1,476
Views
29
CrossRef citations to date
0
Altmetric
Original Articles

DEAD-box helicases: the Yin and Yang roles in viral infections

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 3-32 | Received 11 Sep 2017, Accepted 17 Apr 2018, Published online: 09 May 2018

References

  • Akter, K. A., Mansour, M. A., Hyodo, T., & Senga, T. (2016). FAM98A associates with DDX1-C14orf166-FAM98B in a novel complex involved in colorectal cancer progression. Journal of Biochemistry & Cell Biology, 84, 1–13. doi:10.1016/j.biocel.2016.12.013
  • Amaya, M., Brooks-Faulconer, T., Lark, T., Keck, F., Bailey, C., Raman, V., & Narayanan, A. (2016). Venezuelan equine encephalitis virus non-structural protein 3 (nsP3) interacts with RNA helicases DDX1 and DDX3 in infected cells. Antiviral Research, 131, 49–60. doi:10.1016/j.antiviral.2016.04.008.
  • Amaya, M., Voss, K., Sampey, G., Senina, S., de la Fuente, C., Mueller, C., … Narayanan, A. (2014). The role of IKKβ in Venezuelan equine encephalitis virus infection. PLoS ONE, 9(2), e86745. doi:10.1371/journal.pone.0086745.
  • Angus, A. G. N., Dalrymple, D., Boulant, S., McGivern, D. R., Clayton, R. F., Scott, M. J., … Patel, A. H. (2010). Requirement of cellular DDX3 for hepatitis C virus replication is unrelated to its interaction with the viral core protein. Journal of General Virology, 91(Pt 1), 122–132. doi:10.1099/vir.0.015909-0.
  • Ariumi, Y. (2014). Multiple functions of DDX3 RNA helicase in gene regulation, tumorigenesis, and viral infection. Frontiers in Genetics, 5, 423. doi:10.3389/fgene.2014.00423.
  • 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. Journal of Virology, 81(24), 13922–13926. doi:10.1128/JVI.01517-07.
  • Ariumi, Y., Kuroki, M., Kushima, Y., Osugi, K., Hijikata, M., Maki, M., … Kato, N. (2011). Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. Journal of Virology, 85(14), 6882–6892. doi:10.1128/jvi.02418-10.
  • Beckham, C.J., & Parker, R. (2008). P-bodies, stress granules and viral life cycles. Cell Host & Microbe, 3(4), 206–212. doi:10.1016/j.chom.2008.03.004.
  • Bleoo, S., Sun, X., Hendzel, M. J., Rowe, J. M., Packer, M., & Godbout, R. (2001). Association of human DEAD box protein DDX1 with a cleavage stimulation factor involved in 3′-end processing of pre-MRNA. Molecular Biology of the Cell, 12(10), 3046–3059.10.1091/mbc.12.10.3046
  • Bol, G.M., Xie, M., & Raman, V. (2015). DDX3, a potential target for cancer treatment. Molecular Cancer, 14, 499. doi:10.1186/s12943-015-0461-7.
  • Bortz, E., Westera, L., Maamary, J., Steel, J., Albrecht, R. A., Manicassamy, B., … Garcia-Sastre, A. (2011). Host- and strain-specific regulation of influenza virus polymerase activity by interacting cellular proteins. MBio, 2(4), doi:10.1128/mBio.00151-11.
  • Botlagunta, M., Vesuna, F., Mironchik, Y., Raman, A., Lisok, A., Winnard, P., Jr, … Raman, V. (2008). Oncogenic role of DDX3 in breast cancer biogenesis. Oncogene, 27(28), 3912–3922. doi:10.1038/onc.2008.33.
  • Causevic, M., Hislop, R. G., Kernohan, N. M., Carey, F. A., Kay, R. A., Steele, R. J., & Fuller-Pace, F. V. (2001). Overexpression and poly-ubiquitylation of the DEAD-box RNA helicase p68 in colorectal tumours. Oncogene, 20(53), 7734–7743. doi:10.1038/sj.onc.1204976.
  • Chahar, H. S., 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), 1–7. doi:10.1016/j.virol.2012.09.041.
  • Chang, P. C., Chi, C. W., Chau, G. Y., Li, F. Y., Tsai, Y. H., Wu, J. C., & Wu Lee, Y. H. (2006). DDX3, a DEAD box RNA helicase, is deregulated in hepatitis virus-associated hepatocellular carcinoma and is involved in cell growth control. Oncogene, 25(14), 1991–2003. doi:10.1038/sj.onc.1209239.
  • Chao, C. H., Chen, C. M., Cheng, P. L., Shih, J. W., Tsou, A. P., & 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 Research, 66(13), 6579–6588. doi:10.1158/0008-5472.CAN-05-2415.
  • Chen, H. C., Lin, W. C., Tsay, Y. G., Lee, S. C., & Chang, C. J. (2002). An RNA helicase, DDX1, interacting with poly(A) RNA and heterogeneous nuclear ribonucleoprotein K. Journal of Biological Chemistry, 277(43), 40403–40409. doi:10.1074/jbc.M206981200.
  • Chen, C. Y., Chan, C. H., Chen, C. M., Tsai, Y. S., Tsai, T. Y., Wu Lee, Y. H., & You, L. R. (2016). Targeted inactivation of murine Ddx3x: Essential roles of Ddx3x in placentation and embryogenesis. Human Molecular Genetics, 25(14), 2905–2922. doi:10.1093/hmg/ddw143.
  • Chen, G., Guo, X., Lv, F., Xu, Y., & Gao, G. (2008). p72 DEAD box RNA helicase is required for optimal function of the zinc-finger antiviral protein. Proceedings of the National Academy of Sciences, 105(11), 4352–4357. doi:10.1073/pnas.0712276105.
  • Chen, J. Y., Chen, W. N., Poon, K. M., Zheng, B. J., Lin, X., Wang, Y. X., & Wen, Y. M. (2009). Interaction between SARS-CoV helicase and a multifunctional cellular protein (Ddx5) revealed by yeast and mammalian cell two-hybrid systems. Archives of Virology, 154(3), 507–512. doi:10.1007/s00705-009-0323-y.
  • Chiang, K., Liu, H., & Rice, A. P. (2013). miR-132 enhances HIV-1 replication. Virology, 438(1), 1–4. doi:10.1016/j.virol.2012.12.016.
  • Chien, H. L., Liao, C. L., & Lin, Y. L. (2011). FUSE binding protein 1 interacts with untranslated regions of Japanese encephalitis virus RNA and negatively regulates viral replication. Journal of Virology, 85(10), 4698–4706. doi:10.1128/jvi.01950-10.
  • Clark, E. L., Coulson, A., Dalgliesh, C., Rajan, P., Nicol, S. M., Fleming, S., … Robson, C. N. (2008). The RNA helicase p68 is a novel androgen receptor coactivator involved in splicing and is overexpressed in prostate cancer. Cancer Research, 68(19), 7938–7946. doi:10.1158/0008-5472.can-08-0932
  • Cullen, B.R. (2003). Nuclear RNA export. Journal of Cell Science, 116(4), 587–597.10.1242/jcs.00268
  • Dai, T.-Y., Cao, L., Yang, Z.-C., Li, Y.-S., Tan, L., Ran, X.-Z., & Shi, C.-M. (2014). P68 RNA helicase as a molecular target for cancer therapy. Journal of Experimental & Clinical Cancer Research, 33(1), 271. doi:10.1186/s13046-014-0064-y.
  • de Veer, M. J., Holko, M., Frevel, M., Walker, E., Der, S., Paranjape, J. M., … Williams, B. R. (2001). Functional classification of interferon-stimulated genes identified using microarrays. Journal of Leukocyte Biology, 69(6), 912–920.
  • De Vries, D. R., Ter Linde, J. J. M., Van Herwaarden, M. A., Schwartz, M. P., Shephard, P., Geng, M. M., … Samsom, M. (2009). In GERD patients, mucosal repair associated genes are upregulated in non-inflamed oesophageal epithelium. Journal of Cellular and Molecular Medicine, 13(5), 936–947. doi:10.1111/j.1582-4934.2008.00626.x.
  • Dutta, S., Gupta, G., Choi, Y. W., Kotaka, M., Fielding, B. C., Song, J., & Tan, Y. J. (2012). The variable N-terminal region of DDX5 contains structural elements and auto-inhibits its interaction with NS5B of hepatitis C virus. Biochemical Journal, 446(1), 37–46. doi:10.1042/BJ20120001.
  • Edgcomb, S. P., Carmel, A. B., Naji, S., Ambrus-Aikelin, G., Reyes, J. R., Saphire, A. C., … Williamson, J. R. (2012). DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication. Journal of Molecular Biology, 415(1), 61–74. doi:10.1016/j.jmb.2011.10.032.
  • Emery, V. C., & Bishop, D. H. (1987). Characterization of Punta Toro S mRNA species and identification of an inverted complementary sequence in the intergenic region of Punta Toro phlebovirus ambisense S RNA that is involved in mRNA transcription termination. Virology, 156(1), 1–11. doi:10.1016/0042-6822(87)90430-2.10.1016/0042-6822(87)90430-2
  • Fairman-Williams, M. E., Guenther, U. P., & Jankowsky, E. (2010). SF1 and SF2 helicases: Family matters. Current Opinion in Structural Biology, 20(3), 313–324. doi:10.1016/j.sbi.2010.03.011.
  • Fang, J., Kubota, S., Yang, B., Zhou, N., Zhang, H., Godbout, R., & Pomerantz, R. J. (2004). A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev. Virology, 330(2), 471–480. doi:10.1016/j.virol.2004.09.039.
  • Fukuda, T., Yamagata, K., Fujiyama, S., Matsumoto, T., Koshida, I., Yoshimura, K., … Kato, S. (2007). DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nature Cell Biology, 9(5), 604–611. doi:10.1038/ncb1577.
  • Fuller-Pace, F. V. (2006). DExD/H box RNA helicases: Multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Research, 34(15), 4206–4215. doi:10.1093/nar/gkl460.
  • Fuller-Pace, F. V. (2013). The DEAD box proteins DDX5 (p68) and DDX17 (p72): multi-tasking transcriptional regulators. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms, 1829(8), 756–763. doi:10.1016/j.bbagrm.2013.03.004.
  • Germain, D. R., Graham, K., Glubrecht, D. D., Hugh, J. C., Mackey, J. R., & Godbout, R. (2011). DEAD box 1: A novel and independent prognostic marker for early recurrence in breast cancer. Breast Cancer Research and Treatment, 127(1), 53–63. doi:10.1007/s10549-010-0943-7
  • Godbout, R., Hale, M., & Bisgrove, D. (1994). A human DEAD box protein with partial homology to heterogeneous nuclear ribonucleoprotein U. Gene, 138(1–2), 243–245. doi:10.1016/0378-1119(94)90816-8.10.1016/0378-1119(94)90816-8
  • Godbout, R., Packer, M., & Bie, W. (1998). Overexpression of a DEAD box protein (DDX1) in neuroblastoma and retinoblastoma cell lines. Journal of Biological Chemistry, 273(33), 21161–21168. doi:10.1074/jbc.273.33.21161.
  • Goh, P. Y., Tan, Y. J., Lim, S. P., Tan, Y. H., Lim, S. G., Fuller-Pace, F., & Hong, W. (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. Journal of Virology, 78(10), 5288–5298. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15113910. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC400326/pdf/1485-03.pdf10.1128/JVI.78.10.5288-5298.2004
  • Gu, L., Fullam, A., Brennan, R., & Schroder, M. (2013). Human DEAD box helicase 3 couples IkappaB kinase epsilon to interferon regulatory factor 3 activation. Molecular and Cellular Biology, 33(10), 2004–2015. doi:10.1128/mcb.01603-12.
  • Guo, X., Ma, J., Sun, J., & Gao, G. (2007). The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proceedings of the National Academy of Sciences, 104(1), 151–156. doi:10.1073/pnas.0607063104.
  • Han, C., Liu, Y., Wan, G., Choi, H. J., Zhao, L., Ivan, C., … Lu, X. (2014). The RNA-binding protein DDX1 promotes primary microRNA maturation and inhibits ovarian tumor progression. Cell Reports, 8(5), 1447–1460. doi:10.1016/j.celrep.2014.07.058.
  • Harris, M. E., & Hope, T. J. (2000). RNA export: Insights from viral models. Essays In Biochemistry, 36, 115–127. doi:10.1042/bse0360115.10.1042/bse0360115
  • Harris, D., Zhang, Z., Chaubey, B., & Pandey, V. N. (2006). Identification of cellular factors associated with the 3′-nontranslated region of the hepatitis C virus genome. Molecular & Cellular Proteomics, 5(6), 1006–1018. doi:10.1074/mcp.M500429-MCP200.
  • He, L., Chen, Y., Wu, Y., Xu, Y., Zhang, Z., & Liu, Z. (2017). Nucleic acid sensing pattern recognition receptors in the development of colorectal cancer and colitis. Cellular and Molecular Life Sciences, 74(13), 2395–2411. doi:10.1007/s00018-017-2477-1.
  • Heerma van Voss, M. R., Vesuna, F., Trumpi, K., Brilliant, J., Berlinicke, C., de Leng, W., … Raman, V. (2015). Identification of the DEAD box RNA helicase DDX3 as a therapeutic target in colorectal cancer. Oncotarget, 6(29), 28312–28326. doi:10.18632/oncotarget.4873.
  • Heerma van Voss, M. R., Schrijver, W. A., Ter Hoeve, N. D., Hoefnagel, L. D., Manson, Q. F., van der Wall, E., … Dutch Distant Breast Cancer Metastases, C. (2017). The prognostic effect of DDX3 upregulation in distant breast cancer metastases. Clinical & Experimental Metastasis, 34(1), 85–92. doi:10.1007/s10585-016-9832-8.
  • Hilbert, M., Karow, A. R., & Klostermeier, D. (2009). The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biological Chemistry , 390(12), 1237–1250. doi:10.1515/bc.2009.135
  • Hirling, H., Scheffner, M., Restle, T., & Stahl, H. (1989). RNA helicase activity associated with the human p68 protein. Nature, 339(6225), 562–564. doi:10.1038/339562a0
  • Hope, T., & Pomerantz, R.J. (1995). The human immunodeficiency virus type 1 Rev protein: A pivotal protein in the viral life cycle. Current Topics in Microbiology and Immunology, 193, 91–105. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/7648880
  • Huang, H., Shiffman, M. L., Cheung, R. C., Layden, T. J., Friedman, S., Abar, O. T., … Wright, T. L. (2006). Identification of two gene variants associated with risk of advanced fibrosis in patients with chronic hepatitis C. Gastroenterology, 130(6), 1679–1687. doi:10.1053/j.gastro.2006.02.032
  • Huang, J. S., Chao, C. C., Su, T. L., Yeh, S. H., Chen, D. S., Chen, C. T., … Jou, Y. S. (2004). Diverse cellular transformation capability of overexpressed genes in human hepatocellular carcinoma. Biochemical and Biophysical Research Communications, 315(4), 950–958. doi:10.1016/j.bbrc.2004.01.151
  • Huang, W., Thomas, B., Flynn, R. A., Gavzy, S. J., Wu, L., Kim, S. V., … Littman, D. R. (2015). DDX5 and its associated lncRNA Rmrp modulate TH17 cell effector functions. Nature, 528(7583), 517–522. doi:10.1038/nature16193.
  • Ishaq, M., Ma, L., Wu, X., Mu, Y., Pan, J., Hu, J., … Guo, D. (2009). The DEAD-box RNA helicase DDX1 interacts with RelA and enhances nuclear factor kappaB-mediated transcription. Journal of Cellular Biochemistry, 106(2), 296–305. doi:10.1002/jcb.22004
  • Iyer, R. S., Nicol, S. M., Quinlan, P. R., Thompson, A. M., Meek, D. W., & Fuller-Pace, F. V. (2014). The RNA helicase/transcriptional co-regulator, p68 (DDX5), stimulates expression of oncogenic protein kinase, Polo-like kinase-1 (PLK1), and is associated with elevated PLK1 levels in human breast cancers. Cell Cycle, 13(9), 1413–1423. doi:10.4161/cc.28415.
  • Jalal, C., Uhlmann-Schiffler, H., & Stahl, H. (2007). Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Research, 35(11), 3590–3601. doi:10.1093/nar/gkm058.
  • Janknecht, R. (2010). Multi-talented DEAD-box proteins and potential tumor promoters: P68 RNA helicase (DDX5) and its paralog, p72 RNA helicase (DDX17). American Journal of Translational Research, 2(3), 223–234. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2892403/
  • Jankowsky, E., & Fairman, M.E. (2007). RNA helicases–one fold for many functions. Current Opinion in Structural Biology, 17(3), 316–324. doi:10.1016/j.sbi.2007.05.007
  • Jiang, X., Kanda, T., Wu, S., Nakamura, M., Miyamura, T., Nakamoto, S., … Yokosuka, O. (2014). Regulation of microRNA by hepatitis B virus infection and their possible association with control of innate immunity. World Journal of Gastroenterology, 20(23), 7197–7206. doi:10.3748/wjg.v20.i23.7197.
  • Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., … Akira, S. (2006). Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature, 441(7089), 101–105. doi:10.1038/nature04734
  • Kellner, J. N., & Meinhart, A. (2015). Structure of the SPRY domain of the human RNA helicase DDX1, a putative interaction platform within a DEAD-box protein. Acta Crystallographica Section F Structural Biology Communications, 71(9), 1176–1188. doi:10.1107/S2053230X15013709
  • Khadivjam, B., Stegen, C., Hogue-Racine, M. A., El Bilali, N., Dohner, K., Sodeik, B., & Lippe, R. (2017). The ATP-dependent RNA helicase DDX3X modulates herpes simplex virus 1 gene expression. Journal of Virology , 91(8), doi:10.1128/jvi.02411-16.
  • Ko, C., Lee, S., Windisch, M. P., & Ryu, W. S. (2014). DDX3 DEAD-box RNA helicase is a host factor that restricts hepatitis B virus replication at the transcriptional level. Journal of Virology, 88(23), 13689–13698. doi:10.1128/JVI.02035-14.
  • Krishnan, V., & Zeichner, S.L. (2004). Host cell gene expression during human immunodeficiency virus type 1 latency and reactivation and effects of targeting genes that are differentially expressed in viral latency. Journal of Virology, 78(17), 9458–9473. doi:10.1128/jvi.78.17.9458-9473.2004.
  • Kubota, S., & Pomerantz, R. J. (2000). The nuclear function of the nuclear diffusion inhibitory signal of human immunodeficiency virus type 1: Critical roles in dominant nuclear localization and intracellular stability. Journal of Human Virology, 3(4), 173–181. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10990165
  • Lagos, D., Pollara, G., Henderson, S., Gratrix, F., Fabani, M., Milne, R. S., … Boshoff, C. (2010). miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nature Cell Biology, 12(5), 513–519. doi:10.1038/ncb2054.
  • Lamm, G. M., Nicol, S. M., Fuller-Pace, F. V., & Lamond, A. I. (1996). p72: A human nuclear DEAD box protein highly related to p68. Nucleic Acids Research, 24(19), 3739–3747. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC146168/, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC146168/pdf/243739.pdf10.1093/nar/24.19.3739
  • Lee, C.G. (2002). RH70, a bidirectional RNA helicase, co-purifies with U1snRNP. Journal of Biological Chemistry, 277(42), 39679–39683. doi:10.1074/jbc.C200337200
  • Li, C., Ge, L.L., Li, P. P., Wang, Y., Sun, M. X., Huang, L., … Mao, X. (2013). The DEAD-box RNA helicase DDX5 acts as a positive regulator of Japanese encephalitis virus replication by binding to viral 3′ UTR. Antiviral Research, 100(2), 487–499. doi:10.1016/j.antiviral.2013.09.002.
  • Li, C., Ge, L. L., Li, P. P., Wang, Y., Dai, J. J., Sun, M. X., … Mao, X. (2014). 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.
  • Li, Q., Pene, V., Krishnamurthy, S., Cha, H., & Liang, T. J. (2013). Hepatitis C virus infection activates an innate pathway involving IKK-alpha in lipogenesis and viral assembly. Nature Medicine, 19(6), 722–729. doi:10.1038/nm.3190.
  • Lin, S., Tian, L., Shen, H., Gu, Y., Li, J.L., Chen, Z., … Wu, L. (2013). DDX5 is a positive regulator of oncogenic NOTCH1 signaling in T cell acute lymphoblastic leukemia. Oncogene, 32(40), 4845–4853. doi:10.1038/onc.2012.482.
  • Lin, M.H., Sivakumaran, H., Jones, A., Li, D., Harper, C., Wei, T., … Harrich, D. (2014). A HIV-1 Tat mutant protein disrupts HIV-1 Rev function by targeting the DEAD-box RNA helicase DDX1. Retrovirology, 11, 491. doi:10.1186/s12977-014-0121-9.
  • Linder, P., & Jankowsky, E. (2011). From unwinding to clamping – The DEAD box RNA helicase family. Nature Reviews Molecular Cell Biology, 12(8), 505–516. doi:10.1038/nrm3154.
  • Linder, P., Lasko, P. F., Ashburner, M., Leroy, P., Nielsen, P. J., Nishi, K., … Slonimski, P. P. (1989). Birth of the D-E-A-D box. Nature, 337(6203), 121–122. doi:10.1038/337121a0
  • Liu, F., Putnam, A., & Jankowsky, E. (2008). ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proceedings of the National Academy of Sciences, 105(51), 20209–20214. doi:10.1073/pnas.0811115106.
  • Long, J. S., Howard, W. A., Nunez, A., Moncorge, O., Lycett, S., Banks, J., & Barclay, W. S. (2013). The effect of the PB2 mutation 627K on highly pathogenic H5N1 avian influenza virus is dependent on the virus lineage. Journal of Virology, 87(18), 9983–9996. doi:10.1128/jvi.01399-13
  • Loret, S., Guay, G., & Lippe, R. (2008). Comprehensive characterization of extracellular herpes simplex virus type 1 virions. Journal of Virology, 82(17), 8605–8618. doi:10.1128/jvi.00904-08.
  • Lorgeoux, R. P., Pan, Q., Le Duff, Y., & Liang, C. (2013). DDX17 promotes the production of infectious HIV-1 particles through modulating viral RNA packaging and translation frameshift. Virology, 443(2), 384–392. doi:10.1016/j.virol.2013.05.026.
  • Ma, Z., Feng, J., Guo, Y., Kong, R., Ma, Y., Sun, L., … Liu, S. (2017). Knockdown of DDX5 Inhibits the Proliferation and Tumorigenesis in Esophageal Cancer. Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics, 25(6), 887–895. doi:10.3727/096504016x14817158982636
  • Maga, G., Falchi, F., Radi, M., Botta, L., Casaluce, G., Bernardini, M., … Botta, M. (2011). Toward the discovery of novel anti-HIV drugs. Second-generation inhibitors of the cellular ATPase DDX3 with improved anti-HIV activity: Synthesis, structure–activity relationship analysis, cytotoxicity studies, and target validation. ChemMedChem, 6(8), 1371–1389. doi:10.1002/cmdc.201100166.
  • Mallam, A. L., Campo, M. D., Gilman, B., Sidote, D. J., & Lambowitz, A. M. (2012). Structural basis for RNA duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature, 490(7418), 121–125. doi:10.1038/nature11402.
  • Mallam, A. L., Jarmoskaite, I., Tijerina, P., Del Campo, M., Seifert, S., Guo, L., … Lambowitz, A. M. (2011). Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail. Proceedings of the National Academy of Sciences, 108(30), 12254–12259. doi:10.1073/pnas.1109566108. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3145681/, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3145681/pdf/pnas.1109566108.pdf
  • Mamiya, N., & Worman, H. J. (1999). Hepatitis C virus core protein binds to a DEAD box RNA helicase. Journal of Biological Chemistry, 274(22), 15751–15756. Retrieved from http://www.jbc.org/content/274/22/15751.full.pdf10.1074/jbc.274.22.15751
  • Mazurek, A., Park, Y., Miething, C., Wilkinson, J. E., Gillis, J., Lowe, S. W., … Stillman, B. (2014). Acquired dependence of acute myeloid leukemia on the DEAD-box RNA helicase DDX5. Cell Reports, 7(6), 1887–1899. doi:10.1016/j.celrep.2014.05.019. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/24910429, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4100070/pdf/nihms599050.pdf
  • McCormick, C., & Khaperskyy, D.A. (2017). Translation inhibition and stress granules in the antiviral immune response. Nature Reviews Immunology. doi:10.1038/nri.2017.63. Retrieved from http://www.nature.com/articles/nri.2017.63
  • Meyerhans, A., Martinez De La Sierra, M. A., Brai, A., Fazi, R., Tintori, C., Botta, M., … Martinez, J. (2018). Human helicase ddx3 inhibitors as therapeutic agents. U. S. Patent No. 20180016243 Retrieved from https://patents.google.com/patent/US20180016243A1/en
  • Moy, R. H., Cole, B. S., Yasunaga, A., Gold, B., Shankarling, G., Varble, A., … Cherry, S. (2014). Stem-loop recognition by DDX17 facilitates miRNA processing and antiviral defense. Cell, 158(4), 764–777. doi:10.1016/j.cell.2014.06.023.
  • Müller, S., Möller, P., Bick, M. J., Wurr, S., Becker, S., Günther, S., & Kümmerer, B. M. (2007). Inhibition of filovirus replication by the zinc finger antiviral protein. Journal of Virology, 81(5), 2391–2400. doi:10.1128/JVI.01601-06.
  • Naji, S., Ambrus, G., Cimermancic, P., Reyes, J. R., Johnson, J. R., Filbrandt, R., … Gerace, L. (2012). Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Molecular & Cellular Proteomics, 11(4), M111.015313. doi:10.1074/mcp.M111.015313.
  • Nicol, S. M., & Fuller-Pace, F. V. (2010). Analysis of the RNA helicase p68 (Ddx5) as a transcriptional regulator. Methods in Molecular Biology, 587, 265–279. doi:10.1007/978-1-60327-355-8_19.
  • Owsianka, A. M., & Patel, A. H. (1999). Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology, 257(2), 330–340. doi:10.1006/viro.1999.9659.
  • Parker, R., & Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Molecular Cell, 25(5), 635–646. doi:10.1016/j.molcel.2007.02.011
  • Pene, V., Li, Q., Sodroski, C., Hsu, C. S., & Liang, T. J. (2015). Dynamic interaction of stress granules, DDX3X, and IKK-alpha mediates multiple functions in hepatitis C virus infection. Journal of Virology, 89(10), 5462–5477. doi:10.1128/jvi.03197-14.
  • PyMOL. The PyMOL Molecular Graphics System (Version 1.8): Schrödinger, LLC. Retrieved from https://pymol.org/2/
  • Radi, M., Botta, M., Falchi, F., Maga, G., Baldanti, F., & Paolucci, S. (2011). Compounds with ddx3 inhibitory activity and uses thereof. Retrieved from https://patents.google.com/patent/WO2011039735A2/enIt
  • Radi, M., Botta, M., Falchi, F., Maga, G., Baldanti, F., & Paolucci, S. (2012). Retrieved from https://patents.google.com/patent/US20120202814A1/en
  • Radi, M., Falchi, F., Garbelli, A., Samuele, A., Bernardo, V., Paolucci, S., … Botta, M. (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. Bioorganic & Medicinal Chemistry Letters, 22(5), 2094–2098. doi:10.1016/j.bmcl.2011.12.135.
  • Remenyi, J., Bajan, S., Fuller-Pace, F. V., Arthur, J. S., & Hutvagner, G. (2016). The loop structure and the RNA helicase p72/DDX17 influence the processing efficiency of the mice miR-132. Scientific Reports, 6, 415. doi:10.1038/srep22848.
  • Rössler, O. G., Straka, A., & Stahl, H. (2001). Rearrangement of structured RNA via branch migration structures catalysed by the highly related DEAD-box proteins p68 and p72. Nucleic Acids Research, 29(10), 2088–2096. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC55448/
  • Saban, M. R., Hellmich, H. L., Turner, M., Nguyen, N.-B., Vadigepalli, R., Dyer, D. W., … Saban, R. (2006). The inflammatory and normal transcriptome of mouse bladder detrusor and mucosa. BMC Physiology, 6, 1–1. doi:10.1186/1472-6793-6-1.
  • Sathish, N., & Yuan, Y. (2011). Evasion and subversion of interferon-mediated antiviral immunity by Kaposi’s Sarcoma-associated herpesvirus: An overview. Journal of Virology, 85(21), 10934–10944. doi:10.1128/JVI.00687-11.
  • Sato, S., Fukasawa, M., Yamakawa, Y., Natsume, T., Suzuki, T., Shoji, I., … Nishijima, M. (2006). Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. The Journal of Biochemistry, 139(5), 921–930. doi:10.1093/jb/mvj104.
  • Schroder, M. (2011). Viruses and the human DEAD-box helicase DDX3: Inhibition or exploitation? Biochemical Society Transactions, 39(2), 679–683. doi:10.1042/BST0390679.
  • Schroder, M., Baran, M., & Bowie, A. G. (2008). Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. The EMBO Journal, 27(15), 2147–2157. doi:10.1038/emboj.2008.143.
  • Schutz, P., Karlberg, T., van den Berg, S., Collins, R., Lehtio, L., Hogbom, M., … Schuler, H. (2010). Comparative structural analysis of human DEAD-box RNA helicases. PLoS ONE, 5(9). doi:10.1371/journal.pone.0012791.
  • Sharma, D., & Jankowsky, E. (2014). The Ded1/DDX3 subfamily of DEAD-box RNA helicases. Critical Reviews in Biochemistry and Molecular Biology, 49(4), 343–360. doi:10.3109/10409238.2014.931339.
  • Shih, J. W., Wang, W. T., Tsai, T. Y., Kuo, C. Y., Li, H. K., & Wu Lee, Y. H. (2012). Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. Biochemical Journal, 441(1), 119–129. doi:10.1042/bj20110739.
  • Shin, S., Rossow, K. L., Grande, J. P., & Janknecht, R. (2007). Involvement of RNA helicases p68 and p72 in colon cancer. Cancer Research, 67(16), 7572–7578. doi:10.1158/0008-5472.CAN-06-4652.
  • Soulat, D., Burckstummer, T., Westermayer, S., Goncalves, A., Bauch, A., Stefanovic, A., … Superti-Furga, G. (2008). The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. The EMBO Journal, 27(15), 2135–2146. doi:10.1038/emboj.2008.126.
  • Stegen, C., Yakova, Y., Henaff, D., Nadjar, J., Duron, J., & Lippe, R. (2013). Analysis of virion-incorporated host proteins required for herpes simplex virus type 1 infection through a RNA interference screen. PLoS ONE, 8(1), e53276. doi:10.1371/journal.pone.0053276.
  • Steimer, L., & Klostermeier, D. (2012). RNA helicases in infection and disease. RNA Biology, 9(6), 751–771. doi:10.4161/rna.20090.
  • Su, C. Y., Lin, T. C., Lin, Y. F., Chen, M. H., Lee, C. H., Wang, H. Y., … Hsiao, M. (2015). DDX3 as a strongest prognosis marker and its downregulation promotes metastasis in colorectal cancer. Oncotarget, 6(21), 18602–18612. doi:10.18632/oncotarget.4329.
  • Sun, C., Pager, C. T., Luo, G., Sarnow, P., & Cate, J. H. (2010). Hepatitis C virus core-derived peptides inhibit genotype 1b viral genome replication via interaction with DDX3X. PLoS ONE, 5(9), doi:10.1371/journal.pone.0012826.
  • Sunden, Y., Semba, S., Suzuki, T., Okada, Y., Orba, Y., Nagashima, K., … Sawa, H. (2007a). DDX1 promotes proliferation of the JC virus through transactivation of its promoter. Microbiology and Immunology, 51(3), 339–347. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/17380054, http://onlinelibrary.wiley.com/store/10.1111/j.1348-0421.2007.tb03907.x/asset/mim03907.pdf?v=1&t=iplgs1e0&s=9c64859a5d6952f55f28d81e56653b1cb144b04810.1111/mim.2007.51.issue-3
  • Sunden, Y., Semba, S., Suzuki, T., Okada, Y., Orba, Y., Nagashima, K., … Sawa, H. (2007). Identification of DDX1 as a JC virus transcriptional control region-binding protein. Microbiology and Immunology, 51(3), 327–337. Retrieved from http://onlinelibrary.wiley.com/store/10.1111/j.1348-0421.2007.tb03915.x/asset/mim03915.pdf?v=1&t=j72s86mi&s=ad447cb3c2e2473405bd485041633db21adc7abb10.1111/mim.2007.51.issue-3
  • Tanaka, K., Okamoto, S., Ishikawa, Y., Tamura, H., & Hara, T. (2009). DDX1 is required for testicular tumorigenesis, partially through the transcriptional activation of 12p stem cell genes. Oncogene, 28(21), 2142–2151. doi:10.1038/onc.2009.89.
  • Taniguchi, T., Iizumi, Y., Watanabe, M., Masuda, M., Morita, M., Aono, Y., … Sakai, T. (2016). Resveratrol directly targets DDX5 resulting in suppression of the mTORC1 pathway in prostate cancer. Cell Death & Disease, 7, e2211. doi:10.1038/cddis.2016.114
  • Theissen, B., Karow, A.R., Köhler, J., Gubaev, A., & Klostermeier, D. (2008). Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proceedings of the National Academy of Sciences, 105(2), 548–553. doi:10.1073/pnas.0705488105.
  • Thulasi Raman, S. N., Liu, G., Pyo, H. M., Cui, Y. C., Xu, F., Ayalew, L. E., … Zhou, Y. (2016). DDX3 interacts with influenza A virus NS1 and NP proteins and exerts antiviral function through regulation of stress granule formation. Journal of Virology, 90(7), 3661–3675. doi:10.1128/jvi.03010-15.
  • Tingting, P., Caiyun, F., Zhigang, Y., Pengyuan, Y., & 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. Biochemical and Biophysical Research Communications, 347(3), 683–691. doi:10.1016/j.bbrc.2006.06.144.
  • Uhlmann-Schiffler, H., Rossler, O. G., & Stahl, H. (2002). The mRNA of DEAD box protein p72 is alternatively translated into an 82-kDa RNA helicase. Journal of Biological Chemistry, 277(2), 1066–1075. doi:10.1074/jbc.M107535200.
  • Upadya, M. H., Aweya, J. J., & Tan, Y. J. (2014). Understanding the interaction of hepatitis C virus with host DEAD-box RNA helicases. World Journal of Gastroenterology, 20(11), 2913–2926. doi:10.3748/wjg.v20.i11.2913.
  • Varnum, S.M., Streblow, D.N., Monroe, M.E., Smith, P., Auberry, K.J., Pasa-Tolic, L., … Wang, D. (2004). Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. Journal of Virology, 78(20), 10960–10966. doi:10.1128/jvi.78.20.10960-10966.2004
  • Vashist, S., Urena, L., Chaudhry, Y., & Goodfellow, I. (2012). Identification of RNA-protein interaction networks involved in the norovirus life cycle. Journal of Virology, 86(22), 11977–11990. doi:10.1128/jvi.00432-12.
  • Wang, H., Gao, X., Huang, Y., Yang, J., & Liu, Z.-R. (2009). P68 RNA helicase is a nucleocytoplasm shuttling protein. Cell Research, 19(12), 1388–1400. doi:10.1038/cr.2009.113.
  • Wang, D., Huang, J., & Hu, Z. (2012). RNA helicase DDX5 regulates microRNA expression and contributes to cytoskeletal reorganization in basal breast cancer cells. Molecular & Cellular Proteomics, 11(2), M111.011932. doi:10.1074/mcp.M111.011932.
  • Wang, H., Kim, S., & Ryu, W. S. (2009). DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. Journal of Virology, 83(11), 5815–5824. doi:10.1128/JVI.00011-09.
  • Wang, H., & Ryu, W. S. (2010). Hepatitis B virus polymerase blocks pattern recognition receptor signaling via interaction with DDX3: Implications for immune evasion. PLoS Pathogens, 6(7), e1000986. doi:10.1371/journal.ppat.1000986.
  • Wilson, B. J., Bates, G. J., Nicol, S. M., Gregory, D. J., Perkins, N. D., & Fuller-Pace, F. V. (2004). The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. BMC Molecular Biology, 5, doi:10.1186/1471-2199-5-11.
  • Wortham, N. C., Ahamed, E., Nicol, S. M., Thomas, R. S., Periyasamy, M., Jiang, J., … Fuller-Pace, F. V. (2009). The DEAD-box protein p72 regulates ERalpha-/oestrogen-dependent transcription and cell growth, and is associated with improved survival in ERalpha-positive breast cancer. Oncogene, 28, doi:10.1038/onc.2009.261.
  • Wu, C. H., Chen, P. J., & Yeh, S. H. (2014). Nucleocapsid phosphorylation and RNA helicase DDX1 recruitment enables coronavirus transition from discontinuous to continuous transcription. Cell Host & Microbe, 16(4), 462–472. doi:10.1016/j.chom.2014.09.009.
  • Xu, L., Khadijah, S., Fang, S., Wang, L., Tay, F. P., & Liu, D. X. (2010). The cellular RNA helicase DDX1 interacts with coronavirus nonstructural protein 14 and enhances viral replication. Journal of Virology, 84(17), 8571–8583. doi:10.1128/JVI.00392-10.
  • Yamada, S., Hatta, M., Staker, B. L., Watanabe, S., Imai, M., Shinya, K., … Kawaoka, Y. (2010). Biological and structural characterization of a host-adapting amino acid in influenza virus. PLoS Pathogens, 6(8), e1001034. doi:10.1371/journal.ppat.1001034
  • Yasuda-Inoue, M., Kuroki, M., & Ariumi, Y. (2013). DDX3 RNA helicase is required for HIV-1 Tat function. Biochemical and Biophysical Research Communications, 441(3), 607–611. doi:10.1016/j.bbrc.2013.10.107.
  • Yedavalli, V. S., Neuveut, C., Chi, Y. H., Kleiman, L., & Jeang, K. T. (2004). Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell, 119(3), 381–392. doi:10.1016/j.cell.2004.09.029.
  • You, L. R., Chen, C. M., Yeh, T. S., Tsai, T. Y., Mai, R. T., Lin, C. H., & Lee, Y. H. (1999). Hepatitis C virus core protein interacts with cellular putative RNA helicase. Journal of Virology, 73(4), 2841–2853. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10074132, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC104042/pdf/jv002841.pdf
  • Zhao, S., Ge, X., Wang, X., Liu, A., Guo, X., Zhou, L., … Yang, H. (2015). The DEAD-box RNA helicase 5 positively regulates the replication of porcine reproductive and respiratory syndrome virus by interacting with viral Nsp9 in vitro. Virus Research, 195, 217–224. doi:10.1016/j.virusres.2014.10.021.
  • Zhou, X., Luo, J., Mills, L., Wu, S., Pan, T., Geng, G., … Zhang, H. (2013). DDX5 facilitates HIV-1 replication as a cellular co-factor of Rev. PLoS ONE, 8(5), e65040. doi:10.1371/journal.pone.0065040.
  • Zhou, Y., Wu, W., Xie, L., Wang, D., Ke, Q., Hou, Z., … Fang, L. (2017). Cellular RNA helicase DDX1 is involved in transmissible gastroenteritis virus nsp14-induced interferon-beta production. [Original Research]. Frontiers in Immunology , 8(940), doi:10.3389/fimmu.2017.00940.
  • Zhu, Y., Chen, G., Lv, F., Wang, X., Ji, X., Xu, Y., … Gao, G. (2011). Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation. Proceedings of the National Academy of Sciences, 108(38), 15834–15839. doi:10.1073/pnas.1101676108.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.