β-HPV 5 and 8 E6 Disrupt Homology Dependent Double Strand Break Repair by Attenuating BRCA1 and BRCA2 Expression and Foci Formation

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-24

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

^a Fred Hutchinson Cancer Research Center   (United States)

^b PUGET SOUND BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; E1A ASSOCIATED P300 PROTEIN; GREEN FLUORESCENT PROTEIN; HISTONE ACETYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN E6; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN, HUMAN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 5; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 8; ONCOPROTEIN;

ARTICLE; BETA HUMAN PAPILLOMAVIRUS TYPE 5; BINDING KINETICS; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME FRAGILITY; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GAMMAPAPILLOMAVIRUS; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 8; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IONIZING RADIATION; MUTATION; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; ULTRAVIOLET B RADIATION; BETAPAPILLOMAVIRUS; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PAPILLOMAVIRUS INFECTION; PATHOLOGY; RECOMBINATION REPAIR; SKIN TUMOR; ULTRAVIOLET RADIATION;

HUMAN PAPILLOMAVIRUS;

BETAPAPILLOMAVIRUS; BRCA1 PROTEIN; BRCA2 PROTEIN; CELL LINE; DNA BREAKS, DOUBLE-STRANDED; GENE EXPRESSION REGULATION; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; RECOMBINATIONAL DNA REPAIR; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 84926504982     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004687     Document Type: Article

References (71)

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. doi: 10.1016/j.virol.2010.02.002 20206957
2. zur Hausen H, (1999) Papillomaviruses in human cancers. Proc Assoc Am Physicians 111: 581–587. 10591087
3. zur Hausen H, (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2: 342–350. 12044010
4. 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. 11924829
5. 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. 218721
6. 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. 6330217
7. Pfister H, (1992) Human papillomaviruses and skin cancer. Semin Cancer Biol 3: 263–271. 1335790
8. Akgul B, Cooke JC, Storey A, (2006) HPV-associated skin disease. J Pathol 208: 165–175. 16362995
9. Nindl I, Gottschling M, Stockfleth E, (2007) Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23: 247–259. 17627060
10. Panwar A, Batra R, Lydiatt WM, Ganti AK, (2014) Human papilloma virus positive oropharyngeal squamous cell carcinoma: a growing epidemic. Cancer Treat Rev 40: 215–219. doi: 10.1016/j.ctrv.2013.09.006 24080155
11. Pett M, Coleman N, (2007) Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? J Pathol 212: 356–367. 17573670
12. Desaintes C, Demeret C, Goyat S, Yaniv M, Thierry F, (1997) Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. Embo Journal 16: 504–514. 9034333
13. Desaintes C, Goyat S, Garbay S, Yaniv M, Thierry F, (1999) Papillomavirus E2 induces p53-independent apoptosis in HeLa cells. Oncogene 18: 4538–4545. 10467398
14. Li GL, Jiang W, Xia Q, Chen SH, Ge XR, et al. (2010) HPV E6 down-regulation and apoptosis induction of human cervical cancer cells by a novel lipid-soluble extract (PE) from Pinellia pedatisecta Schott in vitro. J Ethnopharmacol 132: 56–64. doi: 10.1016/j.jep.2010.07.035 20659543
15. Qi Z, Xu X, Zhang B, Li Y, Liu J, et al. (2010) Effect of simultaneous silencing of HPV-18 E6 and E7 on inducing apoptosis in HeLa cells. Biochem Cell Biol 88: 697–704. doi: 10.1139/O10-005 20651842
16. Howie HL, Katzenellenbogen RA, Galloway DA, (2009) Papillomavirus E6 proteins. Virology 384: 324–334. doi: 10.1016/j.virol.2008.11.017 19081593
17. McLaughlin-Drubin ME, Munger K, (2009) The human papillomavirus E7 oncoprotein. Virology 384: 335–344. doi: 10.1016/j.virol.2008.10.006 19007963
18. 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 Journal 10: 4129–4135. 1661671
19. 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. 2175676
20. 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. 8221889
21. 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. 12821782
22. Klingelhutz AJ, Barber SA, Smith PP, Dyer K, McDougall JK, (1994) Restoration of telomeres in human papillomavirus-immortalized human anogenital epithelial cells. Mol Cell Biol 14: 961–969. 8289836
23. Klingelhutz AJ, Foster SA, McDougall JK, (1996) Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380: 79–82. 8598912
24. Phelps WC, Bagchi S, Barnes JA, Raychaudhuri P, Kraus V, et al. (1991) Analysis of trans activation by human papillomavirus type 16 E7 and adenovirus 12S E1A suggests a common mechanism. J Virol 65: 6922–6930. 1834862
25. Phelps WC, Munger K, Yee CL, Barnes JA, Howley PM, (1992) Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J Virol 66: 2418–2427. 1312637
26. Munger K, Werness BA, Dyson N, Phelps WC, Harlow E, et al. (1989) Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. Embo Journal 8: 4099–4105. 2556261
27. Dyson N, Howley PM, Munger K, Harlow E, (1989) The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243: 934–937. 2537532
28. 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. doi: 10.1128/JVI.01818-07 18256157
29. Wallace NA, Robinson K, Howie HL, Galloway DA, (2012) HPV 5 and 8 E6 Abrogate ATR Activity Resulting in Increased Persistence of UVB Induced DNA Damage. PLoS Pathog 8: e1002807. doi: 10.1371/journal.ppat.1002807 22807682
30. Wallace NA, Robinson K, Galloway DA, (2014) Beta human papillomavirus E6 expression inhibits stabilization of p53 and increases tolerance of genomic instability. J Virol 88: 6112–6127. doi: 10.1128/JVI.03808-13 24648447
31. 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. 15150558
32. 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. doi: 10.1371/journal.ppat.1002211 21901101
33. 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. 9925639
34. Liang F, Han M, Romanienko PJ, Jasin M, (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A 95: 5172–5177. 9560248
35. Kakarougkas A, Jeggo PA, (2014) DNA DSB repair pathway choice: an orchestrated handover mechanism. Br J Radiol 87: 20130685. doi: 10.1259/bjr.20130685 24363387
36. Kass EM, Jasin M, (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584: 3703–3708. doi: 10.1016/j.febslet.2010.07.057 20691183
37. Lieber MR, Wilson TE, (2010) SnapShot: Nonhomologous DNA end joining (NHEJ). Cell 142: 496–496 e491. doi: 10.1016/j.cell.2010.07.035 20691907
38. Mazon G, Mimitou EP, Symington LS, (2010) SnapShot: Homologous recombination in DNA double-strand break repair. Cell 142: 646, 646 e641. doi: 10.1016/j.cell.2010.08.006 20723763
39. Ogiwara H, Kohno T, (2012) CBP and p300 histone acetyltransferases contribute to homologous recombination by transcriptionally activating the BRCA1 and RAD51 genes. PLoS One 7: e52810. doi: 10.1371/journal.pone.0052810 23285190
40. Di LJ, Fernandez AG, De Siervi A, Longo DL, Gardner K, (2010) Transcriptional regulation of BRCA1 expression by a metabolic switch. Nat Struct Mol Biol 17: 1406–1413. doi: 10.1038/nsmb.1941 21102443
41. Chen L, Nievera CJ, Lee AY, Wu X, (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 283: 7713–7720. doi: 10.1074/jbc.M710245200 18171670
42. Zhang J, Willers H, Feng Z, Ghosh JC, Kim S, et al. (2004) Chk2 phosphorylation of BRCA1 regulates DNA double-strand break repair. Mol Cell Biol 24: 708–718. 14701743
43. Sugiyama T, Zaitseva EM, Kowalczykowski SC, (1997) A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J Biol Chem 272: 7940–7945. 9065463
44. Zou Y, Liu Y, Wu X, Shell SM, (2006) Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J Cell Physiol 208: 267–273. 16523492
45. Zhang F, Fan Q, Ren K, Andreassen PR, (2009) PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 7: 1110–1118. doi: 10.1158/1541-7786.MCR-09-0123 19584259
46. Zhang F, Ma J, Wu J, Ye L, Cai H, et al. (2009) PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr Biol 19: 524–529. doi: 10.1016/j.cub.2009.02.018 19268590
47. Baumann P, Benson FE, West SC, (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87: 757–766. 8929543
48. Benson FE, Stasiak A, West SC, (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. Embo Journal 13: 5764–5771. 7988572
49. Gupta RC, Bazemore LR, Golub EI, Radding CM, (1997) Activities of human recombination protein Rad51. Proc Natl Acad Sci U S A 94: 463–468. 9012806
50. Pierce AJ, Johnson RD, Thompson LH, Jasin M, (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13: 2633–2638. 10541549
51. 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. 9488723
52. Huyen Y, Zgheib O, Ditullio RA, Jr.Gorgoulis VG, Zacharatos P, et al. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406–411. 15525939
53. 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. 16912319
54. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886–895. 10959836
55. Caestecker KW, Van de Walle GR, (2013) The role of BRCA1 in DNA double-strand repair: past and present. Exp Cell Res 319: 575–587. doi: 10.1016/j.yexcr.2012.11.013 23200932
56. Iyer NG, Chin SF, Ozdag H, Daigo Y, Hu DE, et al. (2004) p300 regulates p53-dependent apoptosis after DNA damage in colorectal cancer cells by modulation of PUMA/p21 levels. Proc Natl Acad Sci U S A 101: 7386–7391. 15123817
57. Huang WC, Chen CC, (2005) Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol Cell Biol 25: 6592–6602. 16024795
58. D'Amours D, Desnoyers S, D'Silva I, Poirier GG, (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342 (Pt 2): 249–268. 10455009
59. Helleday T, Bryant HE, Schultz N, (2005) Poly(ADP-ribose) polymerase (PARP-1) in homologous recombination and as a target for cancer therapy. Cell Cycle 4: 1176–1178. 16123586
60. Wallace NA, Gasior SL, Faber ZJ, Howie HL, Deininger PL, et al. (2013) HPV 5 and 8 E6 expression reduces ATM protein levels and attenuates LINE-1 retrotransposition. Virology.
61. 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. 16397624
62. 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 Journal 10: 4129–4135. 1661671
63. Kessis TD, Slebos RJ, Nelson WG, Kastan MB, Plunkett BS, et al. (1993) Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc Natl Acad Sci U S A 90: 3988–3992. 8387205
64. 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. doi: 10.1128/JVI.00902-08 18715924
65. Thomas M, Banks L, (1998) Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 17: 2943–2954. 9881696
66. Wallace NA, Galloway DA, (2014) Manipulation of cellular DNA damage repair machinery facilitates propagation of human papillomaviruses. Semin Cancer Biol 26C: 30–42.
67. Boyer SN, Wazer DE, Band V, (1996) E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 56: 4620–4624. 8840974
68. Malanchi I, Accardi R, Diehl F, Smet A, Androphy E, et al. (2004) Human papillomavirus type 16 E6 promotes retinoblastoma protein phosphorylation and cell cycle progression. J Virol 78: 13769–13778. 15564485
69. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, et al. (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 17: 688–695. doi: 10.1038/nsmb.1831 20453858
70. Bunting SF, Callen E, Wong N, Chen HT, Polato F, et al. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243–254. doi: 10.1016/j.cell.2010.03.012 20362325
71. Daley JM, Sung P, (2014) 53BP1, BRCA1, and the choice between recombination and end joining at DNA double-strand breaks. Mol Cell Biol 34: 1380–1388. doi: 10.1128/MCB.01639-13 24469398