Dynamic nucleolar targeting of dengue virus polymerase NS5 in response to extracellular pH

Journal of Virology

Volumn 90, Issue 12, 2016, Pages 5797-5807

  Fraser, Johanna E ^a   Rawlinson, Stephen M ^a   Heaton, Steven M ^a,b   Jans, David A ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 5; GREEN FLUORESCENT PROTEIN; NS5 PROTEIN, DENGUE VIRUS; VIRAL PROTEIN;

ARTICLE; CELL PH; CONTROLLED STUDY; DENGUE; EMBRYO; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; HYDROPHOBICITY; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN TRANSPORT; ANIMAL; CELL NUCLEUS; CHEMISTRY; CHLOROCEBUS AETHIOPS; DENGUE VIRUS; ENZYMOLOGY; EXTRACELLULAR SPACE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; METABOLISM; MUTATION; PH; VERO CELL LINE; VIRUS REPLICATION;

ANIMALS; CELL NUCLEOLUS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; DENGUE VIRUS; EXTRACELLULAR SPACE; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MUTATION; PROTEIN TRANSPORT; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84971407801     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02727-15     Document Type: Article

References (53)

1. Mayer C, Grummt I. 2005. Cellular stress and nucleolar function. Cell Cycle 4:1036-1038. http://dx.doi.org/10.4161/cc.4.8.1925.
2. Pederson T. 2011. The nucleolus. Cold Spring Harb Perspect Biol 3:a000638. http://dx.doi.org/10.1101/cshperspect.a000638.
3. Rawlinson SM, Moseley GW. 2015. The nucleolar interface of RNA viruses. Cell Microbiol 17:1108-1120. http://dx.doi.org/10.1111/cmi.12465.
4. Fulcher AJ, Jans DA. 2011. Regulation of nucleocytoplasmic trafficking of viral proteins: an integral role in pathogenesis? Biochim Biophys Acta 1813:2176-2190. http://dx.doi.org/10.1016/j.bbamcr.2011.03.019.
5. Hutten S, Kehlenbach RH. 2007. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 17:193-201. http://dx.doi.org/10.1016/j.tcb.2007.02.003.
6. Kutay U, Guttinger S. 2005. Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol 15:121-124. http://dx.doi.org/10.1016/j.tcb.2005.01.005.
7. Emmott E, Hiscox JA. 2009. Nucleolar targeting: the hub of the matter. EMBO Rep 10:231-238. http://dx.doi.org/10.1038/embor.2009.14.
8. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI. 2002. Directed proteomic analysis of the human nucleolus. Curr Biol 12:1-11. http://dx.doi.org/10.1016/S0960-9822(01)00650-9.
9. Scott MS, Boisvert FM, McDowall MD, Lamond AI, Barton GJ. 2010. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res 38:7388-7399. http://dx.doi.org/10.1093/nar/gkq653.
10. Lam YW, Lamond AI, Mann M, Andersen JS. 2007. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 17:749-760. http://dx.doi.org/10.1016/j.cub.2007.03.064.
11. Sirri V, Hernandez-Verdun D, Roussel P. 2002. Cyclin-dependent ki-nases govern formation and maintenance of the nucleolus. J Cell Biol 156:969-981. http://dx.doi.org/10.1083/jcb.200201024.
12. Hiscox JA. 2003. The interaction of animal cytoplasmic RNA viruses with the nucleus to facilitate replication. Virus Res 95:13-22. http://dx.doi.org/10.1016/S0168-1702(03)00160-6.
13. Salvetti A, Greco A. 2014. Viruses and the nucleolus: the fatal attraction. Biochim Biophys Acta 1842:840-847. http://dx.doi.org/10.1016/j.bbadis.2013.12.010.
14. Hiscox JA, Wurm T, Wilson L, Britton P, Cavanagh D, Brooks G. 2001. The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J Virol 75:506-512. http://dx.doi.org/10.1128/JVI.75.1.506-512.2001.
15. Rowland RR, Kervin R, Kuckleburg C, Sperlich A, Benfield DA. 1999. The localization of porcine reproductive and respiratory syndrome virus nucleocapsid protein to the nucleolus of infected cells and identification of a potential nucleolar localization signal sequence. Virus Res 64:1-12. http://dx.doi.org/10.1016/S0168-1702(99)00048-9.
16. Michel MR, Elgizoli M, Dai Y, Jakob R, Koblet H, Arrigo AP. 1990. Karyophilic properties of Semliki Forest virus nucleocapsid protein. J Virol 64:5123-5131.
17. Balinsky CA, Schmeisser H, Ganesan S, Singh K, Pierson TC, Zoon KC. 2013. Nucleolin interacts with the dengue virus capsid protein and plays a role in formation of infectious virus particles. J Virol 87:13094-13106. http://dx.doi.org/10.1128/JVI.00704-13.
18. Wang SH, Syu WJ, Huang KJ, Lei HY, Yao CW, King CC, Hu ST. 2002. Intracellular localization and determination of a nuclear localization signal of the core protein of dengue virus. J Gen Virol 83:3093-3102. http://dx.doi.org/10.1099/0022-1317-83-12-3093.
19. Hirano M, Kaneko S, Yamashita T, Luo H, Qin W, Shirota Y, Nomura T, Kobayashi K, Murakami S. 2003. Direct interaction between nucleolin and hepatitis C virus NS5B. J Biol Chem 278:5109-5115. http://dx.doi.org/10.1074/jbc.M207629200.
20. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI. 2013. The global distribution and burden of dengue. Nature 496:504-507. http://dx.doi.org/10.1038/nature12060.
21. Pryor MJ, Rawlinson SM, Butcher RE, Barton CL, Waterhouse TA, Vasudevan SG, Bardin PG, Wright PJ, Jans DA, Davidson AD. 2007. Nuclear localization of dengue virus nonstructural protein 5 through its importin alpha/beta-recognized nuclear localization sequences is integral to viral infection. Traffic 8:795-807. http://dx.doi.org/10.1111/j.1600-0854.2007.00579.x.
22. Tay MY, Fraser JE, Chan WK, Moreland NJ, Rathore AP, Wang C, Vasudevan SG, Jans DA. 2013. Nuclear localization of dengue virus (DENV) 1-4 nonstructural protein 5: protection against all 4 DENV serotypes by the inhibitor Ivermectin. Antiviral Res 99:301-306. http://dx.doi.org/10.1016/j.antiviral.2013.06.002.
23. Lindenbach BD, Thiel H, Rice CM. 2007. Flaviviridae: the viruses and their replication, 5th ed. Wolters Kluwer/Lippincott/Williams & Wilkins, Philadelphia, PA.
24. Brooks AJ, Johansson M, John AV, Xu Y, Jans DA, Vasudevan SG. 2002. The interdomain region of dengue NS5 protein that binds to the viral helicase NS3 contains independently functional importin β1 and importin alpha/beta-recognized nuclear localization signals. J Biol Chem 277:36399-36407. http://dx.doi.org/10.1074/jbc.M204977200.
25. Forwood JK, Brooks A, Briggs LJ, Xiao CY, Jans DA, Vasudevan SG. 1999. The 37-amino-acid interdomain of dengue virus NS5 protein contains a functional NLS and inhibitory CK2 site. Biochem Biophys Res Commun 257:731-737. http://dx.doi.org/10.1006/bbrc.1999.0370.
26. Johansson M, Brooks AJ, Jans DA, Vasudevan SG. 2001. A small region of the dengue virus-encoded RNA-dependent RNA polymerase, NS5, confers interaction with both the nuclear transport receptor importinbeta and the viral helicase, NS3. J Gen Virol 82:735-745. http://dx.doi.org/10.1099/0022-1317-82-4-735.
27. Rawlinson SM, Pryor MJ, Wright PJ, Jans DA. 2009. CRM1-mediated nuclear export of dengue virus RNA polymerase NS5 modulates interleukin-8 induction and virus production. J Biol Chem 284:15589-15597. http://dx.doi.org/10.1074/jbc.M808271200.
28. Hannemann H, Sung PY, Chiu HC, Yousuf A, Bird J, Lim SP, Davidson AD. 2013. Serotype-specific differences in dengue virus nonstructural protein 5 nuclear localization. J Biol Chem 288:22621-22635. http://dx.doi.org/10.1074/jbc.M113.481382.
29. Kumar A, Buhler S, Selisko B, Davidson A, Mulder K, Canard B, Miller S, Bartenschlager R. 2013. Nuclear localization of dengue virus nonstructural protein 5 does not strictly correlate with efficient viral RNA replication and inhibition of type I interferon signaling. J Virol 87:4545-4557. http://dx.doi.org/10.1128/JVI.03083-12.
30. Fraser JE, Watanabe S, Wang C, Chan WK, Maher B, Lopez-Denman A, Hick C, Wagstaff KM, Mackenzie JM, Sexton PM, Vasudevan SG, Jans DA. 2014. A nuclear transport inhibitor that modulates the unfolded protein response and provides in vivo protection against lethal dengue virus infection. J Infect Dis 210:1780-1791. http://dx.doi.org/10.1093/infdis/jiu319.
31. Wagstaff KM, Sivakumaran H, Heaton SM, Harrich D, Jans DA. 2012. Ivermectin is a specific inhibitor of importin alpha/beta-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus. Biochem J 443:851-856. http://dx.doi.org/10.1042/BJ20120150.
32. Fraser JE, Rawlinson SM, Wang C, Jans DA, Wagstaff KM. 2014. Investigating dengue virus nonstructural protein 5 (NS5) nuclear import. Methods Mol Biol 1138:301-328. http://dx.doi.org/10.1007/978-1-4939-0348-1_19.
33. Wang QY, Patel SJ, Vangrevelinghe E, Xu HY, Rao R, Jaber D, Schul W, Gu F, Heudi O, Ma NL, Poh MK, Phong WY, Keller TH, Jacoby E, Vasudevan SG. 2009. A small-molecule dengue virus entry inhibitor. Antimicrob Agents Chemother 53:1823-1831. http://dx.doi.org/10.1128/AAC.01148-08.
34. Zhao Y, Moreland NJ, Tay MY, Lee CC, Swaminathan K, Vasudevan SG. 2014. Identification and molecular characterization of human antibody fragments specific for dengue NS5 protein. Virus Res 179:225-230. http://dx.doi.org/10.1016/j.virusres.2013.11.010.
35. Ghildyal R, Ho A, Wagstaff KM, Dias MM, Barton CL, Jans P, Bardin P, Jans DA. 2005. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 44:12887-12895. http://dx.doi.org/10.1021/bi050701e.
36. Roth DM, Moseley GW, Glover D, Pouton CW, Jans DA. 2007. A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 8:673-686. http://dx.doi.org/10.1111/j.1600-0854.2007.00564.x.
37. Dundr M, Misteli T, Olson MO. 2000. The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 150:433-446. http://dx.doi.org/10.1083/jcb.150.3.433.
38. Mekhail K, Gunaratnam L, Bonicalzi ME, Lee S. 2004. HIF activation by pH-dependent nucleolar sequestration of VHL. Nat Cell Biol 6:642-647. http://dx.doi.org/10.1038/ncb1144.
39. Oksayan S, Nikolic J, David CT, Blondel D, Jans DA, Moseley GW. 2014. Identification of a role for nucleolin in rabies virus infection. J Virol 89:1939-1943. http://dx.doi.org/10.1128/JVI.03320-14.
40. Kuusisto HV, Wagstaff KM, Alvisi G, Jans DA. 2008. The C-terminus of apoptin represents a unique tumor cell-enhanced nuclear targeting module. Int J Cancer 123:2965-2969. http://dx.doi.org/10.1002/ijc.23884.
41. Mekhail K, Khacho M, Carrigan A, Hache RR, Gunaratnam L, Lee S. 2005. Regulation of ubiquitin ligase dynamics by the nucleolus. J Cell Biol 170:733-744. http://dx.doi.org/10.1083/jcb.200506030.
42. Mekhail K, Rivero-Lopez L, Al-Masri A, Brandon C, Khacho M, Lee S. 2007. Identification of a common subnuclear localization signal. Mol Biol Cell 18:3966-3977. http://dx.doi.org/10.1091/mbc.E07-03-0295.
43. Ashour J, Laurent-Rolle M, Shi PY, Garcia-Sastre A. 2009. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol 83:5408-5418. http://dx.doi.org/10.1128/JVI.02188-08.
44. Pryor MJ, Carr JM, Hocking H, Davidson AD, Li P, Wright PJ. 2001. Replication of dengue virus type 2 in human monocyte-derived macrophages: comparisons of isolates and recombinant viruses with substitutions at amino acid 390 in the envelope glycoprotein. Am J Trop Med Hyg 65:427-434.
45. Zhao Y, Soh TS, Zheng J, Chan KW, Phoo WW, Lee CC, Tay MY, Swaminathan K, Cornvik TC, Lim SP, Shi PY, Lescar J, Vasudevan SG, Luo D. 2015. A crystal structure of the dengue virus NS5 protein reveals a novel inter-domain interface essential for protein flexibility and virus replication. PLoS Pathog 11:e1004682. http://dx.doi.org/10.1371/journal.ppat.1004682.
46. Lutz P, Puvion-Dutilleul F, Lutz Y, Kedinger C. 1996. Nucleoplasmic and nucleolar distribution of the adenovirus IVa2 gene product. J Virol 70:3449-3460.
47. Dundr M, Leno GH, Hammarskjöld ML, Rekosh D, Helga-Maria C, Olson MO. 1995. The roles of nucleolar structure and function in the subcellular location of the HIV-1 Rev protein. J Cell Sci 108(Pt 8):2811-2823.
48. Siomi H, Shida H, Maki M, Hatanaka M. 1990. Effects of a highly basic region of human immunodeficiency virus Tat protein on nucleolar localization. J Virol 64:1803-1807.
49. Falcon V, Acosta-Rivero N, Chinea G, de la Rosa MC, Menendez I, Duenas-Carrera S, Gra B, Rodriguez A, Tsutsumi V, Shibayama M, Luna-Munoz J, Miranda-Sanchez MM, Morales-Grillo J, Kouri J. 2003. Nuclear localization of nucleocapsid-like particles and HCV core protein in hepatocytes of a chronically HCV-infected patient. Biochem Biophys Res Commun 310:54-58. http://dx.doi.org/10.1016/j.bbrc.2003.08.118.
50. James A, Wang Y, Raje H, Rosby R, DiMario P. 2014. Nucleolar stress with and without p53. Nucleus 5:402-426. http://dx.doi.org/10.4161/nucl.32235.
51. Jacob MD, Audas TE, Uniacke J, Trinkle-Mulcahy L, Lee S. 2013. Environmental cues induce a long noncoding RNA-dependent remodeling of the nucleolus. Mol Biol Cell 24:2943-2953. http://dx.doi.org/10.1091/mbc.E13-04-0223.
52. Malavige GN, Fernando S, Fernando DJ, Seneviratne SL. 2004. Dengue viral infections. Postgrad Med J 80:588-601. http://dx.doi.org/10.1136/pgmj.2004.019638.
53. Buckley A, Gaidamovich S, Turchinskaya A, Gould EA. 1992. Monoclonal antibodies identify the NS5 yellow fever virus nonstructural protein in the nuclei of infected cells. J Gen Virol 73(Pt 5):1125-1130. http://dx.doi.org/10.1099/0022-1317-73-5-1125.