Human papillomavirus E1 helicase interacts with the WD repeat protein p80 to promote maintenance of the viral genome in keratinocytes

Journal of Virology

Volumn 82, Issue 3, 2008, Pages 1271-1283

  Côté Martin, Alexandra ^a,b   Moody, Cary ^c   Fradet Turcotte, Amélie ^a,b   D'Abramo, Claudia M ^a   Lehoux, Michaël ^a,b   Joubert, Simon ^a   Poirier, Guy G ^d   Coulombe, Benoit ^a,b   Laimins, Laimonis A ^c   Archambault, Jacques ^a,b  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E1; HOST FACTOR 1; PROTEIN P80; UNCLASSIFIED DRUG; WD REPEAT PROTEIN P80;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CONTROLLED STUDY; CYTOPLASM; EPISOME; GENETIC CODE; HUMAN; HUMAN CELL; KERATINOCYTE; LIFE CYCLE; MASS SPECTROMETRY; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TARGETING; TANDEM REPEAT; VIRUS GENOME; VIRUS REPLICATION; WART VIRUS;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CELL NUCLEUS; CHROMATOGRAPHY, AFFINITY; DNA HELICASES; DNA, VIRAL; DNA-BINDING PROTEINS; HAPLORHINI; HUMANS; KERATINOCYTES; MASS SPECTROMETRY; MUTAGENESIS, SITE-DIRECTED; PAPILLOMAVIRIDAE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEINS; VIRAL PROTEINS;

ANIMALIA; HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 38349090826     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01405-07     Document Type: Article

References (56)

1. Amin, A. A., S. Titolo, A. Pelletier, D. Fink, M. G. Cordingley, and J. Archambault. 2000. Identification of domains of the HPV11 E1 protein required for DNA replication in vitro. Virology 272:137-150.
2. Bairoch, A., R. Apweiler, C. H. Wu, W. C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M. J. Martin, D. A. Natale, C. O'Donovan, N. Redaschi, and L. S. Yeh. 2005. The Universal Protein Resource (UniProt). Nucleic Acids Res. 33:D154-D159.
3. Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99:7877-7882.
4. Chiang, C. M., M. Ustav, A. Stenlund, T. F. Ho, T. R. Broker, and L. T. Chow. 1992. Viral E1 and E2 proteins support replication of homologous and heterologous papillomaviral origins. Proc. Natl. Acad. Sci. USA 89:5799-5803.
5. Clower, R. V., J. C. Fisk, and T. Melendy. 2006. Papillomavirus E1 protein binds to and stimulates human topoisomerase I. J. Virol. 80:1584-1587.
6. Conger, K. L., J. S. Liu, S. R. Kuo, L. T. Chow, and T. S. Wang. 1999. Human papillomavirus DNA replication. Interactions between the viral E1 protein and two subunits of human DNA polymerase alpha/primase. J. Biol. Chem. 274:2696-2705.
7. 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.
8. Deng, W., G. Jin, B. Y. Lin, B. A. Van Tine, T. R. Broker, and L. T. Chow. 2003. mRNA splicing regulates human papillomavirus type 11 E1 protein production and DNA replication. J. Virol. 77:10213-10226.
9. Deng, W., B. Y. Lin, G. Jin, C. G. Wheeler, T. Ma, J. W. Harper, T. R. Broker, and L. T. Chow. 2004. Cyclin/CDK regulates the nucleocytoplasmic localization of the human papillomavirus E1 DNA helicase. J. Virol. 78:13954-13965.
10. Fehrmann, F., D. J. Klumpp, and L. A. Laimins. 2003. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J. Virol. 77:2819-2831.
11. Ferran, M. C., and A. A. McBride. 1998. Transient viral DNA replication and repression of viral transcription are supported by the C-terminal domain of the bovine papillomavirus type 1 E1 protein. J. Virol. 72:796-801.
12. Fradet-Turcotte, A., C. Vincent, S. Joubert, P. A. Bullock, and J. Archambault. 2007. Quantitative analysis of the binding of simian virus 40 large T antigen to DNA. J. Virol. 81:9162-9174.
13. Goldsborough, M. D., D. DiSilvestre, G. F. Temple, and A. T. Lorincz. 1989. Nucleotide sequence of human papillomavirus type 31: a cervical neoplasia-associated virus. Virology 171:306-311.
14. Han, Y., Y. M. Loo, K. T. Militello, and T. Melendy. 1999. Interactions of the papovavirus DNA replication initiator proteins, bovine papillomavirus type 1 E1 and simian virus 40 large T antigen, with human replication protein A. J. Virol. 73:4899-4907.
15. Hebner, C. M., and L. A. Laimins. 2006. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev. Med. Virol. 16:83-97.
16. Hsu, C. Y., F. Mechali, and C. Bonne-Andrea. 2007. Nucleocytoplasmic shuttling of bovine papillomavirus E1 helicase downregulates viral DNA replication in S phase. J. Virol. 81:384-394.
17. Hu, Y., R. V. Clower, and T. Melendy. 2006. Cellular topoisomerase I modulates origin binding by bovine papillomavirus type 1 E1. J. Virol. 80:4363-4371.
18. Hubert, W. G., T. Kanaya, and L. A. Laimins. 1999. DNA replication of human papillomavirus type 31 is modulated by elements of the upstream regulatory region that lie 5′ of the minimal origin. J. Virol. 73:1835-1845.
19. Jeronimo, C., M. F. Langelier, M. Zeghouf, M. Cojocaru, D. Bergeron, D. Baali, D. Forget, S. Mnaimneh, A. P. Davierwala, J. Pootoolal, M. Chandy, V. Canadien, B. K. Beattie, D. P. Richards, J. L. Workman, T. R. Hughes, J. Greenblatt, and B. Coulombe. 2004. RPAP1, a novel human RNA polymerase II-associated protein affinity purified with recombinant wild-type and mutated polymerase subunits. Mol. Cell. Biol. 24:7043-7058.
20. Klumpp, D. J., and L. A. Laimins. 1999. Differentiation-induced changes in promoter usage for transcripts encoding the human papillomavirus type 31 replication protein E1. Virology 257:239-246.
21. Koonin, E. V. 1993. A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication. Nucleic Acids Res. 21:2541-2547.
22. Kuo, S. R., J. S. Liu, T. R. Broker, and L. T. Chow. 1994. Cell-free replication of the human papillomavirus DNA with homologous viral E1 and E2 proteins and human cell extracts. J. Biol. Chem. 269:24058-24065.
23. Lee, D., H. Sohn, G. V. Kalpana, and J. Choe. 1999. Interaction of E1 and hSNF5 proteins stimulates replication of human papillomavirus DNA. Nature 399:487-491.
24. Lentz, M. R., D. Pak, I. Mohr, and M. R. Botchan. 1993. The E1 replication protein of bovine papillomavirus type 1 contains an extended nuclear localization signal that includes a p34cdc2 phosphorylation site. J. Virol. 67:1414-1423.
25. 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.
26. Li, D., and R. Roberts. 2001. WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell. Mol. Life Sci. 58:2085-2097.
27. Lin, B. Y., T. Ma, J. S. Liu, S. R. Kuo, G. Jin, T. R. Broker, J. W. Harper, and L. T. Chow. 2000. HeLa cells are phenotypically limiting in cyclin E/CDK2 for efficient human papillomavirus DNA replication. J. Biol. Chem. 275:6167-6174.
28. Lin, B. Y., A. M. Makhov, J. D. Griffith, T. R. Broker, and L. T. Chow. 2002. Chaperone proteins abrogate inhibition of the human papillomavirus (HPV) E1 replicative helicase by the HPV E2 protein. Mol. Cell. Biol. 22:6592-6604.
29. Liu, J. S., S. R. Kuo, A. M. Makhov, D. M. Cyr, J. D. Griffith, T. R. Broker, and L. T. Chow. 1998. Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J. Biol. Chem. 273:30704-30712.
30. Loo, Y. M., and T. Melendy. 2004. Recruitment of replication protein A by the papillomavirus E1 protein and modulation by single-stranded DNA. J. Virol. 78:1605-1615.
31. Ma, T., N. Zou, B. Y. Lin, L. T. Chow, and J. W. Harper. 1999. Interaction between cyclin-dependent kinases and human papillomavirus replication-initiation protein E1 is required for efficient viral replication. Proc. Natl. Acad. Sci. USA 96:382-387.
32. Masterson, P. J., M. A. Stanley, A. P. Lewis, and M. A. Romanos. 1998. A C-terminal helicase domain of the human papillomavirus E1 protein binds E2 and the DNA polymerase α-primase p68 subunit. J. Virol. 72:7407-7419.
33. Moody, C. A., A. Fradet-Turcotte, J. Archambault, and L. A. Laimins. Human papillomaviruses activate caspases upon differentiation to promote viral genome amplification. Proc. Natl. Acad. Sci. USA, in press.
34. Ozbun, M. A., and C. Meyers. 1998. Temporal usage of multiple promoters during the life cycle of human papillomavirus type 31b. J. Virol. 72:2715-2722.
35. Park, J., N. H. Cho, J. K. Choi, P. Feng, J. Choe, and J. U. Jung. 2003. Distinct roles of cellular Lck and p80 proteins in herpesvirus saimiri Tip function on lipid rafts. J. Virol. 77:9041-9051.
36. Park, J., B. S. Lee, J. K. Choi, R. E. Means, J. Choe, and J. U. Jung. 2002. Herpesviral protein targets a cellular WD repeat endosomal protein to downregulate T lymphocyte receptor expression. Immunity 17:221-233.
37. Peh, W. L., K. Middleton, N. Christensen, P. Nicholls, K. Egawa, K. Sotlar, J. Brandsma, A. Percival, J. Lewis, W. J. Liu, and J. Doorbar. 2002. Life cycle heterogeneity in animal models of human papillomavirus-associated disease. J. Virol. 76:10401-10416.
38. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Seraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
39. Rocque, W. J., D. J. Porter, J. A. Barnes, E. P. Dixon, D. C. Lobe, J. L. Su, D. H. Willard, R. Gaillard, J. P. Condreay, W. C. Clay, C. R. Hoffman, L. K. Overton, G. Pahel, T. A. Kost, and W. C. Phelps. 2000. Replication-associated activities of purified human papillomavirus type 11 E1 helicase. Protein Expr. Purif. 18:148-159.
40. Rost, B., P. Fariselli, and R. Casadio. 1996. Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 5:1704-1718.
41. Rost, B., and C. Sander. 1993. Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232:584-599.
42. Sénéchal, H., G. G. Poirier, B. Coulombe, L. A. Laimins, and J. Archambault. 2007. Amino acid substitutions that specifically impair the transcriptional activity of papillomavirus E2 affect binding to the long isoform of Brd4. Virology 358:10-17.
43. Smith, T. F., C. Gaitatzes, K. Saxena, and E. J. Neer. 1999. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:181-185.
44. Stenlund, A. 2003. E1 initiator DNA binding specificity is unmasked by selective inhibition of non-specific DNA binding. EMBO J. 22:954-963.
45. Stenlund, A. 2003. Initiation of DNA replication: lessons from viral initiator proteins. Nat. Rev. Mol. Cell Biol. 4:777-785.
46. Sun, Y., H. Han, and D. J. McCance. 1998. Active domains of human papillomavirus type 11 E1 protein for origin replication. J. Gen. Virol. 79:1651-1658.
47. Swindle, C. S., and J. A. Engler. 1998. Association of the human papillomavirus type 11 E1 protein with histone H1. J. Virol. 72:1994-2001.
48. Thomas, J. T., W. G. Hubert, M. N. Ruesch, and L. A. Laimins. 1999. Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes. Proc. Natl. Acad. Sci. USA 96:8449-8454.
49. Titolo, S., K. Brault, J. Majewski, P. W. White, and J. Archambault. 2003. Characterization of the minimal DNA binding domain of the human papillomavirus E1 helicase: fluorescence anisotropy studies and characterization of a dimerization-defective mutant protein. J. Virol. 77:5178-5191.
50. Titolo, S., A. Pelletier, A. M. Pulichino, K. Brault, E. Wardrop, P. W. White, M. G. Cordingley, and J. Archambault. 2000. Identification of domains of the human papillomavirus type 11 E1 helicase involved in oligomerization and binding to the viral origin. J. Virol. 74:7349-7361.
51. 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.
52. Ustav, M., and A. Stenlund. 1991. Transient replication of BPV-1 requires two viral polypeptides encoded by the E1 and E2 open reading frames. EMBO J. 10:449-457.
53. White, P. W., A. Pelletier, K. Brault, S. Titolo, E. Welchner, L. Thauvette, M. Fazekas, M. G. Cordingley, and J. Archambault. 2001. Characterization of recombinant HPV6 and 11 E1 helicases: effect of ATP on the interaction of E1 with E2 and mapping of a minimal helicase domain. J. Biol. Chem. 276:22426-22438.
54. Yang, L., R. Li, I. J. Mohr, R. Clark, and M. R. Botchan. 1991. Activation of BPV-1 replication in vitro by the transcription factor E2. Nature 353:628-632.
55. Yasugi, T., M. Vidal, H. Sakai, P. M. Howley, and J. D. Benson. 1997. Two classes of human papillomavirus type 16 E1 mutants suggest pleiotropic conformational constraints affecting E1 multimerization, E2 interaction, and interaction with cellular proteins. J. Virol. 71:5942-5951.
56. Ziegler, K., T. Bui, R. J. Frisque, A. Grandinetti, and V. R. Nerurkar. 2004. A rapid in vitro polyomavirus DNA replication assay. J. Virol. Methods 122:123-127.