Nuclear trafficking of proteins from RNA viruses: Potential target for antivirals?

Antiviral Research

Volumn 95, Issue 3, 2012, Pages 202-206

  Caly, Leon ^a   Wagstaff, Kylie M ^a   Jans, David A ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Dengue virus NS5; HIV integrase; Influenza A NP; Ivermectin; Nuclear transport; Respiratory syncytial virus matrix; Rift valley fever virus NSs; Venezuelan equine encephalitis virus

Indexed keywords

INTEGRASE; NUCLEOPROTEIN; RIBONUCLEOPROTEIN; RNA POLYMERASE; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; CELL MIGRATION; CELL NUCLEUS MEMBRANE; DENGUE VIRUS; EUKARYOTIC CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS; MOLECULARLY TARGETED THERAPY; NOTE; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA VIRUS; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIVIRAL AGENTS; HUMANS; RNA VIRUS INFECTIONS; RNA VIRUSES; VIRAL PROTEINS;

DENGUE VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RESPIRATORY SYNCYTIAL VIRUS; RIFT VALLEY FEVER VIRUS; RNA VIRUSES; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

EID: 84864029737     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.06.008     Document Type: Note

References (47)

1. Alvisi G., Musiani D., Jans D.A., Ripalti A. An importin alpha/beta-recognized bipartite nuclear localization signal mediates targeting of the human herpes simplex virus type 1 DNA polymerase catalytic subunit pUL30 to the nucleus. Biochemistry 2007, 46:9155-9163.
2. Ao Z., Danappa Jayappa K., Wang B., Zheng Y., Kung S., Rassart E., Depping R., Kohler M., Cohen E.A., Yao X. Importin alpha3 interacts with HIV-1 integrase and contributes to HIV-1 nuclear import and replication. J. Virol. 2010, 84:8650-8663.
3. Ao Z., Huang G., Yao H., Xu Z., Labine M., Cochrane A.W., Yao X. Interaction of human immunodeficiency virus type 1 integrase with cellular nuclear import receptor importin 7 and its impact on viral replication. J. Biol. Chem. 2007, 282:13456-13467.
4. Atasheva S., Fish A., Fornerod M., Frolova E.I. Venezuelan equine Encephalitis virus capsid protein forms a tetrameric complex with CRM1 and importin alpha/beta that obstructs nuclear pore complex function. J. Virol. 2010, 84:4158-4171.
5. Bartenschlager R., Miller S. Molecular aspects of dengue virus replication. Future Microbiol. 2008, 3:155-165.
6. Bird B.H., Albarino C.G., Hartman A.L., Erickson B.R., Ksiazek T.G., Nichol S.T. Rift valley fever virus lacking the NSs and NSm genes is highly attenuated, confers protective immunity from virulent virus challenge, and allows for differential identification of infected and vaccinated animals. J. Virol. 2008, 82:2681-2691.
7. Boivin S., Hart D.J. Interaction of the influenza A virus polymerase PB2 C-terminal region with importin alpha isoforms provides insights into host adaptation and polymerase assembly. J. Biol. Chem. 2011, 286:10439-10448.
8. Bukrinsky M.I., Haggerty S., Dempsey M.P., Sharova N., Adzhubel A., Spitz L., Lewis P., Goldfarb D., Emerman M., Stevenson M. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 1993, 365:666-669.
9. Cros J.F., Garcia-Sastre A., Palese P. An unconventional NLS is critical for the nuclear import of the influenza A virus nucleoprotein and ribonucleoprotein. Traffic 2005, 6:205-213.
10. Davidson A.D. Chapter 2 new insights into flavivirus nonstructural protein 5 2009, 74:41-101.
11. Den Boon J.A., Diaz A., Ahlquist P. Cytoplasmic viral replication complexes. Cell Host Microbe 2010, 8:77-85.
12. Deng T., Engelhardt O.G., Thomas B., Akoulitchev A.V., Brownlee G.G., Fodor E. Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J. Virol. 2006, 80:11911-11919.
13. Fouchier R.A., Meyer B.E., Simon J.H., Fischer U., Malim M.H. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for gag processing but not for post-entry nuclear import. EMBO J. 1997, 16:4531-4539.
14. Frolov I., Akhrymuk M., Akhrymuk I., Atasheva S., Frolova E.I. Early events in alphavirus replication determine the outcome of the infection. J. Virol. 2012.
15. Fulcher A.J., Jans D.A. Regulation of nucleocytoplasmic trafficking of viral proteins: An integral role in pathogenesis?. Biochim. Biophys. Acta 2011, 1813:2176-2190.
16. Ghildyal R., Baulch-Brown C., Mills J., Meanger J. The matrix protein of human respiratory syncytial virus localises to the nucleus of infected cells and inhibits transcription. Arch. Virol. 2003, 148:1419-1429.
17. Ghildyal R., Ho A., Dias M., Soegiyono L., Bardin P.G., Tran K.C., Teng M.N., Jans D.A. The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J. Virol. 2009, 83:5353-5362.
18. Ghildyal R., Ho A., Jans D.A. Central role of the respiratory syncytial virus matrix protein in infection. FEMS Microbiol. Rev. 2006, 30:692-705.
19. Ghildyal R., Ho A., Wagstaff K.M., Dias M.M., Barton C.L., Jans P., Bardin P., Jans D.A. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 2005, 44:12887-12895.
20. Ghildyal R., Li D., Peroulis I., Shields B., Bardin P.G., Teng M.N., Collins P.L., Meanger J., Mills J. Interaction between the respiratory syncytial virus G glycoprotein cytoplasmic domain and the matrix protein. J. Gen. Virol. 2005, 86:1879-1884.
21. Ghildyal R., Mills J., Murray M., Vardaxis N., Meanger J. Respiratory syncytial virus matrix protein associates with nucleocapsids in infected cells. J. Gen. Virol. 2002, 83:753-757.
22. Hearps A.C., Jans D.A. HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem. J. 2006, 398:475-484.
23. Heinzinger N.K., Bukinsky M.I., Haggerty S.A., Ragland A.M., Kewalramani V., Lee M.A., Gendelman H.E., Ratner L., Stevenson M., Emerman M. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc. Nat. Acad. Sci. USA 1994, 91:7311-7315.
24. Hutchinson E.C., Orr O.E., Man Liu S., Engelhardt O.G., Fodor E. Characterization of the interaction between the influenza A virus polymerase subunit PB1 and the host nuclear import factor Ran-binding protein 5. J. Gen. Virol. 2011, 92:1859-1869.
25. Kalveram B., Lihoradova O., Ikegami T. NSs protein of rift valley fever virus promotes posttranslational downregulation of the TFIIH subunit p62. J. Virol. 2011, 85:6234-6243.
26. Koonin E.V. Computer-assisted identification of a putative methyltransferase domain in NS5 protein of flaviviruses and lambda 2 protein of reovirus. J. Gen. Virol. 1993, 74(Pt 4):733-740.
27. Kootstra N.A., Schuitemaker H. Phenotype of HIV-1 lacking a functional nuclear localization signal in matrix protein of gag and Vpr is comparable to wild-type HIV-1 in primary macrophages. Virology 1999, 253:170-180.
28. Kudo R., Khochbin S., Hishi K., Kitano K., Yanagida M., Yoshida M., Horinouchi S. Molecular cloning and cell cycle-dependent expression of mammalian CRM1, a protein involved in nuclear export of proteins. J Biol Chem. 1997, 272:29742-29751.
29. Kuritzkes D.R. Drug resistance in HIV-1. Curr. Opin. Virol. 2011, 1:582-589.
30. Le May N., Dubaele S., Proietti De Santis L., Billecocq A., Bouloy M., Egly J.M. TFIIH transcription factor, a target for the Rift valley hemorrhagic fever virus. Cell 2004, 116:541-550.
31. Le May N., Mansuroglu Z., Leger P., Josse T., Blot G., Billecocq A., Flick R., Jacob Y., Bonnefoy E., Bouloy M. A SAP30 complex inhibits IFN-beta expression in Rift Valley fever virus infected cells. PLoS Pathog. 2008, 4:e13.
32. Levin A., Armon-Omer A., Rosenbluh J., Melamed-Book N., Graessmann A., Waigmann E., Loyter A. Inhibition of HIV-1 integrase nuclear import and replication by a peptide bearing integrase putative nuclear localization signal. Retrovirology 2009, 6:112.
33. Levin A., Hayouka Z., Friedler A., Loyter A. Transportin 3 and importin alpha are required for effective nuclear import of HIV-1 integrase in virus-infected cells. Nucleus 2010, 1:422-431.
34. Loregian A., Marsden H.S., Palu G. Protein-protein interactions as targets for antiviral chemotherapy. Rev. Med. Virol. 2002, 12:239-262.
35. Lu R., Limon A., Devroe E., Silver P.A., Cherepanov P., Engelman A. Class II integrase mutants with changes in putative nuclear localization signals are primarily blocked at a postnuclear entry step of human immunodeficiency virus type 1 replication. J. Virol. 2004, 78:12735-12746.
36. Newlands E.S., Rustin G.J., Brampton M.H. Phase I trial of elactocin. Br. J. Cancer 1996, 74:648-649.
37. Petit C., Schwartz O., Mammano F. The karyophilic properties of human immunodeficiency virus type 1 integrase are not required for nuclear import of proviral DNA. J. Virol. 2000, 74:7119-7126.
38. Piller S.C., Caly L., Jans D.A. Nuclear import of the pre-integration complex (PIC): the Achilles heel of HIV?. Curr. Drug Targets 2003, 4:409-429.
39. Pryor M.J., Rawlinson S.M., Butcher R.E., Barton C.L., Waterhouse T.A., Vasudevan S.G., Bardin P.G., Wright P.J., Jans D.A., Davidson A.D. Nuclear localization of dengue virus nonstructural protein 5 through its importin alpha/beta-recognized nuclear localization sequences is integral to viral infection. Traffic 2007, 8:795-807.
40. Rawlinson S.M., Pryor M.J., Wright P.J., Jans D.A. Dengue virus RNA polymerase NS5: a potential therapeutic target?. Curr. Drug Targets 2006, 7:1623-1638.
41. Rawlinson S.M., Pryor M.J., Wright P.J., Jans D.A. CRM1-mediated nuclear export of dengue virus RNA polymerase NS5 modulates interleukin-8 induction and virus production. J. Biol. Chem. 2009, 284:15589-15597.
42. Reil H., Bukovsky A.A., Gelderblom H.R., Gottlinger H.G. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 1998, 17:2699-2708.
43. Struthers J.K., Swanepoel R., Shepherd S.P. Protein synthesis in Rift valley fever virus-infected cells. Virology 1984, 134:118-124.
44. Wagstaff K.M., Rawlinson S.M., Hearps A.C., Jans D.A. An alphascreen(R)-based assay for high-throughput screening for specific inhibitors of nuclear import. J. Biomol. Screen. 2011, 16:192-200.
45. Wagstaff K.M., Sivakumaran H., Heaton S.M., Harrich D., Jans D.A. Ivermectin is a specific inhibitor of importin alpha/beta-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus. Biochem. J. 2012.
46. Wu W.W., Sun Y.H., Pante N. Nuclear import of influenza A viral ribonucleoprotein complexes is mediated by two nuclear localization sequences on viral nucleoprotein. Virol J. 2007, 4:49.
47. Zhong C., Li C., Wang X., Toyoda T., Gao G., Fan Z. Granzyme K inhibits replication of influenza virus through cleaving the nuclear transport complex importin alpha1/beta dimer of infected host cells. Cell Death Differ. 2012, 19:882-890.