The human papillomavirus type 8 E2 protein suppresses β4-integrin expression in primary human keratinocytes

Journal of Virology

Volumn 78, Issue 19, 2004, Pages 10738-10746

  Oldak, Monika ^a,b   Smola, Hans ^a,c   Aumailley, Monique ^a   Rivero, Francisco ^a   Pfister, Herbert ^a   Smola Hess, Sigrun ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA4 INTEGRIN; CELL DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TYPING; WART VIRUS;

ANTIGENS, CD29; APOPTOSIS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN BETA4; KERATINOCYTES; MICROSCOPY, FLUORESCENCE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PROMOTER REGIONS (GENETICS); TRANS-ACTIVATORS;

EID: 4544348023     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.19.10738-10746.2004     Document Type: Article

References (51)

1. Adams, J. C., and F. M. Watt. 1989. Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature 340:307-309.
2. Aumailley, M., A. El Khal, N. Knoss, and L. Tunggal. 2003. Laminin 5 processing and its integration into the ECM. Matrix Biol. 22:49-54.
3. Boeckle, S., H. Pfister, and G. Steger. 2002. A new cellular factor recognizes E2 binding sites of papillomaviruses which mediate transcriptional repression by E2. Virology 293:103-117.
4. Carter, W. G., P. Kaur, S. G. Gil, P. J. Gahr, and E. A. Wayner. 1990. Distinct functions for integrins alpha 3 beta 1 in focal adhesions and alpha 6 beta 4/bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Biol. 111:3141-3154.
5. Danen, E. H., and A. Sonnenberg. 2003. Integrins in regulation of tissue development and function. J. Pathol. 200:471-480.
6. Demeret, C., A. Garcia-Carranca, and F. Thierry. 2003. Transcription-independent triggering of the extrinsic pathway of apoptosis by human papillomavirus 18 E2 protein. Oncogene 22:168-175.
7. Desaintes, C., C. Demeret, S. Goyat, M. Yaniv, and F. Thierry. 1997. Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J. 16:504-514.
8. Desaintes, C., S. Goyat, S. Garbay, M. Yaniv, and F. Thierry. 1999. Papillomavirus E2 induces p53-independent apoptosis in HeLa cells. Oncogene 18:4538-545.
9. Dong, G., T. R. Broker, and L. T. Chow. 1994. Human papillomavirus type 11 E2 proteins repress the homologous E6 promoter by interfering with the binding of host transcription factors to adjacent elements. J. Virol. 68:1115-1127.
10. Dowling, J., Q. C. Yu, and E. Fuchs. 1996. Beta4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol. 134:559-572.
11. Feltkamp, M. C., R. Broer, F. M. di Summa, L. Struijk, E. van der Meijden, B. P. Verlaan, R. G. Westendorp, J. ter Schegget, W. J. Spaan, and J. N. Bouwes Bavinck. 2003. Seroreactivity to epidermodysplasia verruciformis-related human papillomavirus types is associated with nonmelanoma skin cancer. Cancer Res. 63:2695-2700.
12. Frye, M., C. Gardner, E. R. Li, I. Arnold, and F. M. Watt. 2003. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development 130:2793-2808.
13. Gandarillas, A., and F. M. Watt. 1997. c-Myc promotes differentiation of human epidermal stem cells. Genes Dev. 11:2869-2882.
14. Georges-Labouesse, E., N. Messaddeq, G. Yehia, L. Cadalbert, A. Dierich, and M. Le Meur. 1996. Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat. Genet. 13:370-373.
15. Geuijen, C. A., and A. Sonnenberg. 2002. Dynamics of the alpha6beta4 integrin in keratinocytes. Mol. Biol. Cell 13:3845-3858.
16. Green, H. 1977. Terminal differentiation of cultured human epidermal cells. Cell 11:405-416.
17. Hadaschik, D., K. Hinterkeuser, M. Oldak, H. J. Pfister, and S. Smola-Hess. 2003. The papillomavirus E2 protein binds to and synergizes with C/EBP factors involved in keratinocyte differentiation. J. Virol. 77:5253-5265.
18. Hall, P. A., and F. M. Watt. 1989. Stem cells: the generation and maintenance of cellular diversity. Development 106:619-633.
19. Haller, K., F. Stubenrauch, and H. Pfister. 1995. Differentiation- dependent transcription of the epidermodysplasia verruciformis-associated human papillomavirus type 5 in benign lesions. Virology 214:245-255.
20. Hwang, E. S., D. J. Riese II, J. Settleman, L. A. Nilson, J. Honig, S. Flynn, and D. DiMaio. 1993. Inhibition of cervical carcinoma cell line proliferation by the introduction of a bovine papillomavirus regulatory gene. J. Virol. 67:3720-3729.
21. Jones, P. H., S. Harper, and F. M. Watt. 1995. Stem cell patterning and fate in human epidermis. Cell 80:83-93.
22. Jones, P. H., and F. M. Watt. 1993. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73:713-724.
23. Lee, D., B. Lee, J. Kirn, D. W. Kirn, and J. Choe. 2000. cAMP response element-binding protein-binding protein binds to human papillomavirus E2 protein and activates E2-dependent transcription. J. Biol. Chem. 275:7045-7051.
24. Levy, L., S. Broad, D. Diekmann, R. D. Evans, and F. M. Watt. 2000. beta1 integrins regulate keratinocyte adhesion and differentiation by distinct mechanisms. Mol. Biol. Cell 11:453-466.
25. Marchisio, P. C., S. Bondanza, O. Cremona, R. Cancedda, and M. De Luca. 1991. Polarized expression of integrin receptors (alpha 6 beta 4, alpha 2 beta 1, alpha 3 beta 1, and alpha v beta 5) and their relationship with the cytoskeleton and basement membrane matrix in cultured human keratinocytes. J. Cell Biol. 112:761-773.
26. Masini, C., P. G. Fuchs, F. Gabrielli, S. Stark, F. Sera, M. Ploner, C. F. Melchi, G. Primavera, G. Pirchio, O. Picconi, P. Petasecca, M. S. Cattaruzza, H. J. Pfister, and D. Abeni. 2003. Evidence for the association of human papillomavirus infection and cutaneous squamous cell carcinoma in immunocompetent individuals. Arch. Dermatol. 139:890-894.
27. Massimi, P., D. Pirn, C. Bertoli, V. Bouvard, and L. Banks. 1999. Interaction between the HPV-16 E2 transcriptional activator and p53. Oncogene 18:7748-7754.
28. Müller, A., A. Ritzkowsky, and G. Steger. 2002. Cooperative activation of human papillomavirus type 8 gene expression by the E2 protein and the cellular coactivator p300. J. Virol. 76:11042-11053.
29. Münger, K., B. A. Werness, N. Dyson, W. C. Phelps, E. Harlow. and P. M. Howley. 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105.
30. Niessen, C. M., M. H. van der Raaij-Helmer, E. H. Hulsman, R. van der Neut, M. F. Jonkman, and A. Sonnenberg. 1996. Deficiency of the integrin beta 4 subunit in junctional epidermolysis bullosa with pyloric atresia: consequences for hemidesmosome formation and adhesion properties. J. Cell Sci. 109:1695-1706.
31. Pear, W. S., G. P. Nolan, M. L. Scott, and D. Baltimore. 1993. Production of high-liter helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90:8392-8396.
32. Peng, Y. C., D. E. Breiding, F. Sverdrup, J. Richard, and E. J. Androphy. 2000. AMF-1/Gps2 binds p300 and enhances its interaction with papillomavirus E2 proteins. J. Virol. 74:5872-5879.
33. Quandt, K., K. Frech, H. Karas, E. Wingender, and T. Werner. 1995. MatInd and Matlnspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23:4878-4884.
34. Schetther, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
35. Schlegel, R., W. C. Phelps, Y. L. Zhang, and M. Barbosa. 1988. Quantitative keratinocyte assay detects two biological activities of human papillomavirus DNA and identifies viral types associated with cervical carcinoma. EMBO J. 7:3181-3187.
36. Schmidt, H. M., G. Steger, and H. Pfister. 1997. Competitive binding of viral E2 protein and mammalian core-binding factor to transcriptional control sequences of human papillomavirus type 8 and bovine papillomavirus type 1. J. Virol. 71:8029-8034.
37. Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17:6419.
38. Sonnenberg, A., J. Calafat, H. Janssen, H. Daams, L. M. van der Raaij-Helmer, R. Falcioni, S. J. Kennel, J. D. Aplin, J. Baker, M. Loizidou, et al. 1991. Integrin alpha 6/beta 4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J. Cell Biol. 113:907-917.
39. Stepp, M. A., S. Spurr-Michaud, A. Tisdale, J. Elwell, and I. K. Gipson. 1990. Alpha 6 beta 4 integrin heterodimer is a component of hemidesmosomes. Proc. Natl. Acad. Sci. USA 87:8970-8974.
40. Stevenson, M., L. C. Hudson, J. E. Burns, R. L. Stewart, M. Wells, and N. J. Maitland. 2000. Inverse relationship between the expression of the human papillomavirus type 16 transcription factor E2 and virus DNA copy number during the progression of cervical intraepithelial neoplasia. J. Gen. Virol. 81:1825-1832.
41. Stubenrauch, F., and H. Pfister. 1994. Low-affinity E2-binding site mediates downmodulation of E2 transactivation of the human papillomavirus type 8 late promoter. J. Virol. 68:6959-6966.
42. Takaoka, A. S., T. Yamada, M. Gotoh, Y. Kanai, K. Imai, and S. Hirohashi. 1998. Cloning and characterization of the human beta4-integrin gene promoter and enhancers. J. Biol. Chem. 273:33848-33855.
43. Tan, S. H., L. E. Leong, P. A. Walker, and H. U. Bernard. 1994. The human papillomavirus type 16 E2 transcription factor binds with low cooperativity to two flanking sites and represses the E6 promoter through displacement of Sp1 and TFIID. J. Virol. 68:6411-6420.
44. Tasanen, K., L. Tunggal, G. Chometon, L. Bruckner-Tudennan, and M. Aumailley. 2004. Keratinocytes from patients lacking collagen XVII display a migratory phenotype. Am. J. Pathol. 164:2027-2038.
45. van der Flier, A., and A. Sonnenberg. 2001. Function and interactions of integrins. Cell Tissue Res. 305:285-298.
46. van der Neut, R., P. Krimpenfort, J. Calafat, C. M. Niessen, and A. Sonnenberg. 1996. Epithelial detachment due to absence of hemidesmosomes in integrin beta 4 null mice. Nat. Genet. 13:366-369.
47. Vidal, F., D. Aberdam, C. Miquel, A. M. Christiano, L. Pulkkinen, J. Uitto, J. P. Ortonne, and G. Meneguzzi. 1995. Integrin beta 4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat. Genet. 10:229-234.
48. Watt, F. M. 2002. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21:3919-3926.
49. Watt, F. M., M. D. Kubler, N. A. Hotchin, L. J. Nicholson, and J. C. Adams. 1993. Regulation of keratinocyte terminal differentiation by integrin-extracellular matrix interactions. J. Cell Sci. 106:175-182.
50. Wells, S. I., D. A. Francis, A. Y. Karpova, J. J. Dowhanick, J. D. Benson, and P. M. Howley. 2000. Papillomavirus E2 induces senescence in HPV-positive cells via pRB- and p21(CIP)-dependent pathways. EMBO J. 19:5762-5771.
51. Woodworth, C. D., S. Cheng, S. Simpson, L. Hamacher, L. T. Chow, T. R. Broker, and J. A. DiPaolo. 1992. Recombinant retroviruses encoding human papillomavirus type 18 E6 and E7 genes stimulate proliferation and delay differentiation of human keratinocytes early after infection. Oncogene 7:619-626.