Nuclear import of bovine papillomavirus type 1 E1 protein is mediated by multiple alpha importins and is negatively regulated by phosphorylation near a nuclear localization signal

Journal of Virology

Volumn 81, Issue 6, 2007, Pages 2899-2908

  Bian, Xue Lin ^a   Rosas Acosta, Germán ^a   Wu, Yu Chieh ^a   Wilson, Van G ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; DIGITONIN; GLYCOPROTEIN E1; IMPORTIN ALPHA3; IMPORTIN ALPHA4; IMPORTIN ALPHA5; KARYOPHERIN ALPHA; MUTANT PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; KERATINOCYTE; MUTATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; VIRUS REPLICATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; ANIMALS; BOVINE PAPILLOMAVIRUS 1; CATTLE; CELL NUCLEUS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; TRANSFECTION; VIRAL PROTEINS;

BOVINE PAPILLOMAVIRUS TYPE 1; PAPILLOMAVIRIDAE;

EID: 33947355408     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01850-06     Document Type: Article

References (68)

1. Adam, S. A., R. S. Marr, and L. Gerace. 1990. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:807-816.
2. Alvisi, G., D. A. Jans, J. Guo, L. A. Pinna, and A. Ripalti. 2005. A protein kinase CK2 site flanking the nuclear targeting signal enhances nuclear transport of human cytomegalovirus ppUL44. Traffic 6:1002-1013.
3. Angeline, M., E. Merle, and J. Moroianu. 2003. The E7 oncoprotein of high-risk human papillomavirus type 16 enters the nucleus via a nonclassical Ran-dependent pathway. Virology 317:13-23.
4. Blachon, S., S. Bellanger, C. Demeret, and F. Thierry. 2005. Nucleo-cytoplasmic shuttling of high risk human papillomavirus E2 proteins induces apoptosis. J. Biol. Chem. 280:36088-36098.
5. Bodily, J. M., S. Alam, and C. Meyers. 2006. Regulation of human papillomavirus type 31 late promoter activation and genome amplification by protein kinase C. Virology 348:328-340.
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. Chook, Y. M., A. Jung, M. K. Rosen, and G. Blobel. 2002. Uncoupling Kapbeta2 substrate dissociation and ran binding. Biochemistry 41:6955-6966.
8. Cortes, P., Z. S. Ye, and D. Baltimore. 1994. RAG-1 interacts with the repeated amino acid motif of the human homologue of the yeast protein SRP1. Proc. Natl. Acad. Sci. USA 91:7633-7637.
9. Cueille, N., R. Nougarede, F. Mechali, M. Philippe, and C. Bonne-Andrea. 1998. Functional interaction between the bovine papillomavirus virus type 1 replicative helicase E1 and cyclin E-Cdk2. J. Virol. 72:7255-7262.
10. Cuomo, C. A., S. A. Kirch, J. Gyuris, R. Brent, and M. A. Oettinger. 1994. Rch1, a protein that specifically interacts with the RAG-1 recombination-activating protein. Proc. Natl. Acad. Sci. USA 91:6156-6160.
11. Darshan, M. S., J. Lucchi, E. Harding, and J. Moroianu. 2004. The L2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J. Virol. 78:12179-12188.
12. Denning, M. F. 2004. Epidermal keratinocytes: regulation of multiple cell phenotypes by multiple protein kinase C isoforms. Int. J. Biochem. Cell Biol. 36:1141-1146.
13. Doorbar, J. 2005. The papillomavirus life cycle. J. Clin. Virol. 32(Suppl. 1):S7-S15.
14. Flores, E. R., and P. F. Lambert. 1997. Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J. Virol. 71:7167-7179.
15. Gilbert, D. M., and S. N. Cohen. 1987. Bovine papilloma virus plasmids replicate randomly in mouse fibroblasts throughout S phase of the cell cycle. Cell 50:59-68.
16. Gorlich, D., and U. Kutay. 1999. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:607-660.
17. Harreman, M. T., T. M. Kline, H. G. Milford, M. B. Harben, A. E. Hodel, and A. H. Corbett. 2004. Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J. Biol. Chem. 279:20613-20621.
18. Henderson, B. R., and A. Eleftheriou. 2000. A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp. Cell Res. 256:213-224.
19. Hogarth, C. A., S. Calanni, D. A. Jans, and K. L. Loveland. 2006. Importin alpha mRNAs have distinct expression profiles during spermatogenesis. Dev. Dyn. 235:253-262.
20. Jans, D. A., and S. Hubner. 1996. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76:651-685.
21. Kamei, Y., S. Yuba, T. Nakayama, and Y. Yoneda. 1999. Three distinct classes of the alpha-subunit of the nuclear pore-targeting complex (importin-alpha) are differentially expressed in adult mouse tissues. J. Histochem. Cytochem. 47:363-372.
22. 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.
23. Kobe, B. 1999. Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat. Struct. Biol. 6:388-397.
24. Kohler, M., S. Ansieau, S. Prehn, A. Leutz, H. Haller, and E. Hartmann. 1997. Cloning of two novel human importin-alpha subunits and analysis of the expression pattern of the importin-alpha protein family. FEBS Lett. 417:104-108.
25. Kohler, M., A. Fiebeler, M. Hartwig, S. Thiel, S. Prehn, R. Kettritz, F. C. Luft, and E. Hartmann. 2002. Differential expression of classical nuclear transport factors during cellular proliferation and differentiation. Cell. Physiol. Biochem. 12:335-344.
26. Kohler, M., C. Speck, M. Christiansen, F. R. Bischoff, S. Prehn, H. Haller, D. Gorlich, and E. Hartmann. 1999. Evidence for distinct substrate specificities of importin alpha family members in nuclear protein import. Mol. Cell. Biol. 19:7782-7791.
27. Leng, X., J. H. Ludes-Meyers, and V. G. Wilson. 1997. Isolation of an amino-terminal region of bovine papillomavirus type 1 E1 protein that retains origin binding and E2 interaction capacity. J. Virol. 71:848-852.
28. Leng, X., and V. G. Wilson. 1994. Genetically defined nuclear localization signal sequence of bovine papillomavirus E1 protein is necessary and sufficient for the nuclear localization of E1-beta-galactosidase fusion proteins. J. Gen. Virol. 75:2463-2467.
29. Lentz, M., T. Zanardi, R. Filzen, J. Carter, and M. Hella. 2002. Functional analysis of a carboxyl-terminal phosphorylation mutant of the bovine papillomavirus E1 protein. J. Mol. Biol. 316:599-609.
30. cdc2 phosphorylation site. J. Virol. 67:1414-1423.
31. Lentz, M. R., S. M. Stevens, Jr., J. Raynes, and N. Elkhoury. 2006. A phosphorylation map of the bovine papillomavirus E1 helicase. Virol. J. 3:13.
32. Le Roux, L. G., and J. Moroianu. 2003. Nuclear entry of high-risk human papillomavirus type 16 E6 oncoprotein occurs via several pathways. J. Virol. 77:2330-2337.
33. Macara, I. G. 2001. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65:570-594.
34. Malcles, M. H., N. Cueille, F. Mechali, O. Coux, and C. Bonne-Andrea. 2002. Regulation of bovine papillomavirus replicative helicase E1 by the ubiquitin-proteasome pathway. J. Virol. 76:11350-11358.
35. McBride, K. M., G. Banninger, C. McDonald, and N. C. Reich. 2002. Regulated nuclear import of the STAT1 transcription factor by direct binding of importin-alpha. EMBO. J. 21:1754-1763.
36. McShan, G. D., and V. G. Wilson. 1997. Casein kinase II phosphorylates bovine papillomavirus type 1 E1 in vitro at a conserved motif. J. Gen. Virol. 78:171-177.
37. McShan, G. D., and V. G. Wilson. 2000. Contribution of bovine papillomavirus type 1 E1 protein residue 48 to replication function. J. Gen. Virol. 81:1995-2004.
38. Mechali, F., C. Y. Hsu, A. Castro, T. Lorca, and C. Bonne-Andrea. 2004. Bovine papillomavirus replicative helicase E1 is a target of the ubiquitin ligase APC. J. Virol. 78:2615-2619.
39. Merle, E., R. C. Rose, L. LeRoux, and J. Moroianu. 1999. Nuclear import of HPVIl L1 capsid protein is mediated by karyopherin alpha2betal heterodimers. J. Cell. Biochem. 74:628-637.
40. Nachury, M. V., U. W. Ryder, A. I. Lamond, and K. Weis. 1998. Cloning and characterization of hSRP1 gamma, a tissue-specific nuclear transport factor. Proc. Natl. Acad. Sci. USA 95:582-587.
41. Nelson, L. M., R. C. Rose, L. LeRoux, C. Lane, K. Bruya, and J. Moroianu. 2000. Nuclear import and DNA binding of human papillomavirus type 45 L1 capsid protein. J. Cell. Biochem. 79:225-238.
42. Nelson, L. M., R. C. Rose, and J. Moroianu. 2003. The L1 major capsid protein of human papillomavirus type 11 interacts with Kap beta2 and Kap beta3 nuclear import receptors. Virology 306:162-169.
43. Nelson, L. M., R. C. Rose, and J. Moroianu. 2002. Nuclear import strategies of high risk HPV16 L1 major capsid protein. J. Biol. Chem. 277:23958-23964.
44. Ozbun, M. A., and C. Meyers. 1998. Human papillomavirus type 31b E1 and E2 transcript expression correlates with vegetative viral genome amplification. Virology 248:218-230.
45. Plafker, K., and I. G. Macara. 2002. Fluorescence resonance energy transfer biosensors that detect Ran conformational changes and a Ran - GDP-importin-β-RanBP1 complex in vitro and in intact cells. J. Biol. Chem. 277:30121-30127.
46. Praskova, M., S. Kalenderova, L. Miteva, Y. Poumay, and V. Mitev. 2002. The ornithine decarboxylase inhibitor, difluoromethylornithine, inhibits casein kinase II activity, c-Myc expression and normal human keratinocyte proliferation. Arch. Dermatol. Res. 293:590-593.
47. Quensel, C., B. Friedrich, T. Sommer, E. Hartmann, and M. Kohler. 2004. In vivo analysis of importin alpha proteins reveals cellular proliferation inhibition and substrate specificity. Mol. Cell. Biol. 24:10246-10255.
48. Rangasamy, D., and V. G. Wilson. 2000. Bovine papillomavirus El protein is sumoylated by the host cell Ubc9 protein. J. Biol. Chem. 275:30487-30495.
49. Rangasamy, D., K. Woytek, S. A. Khan, and V. G. Wilson. 2000. SUMO-1 modification of bovine papillomavirus El protein is required for intranuclear accumulation. J. Biol. Chem. 275:37999-38004.
50. Ravnan, J. B., D. M. Gilbert, K. G. Ten Hagen, and S. N. Cohen. 1992. Random-choice replication of extrachromosomal bovine papillomavirus (BPV) molecules in heterogeneous, clonally derived BPV-infected cell lines. J. Virol. 66:6946-6952.
51. Rosas-Acosta, G., M. A. Langereis, A. Deyrieux, and V. G. Wilson. 2005. Proteins of the PIAS family enhance the sumoylation of the papillomavirus E1 protein. Virology 331:190-203.
52. Sachdev, S., S. Bagchi, D. D. Zhang, A. C. Mings, and M. Hannink. 2000. Nuclear import of IκBα ccomplished by a Ran-independent transport pathway. Mol. Cell. Biol. 20:1571-1582.
53. Seki, T., S. Tada, T. Katada, and T. Enomoto. 1997. Cloning of a cDNA encoding a novel importin-alpha homologue, Qip1: discrimination of Qipl and Rch1 from hSrp1 by their ability to interact with DNA helicase Q1/ RecQL. Biochem. Biophys. Res. Commun. 234:48-53.
54. Shin, I., J. Rotty, F. Y. Wu, and C. L. Arteaga. 2005. Phosphorylation of p27Kip1 at Thr-157 interferes with its association with importin alpha during G1 and prevents nuclear re-entry. J. Biol. Chem. 280:6055-6063.
55. Skiadopoulos, M. H., and A. A. McBride. 1996. The bovine papillomavirus type 1 E2 transactivator and repressor proteins use different nuclear localization signals. J. Virol. 70:1117-1124.
56. Sun, S., L. Thorner, M. Lentz, P. MacPherson, and M. Botchan. 1990. Identification of a 68-kilodalton nuclear ATP-binding phosphoprotein encoded by bovine papillomavirus type 1. J. Virol. 64:5093-6105.
57. Titolo, S., A. Pelletier, F. Sauve, K. Brault, E. Wardrop, P. W. White, A. Amin, M. G. Cordingley, and J. Archambault. 1999. Role of the ATP-binding domain of the human papillomavirus type 11 E1 helicase in E2-dependent binding to the origin. J. Virol. 73:5282-5293.
58. Tsuji, L., T. Takumi, N. Imamoto, and Y. Yoneda. 1997. Identification of novel homologues of mouse importin alpha, the alpha subunit of the nuclear pore-targeting complex, and their tissue-specific expression. FEBS Lett. 416: 30-34.
59. Weis, K., I. W. Mattaj, and A. I. Lamond. 1995. Identification of hSRP1 alpha as a functional receptor for nuclear localization sequences. Science 268:1049-1053.
60. Wilson, V. G., and G. Rosas-Acosta. 2003. Molecular targets for papillomavirus therapy. Curr. Drug Targets Infect. Disord. 3:221-239.
61. Wilson, V. G., M. West, K. Woytek, and D. Rangasamy. 2002. Papillomavirus E1 proteins: form, function, and features. Virus Genes 24:275-290.
62. Woytek, K. J., D. Rangasamy, C. Bazaldua-Hernandez, M. West, and V. G. Wilson. 2001. Effects of mutations within two hydrophilic regions of the bovine papillomavirus type 1 E1 DNA-binding domain on E1-E2 interaction. J. Gen. Virol. 82:2341-2351.
63. Yang, W., J. Gelles, and S. M. Musser. 2004. Imaging of single-molecule translocation through nuclear pore complexes. Proc. Natl. Acad. Sci. USA 101:12887-12892.
64. Zanardi, T. A., C. M. Stanley, B. M. Saville, S. M. Spacek, and M. R. Lentz. 1997. Modulation of bovine papillomavirus DNA replication by phosphorylation of the viral E1protein. Virology 228:1-10.
65. Zhang, F., R. L. White, and K. L. Neufeld. 2000. Phosphorylation near nuclear localization signal regulates nuclear import of adenomatous polyposis coli protein. Proc. Natl. Acad. Sci. USA 97:12577-12582.
66. Zhang, G. Q., and J. E. Samuel. 2003. Identification and cloning potentially protective antigens of Coxiella burnetii using sera from mice experimentally infected with Nine Mile phase I. Ann. N. Y. Acad. Sci. 990:510-520.
67. Zou, N., B. Y. Lin, F. Duan, K. Y. Lee, G. Jin, R. Guan, G. Yao, E. J. Lefkowitz, T. R. Broker, and L. T. Chow. 2000. The hinge of the human papillomavirus type 11 E2 protein contains major determinants for nuclear localization and nuclear matrix association. J. Virol. 74:3761-3770.
68. zur Hausen, H. 1996. Papillomavirus infections-a major cause of human cancers. Biochim. Biophys. Acta 1288:F55-F78.