1887

Abstract

Human papillomavirus type 16 (HPV-16) is the dominant risk factor for the development of cervical cancer. The virus encodes three oncoproteins, of which the E7 oncoprotein is the major protein involved in cell immortalization and transformation. E7 is a multi-functional protein. It binds the retinoblastoma tumour-suppressor protein (pRb), which regulates progression through the G restriction point in the cell cycle. The E7 protein interacts with transcription-regulatory proteins such as the TATA box-binding protein and with proteins of the AP1 transcription factor family. To identify additional proteins regulated by E7, differential-display PCR was used to identify differentially expressed mRNAs in cells containing an inducible E7 protein. It is reported that E7 expression leads to regulation of the genes encoding the calcium-binding protein S100P and the mitochondrial ADP/ATP carrier protein. These data identify new functions of the E7 protein and thus expand the number of routes by which HPV-16 influences cell growth control, although the function of S100P has still to be elucidated.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-4-1009
2000-04-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/4/0811009a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-4-1009&mimeType=html&fmt=ahah

References

  1. Antinore, M. J., Birrer, M. J., Patel, D., Nader, L. & McCance, D. J. ( 1996; ). The human papillomavirus type 16 E7 gene product interacts with and trans-activates the AP1 family of transcription factors. EMBO Journal 15, 1950-1960.
    [Google Scholar]
  2. Averboukh, L., Liang, P., Kantoff, P. W. & Pardee, A. B. ( 1996; ). Regulation of S100P expression by androgen. Prostate 29, 350-355.[CrossRef]
    [Google Scholar]
  3. Bates, S., Phillips, A. C., Clark, P. A., Stott, F., Peters, G., Ludwig, R. L. & Vousden, K. H. ( 1998; ). p14ARF links the tumour suppressors RB and p53. Nature 395, 124-125.[CrossRef]
    [Google Scholar]
  4. Baudier, J., Bergeret, E., Bertacchi, N., Weintraub, H., Gagnon, J. & Garin, J. ( 1995; ). Interactions of myogenic bHLH transcription factors with calcium-binding calmodulin and S100a (alpha alpha) proteins. Biochemistry 34, 7834-7846.[CrossRef]
    [Google Scholar]
  5. Becker, T., Gerke, V., Kube, E. & Weber, K. ( 1992; ). S100P, a novel Ca2+-binding protein from human placenta. cDNA cloning, recombinant protein expression and Ca2+ binding properties. European Journal of Biochemistry 207, 541-547.[CrossRef]
    [Google Scholar]
  6. Bertram, J., Palfner, K., Hiddemann, W. & Kneba, M. ( 1998; ). Elevated expression of S100P, CAPL and MAGE 3 in doxorubicin-resistant cell lines: comparison of mRNA differential display reverse transcription-polymerase chain reaction and subtractive suppressive hybridization for the analysis of differential gene expression. Anticancer Drugs 9, 311-317.[CrossRef]
    [Google Scholar]
  7. Donato, R. ( 1991; ). Perspectives in S-100 protein biology. Cell Calcium 12, 713-726.[CrossRef]
    [Google Scholar]
  8. Dyson, N., Howley, P. M., Münger, K. & Harlow, E. ( 1989; ). The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243, 934-937.[CrossRef]
    [Google Scholar]
  9. Dyson, N., Guida, P., Münger, K. & Harlow, E. ( 1992; ). Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. Journal of Virology 66, 6893-6902.
    [Google Scholar]
  10. Edmonds, C. & Vousden, K. H. ( 1989; ). A point mutational analysis of human papillomavirus type 16 E7 protein. Journal of Virology 63, 2650-2656.
    [Google Scholar]
  11. Gossen, M. & Bujard, H. ( 1992; ). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proceedings of the National Academy of Sciences, USA 89, 5547-5551.[CrossRef]
    [Google Scholar]
  12. Grigorian, M., Ambartsumian, N., Lykkesfeldt, A. E., Bastholm, L., Elling, F., Georgiev, G. & Lukanidin, E. ( 1996; ). Effect of mts1 (S100A4) expression on the progression of human breast cancer cells. International Journal of Cancer 67, 831-841.[CrossRef]
    [Google Scholar]
  13. Hawley-Nelson, P., Vousden, K. H., Hubbert, N. L., Lowy, D. R. & Schiller, J. T. ( 1989; ). HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO Journal 8, 3905-3910.
    [Google Scholar]
  14. Heierhorst, J., Kobe, B., Feil, S. C., Parker, M. W., Benian, G. M., Weiss, K. R. & Kemp, B. E. ( 1996; ). Ca2+/S100 regulation of giant protein kinases. Nature 380, 636-639.[CrossRef]
    [Google Scholar]
  15. Hu, J. & Van Eldik, L. J. ( 1996; ). S100 beta induces apoptotic cell death in cultured astrocytes via a nitric oxide-dependent pathway. Biochimica et Biophysica Acta 1313, 239-245.[CrossRef]
    [Google Scholar]
  16. Jewers, R. J., Hildebrandt, P., Ludlow, J. W., Kell, B. & McCance, D. J. ( 1992; ). Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. Journal of Virology 66, 1329-1335.
    [Google Scholar]
  17. Jinquan, T., Vorum, H., Larsen, C. G., Madsen, P., Rasmussen, H. H., Gesser, B., Etzerodt, M., Honore, B., Celis, J. E. & Thestrup-Pedersen, K. ( 1996; ). Psoriasin: a novel chemotactic protein. Journal of Investigative Dermatology 107, 5-10.[CrossRef]
    [Google Scholar]
  18. Jones, D. L., Thompson, D. A. & Münger, K. ( 1997; ). Destabilization of the RB tumor suppressor protein and stabilization of p53 contribute to HPV type 16 E7-induced apoptosis. Virology 239, 97-107.[CrossRef]
    [Google Scholar]
  19. Jørgensen, M., Bévort, M., Kledal, T. S., Hansen, B. V., Dalgaard, M. & Leffers, H. ( 1999; ). Differential display competitive polymerase chain reaction: an optimal tool for assaying gene expression. Electrophoresis 20, 230-240.[CrossRef]
    [Google Scholar]
  20. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef]
    [Google Scholar]
  21. Lam, E. W., Morris, J. D., Davies, R., Crook, T., Watson, R. J. & Vousden, K. H. ( 1994; ). HPV16 E7 oncoprotein deregulates B-myb expression: correlation with targeting of p107/E2F complexes. EMBO Journal 13, 871-878.
    [Google Scholar]
  22. Lam, E. W., Bennett, J. D. & Watson, R. J. ( 1995; ). Cell-cycle regulation of human B-myb transcription. Gene 160, 277-281.[CrossRef]
    [Google Scholar]
  23. Lee, S. W., Tomasetto, C., Swisshelm, K., Keyomarsi, K. & Sager, R. ( 1992; ). Down-regulation of a member of the S100 gene family in mammary carcinoma cells and reexpression by azadeoxycytidine treatment. Proceedings of the National Academy of Sciences, USA 89, 2504-2508.[CrossRef]
    [Google Scholar]
  24. Liang, P. & Pardee, A. B. ( 1992; ). Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967-971.[CrossRef]
    [Google Scholar]
  25. Mariggió, M. A., Fulle, S., Calissano, P., Nicoletti, I. & Fano, G. ( 1994; ). The brain protein S-100ab induces apoptosis in PC12 cells. Neuroscience 60, 29-35.[CrossRef]
    [Google Scholar]
  26. Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vieira, H. L., Prevost, M. C., Xie, Z., Matsuyama, S., Reed, J. C. & Kroemer, G. ( 1998; ). Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281, 2027-2031.[CrossRef]
    [Google Scholar]
  27. Massimi, P., Pim, D., Storey, A. & Banks, L. ( 1996; ). HPV-16 E7 and adenovirus E1a complex formation with TATA box binding protein is enhanced by casein kinase II phosphorylation. Oncogene 12, 2325-2330.
    [Google Scholar]
  28. Massimi, P., Pim, D. & Banks, L. ( 1997; ). Human papillomavirus type 16 E7 binds to the conserved carboxy-terminal region of the TATA box binding protein and this contributes to E7 transforming activity. Journal of General Virology 78, 2607-2613.
    [Google Scholar]
  29. Morgenstern, J. P. & Land, H. ( 1990; ). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Research 18, 3587-3596.[CrossRef]
    [Google Scholar]
  30. Morris, J. D., Crook, T., Bandara, L. R., Davies, R., LaThangue, N. B. & Vousden, K. H. ( 1993; ). Human papillomavirus type 16 E7 regulates E2F and contributes to mitogenic signalling. Oncogene 8, 893-898.
    [Google Scholar]
  31. Münger, K., Phelps, W. C., Bubb, V., Howley, P. M. & Schlegel, R. ( 1989; ). The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. Journal of Virology 63, 4417-4421.
    [Google Scholar]
  32. Newton, R. A. & Hogg, N. ( 1998; ). The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. Journal of Immunology 160, 1427-1435.
    [Google Scholar]
  33. Nishida, M., Miyamoto, S., Kato, H., Miwa, T., Imamura, T., Miwa, K., Yasumoto, S., Barrett, J. C. & Wake, N. ( 1995; ). Transcriptional repression of smooth-muscle alpha-actin gene associated with human papillomavirus type 16 E7 expression. Molecular Carcinogenesis 13, 157-165.[CrossRef]
    [Google Scholar]
  34. Phelps, W. C., Yee, C. L., Münger, K. & Howley, P. M. ( 1988; ). The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53, 539-547.[CrossRef]
    [Google Scholar]
  35. Phillips, A. C. & Vousden, K. H. ( 1997; ). Analysis of the interaction between human papillomavirus type 16 E7 and the TATA-binding protein, TBP. Journal of General Virology 78, 905-909.
    [Google Scholar]
  36. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  37. Schäfer, B. W. & Heizmann, C. W. ( 1996; ). The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends in Biochemical Sciences 21, 134-140.[CrossRef]
    [Google Scholar]
  38. Schäfer, B. W., Wicki, R., Engelkamp, D., Mattei, M. G. & Heizmann, C. W. ( 1995; ). Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics 25, 638-643.[CrossRef]
    [Google Scholar]
  39. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. & Howley, P. M. ( 1990; ). The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129-1136.[CrossRef]
    [Google Scholar]
  40. Scheffner, M., Huibregtse, J. M., Vierstra, R. D. & Howley, P. M. ( 1993; ). The HPV-16 E6 and E6–AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75, 495-505.[CrossRef]
    [Google Scholar]
  41. Schmitt, A., Harry, J. B., Rapp, B., Wettstein, F. O. & Iftner, T. ( 1994; ). Comparison of the properties of the E6 and E7 genes of low- and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1. Journal of Virology 68, 7051-7059.
    [Google Scholar]
  42. Storey, A. & Banks, L. ( 1993; ). Human papillomavirus type 16 E6 gene cooperates with EJ-ras to immortalize primary mouse cells. Oncogene 8, 919-924.
    [Google Scholar]
  43. Takenaga, K., Nakamura, Y., Endo, H. & Sakiyama, S. ( 1994; ). Involvement of S100-related calcium-binding protein pEL98 (or mts1) in cell motility and tumor cell invasion. Japanese Journal of Cancer Research 85, 831-839.[CrossRef]
    [Google Scholar]
  44. Tommasino, M., Adamczewski, J. P., Carlotti, F., Barth, C. F., Manetti, R., Contorni, M., Cavalieri, F., Hunt, T. & Crawford, L. ( 1993; ). HPV16 E7 protein associates with the protein kinase p33CDK2 and cyclin A. Oncogene 8, 195-202.
    [Google Scholar]
  45. Voss, H., Nentwich, U., Duthie, S., Wiemann, S., Benes, V., Zimmermann, J. & Ansorge, W. ( 1997; ). Automated cycle sequencing with Taquenase: protocols for internal labeling, dye primer and ‘doublex’ simultaneous sequencing. Biotechniques 23, 312-318.
    [Google Scholar]
  46. Vousden, K. ( 1993; ). Interactions of human papillomavirus transforming proteins with the products of tumor suppressor genes. FASEB Journal 7, 872-879.
    [Google Scholar]
  47. Wan, J. S., Sharp, S. J., Poirier, G. M., Wagaman, P. C., Chambers, J., Pyati, J., Hom, Y. L., Galindo, J. E., Huvar, A., Peterson, P. A., Jackson, M. R. & Erlander, M. G. ( 1996; ). Cloning differentially expressed mRNAs. Nature Biotechnology 14, 1685-1691.[CrossRef]
    [Google Scholar]
  48. Zwerschke, W., Joswig, S. & Jansen-Dürr, P. ( 1996; ). Identification of domains required for transcriptional activation and protein dimerization in the human papillomavirus type-16 E7 protein. Oncogene 12, 213-220.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-4-1009
Loading
/content/journal/jgv/10.1099/0022-1317-81-4-1009
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error