A functional interaction of E7 with B-Myb-MuvB complex promotes acute cooperative transcriptional activation of both S- and M-phase genes

Oncogene

Volumn 33, Issue 31, 2014, Pages 4039-4049

  Pang, C L ^a,b   Toh, S Y ^a   He, P ^a   Teissier, S ^a   Ben Khalifa, Y ^c   Xue, Y ^a   Thierry, F ^a  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUT PASTEUR   (France)

Author keywords

B Myb; B Myb MuvB complex; Cervical carcinoma; FoxM1; HPV E7; Mitosis

Indexed keywords

PROTEIN E7; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR B MYB; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER STAGING; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CERVICAL CANCER CELL LINE; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VIVO STUDY; PRIMARY CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; UTERINE CERVIX CANCER;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HUMAN PAPILLOMAVIRUS 16; HUMANS; KERATINOCYTES; MITOSIS; MUTATION; NUCLEAR PROTEINS; PAPILLOMAVIRUS E7 PROTEINS; S PHASE; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEINS; UTERINE CERVICAL NEOPLASMS;

EID: 84905401162     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.426     Document Type: Article

References (46)

1. McLaughlin-Drubin ME, Munger K. The human papillomavirus E7 oncoprotein. Virology 2009; 384: 335-344.
2. Dowhanick JJ, McBride AA, Howley PM. Suppression of cellular proliferation by the papillomavirus E2 protein. J Virol 1995; 69: 7791-7799.
3. Desaintes C, Demeret C, Goyat S, Yaniv M, Thierry F. Expression of the papillo-mavirus E2 protein in HeLa cells leads to apoptosis. EMBO J 1997; 16: 504-514.
4. Johung K, Goodwin EC, Dimaio D. Human papillomavirus e7 repression in cervical carcinoma cells initiates a transcriptional cascade driven by the retinoblastoma family, resulting in senescence. J Virol 2007; 81: 2102-2116.
5. Wells SI, Aronow BJ, Wise TM, Williams SS, Couget JA, Howley PM. Transcriptome signature of irreversible senescence in human papillomavirus- positive cervical cancer cells. Proc Natl Acad Sci 2003; 100: 7093-7098.
6. Teissier S, Ben Khalifa Y, Mori M, Pautier P, Desaintes C, Thierry F. A new E6/P63 pathway, together with a strong E7/E2F mitotic pathway, modulates the transcriptome in cervical cancer cells. J Virol 2007; 81: 9368-9376.
7. Thierry F, Benotmane MA, Demeret C, Mori M, Teissier S, Desaintes C. A genomic approach reveals a novel mitotic pathway in papillomavirus carcinogenesis. Cancer Res 2004; 64: 895-903.
8. Lam EW, Morris JD, Davies R, Crook T, Watson RJ, Vousden KH. HPV16 E7 onco-protein deregulates B-myb expression: correlation with targeting of p107/E2F complexes. EMBO J 1994; 13: 871-878.
9. Luscher-Firzlaff JM, Westendorf JM, Zwicker J, Burkhardt H, Henriksson M, Muller R et al. Interaction of the fork head domain transcription factor MPP2 with the human papilloma virus 16 E7 protein: enhancement of transformation and transactivation. Oncogene 1999; 18: 5620-5630.
10. Tanaka Y, Patestos NP, Maekawa T, Ishii S. B-myb is required for inner cell mass formation at an early stage of development. J Biol Chem 1999; 274: 28067-28070.
11. Manak JR, Wen H, Van T, Andrejka L, Lipsick JS. Loss of Drosophila Myb interrupts the progression of chromosome condensation. Nat Cell Biol 2007; 9: 581-587.
12. Fung SM, Ramsay G, Katzen AL. Mutations in Drosophila myb lead to centrosome amplification and genomic instability. Development 2002; 129: 347-359.
13. Katzen AL, Jackson J, Harmon BP, Fung SM, Ramsay G, Bishop JM. Drosophila myb is required for the G2/M transition and maintenance of diploidy. Genes Dev 1998; 12: 831-843.
14. Shepard JL, Amatruda JF, Stern HM, Subramanian A, Finkelstein D, Ziai J et al. A zebrafish bmyb mutation causes genome instability and increased cancer susceptibility. Proc Natl Acad Sci USA 2005; 102: 13194-13199.
15. Georlette D, Ahn S, MacAlpine DM, Cheung E, Lewis PW, Beall EL et al. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 2007; 21: 2880-2896.
16. Pilkinton M, Sandoval R, Colamonici OR. Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 2007; 26: 7535-7543.
17. Pilkinton M, Sandoval R, Song J, Ness SA, Colamonici OR. Mip/LIN-9 regulates the expression of B-Myb and the induction of cyclin A, cyclin B, and CDK1. J Biol Chem 2007; 282: 168-175.
18. Osterloh L, von Eyss B, Schmit F, Rein L, Hubner D, Samans B et al. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J 2007; 26: 144-157.
19. Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B et al. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 2007; 6: 1903-1913.
20. Martinez I, Dimaio D. B-Myb, cancer, senescence, and microRNAs. Cancer Res 2011; 71: 5370-5373.
21. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 2005; 7: 126-136.
22. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ et al. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol 2005; 25: 10875-10894.
23. Down CF, Millour J, Lam EW, Watson RJ. Binding of FoxM1 to G2/M gene promoters is dependent upon B-Myb. Biochim Biophys Acta 2012; 1819: 855-862.
24. Sadasivam S, Duan S, Decaprio JA. The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev 2012; 26: 474-489.
25. Huang C, Qiu Z, Wang L, Peng Z, Jia Z, Logsdon CD et al. A novel FoxM1-caveolin signaling pathway promotes pancreatic cancer invasion and metastasis. Cancer Res 2012; 72: 655-665.
26. Alvarez-Fernandez M, Halim VA, Krenning L, Aprelia M, Mohammed S, Heck AJ et al. Recovery from a DNA-damage-induced G2 arrest requires Cdk-dependent activation of FoxM1. EMBO Rep 2010; 11: 452-458.
27. Li Q, Zhang N, Jia Z, Le X, Dai B, Wei D et al. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res 2009; 69: 3501-3509.
28. Kim IM, Ackerson T, Ramakrishna S, Tretiakova M, Wang IC, Kalin TV et al. The Forkhead Box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res 2006; 66: 2153-2161.
29. Teh MT, Wong ST, Neill GW, Ghali LR, Philpott MP, Quinn AG. FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res 2002; 62: 4773-4780.
30. Kalinichenko VV, Major ML, Wang X, Petrovic V, Kuechle J, Yoder HM et al. Foxm1b transcription factor is essential for development of hepatocellular carcinomas and is negatively regulated by the p19ARF tumor suppressor. Genes Dev 2004; 18: 830-850.
31. Chan DW, Yu SY, Chiu PM, Yao KM, Liu VW, Cheung AN et al. Over-expression of FOXM1 transcription factor is associated with cervical cancer progression and pathogenesis. J Pathol 2008; 215: 245-252.
32. Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S et al. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 2007; 26: 539-551.
33. Nor Rashid N, Yusof R, Watson RJ. Disruption of repressive p130-DREAM complexes by human papillomavirus 16 E6/E7 oncoproteins is required for cell-cycle progression in cervical cancer cells. J Gen Virol 2011; 92: 2620-2627.
34. Phelps WC, Munger K, Yee CL, Barnes JA, Howley PM. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J Virol 1992; 66: 2418-2427.
35. Psyrri A, DeFilippis RA, Edwards AP, Yates KE, Manuelidis L, DiMaio D. Role of the retinoblastoma pathway in senescence triggered by repression of the human papillomavirus E7 protein in cervical carcinoma cells. Cancer Res 2004; 64: 3079-3086.
36. Sage J, Mulligan GJ, Attardi LD, Miller A, Chen S, Williams B et al. Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev 2000; 14: 3037-3050.
37. Shin MK, Sage J, Lambert PF. Inactivating all three rb family pocket proteins is insufficient to initiate cervical cancer. Cancer Res 2012; 72: 5418-5427.
38. Xue Y, Lim D, Zhi L, He P, Abastado JP, Thierry F. Loss of HPV16 E2 protein expression without disruption of the E2 ORF correlates with carcinogenic progression. Open Virol J 2012; 6: 163-172.
39. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008; 26: 317-325.
40. Peter M, Stransky N, Couturier J, Hupe P, Barillot E, de Cremoux P et al. Frequent genomic structural alterations at HPV insertion sites in cervical carcinoma. J Pathol 2010; 221: 320-330.
41. Ueno T, Sasaki K, Yoshida S, Kajitani N, Satsuka A, Nakamura H et al. Molecular mechanisms of hyperplasia induction by human papillomavirus E7. Oncogene 2006; 25: 4155-4164.
42. Balsitis SJ, Sage J, Duensing S, Munger K, Jacks T, Lambert PF. Recapitulation of the effects of the human papillomavirus type 16 E7 oncogene on mouse epithelium by somatic Rb deletion and detection of pRb-independent effects of E7 in vivo. Mol Cell Biol 2003; 23: 9094-9103.
43. Buitrago-Perez A, Hachimi M, Duenas M, Lloveras B, Santos A, Holguin A et al. A humanized mouse model of HPV-associated pathology driven by E7 expression. PLoS One 2012; 7: e41743.
44. Caldeira S, de Villiers EM, Tommasino M. Human papillomavirus E7 proteins stimulate proliferation independently of their ability to associate with retino-blastoma protein. Oncogene 2000; 19: 821-826.
45. Halbert CL, Demers GW, Galloway DA. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol 1991; 65: 473-478.
46. Teissier S, Pang CL, Thierry F. The E2F5 repressor is an activator of E6/E7 transcription and of the S-phase entry in HPV18-associated cells. Oncogene 2010; 29: 5061-5070.