HPV 5 and 8 E6 Abrogate ATR activity resulting in increased persistence of UVB induced DNA damage

PLoS Pathogens

Volumn 8, Issue 7, 2012, Pages 41-

  Wallace, Nicholas A ^a   Robinson, Kristin ^a   Howie, Heather L ^a   Galloway, Denise A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; MESSENGER RNA; PROTEIN E6; PROTEIN P300; SMALL INTERFERING RNA; THYMINE; ATR PROTEIN, HUMAN; CELL CYCLE PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 5; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 8; HISTONE ACETYLTRANSFERASE PCAF; ONCOPROTEIN; P300-CBP-ASSOCIATED FACTOR; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; PYRIMIDINE DIMER;

ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HUMAN PAPILLOMAVIRUS TYPE 5; HUMAN PAPILLOMAVIRUS TYPE 8; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RADIATION RESPONSE; ULTRAVIOLET B RADIATION; VIRUS EXPRESSION; WART VIRUS; BETAPAPILLOMAVIRUS; CELL CULTURE; CELL CYCLE CHECKPOINT; GENETICS; HUMAN; METABOLISM; RADIATION EXPOSURE; RNA INTERFERENCE; SKIN TUMOR; TUMOR CELL LINE; ULTRAVIOLET RADIATION; VIROLOGY;

HUMAN PAPILLOMAVIRUS;

BETAPAPILLOMAVIRUS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; HUMANS; ONCOGENE PROTEINS, VIRAL; P300-CBP TRANSCRIPTION FACTORS; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINE DIMERS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 84864592506     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002807     Document Type: Article

References (64)

1. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, et al. (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401: 70-79.
2. zur Hausen H, (1999) Papillomaviruses in human cancers. Proc Assoc Am Physicians 111: 581-587.
3. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, et al. (2005) Carcinogenicity of human papillomaviruses. Lancet Oncol 6: 204.
4. Lorincz AT, Reid R, Jenson AB, Greenberg MD, Lancaster W, et al. (1992) Human papillomavirus infection of the cervix: relative risk associations of 15 common anogenital types. Obstet Gynecol 79: 328-337.
5. Bouwes Bavinck JN, Feltkamp M, Struijk L, ter Schegget J, (2001) Human papillomavirus infection and skin cancer risk in organ transplant recipients. J Investig Dermatol Symp Proc 6: 207-211.
6. Orth G, Jablonska S, Jarzabek-Chorzelska M, Obalek S, Rzesa G, et al. (1979) Characteristics of the lesions and risk of malignant conversion associated with the type of human papillomavirus involved in epidermodysplasia verruciformis. Cancer Res 39: 1074-1082.
7. Lutzner MA, Blanchet-Bardon C, Orth G, (1984) Clinical observations, virologic studies, and treatment trials in patients with epidermodysplasia verruciformis, a disease induced by specific human papillomaviruses. J Invest Dermatol 83: 18s-25s.
8. Pfister H, (1992) Human papillomaviruses and skin cancer. Semin Cancer Biol 3: 263-271.
9. Akgul B, Cooke JC, Storey A, (2006) HPV-associated skin disease. J Pathol 208: 165-175.
10. Nindl I, Gottschling M, Stockfleth E, (2007) Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23: 247-259.
11. Galloway DA, Howie HL, Katzenellenbogen RA, (2009) Papillomavirus E6 proteins. Virology 384: 324-334.
12. McLaughlin-Drubin ME, Munger K, (2009) The human papillomavirus E7 oncoprotein. Virology 384: 335-344.
13. Huibregtse JM, Scheffner M, Howley PM, (1991) A Cellular Protein Mediates Association of P53 with the E6 Oncoprotein of Human Papillomavirus Type-16 or Type-18. EMBO J 10: 4129-4135.
14. 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.
15. Chen JJ, Hong Y, Rustamzadeh E, Baleja JD, Androphy EJ, (1998) Identification of an alpha helical motif sufficient for association with papillomavirus E6. J Biol Chem 273: 13537-13544.
16. Kuballa P, Matentzoglu K, Scheffner M, (2007) The role of the ubiquitin ligase E6-AP in human papillomavirus E6-mediated degradation of PDZ domain-containing proteins. J Biol Chem 282: 65-71.
17. 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 (Pt 6): 1513-1517.
18. Thomas M, Banks L, (1998) Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 17: 2943-2954.
19. Jing M, Bohl J, Brimer N, Kinter M, Vande Pol SB, (2007) Degradation of tyrosine phosphatase PTPN3 (PTPH1) by association with oncogenic human papillomavirus E6 proteins. J Virol 81: 2231-2239.
20. 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.
21. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, et al. (1998) Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396: 84-88.
22. Klingelhutz AJ, Foster SA, McDougall JK, (1996) Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380: 79-82.
23. Veldman T, Liu X, Yuan H, Schlegel R, (2003) Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter. Proc Natl Acad Sci U S A 100: 8211-8216.
24. Lee SS, Glaunsinger B, Mantovani F, Banks L, Javier RT, (2000) Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J Virol 74: 9680-9693.
25. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, et al. (1997) Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc Natl Acad Sci U S A 94: 11612-11616.
26. Nakagawa S, Huibregtse JM, (2000) Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol Cell Biol 20: 8244-8253.
27. Glaunsinger BA, Lee SS, Thomas M, Banks L, Javier R, (2000) Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 19: 5270-5280.
28. Lee SS, Weiss RS, Javier RT, (1997) Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc Natl Acad Sci U S A 94: 6670-6675.
29. Thomas M, Dasgupta J, Zhang Y, Chen X, Banks L, (2008) Analysis of specificity determinants in the interactions of different HPV E6 proteins with their PDZ domain-containing substrates. Virology 376: 371-378.
30. Bedard KM, Underbrink MP, Howie HL, Galloway DA, (2008) The E6 oncoproteins from human betapapillomaviruses differentially activate telomerase through an E6AP-dependent mechanism and prolong the lifespan of primary keratinocytes. J Virol 82: 3894-3902.
31. 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.
32. Muller-Schiffmann A, Beckmann J, Steger G, (2006) The E6 protein of the cutaneous human papillomavirus type 8 can stimulate the viral early and late promoters by distinct mechanisms. J Virol 80: 8718-8728.
33. Zimmermann H, Degenkolbe R, Bernard HU, O'Connor MJ, (1999) The human papillomavirus type 16 E6 oncoprotein can down-regulate p53 activity by targeting the transcriptional coactivator CBP/p300. J Virol 73: 6209-6219.
34. Patel D, Huang SM, Baglia LA, McCance DJ, (1999) The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J 18: 5061-5072.
35. Muench P, Probst S, Schuetz J, Leiprecht N, Busch M, et al. (2010) Cutaneous papillomavirus E6 proteins must interact with p300 and block p53-mediated apoptosis for cellular immortalization and tumorigenesis. Cancer Res 70: 6913-6924.
36. Howie HL, Koop JI, Weese J, Robinson K, Wipf G, et al. (2011) Beta-HPV 5 and 8 E6 Promote p300 Degradation by Blocking AKT/p300 Association. PLoS Pathog 7: e1002211.
37. Accardi R, Dong W, Smet A, Cui R, Hautefeuille A, et al. (2006) Skin human papillomavirus type 38 alters p53 functions by accumulation of deltaNp73. EMBO Rep 7: 334-340.
38. Gu W, Roeder RG, (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90: 595-606.
39. Giampieri S, Storey A, (2004) Repair of UV-induced thymine dimers is compromised in cells expressing the E6 protein from human papillomaviruses types 5 and 18. Br J Cancer 90: 2203-2209.
40. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, et al. (1998) DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev 12: 2831-2841.
41. Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JN, Cliby WA, et al. (1999) A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 13: 152-157.
42. Haupt Y, Maya R, Kazaz A, Oren M, (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299.
43. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW, (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51: 6304-6311.
44. Maltzman W, Czyzyk L, (1984) UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol 4: 1689-1694.
45. Dohoney KM, Guillerm C, Whiteford C, Elbi C, Lambert PF, et al. (2004) Phosphorylation of p53 at serine 37 is important for transcriptional activity and regulation in response to DNA damage. Oncogene 23: 49-57.
46. Shieh SY, Ikeda M, Taya Y, Prives C, (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
47. Stauffer D, Chang B, Huang J, Dunn A, Thayer M, (2007) p300/CREB-binding protein interacts with ATR and is required for the DNA replication checkpoint. J Biol Chem 282: 9678-9687.
48. Flynn RL, Zou L, (2011) ATR: a master conductor of cellular responses to DNA replication stress. Trends Biochem Sci 36: 133-140.
49. Cleaver JE, Lam ET, Revet I, (2009) Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat Rev Genet 10: 756-768.
50. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
51. Giles RH, Peters DJ, Breuning MH, (1998) Conjunction dysfunction: CBP/p300 in human disease. Trends Genet 14: 178-183.
52. Goodman RH, Smolik S, (2000) CBP/p300 in cell growth, transformation, and development. Genes Dev 14: 1553-1577.
53. Tini M, Benecke A, Um SJ, Torchia J, Evans RM, et al. (2002) Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol Cell 9: 265-277.
54. Barret JM, Cadou M, Hill BT, (2002) Inhibition of nucleotide excision repair and sensitisation of cells to DNA cross-linking anticancer drugs by F 11782, a novel fluorinated epipodophylloid. Biochem Pharmacol 63: 251-258.
55. Nghiem P, Park PK, Kim Y, Vaziri C, Schreiber SL, (2001) ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc Natl Acad Sci U S A 98: 9092-9097.
56. Zhao Y, Lu S, Wu L, Chai G, Wang H, et al. (2006) Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 26: 2782-2790.
57. Geyer RK, Nagasawa H, Little JB, Maki CG, (2000) Role and regulation of p53 during an ultraviolet radiation-induced G1 cell cycle arrest. Cell Growth Differ 11: 149-156.
58. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, et al. (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 58: 4375-4382.
59. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, et al. (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 59: 4375-4382.
60. Ward IM, Chen J, (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276: 47759-47762.
61. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, et al. (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 14: 1448-1459.
62. 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.
63. McGregor JM, Berkhout RJ, Rozycka M, ter Schegget J, Bouwes Bavinck JN, et al. (1997) p53 mutations implicate sunlight in post-transplant skin cancer irrespective of human papillomavirus status. Oncogene 15: 1737-1740.
64. Padlewska K, Ramoz N, Cassonnet P, Riou G, Barrois M, et al. (2001) Mutation and abnormal expression of the p53 gene in the viral skin carcinogenesis of epidermodysplasia verruciformis. J Invest Dermatol 117: 935-942.