A novel MLL5 isoform that is essential to activate E6 and E7 transcription in HPV16/18-associated cervical cancers

Cancer Research

Volumn 71, Issue 21, 2011, Pages 6696-6707

  Yew, Chow Wenn ^a   Lee, Pei ^a   Chan, Wai Keong ^a   Lim, Vania Kai Jun ^a   Tay, Sun Kuie ^b   Tan, Theresa M C ^a   Deng, Lih Wen ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN E6; PROTEIN E7; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR AP 1;

APOPTOSIS; ARTICLE; BINDING SITE; CANCER CELL CULTURE; CARCINOMA CELL; CELL CYCLE; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN TISSUE; MIXED LINEAGE LEUKEMIA 5 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; ONCOGENE E6; ONCOGENE E7; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CARCINOMA;

CARCINOMA, SQUAMOUS CELL; CODON, NONSENSE; DNA-BINDING PROTEINS; EXONS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GENE KNOCKDOWN TECHNIQUES; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION MAPPING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; UTERINE CERVICAL NEOPLASMS;

EID: 80155184163     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1271     Document Type: Article

References (49)

1. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9. (Pubitemid 29406813)
2. zur Hausen H. Viruses in human cancers. Science 1991;254:1167-73.
3. Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J Virol 1989;63:4417-21. (Pubitemid 19229441)
4. Narisawa-Saito M, Kiyono T. Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci 2007;98:1505-11. (Pubitemid 47308443)
5. Incassati A, Patel D, McCance DJ. Induction of tetraploidy through loss of p53 and upregulation of Plk1 by human papillomavirus type-16 E6. Oncogene 2006;25:2444-51.
6. Romanczuk H, Villa LL, Schlegel R, Howley PM. The viral transcriptional regulatory region upstream of the E6 and E7 genes is a major determinant of the differential immortalization activities of human papillomavirus types 16 and 18. J Virol 1991;65:2739-44.
7. Schneider-Gadicke A, Schwarz E. Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. EMBO J 1986;5:2285-92.
8. Smotkin D, Wettstein FO. 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 U S A 1986;83: 4680-4. (Pubitemid 16075465)
9. Chong T, Apt D, Gloss B, Isa M, Bernard HU. The enhancer of human papillomavirus type 16: binding sites for the ubiquitous transcription factors oct-1, NFA, TEF-2, NF1, and AP-1 participate in epithelial cellspecific transcription. J Virol 1991;65:5933-43.
10. Nakshatri H, Pater MM, Pater A. Ubiquitous and cell-type-specific protein interactions with human papillomavirus type 16 and type 18 enhancers. Virology 1990;178:92-103. (Pubitemid 20276671)
11. Sibbet GJ, Campo MS. Multiple interactions between cellular factors and the non-coding region of human papillomavirus type 16. J Gen Virol 1990;71:2699-707. (Pubitemid 20370515)
12. Fischer K, Frohling S, Scherer SW, McAllister Brown J, Scholl C, Stilgenbauer S, et al. Molecular cytogenetic delineation of deletions and translocations involving chromosome band 7q22 in myeloid leukemias. Blood 1997;89:2036-41. (Pubitemid 27132119)
13. Emerling BM, Bonifas J, Kratz CP, Donovan S, Taylor BR, Green ED, et al. MLL5, a homolog of Drosophila trithorax located within a segment of chromosome band 7q22 implicated in myeloid leukemia. Oncogene 2002;21:4849-54. (Pubitemid 34879461)
14. Hughes CL, Liu PZ, Kaufman TC. Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol Dev 2004;6:393-401. (Pubitemid 39554254)
15. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem 2007;282:4408-16. (Pubitemid 47100929)
16. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, et al. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 2004;24:5639-49. (Pubitemid 38787950)
17. Madan V, Madan B, Brykczynska U, Zilbermann F, Hogeveen K, Dohner K, et al. Impaired function of primitive hematopoietic cells in mice lacking the Mixed-Lineage-Leukemia homolog MLL5. Blood 2009;113:1444-54.
18. Fujiki R, Chikanishi T, Hashiba W, Ito H, Takada I, Roeder RG, et al. GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature 2009;459:455-9.
19. Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, Pavlath GK, et al. MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci U S A 2009;106:4719-24.
20. Pijnappel WW, Schaft D, Roguev A, Shevchenko A, Tekotte H, Wilm M, et al. The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev 2001;15:2991-3004. (Pubitemid 33078949)
21. Zhang Y, Wong J, Klinger M, Tran MT, Shannon KM, Killeen N. MLL5 contributes to hematopoietic stem cell fitness and homeostasis. Blood 2009;113:1455-63.
22. Heuser M, Yap DB, Leung M, de Algara TR, Tafech A, McKinney S, et al. Loss of MLL5 results in pleiotropic hematopoietic defects, reduced neutrophil immune function, and extreme sensitivity to DNA demethylation. Blood 2009;113:1432-43.
23. Damm F, Oberacker T, Thol F, Surdziel E, Wagner K, Chaturvedi A, et al. Prognostic importance of histone methyltransferase MLL5 expression in acute myeloid leukemia. J Clin Oncol 2011;29: 682-9.
24. Deng LW, Chiu I, Strominger JL. MLL 5 protein forms intranuclear foci, and overexpression inhibits cell cycle progression. Proc Natl Acad Sci U S A 2004;101:757-62. (Pubitemid 38121031)
25. Cheng F, Liu J, Zhou SH, Wang XN, Chew JF, Deng LW. RNA interference against mixed lineage leukemia 5 resulted in cell cycle arrest. Int J Biochem Cell Biol 2008;40:2472-81.
26. Liu J, Wang XN, Cheng F, Liou YC, Deng LW. Phosphorylation of mixed lineage leukemia 5 by CDC2 affects its cellular distribution and is required for mitotic entry. J Biol Chem 2010;285:20904-14.
27. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, et al. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004;116:499-509. (Pubitemid 38264428)
28. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B, Stremlau A, et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985;314:111-4. (Pubitemid 15142033)
29. Yasumoto S, Taniguchi A, Sohma K. Epidermal growth factor (EGF) elicits down-regulation of human papillomavirus type 16 (HPV-16) E6/ E7 mRNA at the transcriptional level in an EGF-stimulated human keratinocyte cell line: functional role of EGF-responsive silencer in the HPV-16 long control region. J Virol 1991;65:2000-9.
30. Lace MJ, Anson JR, Haugen TH, Turek LP. Interferon regulatory factor (IRF)-2 activates the HPV-16 E6-E7 promoter in keratinocytes. Virology 2010;399:270-9.
31. Howley PM. Role of the human papillomaviruses in human cancer. Cancer Res 1991;51:5019s-22s.
32. Farre D, Roset R, Huerta M, Adsuara JE, Rosello L, Alba MM, et al. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 2003;31: 3651-3. (Pubitemid 37442215)
33. Nakamura T, Mori T, Tada S, Krajewski W, Rozovskaia T, Wassell R, et al. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol Cell 2002;10:1119-28. (Pubitemid 35453829)
34. Ansari KI, Mandal SS. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J 2010;277: 1790-804.
35. Jiang M, Milner J. Selective silencing of viral gene expression in HPVpositive human cervical carcinoma cells treated with siRNA, a primer of RNA interference. Oncogene 2002;21:6041-8.
36. Jonson AL, Rogers LM, Ramakrishnan S, Downs LS Jr. Gene silencing with siRNA targeting E6/E7 as a therapeutic intervention in a mouse model of cervical cancer. Gynecol Oncol 2008;111:356-64.
37. Yamato K, Yamada T, Kizaki M, Ui-Tei K, Natori Y, Fujino M, et al. New highly potent and specific E6 and E7 siRNAs for treatment of HPV16 positive cervical cancer. Cancer Gene Ther 2008;15:140-53. (Pubitemid 351240669)
38. Sakurai Y, Komatsu K, Agematsu K, Matsuoka M. DNA double strand break repair enzymes function at multiple steps in retroviral infection. Retrovirology 2009;6:114.
39. Smith CE, Lam AF, Symington LS. Aberrant double-strand break repair resulting in half crossovers in mutants defective for Rad51 or the DNA polymerase delta complex. Mol Cell Biol 2009;29:1432-41.
40. Thorland EC, Myers SL, Persing DH, Sarkar G, McGovern RM, Gostout BS, et al. Human papillomavirus type 16 integrations in cervical tumors frequently occur in common fragile sites. Cancer Res 2000;60:5916-21.
41. Li H, Wang J, Mor G, Sklar J. A neoplastic gene fusion mimics transsplicing of RNAs in normal human cells. Science 2008;321:1357-61.
42. Caudevilla C, Serra D, Miliar A, Codony C, Asins G, Bach M, et al. Natural trans-splicing in carnitine octanoyltransferase pre-mRNAs in rat liver. Proc Natl Acad Sci U S A 1998;95:12185-90. (Pubitemid 28483740)
43. Cripe TP, Alderborn A, Anderson RD, Parkkinen S, Bergman P, Haugen TH, et al. Transcriptional activation of the human papillomavirus-16 P97 promoter by an 88-nucleotide enhancer containing distinct cell-dependent and AP-1-responsive modules. New Biol 1990;2:450-63. (Pubitemid 20235658)
44. Gloss B, Bernard HU. The E6/E7 promoter of human papillomavirus type 16 is activated in the absence of E2 proteins by a sequence-aberrant Sp1 distal element. J Virol 1990;64:5577-84. (Pubitemid 20364552)
45. Thierry F, Spyrou G, Yaniv M, Howley P. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J Virol 1992;66:3740-8.
46. Chin MT, Broker TR, Chow LT. Identification of a novel constitutive enhancer element and an associated binding protein: implications for human papillomavirus type 11 enhancer regulation. J Virol 1989;63: 2967-76. (Pubitemid 19156016)
47. Cripe TP, Haugen TH, Turk JP, Tabatabai F, Schmid PG III, Durst M, et al. Transcriptional regulation of the human papillomavirus-16 E6-E7 promoter by a keratinocyte-dependent enhancer, and by viral E2 transactivator and repressor gene products: implications for cervical carcinogenesis. EMBO J 1987;6:3745-53.
48. Demeret C, Yaniv M, Thierry F. The E2 transcriptional repressor can compensate for Sp1 activation of the human papillomavirus type 18 early promoter. J Virol 1994;68:7075-82. (Pubitemid 24328758)
49. Stunkel W, Bernard HU. The chromatin structure of the long control region of human papillomavirus type 16 represses viral oncoprotein expression. J Virol 1999;73:1918-30. (Pubitemid 29098093)