A synthetic E7 gene of human papillomavirus type 16 that yields enhanced expression of the protein in mammalian cells and is useful for DNA immunization studies

Journal of Virology

Volumn 77, Issue 8, 2003, Pages 4928-4937

  Cid Arregui, Angel ^a   Juárez, Victoria ^b   Zur Hausen, Harald ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN E7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CODON; CONTROLLED STUDY; GENETIC STABILITY; HOST CELL; HUMAN; HUMAN CELL; IMMUNIZATION; INOCULATION; MOUSE; NONHUMAN; PAPILLOMA VIRUS; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSLATION REGULATION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; BASE SEQUENCE; CELL LINE; CODON; HUMANS; IMMUNIZATION; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; SEQUENCE ANALYSIS, DNA; TRANSFECTION; TUMOR VIRUS INFECTIONS; VACCINES, DNA; VIRAL VACCINES;

EID: 0345578684     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.8.4928-4937.2003     Document Type: Article

References (57)

1. Alunni-Fabbroni, M., T. Littlewood, L. Deleu, S. Caldeira, M. Giarre, M. Dell'Orco, and M. Tommasino. 2000. Induction of S phase and apoptosis by the human papillomavirus type 16 E7 protein are separable events in immortalized rodent fibroblasts. Oncogene 19:2277-2285.
2. Auewarakul, P., L. Gissmann, and A. Cid-Arregui. 1994. Targeted expression of the E6 and E7 oncogenes of human papillomavirus type 16 in the epidermis of transgenic mice elicits generalized epidermal hyperplasia involving autocrine factors. Mol. Cell. Biol. 14:8250-8258.
3. Berumen, J., L. Casas, E. Segura, J. L. Arnezcua, and A. Garcia-Carranca. 1994. Genome amplification of human papillomavirus types 16 and 18 in cervical carcinomas is related to the retention of E1/E2 genes. Int. J. Cancer 56:640-645.
4. Bible, J. M., C. Mant, J. M. Best, B. Kell, W. G. Starkey, K. Shanti Raju, P. Seed, C. Biswas, P. Muir, J. E. Banatvala, and J. Cason. 2000. Cervical lesions are associated with human papillomavirus type 16 intratypic variants that have high transcriptional activity and increased usage of common mammalian codons. J. Gen. Virol. 81(Pt 6):1517-1527.
5. Boshart, M., L. Gissmann, H. Ikenberg, A. Kleinheinz, W. Scheurlen, and H. zur Hausen. 1984. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer, EMBO J. 3:1151-1157.
6. Brinster, R. L., S. Brunner, X. Joseph, and I. L. Levey. 1979. Protein degradation in the mouse blastocyst. J. Biol. Chem. 254:1927-1931.
7. Casas, L., S. C. Galvan, R. M. Ordonez, N. Lopez, M. Guido, and J. Berumen. 1999. Asian-American variants of human papillomavirus type 16 have extensive mutations in the E2 gene and are highly amplified in cervical carcinomas. Int. J. Cancer 83:449-455.
8. Cid, A., P. Auewarakul, A. Garcia-Carranca, R. Ovseiovich, H. Gaissert, and L. Gissmann. 1993. Cell-type-specific activity of the human papillomavirus type 18 upstream regulatory region in transgenic mice and its modulation by tetradecanoyl phorbol acetate and glucocorticoids. J. Virol. 67:6742-6752.
9. Crook, T., J. P. Morgenstern, L. Crawford, and L. Banks. 1989. Continued expression of HPV-16 E7 protein is required for maintenance of the transformed phenotype of cells co-transformed by HPV-16 plus EJ-ras. EMBO J. 8:513-519.
10. Durst, M., R. T. Dzarlieva Petrusevska, P. Boukamp, N. E. Fusenig, and L. Gissmann. 1987. Molecular and cytogenetic analysis of immortalized human primary, keratinocytes obtained after transfection with human papillomavirus type 16 DNA. Oncogene 1:251-256.
11. Durst, M., D. Glitz, A. Schneider, and H. zur Hausen. 1992. Human papillomavirus type 16 (HPV 16) gene expression and DNA replication in cervical neoplasia: analysis by in situ hybridization, Virology 189:132-1340.
12. Fujikawa, K., M. Furuse, K. Uwabe, H. Maki, and O. Yoshie. 1994. Nuclear localization and transforming activity of human papillomavirus type 16 E7-beta-galactosidase fusion protein: characterization of the nuclear localization sequence. Virology 204:789-793.
13. Fujinaga, Y., K. Okazawa, A. Nishikawa, Y. Yamakawa, M. Fukushima, I. Kato, and K. Fujinaga. 1994. Sequence variation of human papilomavirus type 16 E7 in preinvasive and invasive cervical neoplasias. Virus Genes 9:85-92.
14. Grantham, R., C. Gautier, and M. Gouy. 1980. Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res. 8:1893-1912.
15. Greenfield, I., J. Nickerson, S. Penman, and M. Stanley. 1991. Human papillomavirus 16 E7 protein is associated with the nuclear matrix. Proc. Natl. Acad. Sci. USA 88:11217-11221.
16. Guccione, E., P. Massimi, A. Bernat, and L. Banks. 2002. Comparative analysis of the intracellular location of the high- and low-risk human papillomavirus oncoproteins. Virology 293:20-25.
17. Haas, J., E. C. Park, and B. Seed. 1996. Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr. Biol. 6:315-324.
18. Hansen, M. B., S. E. Nielsen, and K. Berg. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 119:203-210.
19. Hawley Nelson, P., K. H. Vousden, N. L. Hubbert, D. R. Lowy, and J. T. Schiller. 1989. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 8:3905-3910.
20. Iglesias, M., K. Yen, D. Gaiotti, A. Hildesheim, M. H. Stoler, and C. D. Woodworth. 1998. Human papillomavirus type 16 E7 protein sensitizes cervical keratinocytes to apoptosis and release of interleukin-la. Oncogene 17:1195-1205.
21. Ikemura, T. 1982. Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J. Mol. Biol. 158:573-597.
22. Jones, D. L., D. A. Thompson, and K. Munger. 1997. Destabilization of the RB tumor suppressor protein and stabilization of p53 contribute to HPV type 16 E7-induced apoptosis. Virology 239:97-107.
23. Josefsson, A. M., P. K. E. Magnusson, N. Ylitalo, P. Sørensen, P. Qwarforth-Tubbin, P. K. Andersen, M. Melbye, H. O. Adami, and U. B. Gyllensten. 2000. Viral load of human papilloma virus 16 as a determinant for development of cervical carcinoma in situ: a nested case-control study. Lancet 355:2189-2193.
24. Kanda, T., A. Furuno, and K. Yoshilke. 1988. Human papillomavirus type 16 open reading frame E7 encodes a transforming gene for rat 3Y1 cells. J. Virol. 62:610-613.
25. Kanda, T., S. Zanma, S. Watanabe, A. Furuno, and K. Yoshiike. 1991. Two immunodominant regions of the human papillomavirus type 16 E7 protein are masked in the nuclei of monkey COS-1 cells. Virology 182:723-731.
26. Karlin, S., B. E. Blaisdell, and G. A. Schachtel. 1990. Contrasts in codon usage of latent versus productive genes of Epstein-Barr virus: data and hypotheses J. Virol. 64:4264-4273.
27. Kozak, M. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125-8148.
28. Lambert, P. F., H. Pan, H. C. Pitot, A. Liem, M. Jackson, and A. E. Griep. 1993. Epidermal cancer associated with expression of human papillomavirus type 16 E6 and E7 oncogenes in the skin of transgenic mice. Proc. Natl. Acad. Sci. USA 90:5583-5587.
29. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63.
30. Munger, 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.
31. Nakamura, Y., T. Gojobori, and T. Ikemura. 2000. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res. 28:292.
32. Nauenburg, S., W. Zwerschke, and P. Jansen Durr. 2001. Induction of apoptosis in cervical carcinoma cells by peptide aptamers that bind to the HPV-16 E7 oncoprotein. FASEB J. 15:592-594.
33. Pan, H., and A. E. Griep. 1994. Altered cell cycle regulation in the lens of HPV- 16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev. 8:1285-1299.
34. Phelps, W. C., C. L. Yee, K. Munger, and P. M. Howley. 1988. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53:539-547.
35. Reinstein, E., M. Scheffner, M. Oren, A. Ciechanover, and A. Schwartz. 2000. Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Oncogene 19:5944-5950.
36. Romanczuk, H., and P. M. Howley. 1992. Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl. Acad. Sci. USA 89:3159-3163.
37. Seedorf, K., G. Krammer, M. Durst, S. Subai, and W. G. Rowekamp. 1985. Human papillomavirus type 16 DNA sequence. Virology 145:181-185.
38. Shah, K. V., and P. M. Howley. 1996. Papillomaviruses, p. 2077-2109. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed., vol. 2. Lippincott-Raven, Philadelphia, Pa.
39. Smotkin, D., and F. O. Wettstein. 1987. The major human papillomavirus protein in cervical cancers is a cytoplasmic phosphoprotein. J. Virol. 61:1686-1689.
40. Smotkin, D., and F. O. Wettstein. 1986. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc. Natl. Acad. Sci. USA 83:4680-4684.
41. Soto, U., B. C. Das, M. Lengert, P. Finzer, H. zur Hausen, and F. Rosl. 1999. Conversion of HPV 18 positive non-tumorigenic HeLa-fibroblast hybrids to invasive growth involves loss of TNF-alpha mediated repression of viral transcription and modification of the AP-1 transcription complex. Oncogene 18:3187-3198.
42. 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(Pt 7):1825-1832.
43. Stoler, M. H., C. R. Rhodes, A. Whitbeck, S. M. Wolinsky, L. T. Chow, and T. R. Broker. 1992. Human papillomavirus type 16 and 18 gene expression in cervical neoplasias. Hum. Pathol. 23:117-128.
44. Stoppler, H., M. C. Stoppler, E. Johnson, C. M. Simbulan-Rosenthal, M. E. Smulson, S. lyer, D. S. Rosenthal, and R. Schlegel. 1998. The E7 protein of human papiliomavirus type 16 sensitizes primary human keratinocytes to apoptosis. Oncogene 17:1207-1214.
45. Strauss, E. G., J. M. Strauss, and A. J. Levine. 1996. Virus evolution, p. 153-171. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed., vol. 2. Lippincott-Raven, Philadelphia, Pa.
46. Thompson, D. A., V. Zacny, G. S. Belinsky, M. Classon, D. L. Jones, R. Schlegel, and K. Munger. 2001. The HPV E7 oncoprotein inhibits tumor necrosis factor alpha-mediated apoptosis in normal human fibroblasts. Oncogene 20:3629-3640.
47. Tonon, S. A., M. A. Picconi, P. D. Bos, J. B. Zinovich, J. Galuppo, L. V. Alonio, and A. R. Teyssie. 2001. Physical status of the E2 human papilloma virus 16 viral gene in cervical preneoplastic and neoplastic lesions. J. Clin. Virol. 21:129-134.
48. von Knebel Doeberitz, M., T. Bauknecht, D. Bartsch, and H. zur Hausen. 1991. Influence of chromosomal integration on glucocorticoid-regulated transcription of growth-stimulating papillomavirus genes E6 and E7 in cervical carcinoma cells. Proc. Natl. Acad. Sci. USA 88:1411-1415.
49. von Knebel Doeberitz, M., C. Rittmuller, H. zur Hausen, and M. Durst. 1992. Inhibition of tumorigenicity of cervical cancer cells in nude mice by HPV E6- E7 anti-sense RNA. Int. J. Cancer 51:831-834.
50. Wain Hobson, S., R. Nussinov, R. J. Brown, and J. L. Sussman. 1981. Preferential codon usage in genes. Gene 13:355-364.
51. White, A. E., E. M. Livanos, and T. D. Tisty. 1994. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV on coproteins. Genes Dev. 8:666-677.
52. Yoshinouchi, M., A. Hongo, K. Nakamura, J. Kodama, S. Itoh, H. Sakai, and T. Kudo. 1999. Analysis by multiplex PCR of the physical status of human papillomavirus type 16 DNA in cervical cancers. J. Clin. Microbiol. 37:3514-3517.
53. Zatsepina, O., J. Braspenning, D. Robberson, M. A. Hajibagheri, K. J. Blight, S. Ely, M. Hibma, D. Spitkovsky, M. Trendelenburg, L. Crawford, and M. Tommasino. 1997. The human papillomavirus type 16 E7 protein is associated with the nucleolus in mammalian and yeast cells. Oncogene 14:1137-1145.
54. Zhou, J., W. J. Liu, S. W. Peng, X. Y. Sun, and I. Frazer. 1999. Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J. Virol. 73:4972-4982.
55. zur Hausen, H. 1996. Papillomavirus infections - a major cause of human cancers. Biochim. Biophys. Acta 1288:F55-F78.
56. zur Hausen, H. 1991. Viruses in human cancers. Science 254:1167-1173.
57. Zwerschke, W., S. Mazurek, P. Massimi, L. Banks, E. Eigenbrodt, and P. Jansen Durr. 1999. Modulation of type M2 pyruvate kinase activity by the human paplllomavirus type 16 E7 oncoprotein. Proc. Natl. Acad. Sci. USA 96:1291-1296.