Characterization of the human herpesvirus 6 U69 gene product and identification of its nuclear localization signal

Journal of Virology

Volumn 82, Issue 2, 2008, Pages 710-718

  Isegawa, Yuji ^a   Miyamoto, Yoichi ^b   Yasuda, Yoshinari ^b   Semi, Katsunori ^a,d   Tsujimura, Kenji ^a,d   Fukunaga, Rikiro ^b   Ohshima, Atsushi ^d   Horiguchi, Yasuhiro ^c   Yoneda, Yoshihiro ^b   Sugimoto, Nakaba ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; PROTEIN KINASE; PROTEIN KINASE U69; RAN PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; MICROINJECTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS CELL INTERACTION;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE; CELL NUCLEUS; CELLS, CULTURED; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; HERPESVIRUS 6, HUMAN; HUMANS; MICROSCOPY, FLUORESCENCE; NUCLEAR LOCALIZATION SIGNALS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 6; TRITICUM AESTIVUM;

EID: 37849018208     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00736-07     Document Type: Article

References (55)

1. L13 viral genes. J. Virol. 74:8-15.
2. Ansari, A., and V. C. Emery. 1999. The U69 gene of human herpesvirus 6 encodes a protein kinase which can confer ganciclovir sensitivity to baculoviruses. J. Virol. 73:3284-3291.
3. Aratani, S., T. Oishi, H. Fujita, M. Nakazawa, R. Fujii, N. Imamoto, Y. Yoneda, A. Fukamizu, and T. Nakajima. 2006. The nuclear import of RNA helicase A is mediated by importin-α3. Biochem. Biophys. Res. Commun. 340:125-133.
4. Conti, E. 2002. Structures of importins. Results Probl. Cell Differ. 35:93-113.
5. L13 virion protein of herpes simplex virus type 1 is phosphorylated by a novel virus-induced protein kinase. J. Gen. Virol. 73:303-311.
6. Dang, C. V., and W. M. Lee. 1989. Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J. Biol. Chem. 264:18019-18023.
7. de Bolle, L., D. Michel, T. Mertens, C. Manichanh, H. Agut, E. de Clercq, and L. Naesens. 2002. Role of the human herpesvirus 6 U69-encodes kinase in the phosphorylation of ganciclovir. Mol. Pharmacol. 62:714-721.
8. de Bolle, L., L. Naesens, and E. de Clercq. 2005. Update on human herpesvirus 6 biology, clinical features, and therapy. Clin. Microbiol. Rev. 18:217-245.
9. Dingwall, C., and R. A. Laskey. 1991. Nuclear targeting sequences - a consensus? Trends Biochem. Sci. 16:478-481.
10. Dominguez, G., T. R. Dambaugh, F. R. Stamey, S. Dewhurst, N. Inoue, and P. E. Pellett. 1999. Human herpesvirus 6B genome sequence: coding content and comparison with human herpesvirus 6A. J. Virol. 73:8040-8052.
11. Erice, A. 1999. Resistance of human cytomegalovirus to antiviral drugs. Clin. Microbiol. Rev. 12:286-297.
12. Finlay, D. R., D. D. Newmeyer, T. M. Price, and D. J. Forbes. 1987. Inhibition of in vitro transport by a lectin that binds to nuclear pores. J. Cell Biol. 104:189-200.
13. Gompels, U. A., J. Nicholas, G. Lawrence, M. Jones, B. J. Thomson, M. E. Martin, S. Efstathiou, M. Craxton, and H. A. Macaulay. 1995. The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 209:29-51.
14. Hieda, M., T. Tachibana, M. Fukumoto, and Y. Yoneda. 2001. Nuclear import of the U1A splicesome protein is mediated by importin α/β and Ran in living mammalian cells. J. Biol. Chem. 276:16824-16832.
15. Imamoto, N., T. Shimamoto, T. Takao, T. Tachibana, S. Kose, M. Matsubae, T. Sekimoto, Y. Shimonishi, and Y. Yoneda. 1995. In vivo evidence for involvement of a 58 kDa component of nuclear pore-targeting complex in nuclear protein import. EMBO J. 14:3617-3626.
16. Isegawa, Y., T. Mukai, K., Nakano, M. Kagawa, J. Chen, Y. Mori, T. Sunagawa, K. Kawanishi, J. Sashihara, A. Hata, P. Zou, H. Kosuge, and K. Yamanishi. 1999. Comparison of the complete DNA sequences between human herpesvirus 6 variants A and B. J. Virol. 73:8053-8063.
17. Isegawa, Y., Z. Ping, K. Nakano, N. Sugimoto, and K. Yamanishi. 1998. Human herpesvirus 6 open reading frame U12 encodes a functional β-chemokine receptor. J. Virol. 72:6104-6112.
18. Isegawa, Y., M. Takemoto, K. Yamanishi, A. Ohshima, and N. Sugimoto. 2007. Real-time PCR determination of human herpesvirus 6 antiviral drug susceptibility. J. Virol. Methods 140:25-31.
19. Jans, D. A., and S. Hubner. 1996. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76:651-685.
20. Jiang, C.-J., N. Imamoto, R. Matsuki, Y. Yoneda, and N. Yamamoto. 1998. Functional characterization of a plant importin α homologue. Nuclear localization signal (NLS)-selective binding and mediation of nuclear import of NLS proteins in vitro. J. Biol. Chem. 273:24083-24087.
21. Kamata, M., Y. Nitahara-Kasahara, Y. Miyamoto, Y. Yoneda, and Y. Aida. 2005. Importin-α promotes passage through the nuclear pore complex of human immunodeficiency virus type 1 Vpr. J. Virol. 79:3557-3564.
22. Kawaguchi, Y., R. Bruni, and B. Roizman. 1997. Interaction of herpes simplex virus 1 α regulatory protein ICP0 with elongation factor 1δ: ICP0 affects translational machinery. J. Virol. 71:1019-1024.
23. Kawaguchi, Y., T. Matsumura, B. Roizman, and K. Hirai. 1999. Cellular elongation factor 1δ is modified in cells infected with representative alpha-, beta-, or gammaherpesviruses. J. Virol. 73:4456-4460.
24. L13 gene of herpes simplex virus 1. J. Virol. 72:1731-1736.
25. Kitamura, R., T. Sekimoto, S. Ito, S. Harada, H. Yamagata, H. Masai, Y. Yoneda, and K. Yanagi. 2006. Nuclear import of Epstein-Barr virus nuclear antigen 1 mediated by NPI-1 (importin α5) is up- and down-regulated by phosphorylation of the nuclear localization signal for which Lys379 and Arg380 are essential. J. Virol. 80:1979-1991.
26. Köhler, M., S. Ansieau, S. Prehn, A. Leutz, H. Haller, and E. Hartmann. 1997. Cloning of two novel human importin-α subunits and analysis of the expression pattern of the importin-α protein family. FEBS Lett. 417:104-108.
27. Krosky, P. M., M.-C. Baek, and D. M. Coen. 2003. The human cytomegalovirus UL97 protein kinase, an antiviral drug target, is required at the stage of nuclear egress. J. Virol. 77:905-914.
28. Lawrence, G. L., J. Nicholas, and B. G. Barrell. 1995. Human herpesvirus 6 (strain U1102) encodes homologues of the conserved herpesvirus glycoprotein gM and the alphaherpesvirus origin-binding protein. J. Gen. Virol. 76:147-152.
29. Manichanh, C., C. Olivier-Aubron, J. P. Lagarde, J. T. Aubin, P. Bossi, A. Gautheret-Dejean, J. M. Hurraux, and H. Agut. 2001. Selection of the same mutation in the U69 protein kinase gene of human herpesvirus 6 after prolonged exposure to ganciclovir in vitro and in vivo. J. Gen. Virol. 82: 2767-2776.
30. Mattaj, I. W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306.
31. Michel, D., I. Pavic, A. Zimmermann, E. Haupt, K. Wunderlich, M. Heuschmid, and T. Mertens. 1996. The UL97 gene product of human cytomegalovirus is an early-late protein with a nuclear localization but is not a nucleoside kinase. J. Virol. 70:6340-6346.
32. Miyamoto, Y., M. Hieda, M. T. Harreman, M. Fukumoto, T. Saiwaki, A. E. Hodel, A. H. Corbett, and Y. Yoneda. 2002. Importin α can migrate into the nucleus in an importin β- and Ran-independent manner. EMBO J. 21:5833-5842.
33. Moore, M. S., and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365:661-663.
34. Moss, P., and A. Rickinson. 2005. Cellular immunotherapy for viral infection after HSC transplantation. Nat. Rev. Immunol. 5:9-20.
35. L13 protein kinase of herpes simplex virus 1 complexes with glycoprotein E and mediates the phosphorylation of the viral Fc receptor: glycoprotein E and I. Virology 241:37-48.
36. L13 gene by the human cytomegalovirus UL97 gene. Virology 225:347-358.
37. L13 protein kinase and the infected cell type are determinants of posttranslational modification of ICP0. Virology 235:406-413.
38. Okuno, T., H. Sao, H. Asada, K. Shiraki, M. Takahashi, and K. Yamanishi. 1990. Analysis of a glycoprotein of human herpesvirus 6 (HHV-6) using monoclonal antibodies. Virology 176:625-628.
39. L13 encodes a phosphoprotein that is a component of the virion. Virology 190:184-192.
40. Palacios, I., K. Weis, C. Kiebe, I. W. Mattaj, and C. Dingwall. 1996. Ran/TC4 mutants identify a common requirement for snRNA and protein import into the nucleus. J. Cell Biol. 133:485-494.
41. Prichard, M. N., N. Gao, S. Jairath, G. Mulamba, P. Krosky, D. M. Coen, B. O. Parker, and G. S. Pari. 1999. A recombinant human cytomegalovirus with a large deletion in UL97 has a severe replication deficiency. J. Virol. 73:5663-5670.
42. L13 gene of herpes simplex virus 1 encodes the functions for posttranslational processing associated with phosphorylation of the regulatory protein α22. Proc. Natl. Acad. Sci. USA 89:7310-7314.
43. Robbins, J., S. M. Dilworth, R. A. Laskey, and C. Dingwall. 1991. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:615-623.
44. Roberts, B. 1989. Nuclear location signal-mediated protein transport. Biochim. Biophys. Acta 1008:263-280.
45. Salahuddin, S. Z., D. V. Ablashi, P. Markham, S. F. Josephs, S. Sturzegger, M. Kaplan, G. Halligan, P. Biberfeld, F. Wong-Staal, B. Kramarsky, and R. C. Gallo. 1986. Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science 234:596-601.
46. Santoro, F., P. E. Kennedy, G. Locatelli, M. S. Malnati, E. A. Berger, and P. Lusso. 1999. CD46 is a cellular receptor for human herpesvirus 6. Cell 99:817-827.
47. Shapiro, D. J., P. A. Sharp, W. W. Wahl, and M. J. Keller. 1988. A high-efficiency HeLa cell nuclear transcription extract. DNA 7:47-55.
48. Smith, I. L., J. M. Cherrington, R. E. Jiles, M. D. Fuller, W. R. Freeman, and S. A. Spector. 1997. High-level resistance of cytomegalovirus to ganciclovir is associated with alterations in both the UL97 and DNA polymerase genes. J. Infect. Dis. 176:69-77.
49. Soldan, S. S., R. Berti, N. Salem, P. Secchiero, L. Flamand, P. A. Calabresi, M. B. Brennan, H. W. Moloni, H. F. McFarland, H. C. Lin, M. Patnaik, and S. Jacobson. 1997. Association of human herpes virus 6 (HHV-6) with multiple sclerosis: increased IgM response to HHV-6 early antigen and detection of serum HHV-6 DNA. Nat. Med. 3:1394-1397.
50. Takahashi, K., S. Sonoda, K. Higashi, T. Kondo, H. Takahashi, M. Takahashi, and K. Yamanishi. 1989. Predominant CD4 T-lymphocyte tropism of human herpesvirus 6-related virus. J. Virol. 63:3161-3163.
51. Takemoto, M., T. Shimamoto, Y. Isegawa, and K. Yamanishi. 2001. The R3 region, one of three major repetitive regions of human herpesvirus 6, is a strong enhancer of immediate-early gene U95. J. Virol. 75:10149-10160.
52. Watanabe-Fukunaga, R., S. Iida, Y. Shimizu, S. Nagata, and R. Fukunaga. 2005. SEI family of nuclear factors regulates p53-dependent transcriptional activation. Genes Cells 10:851-860.
53. Yamanishi, K., T. Okuno, K. Shiraki, M. Takahashi, T. Kondo, Y. Asano, and T. Kurata. 1988. Identification of human herpesvirus-6 as a causal agent for exanthema subitum. Lancet i:1056-1067.
54. Yasuhara, N., N. Shibazaki, S. Tanaka, M. Nagai, Y. Kamikawa, S. Oe, Y. Kamachi, H. Kondoh, and Y. Yoneda. 2007. Triggering neural differentiation of ES cells by subtype switching of importin-α. Nat. Cell Biol. 9:72-79.
55. Yoneda, Y., N. Imamoto-Sonobe, M. Yamaizumi, and T. Uchida. 1987. Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into culture cells. Exp. Cell Res. 173:586-595.