p53 degradation activity, expression, and subcellular localization of E6 proteins from 29 human papillomavirus genotypes

Journal of Virology

Volumn 86, Issue 1, 2012, Pages 94-107

  Mesplède, Thibault ^a,b   Gagnon, David ^a,b   Bergeron Labrecque, Fanny ^a,b   Azar, Ibrahim ^a,c   Sénéchal, Hélène ^a,b   Coutlée, François ^b,c,d   Archambault, Jacques ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN E6; PROTEIN P53; RENILLA LUCIFERIN 2 MONOOXYGENASE;

ALPHAPAPILLOMAVIRUS; AMINO ACID SUBSTITUTION; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; ENZYME ACTIVITY; EXPRESSION VECTOR; FEMALE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; HUMAN PAPILLOMAVIRUS TYPE 33; HUMAN PAPILLOMAVIRUS TYPE 58; HUMAN PAPILLOMAVIRUS TYPE 66; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; RNA SPLICING; STEADY STATE; WART VIRUS;

ALPHAPAPILLOMAVIRUS; AMINO ACID SEQUENCE; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, VIRAL; GENOTYPE; HUMANS; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PHYLOGENY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE; RENILLA LUCIFERASE;

EID: 84855945551     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00751-11     Document Type: Article

References (74)

1. Bernard HU, et al. 2010. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401: 70-79.
2. Bohm S, Wilczynski SP, Pfister H, Iftner T. 1993. The predominant mRNA class in HPV16-infected genital neoplasias does not encode the E6 or the E7 protein. Int. J. Cancer 55:791-798.
3. Boukamp P, et al. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106: 761-771.
4. Bouvard V, et al. 2009. A review of human carcinogens. B. Biological agents. Lancet Oncol. 10:321-322.
5. Brimer N, Lyons C, Vande Pol SB. 2007. Association of E6AP (UBE3A) with human papillomavirus type 11 E6 protein. Virology 358:303-310.
6. Brosh R, Rotter V. 2009. When mutants gain new powers: news from the mutant p53 field. Nat. Rev. Cancer 9:701-713.
7. Brown DR, McClowry TL, Woods K, Fife KH. 1999. Nucleotide sequence and characterization of human papillomavirus type 83, a novel genital papillomavirus. Virology 260:165-172.
8. Bruni L, et al. 2010. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J. Infect. Dis. 202:1789 -1799.
9. Camus S, et al. 2007. Ubiquitin-independent degradation of p53 mediated by high-risk human papillomavirus protein E6. Oncogene 26: 4059-4070.
10. Cheng S, Schmidt-Grimminger DC, Murant T, Broker TR, Chow LT. 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 9:2335-2349.
11. Crook T, Tidy JA, Vousden KH. 1991. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell 67:547-556.
12. de Sanjose S, et al. 2010. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 11:1048 -1056.
13. Doorbar J, et al. 1990. Detection of novel splicing patterns in a HPV16-containing keratinocyte cell line. Virology 178:254 -262.
14. Du J, et al. 2004. Resistance to apoptosis of HPV 16-infected laryngeal cancer cells is associated with decreased Bak and increased Bcl-2 expression. Cancer Lett. 205:81- 88.
15. Duensing S, et al. 2000. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc. Natl. Acad. Sci. U. S. A. 97:10002-10007.
16. Duensing S, Munger K. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075-7082.
17. Elbel M, Carl S, Spaderna S, Iftner T. 1997. A comparative analysis of the interactions of the E6 proteins from cutaneous and genital papillomaviruses with p53 and E6AP in correlation to their transforming potential. Virology 239:132-149.
18. Ellis JR, et al. 1995. The association of an HPV16 oncogene variant with HLA-B7 has implications for vaccine design in cervical cancer. Nat. Med. 1:464-470.
19. Filippova M, et al. 2007. The large and small isoforms of human papillomavirus type 16 E6 bind to and differentially affect procaspase 8 stability and activity. J. Virol. 81:4116-4129.
20. Fu L, et al. 2010. Degradation of p53 by human Alphapapillomavirus E6 proteins shows a stronger correlation with phylogeny than oncogenicity. PLoS One 5:e12816.
21. Gagnon D, et al. 2009. Proteasomal degradation of the papillomavirus E2 protein is inhibited by overexpression of bromodomain-containing protein J. Virol. 83:4127- 4139.
22. Gagnon S, et al. 2004. Viral polymorphism in human papillomavirus types 33 and 35 and persistent and transient infection in the genital tract of women. J. Infect. Dis. 190:1575-1585.
23. Giannoudis A, Herrington CS. 2001. Human papillomavirus variants and squamous neoplasia of the cervix. J. Pathol. 193:295-302.
24. Guccione E, Massimi P, Bernat A, Banks L. 2002. Comparative analysis of the intracellular location of the high- and low-risk human papillomavirus oncoproteins. Virology 293:20 -25.
25. Herber R, Liem A, Pitot H, Lambert PF. 1996. Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene. J. Virol. 70:1873-1881.
26. Hiller T, Poppelreuther S, Stubenrauch F, Iftner T. 2006. Comparative analysis of 19 genital human papillomavirus types with regard to p53 degradation, immortalization, phylogeny, and epidemiologic risk classification. Cancer Epidemiol. Biomarkers Prev. 15:1262-1267.
27. Huibregtse JM, Scheffner M, Howley PM. 1991. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 10:4129-4135.
28. Huibregtse JM, Scheffner M, Howley PM. 1993. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell. Biol. 13:775-784.
29. Hummel M, Hudson JB, Laimins LA. 1992. Differentiation-induced and constitutive transcription of human papillomavirus type 31b in cell lines containing viral episomes. J. Virol. 66:6070-6080.
30. Jackson S, Harwood C, Thomas M, Banks L, Storey A. 2000. Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins. Genes Dev. 14:3065-3073.
31. Kehmeier E, et al. 2002. Cellular steady-state levels of "high risk" but not "low risk" human papillomavirus (HPV) E6 proteins are increased by inhibition of proteasome-dependent degradation independent of their p53- and E6AP-binding capabilities. Virology 299:72- 87.
32. Khouadri S, et al. 2006. Human papillomavirus type 33 polymorphisms and high-grade squamous intraepithelial lesions of the uterine cervix. J. Infect. Dis. 194:886-894.
33. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
34. Lechner MS, Laimins LA. 1994. Inhibition of p53 DNA binding by human papillomavirus E6 proteins. J. Virol. 68:4262- 4273.
35. Lee C, Wooldridge TR, Laimins LA. 2007. Analysis of the roles of E6 binding to E6TP1 and nuclear localization in the human papillomavirus type 31 life cycle. Virology 358:201-210.
36. Lehoux M, D'Abramo CM, Archambault J. 2009. Molecular mechanisms of human papillomavirus-induced carcinogenesis. Public Health Genomics 12:268 -280.
37. Le Roux LG, Moroianu J. 2003. Nuclear entry of high-risk human papillomavirus type 16 E6 oncoprotein occurs via several pathways. J. Virol. 77:2330 -2337.
38. Lin DL, Chang C. 1996. p53 is a mediator for radiation-repressed human TR2 orphan receptor expression in MCF-7 cells, a new pathway from tumor suppressor to member of the steroid receptor superfamily. J. Biol. Chem. 271:14649 -14652.
39. Liu Y, et al. 1999. Multiple functions of human papillomavirus type 16 E6 contribute to the immortalization of mammary epithelial cells. J. Virol. 73:7297-7307.
40. Massimi P, Shai A, Lambert P, Banks L. 2008. HPV E6 degradation of p53 and PDZ containing substrates in an E6AP null background. Oncogene 27:1800 -1804.
41. Masson M, et al. 2003. Preferential nuclear localization of the human papillomavirus type 16 E6 oncoprotein in cervical carcinoma cells. J. Gen. Virol. 84:2099 -2104.
42. Moody CA, Laimins LA. 2010. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10:550 -560.
43. Munoz N, et al. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348:518 -527.
44. Negrini S, Gorgoulis VG, Halazonetis TD. 2010. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11:220-228.
45. Pim d, Massimi P, Banks L. 1997. Alternatively spliced HPV-18 E6* protein inhibits E6 mediated degradation of p53 and suppresses transformed cell growth. Oncogene 15:257-264.
46. Pim D, Banks L. 1999. HPV-18 E6*1 protein modulates the E6-directed degradation of p53 by binding to full-length HPV-18 E6. 18:7403-7408.
47. Pim D, Tomaic V, Banks L. 2009. The human papillomavirus (HPV) E6* proteins from high-risk, mucosal HPVs can direct degradation of cellular proteins in the absence of full-length E6 protein. J. Virol. 83:9863-9874.
48. Richard C, et al. 2010. The immortalizing and transforming ability of two common human papillomavirus 16 E6 variants with different prevalences in cervical cancer. Oncogene 29:3435-3445.
49. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
50. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129 -1136.
51. Sherman L, Alloul N, Golan I, Durst M, Baram A. 1992. Expression and splicing patterns of human papillomavirus type-16 mRNAs in precancerous lesions and carcinomas of the cervix, in human keratinocytes immortalized by HPV 16, and in cell lines established from cervical cancers. Int. J. Cancer 50:356 -364.
52. Simmonds M, Storey A. 2008. Identification of the regions of the HPV 5 E6 protein involved in Bak degradation and inhibition of apoptosis. Int. J. Cancer 123:2260 -2266.
53. Slebos RJ, et al. 1995. Functional consequences of directed mutations in human papillomavirus E6 proteins: abrogation of p53-mediated cell cycle arrest correlates with p53 binding and degradation in vitro. Virology 208: 111-120.
54. Smotkin D, Prokoph H, Wettstein FO. 1989. Oncogenic and nononcogenic human genital papillomaviruses generate the E7 mRNA by different mechanisms. J. Virol. 63:1441-1447.
55. Song S, Liem A, Miller JA, Lambert PF. 2000. Human papillomavirus types 16 E6 and E7 contribute differently to carcinogenesis. Virology 267: 141-150.
56. Song S, Pitot HC, Lambert PF. 1999. The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals. J. Virol. 73:5887-5893.
57. Steger G, Corbach S. 1997. Dose-dependent regulation of the early promoter of human papillomavirus type 18 by the viral E2 protein. J. Virol. 71:50 -58.
58. Stewart D, Ghosh A, Matlashewski G. 2005. Involvement of nuclear export in human papillomavirus type 18 E6-mediated ubiquitination and degradation of p53. J. Virol. 79:8773- 8783.
59. Stoppler MC, et al. 1996. Natural variants of the human papillomavirus type 16 E6 protein differ in their abilities to alter keratinocyte differentiation and to induce p53 degradation. J. Virol. 70:6987- 6993.
60. Sun L, et al. 2010. The location of endogenous wild-type p53 protein in 293T and HEK293 cells expressing low-risk HPV-6E6 fusion protein with GFP. Acta Biochim. Biophys. Sin. (Shanghai) 42:230 -235.
61. Sun L, et al. 2008. Two different HPV-11E6 fusion proteins trap p53 in the cytoplasm and induce apoptosis. Cancer Biol. Ther. 7:1909 -1915.
62. Talis AL, Huibregtse JM, Howley PM. 1998. The role of E6AP in the regulation of p53 protein levels in human papillomavirus (HPV)-positive and HPV-negative cells. J. Biol. Chem. 273:6439-6445.
63. Tang S, Tao M, McCoy JP, Jr, Zheng ZM. 2006. The E7 oncoprotein is translated from spliced E6*I transcripts in high-risk human papillomavirus type 16- or type 18-positive cervical cancer cell lines via translation reinitiation. J. Virol. 80:4249-4263.
64. Tao M, Kruhlak M, Xia S, Androphy E, Zheng ZM. 2003. Signals that dictate nuclear localization of human papillomavirus type 16 oncoprotein E6 in living cells. J. Virol. 77:13232-13247.
65. Thomas M, Banks L. 1999. Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types. J. Gen. Virol. 80:1513-1517.
66. Thomas M, Banks L. 1998. Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 17:2943-2954.
67. Thomas MC, Chiang CM. 2005. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol. Cell 17:251-264.
68. Tomaic V, et al. 2011. Regulation of the HPV-18 E6/E6AP ubiquitin ligase complex by the HECT domain-containing protein EDD. J. Virol. 85:3120 -3127.
69. Tungteakkhun SS, Filippova M, Fodor N, Duerksen-Hughes PJ. 2010. The full-length isoform of human papillomavirus 16 E6 and its splice variant E6* bind to different sites on the procaspase 8 death effector domain. J. Virol. 84:1453-1463.
70. Underbrink MP, Howie HL, Bedard KM, Koop JI, Galloway DA. 2008. E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J. Virol. 82:10408 -10417.
71. Vaeteewoottacharn K, Chamutpong S, Ponglikitmongkol M, Angeletti PC. 2005. Differential localization of HPV16 E6 splice products with E6-associated protein. Virol. J. 2:50.
72. Werness BA, Levine AJ, Howley PM. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76 -79.
73. Wheeler CM, Yamada T, Hildesheim A, Jenison SA. 1997. Human papillomavirus type 16 sequence variants: identification by E6 and L1 lineage-specific hybridization. J. Clin. Microbiol. 35:11-19.
74. Xin CY, et al. 2001. Analysis of E6 variants of human papillomavirus type 33, 52 and 58 in Japanese women with cervical intraepithelial neoplasia/cervical cancer in relation to their oncogenic potential. Cancer Lett. 170:19-24.