RNA helicase MOV10 functions as a co-factor of HIV-1 Rev to facilitate Rev/RRE-dependent nuclear export of viral mRNAs

Virology

Volumn 486, Issue , 2015, Pages 15-26

  Huang, Feng ^a   Zhang, Junsong ^a   Zhang, Yijun ^a   Geng, Guannan ^a   Liang, Juanran ^a   Li, Yingniang ^a   Chen, Jingliang ^a   Liu, Chao ^a   Zhang, Hui ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

HIV 1; MOV10; Rev; RNA transport; RRE

Indexed keywords

GAG PROTEIN; MUTANT PROTEIN; PROTEIN MOV10; REV PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG; VIRUS MESSENGER RNA; MESSENGER RNA; MOV10 PROTEIN, HUMAN; PROTEIN BINDING; VIRUS RNA;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA TRANSPORT; VIRUS CELL INTERACTION; VIRUS REPLICATION; CHEMISTRY; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY;

BIOLOGICAL TRANSPORT; GENE PRODUCTS, GAG; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RESPONSE ELEMENTS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA HELICASES; RNA, MESSENGER; RNA, VIRAL;

EID: 84942036816     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.08.026     Document Type: Article

References (81)

1. Abudu A., Wang X., Dang Y., Zhou T., Xiang S.H., Zheng Y.H. Identification of molecular determinants from Moloney leukemia virus 10 homolog (MOV10) protein for virion packaging and anti-HIV-1 activity. J. Biol. Chem. 2012, 287:1220-1228.
2. Arjan-Odedra S., Swanson C.M., Sherer N.M., Wolinsky S.M., Malim M.H. Endogenous MOV10 inhibits the retrotransposition of endogenous retroelements but not the replication of exogenous retroviruses. Retrovirology 2012, 9:53.
3. Askjaer P., Jensen T.H., Nilsson J., Englmeier L., Kjems J. The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J. Biol. Chem. 1998, 273:33414-33422.
4. Askjaer P., Rosendahl R., Kjems J. Nuclear export of the DEAD box An3 protein by CRM1 is coupled to An3 helicase activity. J. Biol. Chem. 2000, 275:11561-11568.
5. Banerjee A., Benjamin R., Balakrishnan K., Ghosh P., Banerjee S. Human protein Staufen-2 promotes HIV-1 proliferation by positively regulating RNA export activity of viral protein. Rev. Retrovirol. 2014, 11:18.
6. Barr S.D., Smiley J.R., Bushman F.D. The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog. 2008, 4:e1000007.
7. Battiste J.L., Mao H., Rao N.S., Tan R., Muhandiram D.R., Kay L.E., Frankel A.D., Williamson J.R. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science 1996, 273:1547-1551.
8. Bear J., Tan W., Zolotukhin A.S., Tabernero C., Hudson E.A., Felber B.K. Identification of novel import and export signals of human TAP, the protein that binds to the constitutive transport element of the type D retrovirus mRNAs. Mol. Cell. Biol. 1999, 19:6306-6317.
9. Brass A.L., Dykxhoorn D.M., Benita Y., Yan N., Engelman A., Xavier R.J., Lieberman J., Elledge S.J. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319:921-926.
10. Burdick R., Smith J.L., Chaipan C., Friew Y., Chen J., Venkatachari N.J., Delviks-Frankenberry K.A., Hu W.S., Pathak V.K. P body-associated protein Mov10 inhibits HIV-1 replication at multiple stages. J. Virol. 2010, 84:10241-10253.
11. Cano J., Kalpana G.V. Inhibition of early stages of HIV-1 assembly by INI1/hSNF5 transdominant negative mutant S6. J. Virol. 2011, 85:2254-2265.
12. Chen C.Y., Liu X., Boris-Lawrie K., Sharma A., Jeang K.T. Cellular RNA helicases and HIV-1: insights from genome-wide, proteomic, and molecular studies. Virus Res. 2013, 171:357-365.
13. Clouse K.N., Luo M.J., Zhou Z., Reed R. A Ran-independent pathway for export of spliced mRNA. Nat. Cell Biol. 2001, 3:97-99.
14. Cordin O., Banroques J., Tanner N.K., Linder P. The DEAD-box protein family of RNA helicases. Gene 2006, 367:17-37.
15. Cuevas R., Hornung V., Coyne C., Sarkar S. MOV10 provides antiviral activity against RNA viruses by enhancing IFN induction through IKKε and IRF3.(INC8P. 441). J. Immunol. 2014, 192:1-14. 187.114.
16. Cullen B.R. Viral RNAs: lessons from the enemy. Cell 2009, 136:592-597.
17. Doria M., Neri F., Gallo A., Farace M.G., Michienzi A. Editing of HIV-1 RNA by the double-stranded RNA deaminase ADAR1 stimulates viral infection. Nucleic Acids Res. 2009, 37:5848-5858.
18. Edgcomb S.P., Carmel A.B., Naji S., Ambrus-Aikelin G., Reyes J.R., Saphire A.C., Gerace L., Williamson J.R. DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication. J. Mol. Biol. 2012, 415:61-74.
19. El Messaoudi-Aubert S., Nicholls J., Maertens G.N., Brookes S., Bernstein E., Peters G. Role for the MOV10 RNA helicase in polycomb-mediated repression of the INK4a tumor suppressor. Nat. Struct. Mol. Biol. 2010, 17:862-868.
20. Fang J.H., Kubota S., Yang B., Zhou N.M., Zhang H., Godbout R., Pomerantz R.J. A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev. Virology 2004, 330:471-480.
21. Fukuda M., Asano S., Nakamura T., Adachi M., Yoshida M., Yanagida M., Nishida E. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 1997, 390:308-311.
22. Furtak V., Mulky A., Rawlings S.A., Kozhaya L., Lee K., Kewalramani V.N., Unutmaz D. Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PloS One 2010, 5:e9081.
23. Gallois-Montbrun S., Kramer B., Swanson C.M., Byers H., Lynham S., Ward M., Malim M.H. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J. Virol. 2007, 81:2165-2178.
24. Garrett E.D., Tiley L.S., Cullen B.R. Rev activates expression of the human immunodeficiency virus type 1 vif and vpr gene products. J. Virol. 1991, 65:1653-1657.
25. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Cote M., Rich R.L., Myszka D.G., Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001, 107:55-65.
26. Goodier J.L., Cheung L.E., Kazazian H.H. MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet. 2012, 8:e1002941.
27. Gottlinger H.G., Dorfman T., Sodroski J.G., Haseltine W.A. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 1991, 88:3195-3199.
28. Gregersen L.H., Schueler M., Munschauer M., Mastrobuoni G., Chen W., Kempa S., Dieterich C., Landthaler M. MOV10 Is a 5' to 3' RNA helicase contributing to UPF1 mRNA target degradation by translocation along 3' UTRs. Mol. Cell 2014, 54:573-585.
29. Haussecker D., Cao D., Huang Y., Parameswaran P., Fire A.Z., Kay M.A. Capped small RNAs and MOV10 in human hepatitis delta virus replication. Nat. Struct. Mol. Biol. 2008, 15:714-721.
30. Heaphy S., Dingwall C., Ernberg I., Gait M.J., Green S.M., Karn J., Lowe A.D., Singh M., Skinner M.A. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 1990, 60:685-693.
31. Herbeuval J.P., Shearer G.M. HIV-1 immunopathogenesis: how good interferon turns bad. Clin. Immunol. 2007, 123:121-128.
32. Hermida-Matsumoto L., Resh M.D. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 2000, 74:8670-8679.
33. Huang J., Wang F., Argyris E., Chen K., Liang Z., Tian H., Huang W., Squires K., Verlinghieri G., Zhang H. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 2007, 13:1241-1247.
34. Izumi T., Burdick R., Shigemi M., Plisov S., Hu W.S., Pathak V.K. Mov10 and APOBEC3G localization to processing bodies is not required for virion incorporation and antiviral activity. J. Virol. 2013, 87:11047-11062.
35. Jaenisch R., Jahner D., Nobis P., Simon I., Lohler J., Harbers K., Grotkopp D. Chromosomal position and activation of retroviral genomes inserted into the germ line of mice. Cell 1981, 24:519-529.
36. Jager S., Cimermancic P., Gulbahce N., Johnson J.R., McGovern K.E., Clarke S.C., Shales M., Mercenne G., Pache L., Li K., Hernandez H., Jang G.M., Roth S.L., Akiva E., Marlett J., Stephens M., D'Orso I., Fernandes J., Fahey M., Mahon C., O'Donoghue A.J., Todorovic A., Morris J.H., Maltby D.A., Alber T., Cagney G., Bushman F.D., Young J.A., Chanda S.K., Sundquist W.I., Kortemme T., Hernandez R.D., Craik C.S., Burlingame A., Sali A., Frankel A.D., Krogan N.J. Global landscape of HIV-human protein complexes. Nature 2012, 481:365-370.
37. Jager S., Kim D.Y., Hultquist J.F., Shindo K., LaRue R.S., Kwon E., Li M., Anderson B.D., Yen L., Stanley D., Mahon C., Kane J., Franks-Skiba K., Cimermancic P., Burlingame A., Sali A., Craik C.S., Harris R.S., Gross J.D., Krogan N.J. Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 2012, 481:371-375.
38. Kenny P.J., Zhou H., Kim M., Skariah G., Khetani R.S., Drnevich J., Arcila M.L., Kosik K.S., Ceman S. MOV10 and FMRP regulate AGO2 association with microRNA recognition elements. Cell Rep. 2014, 9:1729-1741.
39. Kim Y.K., Furic L., Desgroseillers L., Maquat L.E. Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay. Cell 2005, 120:195-208.
40. Kozak S.L., Marin M., Rose K.M., Bystrom C., Kabat D. The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J. Biol. Chem. 2006, 281:29105-29119.
41. Li S., Wang L., Berman M., Kong Y.Y., Dorf M.E. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 2011, 35:426-440.
42. Li X., Zhang J., Jia R., Cheng V., Xu X., Qiao W., Guo F., Liang C., Cen S. The MOV10 helicase inhibits LINE-1 mobility. J. Biol. Chem. 2013, 288:21148-21160.
43. Linder P., Tanner N.K., Banroques J. From RNA helicases to RNPases. Trends Biochem. Sci. 2001, 26:339-341.
44. Liu C., Zhang X., Huang F., Yang B., Li J., Liu B.F., Luo H.H., Zhang P., Zhang H. APOBEC3G inhibits MicroRNA-mediated repression of translation by interfering with the interaction between Argonaute-2 and MOV10. J. Biol. Chem. 2012, 287:29373-29383.
45. Malim M.H., Hauber J., Le S.Y., Maizel J.V., Cullen B.R. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989, 338:254-257.
46. Mariani R., Rutter G., Harris M.E., Hope T.J., Krausslich H.G., Landau N.R. A block to human immunodeficiency virus type 1 assembly in murine cells. J. Virol. 2000, 74:3859-3870.
47. Meister G., Landthaler M., Peters L., Chen P.Y., Urlaub H., Luhrmann R., Tuschl T. Identification of novel argonaute-associated proteins. Curr. Biol. 2005, 15:2149-2155.
48. Meister G., Landthaler M., Peters L., Chen P.Y., Urlaub H., Luhrmann R., Tuschl T. Identification of novel argonaute-associated proteins. Curr. Biol. 2005, 15:2149-2155.
49. Miki T., Kamikawa Y., Kurono S., Kaneko Y., Katahira J., Yoneda Y. Cell type-dependent gene regulation by Staufen2 in conjunction with Upf1. BMC Mol. Biol. 2011, 12:48.
50. Mogensen T.H., Melchjorsen J., Larsen C.S., Paludan S.R. Innate immune recognition and activation during HIV infection. Retrovirology 2010, 7:54.
51. Naji S., Ambrus G., Cimermancic P., Reyes J.R., Johnson J.R., Filbrandt R., Huber M.D., Vesely P., Krogan N.J., Yates J.R., Saphire A.C., Gerace L. Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell. Proteom. 2012, 11. M111 015313, 1-14.
52. Nakano M., Kakiuchi Y., Shimada Y., Ohyama M., Ogiwara Y., Sasaki-Higashiyama N., Yano N., Ikeda F., Yamada E., Iwamatsu A., Kobayashi K., Nishiyama K., Ichikawa S., Kaji K., Ide T., Murofushi H., Murakami-Murofushi K. MOV10 as a novel telomerase-associated protein. Biochem. Biophys. Res. Commun. 2009, 388:328-332.
53. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
54. Neville M., Stutz F., Lee L., Davis L.I., Rosbash M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 1997, 7:767-775.
55. Ossareh-Nazari B., Bachelerie F., Dargemont C. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 1997, 278:141-144.
56. Pasquinelli A.E., Ernst R.K., Lund E., Grimm C., Zapp M.L., Rekosh D., Hammarskjold M.L., Dahlberg J.E. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 1997, 16:7500-7510.
57. Perez-Caballero D., Zang T., Ebrahimi A., McNatt M.W., Gregory D.A., Johnson M.C., Bieniasz P.D. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 2009, 139:499-511.
58. Phuphuakrat A., Kraiwong R., Boonarkart C., Lauhakirti D., Lee T.H., Auewarakul P. Double-stranded RNA adenosine deaminases enhance expression of human immunodeficiency virus type 1 proteins. J. Virol. 2008, 82:10864-10872.
59. Pollard V.W., Malim M.H. The HIV-1 Rev protein. Annu. Rev. Microbiol. 1998, 52:491-532.
60. Purcell D.F., Martin M.A. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 1993, 67:6365-6378.
61. Saavedra C., Felber B., Izaurralde E. The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export. Curr. Biol. 1997, 7:619-628.
62. Schnieke A., Harbers K., Jaenisch R. Embryonic lethal mutation in mice induced by retrovirus insertion into the alpha 1(I) collagen gene. Nature 1983, 304:315-320.
63. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., Rice C.M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
64. Schwartz S., Felber B.K., Benko D.M., Fenyo E.M., Pavlakis G.N. Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J. Virol. 1990, 64:2519-2529.
65. Schwartz S., Felber B.K., Fenyo E.M., Pavlakis G.N. Env and Vpu proteins of human immunodeficiency virus type 1 are produced from multiple bicistronic mRNAs. J. Virol. 1990, 64:5448-5456.
66. Sheehy A.M., Gaddis N.C., Malim M.H. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 2003, 9:1404-1407.
67. Sievers C., Schlumpf T., Sawarkar R., Comoglio F., Paro R. Mixture models and wavelet transforms reveal high confidence RNA-protein interaction sites in MOV10 PAR-CLIP data. Nucleic Acids Res. 2012, 40:e160.
68. Sim S., Yao J., Weinberg D.E., Niessen S., Yates J.R., Wolin S.L. The zipcode-binding protein ZBP1 influences the subcellular location of the Ro 60-kDa autoantigen and the noncoding Y3 RNA. RNA 2012, 18:100-110.
69. Song Z.W., Ma Y.X., Fu B.Q., Teng X., Chen S.J., Xu W.Z., Gu H.X. Altered mRNA levels of MOV10, A3G, and IFN-alpha in patients with chronic hepatitis B. J. Microbiol. 2014, 52:510-514.
70. Stutz F., Bachi A., Doerks T., Braun I.C., Seraphin B., Wilm M., Bork P., Izaurralde E. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000, 6:638-650.
71. Tanner N.K., Linder P. DExD/H box RNA helicases: From generic motors to specific dissociation functions. Mol. Cell 2001, 8:251-262.
72. Van Baalen C.A., Schutten M., Huisman R.C., Boers P.H., Gruters R.A., Osterhaus A.D. Kinetics of antiviral activity by human immunodeficiency virus type 1-specific cytotoxic T lymphocytes (CTL) and rapid selection of CTL escape virus in vitro. J. Virol. 1998, 72:6851-6857.
73. Wang X., Han Y., Dang Y., Fu W., Zhou T., Ptak R.G., Zheng Y.H. Moloney leukemia virus 10 (MOV10) protein inhibits retrovirus replication. J. Biol. Chem. 2010, 285:14346-14355.
74. Yan N., Chen Z.J. Intrinsic antiviral immunity. Nat. Immunol. 2012, 13:214-222.
75. Yedavalli V.S.R.K., Neuveut C., Chi Y.H., Kleiman L., Jeang K.T. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 2004, 119:381-392.
76. Yin Y., Zhang S., Luo H., Zhang X., Geng G., Li J., Guo X., Cai W., Li L., Liu C., Zhang H. Interleukin 7 up-regulates CD95 protein on CD4+ T cells by affecting mRNA alternative splicing: priming for a synergistic effect on HIV-1 reservoir maintenance. J. Biol. Chem. 2015, 290:35-45.
77. Zhang Y., Fan M., Geng G., Liu B., Huang Z., Luo H., Zhou J., Guo X., Cai W., Zhang H. A novel HIV-1-encoded microRNA enhances its viral replication by targeting the TATA box region. Retrovirology 2014, 11:23.
78. Zhang Y., Fan M., Zhang X., Huang F., Wu K., Zhang J., Liu J., Huang Z., Luo H., Tao L., Zhang H. Cellular microRNAs up-regulate transcription via interaction with promoter TATA-box motifs. RNA 2014, 20:1878-1889.
79. Zhao K., Du J., Han X., Goodier J.L., Li P., Zhou X., Wei W., Evans S.L., Li L., Zhang W., Cheung L.E., Wang G., Kazazian H.H., Yu X.F. Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 2013, 4:1108-1115.
80. Zhou X., Luo J., Mills L., Wu S., Pan T., Geng G., Zhang J., Luo H., Liu C., Zhang H. DDX5 facilitates HIV-1 replication as a cellular co-factor of Rev. PLoS One 2013, 8:e65040.
81. Zhou X.X., Luo J., Mills L., Wu S.X., Pan T., Geng G.N., Zhang J., Luo H.H., Liu C., Zhang H. DDX5 facilitates HIV-1 replication as a cellular co-factor of Rev. PLoS One 2013, 8:e65040.