromosome mapping of its related sequences. Mol. Cells 12, 209-214.
50. Ko, C., Lee, S., Windisch, M. P., and Ryu, W. S. (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. doi: 10.1128/JVI.02035-14
51. Kuroki, M., Ariumi, Y., Hijikata, M., Ikeda, M., Dansako, H., Wakita, T.,et al. (2013). PML tumor suppressor protein is required for HCV production. Biochem. Biophys. Res. Commun. 430, 592-597. doi: 10.1016/j.bbrc.2012.11.108
52. Kwong, A. D., Rao, B. G., and Jeang, K. T. (2005). Viral and cellular RNA helicases as antiviral targets. Nat. Rev. Drug Discov. 4, 845-853. doi: 10.1038/nrd1853
53. Lahn, B. T., and Page, D. C. (1997). Functional coherence of the human Y chromosome. Science 278, 675-680. doi: 10.1126/science.278.5338.675
54. Lai, M. C., Chang, W. C., Shieh, S. Y., and Tarn, W. Y. (2010). DDX3 regulates cell growth through translational control of cyclin E1. Mol. Cell Biol. 30, 5444-5453. doi: 10.1128/MCB.00560-10
55. Lai, M. C., Lee, Y. H., and Tarn, W. Y. (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. doi: 10.1091/mbc.E07-12-1264
56. Lai, M. C., Wang, S. W., Cheng, L., Tarn, W. Y., Tsai, S. J., and Sun, H. S. (2013). Human DDX3 interacts with the HIV-1 Tat protein to facilitate viral mRNA translation. PLoS ONE 8:e68665. doi: 10.1371/journal.pone.0068665
57. Lee, C. H., Lin, S. H., Yang, S. F., Yang, S. M., Chen, M. K., Lee, H.,et al. (2014). Low/negative expression of DDX3 might predict poor prognosis in non-smoker patients with oral cancer. Oral Dis. 20, 76-83. doi: 10.1111/odi.12076
58. Lee, C. S., Dias, A. P., Jedrychowski, M., Patel, A. H., Hsu, J. L., and Reed, R. (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
59. Leory, P., Alzari, P., Sassoon, D., Wolgemuth, D., and Fellous, M. (1989). The protein encoded by a murine male germ cell-specific transcript is a putative ATP-dependent RNA helicase. Cell 57, 549-559. doi: 10.1016/0092-8674(89)90125-6
60. Li, C., Ge, L. L., Li, P. P., Wang, Y., Dai, J. J., Sun, M. X.,et al. (2014a). Cellular DDX3 regulates Japanese encephalitis virus replication by interacting with viral un-translated regions. Virology 449, 70-81. doi: 10.1016/j.virol.2013.11.008
61. Li, Q., Zhang, P., Zhang, C., Wang, Y., Wan, R., Yang, Y.,et al. (2014b). DDX3X regulates cell survival and cell cycle during mouse early embryonic development. J. Biomed. Res. 28, 282-291. doi: 10.7555/JBR.27.20130047
62. Li, J., Tang, H., Mullen, T. M., Westberg, C., Reddy, T. R., Rose, D. W.,et al. (1999). A role for RNA helicase A in post-transcriptional regulation of HIV type 1. Proc. Natl. Acad. Sci. U.S.A. 96, 709-714. doi: 10.1073/pnas.96.2.709
63. Linder, P. (2008). mRNA export: RNP remodeling by DEAD-box proteins. Curr. Biol. 18, R297-R299. doi: 10.1016/j.cub.2008.02.027
64. Linder, P., and Lasko, P. (2006). Bent out of shape: RNA unwinding by the DEAD-box helicase Vasa. Cell 125, 219-221. doi: 10.1016/j.cell.2006.03.030
65. Listenberger, L. L., and Brown, D. A. (2007). Fluorescent detection of lipid droplets and associated proteins. Curr. Protoc. Cell Biol. 35, 24.2.1-24.2.11. doi: 10.1002/0471143030.cb2402s35
66. Lorgeoux, R. P., Guo, F., and Liang, C. (2012). From promoting to inhibiting: diverse roles of helicases in HIV-1 replication. Retrovirology 9, 79. doi: 10.1186/1742-4690-9-79
67. Maga, G., Falchi, F., Garbelli, A., Belfiore, A., Witvrouw, M., Manetti, F.,et al. (2008). Pharmacophore modeling and molecular docking led to the discovery of inhibitors of human immunodeficiency virus-1 replication targeting the human cellular aspartic acid-glutamic acid-alanine-aspartic acid box polypeptide 3. J. Med. Chem. 51, 6635-6638. doi: 10.1021/jm8008844
68. Maga, G., Falchi, F., Radi, M., Botta, L., Casaluce, G., Bernardini, M.,et al. (2011). Toward the discover of novel anti-HIV drug. Second-generation inhibitors of the cellular ATPase DDX3 with improved anti-HIV activity: synthesis, structure-activity relationship analysis, cytotoxicity studies, and target validation. Chem. Med. Chem. 6, 1371-1389. doi: 10.1002/cmdc.201100166
69. Mamiya, N., and Worman, H. J. (1999). Hepatitis C virus core protein binds to a DEAD box RNA helicase. J. Biol. Chem. 274, 15751-15756. doi: 10.1074/jbc.274.22.15751
70. Mazeyrat, S., Saut, N., Sargent, C. A., Grimmond, S., Longepied, G., Ehrmann, I. E.,et al. (1998). The mouse Y chromosome interval necessary for spermatogonial proliferation is gene dense with syntenic homology to the human AZFa region. Hum. Mol. Genet. 7, 1713-1724. doi: 10.1093/hmg/7.11.1713
71. McGivern, D. R., and Lemon, S. M. (2009). Tumor suppressors, chromosomal instability, and hepatitis C virus-associated liver cancer. Annu. Rev. Pathol. 4, 399-415. doi: 10.1146/annurev.pathol.4.110807.092202
72. Merz, C., Urlaub, H., Will, C. L., and Lührmann, R. (2007). Protein composition of human mRNPs spliced in vitro and differential requirement for mRNP protein recruitment. RNA 13, 116-128. doi: 10.1261/rna.336807
73. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R.,et al. (2005). Cardif is an adaptor protein in the RIG-1 antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172. doi: 10.1038/nature04193
74. Miao, X., Yang, Z. L., Xiong, L., Zou, Q., Yuan, Y., Li, J.,et al. (2013). Nectin-2 and DDX3 are biomarkers for metastasis and poor prognosis of squamous cell/adenosquamous carcinomas and adenocarcinoma of gallbladder. Int. J. Clin. Exp. Pathol. 6, 179-190.
75. Miyanari, Y., Atsuzawa, K., Usuda, N., Watashi, K., Hishiki, T., Zayas, M.,et al. (2007). The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9, 1089-1097. doi: 10.1038/ncb1631
76. Naji, S., Ambrus, G., Cimermancic, P., Reyes, J. R., Johnson, J. R., Filbrandt, R.,et al. (2012). Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell. Proteomics 11, M111.015313. doi: 10.1074/mcp.M111.015313
77. Oda, S., Schröder, M., and Khan, A. R. (2009). Structural basis for targeting of human RNA helicase DDX3 by poxvirus protein K7. Structure 17, 1528-1537. doi: 10.1016/j.str.2009.09.005
78. Oshiumi, H., Ikeda, M., Matsumoto, M., Watanabe, A., Takeuchi, O., Akira, S.,et al. (2010a). Hepatitis C virus core protein abrogates the DDX3 function that enhances IPS-1-mediated IFN-beta induction. PLoS ONE 5:e14258. doi: 10.1371/journal.pone.0014258
79. Oshiumi, H., Sakai, K., Matsumoto, M., and Seya, T. (2010b). DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. Eur. J. Iummunol. 40, 940-948. doi: 10.1002/eji.200940203
80. Owsianka, A. M., and Patel, A. H. (1999). Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257, 330-340. doi: 10.1006/viro.1999.9659
81. Park, S. H., Lee, S. G., Kim, Y., and Song, K. (1998). Assignment of a human putative RNA helicase gene, DDX3, to human X chromosome bands p11.3--> p11.23. Cytogenet. Cell Genet. 81, 178-179. doi: 10.1159/000015022
82. Parker, R., and Sheth, U. (2007). P bodies and the control of mRNA trabslation and degradation. Mol. Cell 25, 635-646. doi: 10.1016/j.molcel.2007.02.011
83. Pollard, V. W., and Malim, M. H. (1998). The HIV-1 Rev protein. Annu. Rev. Microbiol. 52, 491-532. doi: 10.1146/annurev.micro.52.1.491
84. Radi, M., Falchi, F., Garbelli, A., Samuele, A., Bernardo, V., Paolucci, S.,et al. (2012). Discovery of the first small molecule inhibitor of human DDX3 specifically designed to target the RNA binding site: towards the next generation HIV-1 inhibitors. Bioorg. Med. Chem. Lett. 22, 2094-2098. doi: 10.1016/j.bmcl.2011.12.135
85. Randall, G., Panis, M., Cooper, J. D., Tellinghuisen, T. L., Sukhodolets, K. E., Pfeffer, S.,et al. (2007). Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. U.S.A. 104, 12884-12889. doi: 10.1073/pnas.0704894104
86. Robertson-Anderson, R. M., Wang, J., Edgcomb, S. P., Carmel, A. B., Williamson, J. R., and Millar, D. P. (2011). Single-molecule studies reveal that DEAD box protein DDX1 promotes oligomerization of HIV-1 Rev on the Rev responsive element. J. Mol. Biol. 410, 959-971. doi: 10.1016/j.jmb.2011.04.026
87. Saito, T., and Gale, M. Jr. (2007). Principles of intracellular viral recognition. Curr. Opin. Immunol. 19, 17-23. doi: 10.1016/j.coi.2006.11.003
88. Scheller, N., Mina, L. B., Galão, R. P., Chari, A., Giménez-Barcons, M., Noueiry, A.,et al. (2009). Translation and replication of hepatitis C virus genomic RNA dependes on ancient cellular proteins that control mRNA fates. Proc. Natl. Acad. Sci. U.S.A. 106, 13517-13522. doi: 10.1073/pnas.0906413106
89. Schröder, 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. Biochem. Pharmcol. 79, 297-306. doi: 10.1016/j.bcp.2009.08.032
90. Schröder, M., Baran, M., and Bowie, A. G. (2008). Viral targeting of DEAD box protein 3 reveals its role in TBK/IKKepsilon-mediated IRF activation. EMBO J. 27, 2147-2157. doi: 10.1038/emboj.2008.143
91. Sekiguchi, T., Kurihara, Y., and Fukumura, J. (2007). Phosphorylation of threonine 204 of DEAD-box RNA helicase DDX3 by cyclin B/cdc2 in vitro. Biochem. Biophys. Res. Commun. 356, 668-673. doi: 10.1016/j.bbrc.2007.03.038
92. Seth, R. B., Sun, L., Ea, C. K., and Chen, Z. J. (2005). Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-B and IRF3. Cell 122, 669-682. doi: 10.1016/j.cell.2005.08.012
93. Sharma, A., Awasthi, S., Harrod, C. K., Matlock, E. F., Khan, S., Xu, L.,et al. (2007). The Werner syndrome helicase is a cofactor for HIV-1 long terminal repeat transactivation and retroviral replication. J. Biol. Chem. 282, 12048-12057. doi: 10.1074/jbc.M608104200
94. Shih, J. W., Tsai, T. Y., Chao, C. H., and Wu Lee, Y. H. (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
95. Shih, J. W., Wang, W. T., Tsai, T. Y., Kuo, C. Y., Li, H. K., and Wu Lee, Y. H. (2012). Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. Biochem. J. 441, 119-1129. doi: 10.1042/BJ20110739
96. Soto-Rifo, R., Rubilar, P. S., Limousin, T., de Breyne, S., Décimo, D., and Ohlmann, T. (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
97. Soto-Rifo, R., Rubilar, P. S., and Ohlmann, T. (2013). The DEAD-box helicase DDX3 substitutes for the cap-binding protein eIF4E to promote compartmentalized translation initiation of the HIV-1 genomic RNA. Nucleic Acids Res. 41, 6286-6299. doi: 10.1093/nar/gkt306
98. Soulat, D., Burckstummer, T., Westermayer, S., Goncalves, A., Bauch, A., Stefanovic, A.,et al. (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. doi: 10.1038/emboj.2008.126
99. Sun, C., Pager, C. T., Luo, G., Sarnow, P., and Cate, J. H. (2010). Hepatitis C virus core-derived peptides inhibit genotype 1b viral genome replication via interaction with DDX3X. PLoS ONE 5:e12826. doi: 10.1371/journal.pone.0012826
100. Sun, M., Song, L., Li, Y., Zhou, T., and Jope, R. S. (2008). Identification of an antiapoptotic protein complex at death receptors. Cell Death Differ. 15, 1887-1900. doi: 10.1038/cdd.2008.124
101. Sun, M., Song, L., Zhou, T., Gillespie, G. Y., and Jope, R. S. (2011). The role of DDX3 in regulating Snail. Biochim. Biophys. Acta 1813, 438-447. doi: 10.1016/j.bbamcr.2011.01003
102. Sun, M., Zhou, T., Jonasch, E., and Jope, R. S. (2013). DDX3 regulates DNA damage-induced apoptosis and p53 stabilization. Biochem. Biophys. Acta 1833, 1489-1497. doi: 10.1016/j.bbamcr.2013.02.026
103. Tingting, P., Caiyun, F., Zhigang, Y., Pengyuan, Y., and Zhenghong, Y. (2006). Subproteomic analysis of the cellular proteins associated with the 3' untranslated region of the hepatitis C virus genome in human liver cells. Biochem. Biophys. Res. Commun. 347, 683-691. doi: 10.1016/j.bbrc.2006.06.144
104. Tsai, W. C., and Lloyd, R. E. (2014). Cytoplasmic RNA granules and viral infection. Annu. Rev. Virol. 1, 147-170. doi: 10.1146/annurev-virology-031413-085505
105. Upadya, M. H., Aweya, J. J., and Tan, Y. J. (2014). Understanding the interaction of hepatitis C virus with host DEAD-box RNA helicases. World J. Gastroenterol. 20, 2913-2926. doi: 10.3748/wjg.v20.i11.2913
106. Utama, A., Shimizu, H., Hasebe, F., Morita, K., Igarashi, A., Shoji, I.,et al. (2000). Role of the DExH motif of the Japanese encephalitis virus and hepatitis C virus NS3 proteins in the ATPase and RNA helicase activities. Virology 273, 316-324. doi: 10.1006/viro.2000.0417
107. Vashist, S., Urena, L., Chaudhry, Y., and Goodfellow, I. (2012). Identification of RNA-protein interaction networks involved in the norovirus life cycle. J. Virol. 86, 11977-11990. doi: 10.1128/JVI.00432-12
108. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z.,et al. (2005). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11, 791-796. doi: 10.1038/nm1268
109. Wang, H., Kim, S., and Ryu, W. S. (2009). DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. J. Virol. 83, 5815-5824. doi: 10.1128/JVI.00011-09
110. Wang, H., and Ryu, W. S. (2010). Hepatitis B virus polymerase blocks pattern recognition receptor signaling via interaction with DDX3: implications for immune evasion. PLoS Pathog. 6:e1000986. doi: 10.1371/journal.ppat.1000986
111. Wu, D. W., Lee, M. C., Wang, J., Chen, C. Y., Cheng, Y. W., and Lee, H. (2014). DDX3 loss by p53 inactivation promotes tumor malignancy via the MDM2/Slug/E-cadherin pathway and poor patient outcome in non-small-cell lung cancer. Oncogene 33, 1515-1526. doi: 10.1038/onc.2013.107
112. Wu, D. W., Liu, W. S., Wang, J., Chen, C. Y., Cheng, Y. W., and Lee, H. (2011). Reduced p21(WAF1/CIP1) via alteration of p53-DDX3 pathway is associated with poor relapse-free survival in early-stage human papillomavirus-associated lung cancer. Clin. Cancer Res. 17, 1895-1905. doi: 10.1158/1078-0432.CCR-10-2316
113. Xu, L. G., Wang, Y. Y., Han, K. J., Li, L. Y., Zhai, Z., and Shu, H. B. (2005). VISA is an adaptor protein required for virus-triggered IFN- signaling. Mol. Cell 19, 727-740. doi: 10.1016/j.molcel.2005.08.014
114. Yasuda-Inoue, M., Kuroki, M., and Ariumi, Y. (2013a). Distinct DDX DEAD-box RNA helicases cooperate to modulate the HIV-1 Rev function. Biochem. Biophys. Res. Commun. 434, 803-808. doi: 10.1016/j.bbrc.2013.04.016
115. Yasuda-Inoue, M., Kuroki, M., and Ariumi, Y. (2013b). DDX3 RNA helicase is required for HIV-1 Tat function. Biochem. Biophys. Res. Commun. 441, 607-611. doi: 10.1016/j.bbrc.2013.10.107
116. Yedavalli, V. S., Neuveut, C., Chi, Y. H., Kleiman, L., and Jeang, K. T. (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
117. Yedavalli, V. S., Zhang, N., Cai, H., Zhang, P., Starost, M. F., Hosmane, R. S.,et al. (2008). Ring expanded nucleoside analogues inhibit RNA helicase and intracellular human immunodeficiency virus type 1 replication. J. Med. Chem. 51, 5043-5051. doi: 10.1021/jm800332m
118. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M.,et al. (2004). The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral response. Nat. Immunol. 5, 730-737. doi: 10.1038/ni1087
119. You, L. R., Chen, C. M., Yeh, T. S., Tsai, T. Y., Mai, R. T., Lin, C. H.,et al. (1999). Hepatitis C virus core protein interacts with cellular putative RNA helicase. J. Virol. 73, 2841-2853.
120. Yu, S., Chen, J., Wu, M., Chen, H., Kato, N., and Yuan, Z. (2010). Hepatitis B virus polymerase inhibits RIG-I- and Toll-like receptor 3-mediated beta interferon induction in human hepatocytes through interference with interferon regulatory factor 3 activation and dampening of the interaction between TBK1/IKKepsilon and DDX3. J. Gen. Virol. 91, 2080-2090. doi: 10.1099/vir.0.020552-0
121. Zhou, X., Luo, J., Mills, L., Wu, S., Pan, T., Geng, G.,et al. (2013). DDX5 facilitates HIV-1 replication as a cellular co-factor of Rev. PLoS ONE 8:e65040. doi: 10.1371/journal.pone.0065040