Conditionally activated E7 proteins of high-risk and low-risk human papillomaviruses induce S phase in postmitotic, differentiated human keratinocytes

Journal of Virology

Volumn 80, Issue 13, 2006, Pages 6517-6524

  Banerjee, N Sanjib ^a   Genovese, Nicholas J ^a   Noya, Francisco ^a,b   Chien, Wei Ming ^a,c   Broker, Thomas R ^a   Chow, Louise T ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^c Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; ESTRADIOL; ESTROGEN RECEPTOR; PROTEIN E7;

ARTICLE; CELL CULTURE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL TRANSPORT; CONSENSUS SEQUENCE; CULTURE MEDIUM; CYTOPLASM; GENOTYPE; HUMAN; HUMAN CELL; KERATINOCYTE; LIGAND BINDING; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; WART VIRUS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL NUCLEUS; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOPLASM; EPITHELIUM; ESTRADIOL; GENOTYPE; HUMAN PAPILLOMAVIRUS 16; HUMANS; KERATINOCYTES; MALE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PROTEIN BINDING; RECEPTORS, ESTROGEN; RECOMBINANT FUSION PROTEINS; RISK FACTORS; S PHASE; TIME FACTORS; VIRUS REPLICATION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

EID: 33745270792     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02499-05     Document Type: Article

References (47)

1. Armstrong, D. J., and A. Roman. 1992. Mutagenesis of human papillomavirus types 6 and 16 E7 open reading frames alters the electrophoretic mobility of the expressed proteins. J. Gen. Virol. 73:1275-1279.
2. Banerjee, N. S., L. T. Chow, and T. R. Broker. 2005. Retrovirus mediated gene transfer to analyze HPV gene regulation and protein functions in "organotypic" raft culture, p. 187-202. In C. Davy and J. Doorbar (ed.), Human papillomaviruses: methods and protocols, methods in molecular medicine. Humana Press, Totowa, N.J.
3. Cheng, S., D.-C. Schmidt-Grimminger, T. Murant, T. R. Broker, and L. T. Chow. 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 9:2335-2349.
4. Chien, W.-M., F. Noya, H. M. Benedict-Hamilton, T. R. Broker, and L. T. Chow. 2002. Alternative fates of keratinocytes transduced by human papillomavirus type 18 E7 during squamous differentiation. J. Virol. 76:2964-2972.
5. Chien, W.-M., J. N. Parker, D.-C. Schmidt-Grimminger, T. R. Broker, and L. T. Chow. 2000. Casein kinase II phosphorylation of the human papillomavirus-18 E7 protein is critical for promoting S-phase entry. Cell Growth Differ. 11:425-435.
6. Chow, L. T., and T. R. Broker. Human papillomavirus RNA transcription. In D. DiMaio and R. Garcea (ed.), The papillomaviruses, in press. Plenum Publishers, New York, N.Y.
7. Chow, L. T., and T. R. Broker. 2006. Mechanisms and regulation of papillomavirus DNA replication, p. 53-71. In M. S. Campo (ed.), Papillomavirus research: from natural history to vaccines and beyond. Caister Academic Press, Norwich, United Kingdom.
8. Classon, M., and N. Dyson. 2001. p107 and p130: versatile proteins with interesting pockets. Exp. Cell Res. 264:135-147.
9. Dollard, S. C., J. L. Wilson, L. M. Demeter, W. Bonnez, R. C. Reichman, T. R. Broker, and L. T. Chow. 1992. Production of human papillomavirus and modulation of the infectious program in epithelial raft cultures. Genes Dev. 6:1131-1142.
10. Draganov, P., S. Todorov, I. Todorov, T. Karchev, and Z. Kalvatchev. 2006. Identification of HPV DNA in patients with juvenile-onset recurrent respiratory papillomatosis using SYBR Green real-time PCR. Int. J. Pediatr. Otorhinolaryngol. 70:469-473.
11. Flores, E. R., B. L. Allen-Hoffmann, D. Lee, and P. F. Lambert. 2000. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J. Virol. 74:6622-6631.
12. Frattini, M. G., H. B. Lim, J. Doorbar, and L. A. Laimins. 1997. Induction of human papillomavirus type 18 late gene expression and genomic amplification in organotypic cultures from transfected DNA templates. J. Virol. 71:7068-7072.
13. Frattini, M. G., H. B. Lim, and L. A. Laimins. 1996. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiation-dependent late expression. Proc. Natl. Acad. Sci. USA 93:3062-3067.
14. Funk, J. O., S. Waga, J. B. Harry, E. Espling, B. Stillman, and D. A. Galloway. 1997. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev. 11:2090-2100.
15. Halbert, C. L., G. W. Demers, and D. A. Galloway. 1992. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J. Virol. 66:2125-2134.
16. Heck, D. V., C. L. Yee, P. M. Howley, and K. Münger. 1992. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89:4442-4446.
17. Jian, Y., D.-C. Schmidt-Grimminger, W.-M. Chien, X. Wu, T. R. Broker, and L. T. Chow. 1998. Post-transcriptional induction of p21cip1 protein by human papillomavirus E7 inhibits unscheduled DNA synthesis reactivated in differentiated keratinocytes. Oncogene 17:2027-2038.
18. Jian, Y., B. A. Van Tine, W.-M. Chien, G. M. Shaw, T. R. Broker, and L. T. Chow. 1999. Concordant induction of cyclin E and p21cip1 in differentiated keratinocytes by the human papillomavirus E7 protein inhibits cellular and viral DNA synthesis. Cell Growth Differ. 10:101-111.
19. Jones, D. L., R. M. Alani, and K. Münger. 1997. The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21Cip1-mediated inhibition of cdk2. Genes Dev. 11:2101-2111.
20. Kumar, V., S. Green, A. Staub, and P. Chambon. 1986. Localisation of the oestradiol-binding and putative DNA-binding domains of the human oestrogen receptor. EMBO J. 5:2231-2236.
21. McLaughlin-Drubin, M. E., J. L. Bromberg-White, and C. Meyers. 2005. The role of the human papillomavirus type 18 E7 oncoprotein during the complete viral life cycle. Virology 338:61-68.
22. Meyers, C., M. G. Frattini, J. B. Hudson, and L. A. Laimins. 1992. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science 257:971-973.
23. Meyers, C., T. J. Mayer, and M. A. Ozbun. 1997. Synthesis of infectious human papillomavirus type 18 in differentiating epithelium transfected with viral DNA. J. Virol. 71:7381-7386.
24. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
25. Münger, K., A. Baldwin, K. M. Edwards, H. Hayakawa, C. L. Nguyen, M. Owens, M. Grace, and K. Huh. 2004. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78:11451-11460.
26. Münger, K., W. C. Phelps, V. Bubb, P. M. Howley, and R. Schlegel. 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:4417-4421.
27. Noya, F., W.-M. Chien, T. R. Broker, and L. T. Chow. 2001. p21cip1 degradation in differentiated keratinocytes is abrogated by costabilization with cyclin E induced by human papillomavirus E7. J. Virol. 75:6121-6134.
28. Ozbun, M. A., and C. Meyers. 1997. Characterization of late gene transcripts expressed during vegetative replication of human papillomavirus type 31b. J. Virol. 71:5161-5172.
29. Parker, J. N., W. Zhao, K. J. Askins, T. R. Broker, and L. T. Chow. 1997. Mutational analyses of differentiation-dependent human papillomavirus type 18 enhancer elements in epithelial raft cultures of neonatal foreskin keratinocytes. Cell Growth Differ. 8:751-762.
30. Rabah, R., W. D. Lancaster, R. Thomas, and L. Gregoire. 2001. Human papillomavirus-11-associated recurrent respiratory papillomatosis is more aggressive than human papillomavirus-6-associated disease. Pediatr. Dev. Pathol. 4:68-72.
31. Romanczuk, H., L. L. Villa, R. Schlegel, and P. M. Howley. 1991. The viral transcriptional regulatory region upstream of the E6 and E7 genes is a major determinant of the differential immortalization activities of human papillomavirus types 16 and 18. J. Virol. 65:2739-2744.
32. Sang, B. C., and M. S. Barbosa. 1992. Single amino acid substitutions in "low-risk" human papillomavirus (HPV) type 6 E7 protein enhance features characteristic of the "high-risk" HPV E7 oncoproteins. Proc. Natl. Acad. Sci. USA 89:8063-8067.
33. Schmidt-Grimminger, D.-C., X. Wu, Y. Jian, T. R. Broker, and L. T. Chow. 1998. Post-transcriptional induction of p21cip1 protein in condylomata and dysplasias is inversely related to human papillomavirus activities. Am. J. Pathol. 152:1015-1024.
34. 1-phase progression. Genes Dev. 13:1501-1512.
35. Smith-McCune, K., D. Kalman, C. Robbins, S. Shivakumar, L. Yuschenkoff, and J. M. Bishop. 1999. Intranuclear localization of human papillomavirus 16 E7 during transformation and preferential binding of E7 to the Rb family member p130. Proc. Natl. Acad. Sci. USA 96:6999-7004.
36. Stoler, M. H., S. M. Wolinsky, A. Whitbeck, T. R. Broker, and L. T. Chow. 1989. Differentiation-linked human papillomavirus types 6 and 11 transcription in genital condylomata revealed by in situ hybridization with message-specific RNA probes. Virology 172:331-340.
37. Thomas, J. T., S. T. Oh, S. S. Terhune, and L. A. Laimins. 2001. Cellular changes induced by low-risk human papillomavirus type 11 in keratinocytes that stably maintain viral episomes. J. Virol. 75:7564-7571.
38. Villa, L. L., and R. Schlegel. 1991. Differences in transformation activity between HPV-18 and HPV-16 map to the viral LCR-E6-E7 region. Virology 181:374-377.
39. Wiatrak, B. J., D. W. Wiatrak, T. R. Broker, and L. Lewis. 2004. Recurrent respiratory papillomatosis: a longitudinal study comparing severity associated with human papilloma viral types 6 and 11 and other risk factors in a large pediatric population. Laryngoscope 114(Suppl. 104):1-23.
40. Wilson, J. L., S. C. Dollard, L. T. Chow, and T. R. Broker. 1992. Epithelial-specific gene expression during differentiation of stratified primary human keratinocyte cultures. Cell Growth Differ. 3:471-483.
41. Zehbe, I., A. Ratsch, A., M. Alunni-Fabbroni, A. Burzlaff, E. Bakos, M. Dürst, E. Wilander, and M. Tommasino. 1999. Overriding of cyclin-dependent kinase inhibitors by high and low risk human papillomavirus types: evidence for an in vivo role in cervical lesions. Oncogene 18:2201-2211.
42. Zerfass-Thome, K., W. Zwerschke, B. Mannhardt, R. Tindle, J. W. Botz, and P. Jansen-Dürr. 1996. Inactivation of the cdk inhibitor p27KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene 13:2323-2330.
43. Zhang, B., W. Chen, and A. Roman. 2005. The E7 proteins of low- and high-risk human papillomaviruses share the ability to target the pRB family member p130 for degradation. Proc. Natl. Acad. Sci. USA 103:437-442.
44. Zhao, W., L. T. Chow, and T. R. Broker. 1999. A distal element in the HPV-11 upstream regulatory region contributes to promoter repression in basal keratinocytes in squamous epithelium. Virology 253:219-229.
45. Zhao, W., L. T. Chow, and T. R. Broker. 1997. Transcription activities of human papillomavirus type 11 E6 promoter-proximal elements in raft and submerged cultures of foreskin keratinocytes. J. Virol. 71:8832-8840.
46. Zhao, W., F. Noya, W. Y. Chen, T. M. Townes, L. T. Chow, and T. R. Broker. 1999. Trichostatin A up-regulates human papillomavirus type 11 upstream regulatory region-E6 promoter activity in undifferentiated primary human keratinocytes. J. Virol. 73:5026-5033.
47. zur Hausen, H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nature 2:342-350.