The HPV E6 oncoprotein targets histone methyltransferases for modulating specific gene transcription

Oncogene

Volumn 31, Issue 18, 2012, Pages 2335-2349

  Hsu, C H ^a   Peng, K L ^a,b   Jhang, H C ^a   Lin, C H ^a,c,d   Wu, S Y ^e   Chiang, C M ^e   Lee, S C ^c   Yu, W C Y ^d   Juan, L J ^a,b,c  

^a GENOMICS RESEARCH CENTER   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

chromatin; E6; HMT; HPV; p53

Indexed keywords

HISTONE METHYLTRANSFERASE; PROTEIN CARM1; PROTEIN E6; PROTEIN P53; PROTEIN PRMT1; PROTEIN SET7; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; EPIGENETICS; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS CELL TRANSFORMATION; WART VIRUS;

CELL TRANSFORMATION, VIRAL; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; ONCOGENE PROTEINS, VIRAL; PROTEIN-ARGININE N-METHYLTRANSFERASES; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

HUMAN PAPILLOMAVIRUS;

EID: 84861346513     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.415     Document Type: Article

References (62)

1. An W, Kim J, Roeder RG. (2004). Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117: 735-748. (Pubitemid 38748890)
2. Boisvert FM, Dery U, Masson JY, Richard S. (2005a). Arginine methylation of MRE11 by PRMT1 is required for DNA damage checkpoint control. Gene Dev 19: 671-676. (Pubitemid 40395078)
3. Boisvert FM, Rhie A, Richard S, Doherty AJ. (2005b). The GAR motif of 53BP1 is arginine methylated by PRMT1 and is necessary for 53BP1 DNA binding activity. Cell Cycle 4: 1834-1841. (Pubitemid 41827331)
4. Campos EI, Reinberg D. (2009). Histones: annotating chromatin. Annu Rev Genet 43: 559-599.
5. Camus S, Menendez S, Cheok CF, Stevenson LF, Lain S, Lane DP. (2007). Ubiquitin-independent degradation of p53 mediated by high-risk human papillomavirus protein E6. Oncogene 26: 4059-4070. (Pubitemid 46920172)
6. Chen DG, Ma H, Hong H, Koh SS, Huang SM, Schurter BT ,et al. (1999). Regulation of transcription by a protein methyltransferase. Science 284: 2174-2177. (Pubitemid 29297477)
7. Chen YC, Chen JH, Richard K, Chen PY, Christiani DC. (2004). Lung adenocarcinoma and human papillomavirus infection. Cancer 101: 1428-1436. (Pubitemid 39180399)
8. Chuikov S, Kurash JK, Wilson JR, Xiao B, Justin N, Ivanov GS ,et al. (2004). Regulation of p53 activity through lysine methylation. Nature 432: 353-360. (Pubitemid 39551664)
9. 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 transactivation. Cell 67: 547-556. (Pubitemid 121001469)
10. Ea CK, Baltimore D. (2009). Regulation of NF-kappa B activity through lysine monomethylation of p65. Proc Natl Acad Sci USA 106: 18972-18977.
11. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM,et al.1993 WAF1, a potential mediator of p53 tumor suppression. Cell,75, 817-825. (Pubitemid 23346378)
12. Esteve PO, Chin HG, Benner J, Feehery GR, Samaranayake M, Horwitz GA ,et al. (2009). Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc Natl Acad Sci USA 106: 5076-5081.
13. Ganguly N, Parihar SP. (2009). Human papillomavirus E6 and E7 oncoproteins as risk factors for tumorigenesis. J Biosci 34: 113-123.
14. Ghosh MK, Harter ML. (2003). A viral mechanism for remodeling chromatin structure in G0 cells. Mol Cell 12: 255-260. (Pubitemid 36945049)
15. Howie HL, Katzenellenbogen RA, Galloway DA. (2009). Papillomavirus E6 proteins. Virology 384: 324-334.
16. Howley PM. (2006). Warts, cancer and ubiquitylation: lessons from the papillomaviruses. Trans Am Clin Climatol Assoc 117: 113-126; discussion 126-127.
17. Howley PM, Livingston DM. (2009). Small DNA tumor viruses: large contributors to biomedical sciences. Virology 384: 256-259.
18. Hsu CH, Chang MD, Tai KY, Yang YT, Wang PS, Chen CJ ,et al. (2004). HCMV IE2-mediated inhibition of HAT activity downregulates p53 function. EMBO J 23: 2269-2280. (Pubitemid 38833236)
19. Hu D, Goldie S. (2008). The economic burden of noncervical human papillomavirus disease in the United States. Am J Obstet Gynecol 198: 500.e1-500.e7.
20. Huang J, Perez-Burgos L, Placek BJ, Sengupta R, Richter M, Dorsey JA ,et al. (2006). Repression of p53 activity by Smyd2-mediated methylation. Nature 444: 629-632. (Pubitemid 44864441)
21. Ivanov GS, Ivanova T, Kurash J, Ivanov A, Chuikov S, Gizatullin F ,et al. (2007). Methylation-acetylation interplay activates p53 in response to DNA damage. Mol Cell Biol 27: 6756-6769. (Pubitemid 47483627)
22. Jha S, Pol SV, Banerjee NS, Dutta AB, Chow LT, Dutta A. (2010). Destabilization of TIP60 by human papillomavirus E6 results in attenuation of TIP60-dependent transcriptional regulation and apoptotic pathway. Mol Cell 38: 700-711.
23. Juan LJ, Shia WJ, Chen MH, Yang WM, Seto E, Lin YS ,et al. (2000). Histone deacetylases specifically downregulate p53-dependent gene activation. J Biol Chem 275: 20436-20443. (Pubitemid 30457621)
24. Kouskouti A, Scheer E, Staub A, Tora L, Talianidis I. (2004). Gene-specific modulation of TAF10 function by SET9-mediated methylation. Mol Cell 14: 175-182. (Pubitemid 38515645)
25. Kouzarides T. (2007). Chromatin modifications and their function. Cell 128: 693-705. (Pubitemid 46273577)
26. Kruse JP, Gu W. (2008). SnapShot: p53 posttranslational modifications. Cell 133: 930.e1.
27. Kurash JK, Lei H, Shen Q, Marston WL, Granda BW, Fan H ,et al. (2008). Methylation of p53 by Set7/9 mediates p53 acetylation and activity in vivo. Mol Cell 29: 392-400. (Pubitemid 351215939)
28. Lacey CJN, Lowndes CM, Shah KV. (2006). Burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine 24: 35-41.
29. Lee DY, Ianculescu I, Purcell D, Zhang X, Cheng XD, Stallcup MR. (2007). Surface-scanning mutational analysis of protein arginine methyltransferase 1: roles of specific amino acids in methyltransferase substrate specificity, oligomerization, and coactivator function. Mol Endocrinol 21: 1381-1393. (Pubitemid 46984744)
30. Lee YH, Koh SS, Zhang X, Cheng XD, Stallcup MR. (2002). Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol Cell Biol 22: 3621-3632. (Pubitemid 34525206)
31. Lee YH, Stallcup MR. (2009). Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol Endocrinol 23: 425-433.
32. Li M, Luo J, Brooks CL, Gu W. (2002). Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 277: 50607-50611. (Pubitemid 36042220)
33. Liang Y, Vogel JL, Narayanan A, Peng H, Kristie TM. (2009). Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat Med 15: 1312-1317.
34. 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. (Pubitemid 351380264)
35. McLaughlin-Drubin ME, Munger K. (2009). Oncogenic activities of human papillomaviruses. Virus Res 143: 195-208.
36. Miremadi A, Oestergaard MZ, Pharoah PDP, Caldas C. (2007). Cancer genetics of epigenetic genes. Hum Mol Genet 16: R28-R49. (Pubitemid 47241841)
37. Mujtaba S, Manzur KL, Gurnon JR, Kang M, Van Etten JL, Zhou MM. (2008). Epigenetic transcriptional repression of cellular genes by a viral SET protein. Nat Cell Biol 10: 1114-1122.
38. Munger K, Howley PM. (2002). Human papillomavirus immortalization and transformation functions. Virus Res 89: 213-228. (Pubitemid 35351540)
39. Nishioka K, Chuikov S, Sarma K, Erdjument-Bromage H, Allis CD, Tempst P ,et al. (2002). Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Gene Dev 16: 479-489. (Pubitemid 34165104)
40. Nomine Y, Masson M, Charbonnier S, Zanier K, Ristriani T, Deryckere F ,et al. (2006). Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirus-mediated pathogenesis. Mol Cell 21: 665-678. (Pubitemid 43290733)
41. Ou YH, Chung PH, Sun TP, Shieh SY. (2005). p53 C-terminal phosphorylation by CHK1 and CHK2 participates in the regulation of DNA-damage-induced C-terminal acetylation. Mol Biol Cell 16: 1684-1695.
42. Pahlich S, Zakaryan RP, Gehring H. (2006). Protein arginine methylation: cellular functions and methods of analysis. Biochim Biophys Acta 1764: 1890-1903. (Pubitemid 44895022)
43. Pal S, Sif S. (2007). Interplay between chromatin remodelers and protein arginine methyltransferases. J Cell Physiol 213: 306-315. (Pubitemid 47509707)
44. 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. (Pubitemid 29443808)
45. Pim D, Banks L. (2010). Interaction of viral oncoproteins with cellular target molecules: infection with high-risk vs low-risk human papillomaviruses. APMIS 118: 471-493.
46. Pradhan S, Chin HG, Esteve PO, Jacobsen SE. (2009). SET7/9 mediated methylation of non-histone proteins in mammalian cells. Epigenetics 4: 282-285.
47. Reeves M, Murphy J, Greaves R, Fairley J, Brehm A, Sinclair J. (2006). Autorepression of the human cytomegalovirus major immediate-early promoter/enhancer at late times of infection is mediated by the recruitment of chromatin remodeling enzymes by IE86. J Virol 80: 9998-10009. (Pubitemid 44522594)
48. 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. (Pubitemid 120035062)
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. (Pubitemid 23335075)
50. Shukla A, Chaurasia P, Bhaumik SR. (2009). Histone methylation and ubiquitination with their cross-talk and roles in gene expression and stability. Cell Mol Life Sci 66: 1419-1433.
51. Strahl BD, Allis CD. (2000). The language of covalent histone modifications. Nature 403: 41-45. (Pubitemid 30038513)
52. Strahl BD, Briggs SD, Brame CJ, Caldwell JA, Koh SS, Ma H ,et al. (2001). Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr Biol 11: 996-1000. (Pubitemid 32589194)
53. Subramanian K, Jia D, Kapoor-Vazirani P, Powell DR, Collins RE, Sharma D ,et al. (2008). Regulation of estrogen receptor alpha by the SET7 lysine methyltransferase. Mol Cell 30: 336-347. (Pubitemid 351615317)
54. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF. (1984). Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase-II. Science 226: 466-468. (Pubitemid 14012819)
55. 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. (Pubitemid 40138619)
56. Trojer P, Reinberg D. (2007). Facultative heterochromatin: is there a distinctive molecular signature? Mol Cell 28: 1-13. (Pubitemid 47531977)
57. Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P ,et al. (2001). Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8: 1207-1217. (Pubitemid 34084993)
58. Wang YH, Tsay YG, Tan BC, Lo WY, Lee SC. (2003). Identification and characterization of a novel p300-mediated p53 acetylation site, lysine 305. J Biol Chem 278: 25568-25576. (Pubitemid 36835309)
59. Wolf SS. (2009). The protein arginine methyltransferase family: an update about function, new perspectives and the physiological role in humans. Cell Mol Life Sci 66: 2109-2121.
60. Yang XD, Huang B, Li MX, Lamb A, Kelleher NL, Chen LF. (2009). Negative regulation of NF-kappa B action by Set9-mediated lysine methylation of the RelA subunit. EMBO J 28: 1055-1066.
61. Yu ZB, Chen TP, Hebert J, Li E, Richard S. (2009). A mouse PRMT1 null allele defines an essential role for arginine methylation in genome maintenance and cell proliferation.Mol Cell Biol 29: 2982-2996.
62. Zimmermann H, Degenkolbe R, Bernard HU, O'Connor MJ. (1999). The human papillomavirus type 16 E6 oncoprotein can downregulate p53 activity by targeting the transcriptional coactivator CBP/p300. J Virol 73: 6209-6219. (Pubitemid 29327795)