E2F1-mediated apoptosis as a target of cancer therapy

Current Molecular Pharmacology

Volumn 2, Issue 2, 2009, Pages 149-160

  Wu, Zhenlong ^a   Yu, Qiang ^a  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

Apoptosis; Cancer; E2f1; Therapeutic target

Indexed keywords

ANTINEOPLASTIC AGENT; BETA LAPACHONE; HISTONE DEACETYLASE INHIBITOR; NUTLIN 3; PROTEIN BCL 2; PROTEIN P53; SIRTUIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR E2F4; TRANSCRIPTION FACTOR E2F5; TRANSCRIPTION FACTOR E2F6; TRANSCRIPTION FACTOR E2F7; TRANSCRIPTION FACTOR E2F8; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER THERAPY; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; DNA BINDING; DNA DAMAGE; DRUG POTENTIATION; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; METABOLISM; NEOPLASM; PHYSIOLOGY; REVIEW;

APOPTOSIS; DNA DAMAGE; E2F1 TRANSCRIPTION FACTOR; HISTONE DEACETYLASE INHIBITORS; HUMANS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77449141085     PISSN: 18744672     EISSN: 18744702     Source Type: Journal    
DOI: 10.2174/1874467210902020149     Document Type: Article

References (143)

1. La Thangue, N. B.; Rigby, P. W. An adenovirus E1A-like transcription factor is regulated during the differentiation of murine embryonal carcinoma stem cells. Cell 1987, 49, 507-513.
2. Yee, A. S.; Reichel, R.; Kovesdi, I.; Nevins, J. R. Promoter interaction of the E1A-inducible factor E2F and its potential role in the formation of a multi-component complex. EMBO J. 1987, 6, 2061-2068.
3. Kovesdi, I.; Reichel, R.; Nevins, J. R. Role of an adenovirus E2 promoter binding factor in E1A-mediated coordinate gene control. Proc. Natl. Acad. Sci. USA 1987, 84, 2180-2184.
4. Stanelle, J.; Putzer, B. M. E2F1-induced apoptosis: turning killers into therapeutics. Trends Mol. Med. 2006, 12, 177-185.
5. Rowland, B. D.; Bernards, R. Re-evaluating cell-cycle regulation by E2Fs. Cell 2006, 127, 871-874.
6. Dimova, D. K.; Dyson, N. J. The E2F transcriptional network: old acquaintances with new faces. Oncogene 2005, 24, 2810-2826.
7. DeGregori, J.; Johnson, D. G. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 2006, 6, 739-748.
8. Trimarchi, J. M.; Fairchild, B.; Wen, J.; Lees, J. A. The E2F6 transcription factor is a component of the mammalian Bmi1-containing polycomb complex. Proc. Natl. Acad. Sci. USA 2001, 98, 1519-1524.
9. Frolov, M. V.; Dyson, N. J. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 2004, 117, 2173-2181.
10. Ferreira, R.; Naguibneva, I.; Mathieu, M.; Ait-Si-Ali, S.; Robin, P.; Pritchard, L. L.; Harel-Bellan, A. Cell cycle-dependent recruitment of HDAC-1 correlates with deacetylation of histone H4 on an Rb-E2F target promoter. EMBO Rep. 2001, 2, 794-799.
11. Helin, K. Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev. 1998, 8, 28-35.
12. Dyson, N. The regulation of E2F by pRB-family proteins. Genes Dev. 1998, 12, 2245-2262.
13. Stevaux, O.; Dyson, N. J. A revised picture of the E2F transcriptional network and RB function. Curr. Opin. Cell Biol. 2002, 14, 684-691.
14. Bracken, A. P.; Ciro, M.; Cocito, A.; Helin, K. E2F target genes: unraveling the biology. Trends Biochem. Sci. 2004, 29, 409-417.
15. Trimarchi, J. M.; Lees, J. A. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 2002, 3, 11-20.
16. Narita, M.; Nunez, S.; Heard, E.; Narita, M.; Lin, A. W.; Hearn, S. A.; Spector, D. L.; Hannon, G. J.; Lowe, S. W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 113, 703-716.
17. Stevens, C.; La Thangue, N. B. The emerging role of E2F-1 in the DNA damage response and checkpoint control. DNA Repair (Amst.) 2004, 3, 1071-1079.
18. Stevens, C.; La Thangue, N. B. E2F and cell cycle control: a dou-ble-edged sword. Arch. Biochem. Biophys. 2003, 412, 157-169.
19. Singh, P.; Wong, S. H.; Hong, W. Overexpression of E2F-1 in rat embryo fibroblasts leads to neoplastic transformation. EMBO J. 1994, 13, 3329-3338.
20. Johnson, D. G.; Cress, W. D.; Jakoi, L.; Nevins, J. R. Oncogenic capacity of the E2F1 gene. Proc. Natl. Acad. Sci. USA 1994, 91, 12823-12827.
21. Miyajima, M.; Nornes, H. O.; Sato, K.; Neuman, T. Overexpression of E2F1 in astrocytes leads to neoplastic transformation and changes in expression of retinoblastoma family members. J. Neuro. sci. Res. 1996, 46, 108-113.
22. Xu, G.; Livingston, D. M.; Krek, W. Multiple members of the E2F transcription factor family are the products of oncogenes. Proc. Natl. Acad. Sci. USA 1995, 92, 1357-1361.
23. Yamasaki, L.; Bronson, R.; Williams, B. O.; Dyson, N. J.; Harlow, E.; Jacks, T. Loss of E2F-1 reduces tumorigenesis and extends the lifespan of Rb1(+/-)mice. Nat. Genet. 1998, 18, 360-364.
24. Hall, M.; Peters, G. Genetic alterations of cyclins, cyclin-dependent kinases, and Cdk inhibitors in human cancer. Adv. Cancer Res. 1996, 68, 67-108.
25. Sherr, C. J. Cancer cell cycles. Science 1996, 274, 1672-1677.
26. Vogelstein, B.; Kinzler, K. W. Cancer genes and the pathways they control. Nat. Med. 2004, 10, 789-799.
27. Johnson, D. G.; Degregori, J. Putting the oncogenic and tumor suppressive activities of E2F into context. Curr. Mol. Med. 2006, 6, 731-738.
28. Pickering, M. T.; Kowalik, T. F. Rb inactivation leads to E2F1-mediated DNA double-strand break accumulation. Oncogene 2006, 25, 746-755.
29. Czermin, B.; Melfi, R.; McCabe, D.; Seitz, V.; Imhof, A.; Pirrotta, V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002, 111, 185-196.
30. Cao, R.; Wang, L.; Wang, H.; Xia, L.; Erdjument-Bromage, H.; Tempst, P.; Jones, R. S.; Zhang, Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298, 1039-1043.
31. Bracken, A. P.; Pasini, D.; Capra, M.; Prosperini, E.; Colli, E.; Helin, K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 2003, 22, 5323-5335.
32. Bracken, A. P.; Kleine-Kohlbrecher, D.; Dietrich, N.; Pasini, D.; Gargiulo, G.; Beekman, C.; Theilgaard-Monch, K.; Minucci, S.; Porse, B. T.; Marine, J. C.; Hansen, K. H.; Helin, K. The Polycomb group proteins bind throughout the INK4A-ARF locus and are dis-associated in senescent cells. Genes Dev. 2007, 21, 525-530.
33. Shan, B.; Lee, W. H. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell Biol. 1994, 14, 8166-8173.
34. Wu, X.; Levine, A. J. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 1994, 91, 3602-3606.
35. Pan, H.; Yin, C.; Dyson, N. J.; Harlow, E.; Yamasaki, L.; Van Dyke, T. Key roles for E2F1 in signaling p53-dependent apoptosis and in cell division within developing tumors. Mol. Cell 1998, 2, 283-292.
36. Tsai, K. Y.; Hu, Y.; Macleod, K. F.; Crowley, D.; Yamasaki, L.; Jacks, T. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell 1998, 2, 293-304.
37. Dimri, G. P.; Itahana, K.; Acosta, M.; Campisi, J. Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14(ARF) tumor suppressor. Mol. Cell Biol. 2000, 20, 273-285.
38. Pediconi, N.; Ianari, A.; Costanzo, A.; Belloni, L.; Gallo, R.; Cimino, L.; Porcellini, A.; Screpanti, I.; Balsano, C.; Alesse, E.; Gulino, A.; Levrero, M. Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat. Cell Biol. 2003, 5, 552-558.
39. Frame, F. M.; Rogoff, H. A.; Pickering, M. T.; Cress, W. D.; Kowalik, T. F. E2F1 induces MRN foci formation and a cell cycle checkpoint response in human fibroblasts. Oncogene 2006, 25, 3258-3266.
40. Qin, X. Q.; Livingston, D. M.; Kaelin, W. G., Jr.; Adams, P. D. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 1994, 91, 10918-10922.
41. Du, W.; Xie, J. E.; Dyson, N. Ectopic expression of dE2F and dDP induces cell proliferation and death in the Drosophila eye. EMBO J. 1996, 15, 3684-3692.
42. Kowalik, T. F.; DeGregori, J.; Schwarz, J. K.; Nevins, J. R. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 1995, 69, 2491-2500.
43. Yamasaki, L.; Jacks, T.; Bronson, R.; Goillot, E.; Harlow, E.; Dyson, N. J. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 1996, 85, 537-548.
44. Field, S. J.; Tsai, F. Y.; Kuo, F.; Zubiaga, A. M.; Kaelin, W. G., Jr.; Livingston, D. M.; Orkin, S. H.; Greenberg, M. E. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 1996, 85, 549-561.
45. DeGregori, J.; Leone, G.; Miron, A.; Jakoi, L.; Nevins, J. R. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 1997, 94, 7245-7250.
46. Dirks, P. B.; Rutka, J. T.; Hubbard, S. L.; Mondal, S.; Hamel, P. A. The E2F-family proteins induce distinct cell cycle regulatory factors in p16-arrested, U343 astrocytoma cells. Oncogene 1998, 17, 867-876.
47. Ziebold, U.; Reza, T.; Caron, A.; Lees, J. A. E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos. Genes Dev. 2001, 15, 386-391.
48. Kowalik, T. F.; DeGregori, J.; Leone, G.; Jakoi, L.; Nevins, J. R. E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ. 1998, 9, 113-118.
49. Lazzerini Denchi, E.; Helin, K. E2F1 is crucial for E2F-dependent apoptosis. EMBO Rep. 2005, 6, 661-668.
50. Hallstrom, T. C.; Nevins, J. R. Specificity in the activation and control of transcription factor E2F-dependent apoptosis. Proc. Natl. Acad. Sci. USA 2003, 100, 10848-10853.
51. Hallstrom, T. C.; Nevins, J. R. Jab1 is a specificity factor for E2F1-induced apoptosis. Genes Dev. 2006, 20, 613-623.
52. Weber, J. D.; Taylor, L. J.; Roussel, M. F.; Sherr, C. J.; Bar-Sagi, D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1999, 1, 20-26.
53. Bates, S.; Phillips, A. C.; Clark, P. A.; Stott, F.; Peters, G.; Ludwig, R. L.; Vousden, K. H. p14ARF links the tumour suppressors RB and p53. Nature 1998, 395, 124-125.
54. Sherr, C. J.; Weber, J. D. The ARF/p53 pathway. Curr. Opin. Genet. Dev. 2000, 10, 94-99.
55. Berkovich, E.; Lamed, Y.; Ginsberg, D. E2F and Ras synergize in transcriptionally activating p14ARF expression. Cell Cycle 2003, 2, 127-133.
56. Russell, J. L.; Powers, J. T.; Rounbehler, R. J.; Rogers, P. M.; Conti, C. J.; Johnson, D. G. ARF differentially modulates apoptosis induced by E2F1 and Myc. Mol. Cell Biol. 2002, 22, 1360-1368.
57. Seavey, S. E.; Holubar, M.; Saucedo, L. J.; Perry, M. E. The E7 oncoprotein of human papillomavirus type 16 stabilizes p53 through a mechanism independent of p19(ARF). J. Virol. 1999, 73, 7590-7598.
58. Tsai, K. Y.; MacPherson, D.; Rubinson, D. A.; Crowley, D.; Jacks, T. ARF is not required for apoptosis in Rb mutant mouse embryos. Curr. Biol. 2002, 12, 159-163.
59. Martelli, F.; Hamilton, T.; Silver, D. P.; Sharpless, N. E.; Bardeesy, N.; Rokas, M.; DePinho, R. A.; Livingston, D. M.; Grossman, S. R. p19ARF targets certain E2F species for degradation. Proc. Natl. Acad. Sci. USA 2001, 98, 4455-4460.
60. Datta, A.; Sen, J.; Hagen, J.; Korgaonkar, C. K.; Caffrey, M.; Quelle, D. E.; Hughes, D. E.; Ackerson, T. J.; Costa, R. H.; Raychaudhuri, P. ARF directly binds DP1: interaction with DP1 coincides with the G1 arrest function of ARF. Mol. Cell Biol. 2005, 25, 8024-8036.
61. Datta, A.; Nag, A.; Raychaudhuri, P. Differential regulation of E2F1, DP1, and the E2F1/DP1 complex by ARF. Mol. Cell Biol. 2002, 22, 8398-8408.
62. Eymin, B.; Karayan, L.; Seite, P.; Brambilla, C.; Brambilla, E.; Larsen, C. J.; Gazzeri, S. Human ARF binds E2F1 and inhibits its transcriptional activity. Oncogene 2001, 20, 1033-1041.
63. Hsieh, J. K.; Yap, D.; O'Connor, D. J.; Fogal, V.; Fallis, L.; Chan, F.; Zhong, S.; Lu, X. Novel function of the cyclin A binding site of E2F in regulating p53-induced apoptosis in response to DNA damage. Mol. Cell Biol. 2002, 22, 78-93.
64. Rogoff, H. A.; Pickering, M. T.; Frame, F. M.; Debatis, M. E.; Sanchez, Y.; Jones, S.; Kowalik, T. F. Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/ Chk2. Mol. Cell Biol. 2004, 24, 2968-2977.
65. Powers, J. T.; Hong, S.; Mayhew, C. N.; Rogers, P. M.; Knudsen, E. S.; Johnson, D. G. E2F1 uses the ATM signaling pathway to induce p53 and Chk2 phosphorylation and apoptosis. Mol. Cancer Res. 2004, 2, 203-214.
66. Rogoff, H. A.; Pickering, M. T.; Debatis, M. E.; Jones, S.; Kowalik, T. F. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol. Cell Biol. 2002, 22, 5308-5318.
67. Chen, D.; Padiernos, E.; Ding, F.; Lossos, I. S.; Lopez, C. D. Apoptosis-stimulating protein of p53-2 (ASPP2/53BP2L) is an E2F target gene. Cell Death Differ. 2005, 12, 358-368.
68. Hershko, T.; Chaussepied, M.; Oren, M.; Ginsberg, D. Novel link between E2F and p53: proapoptotic cofactors of p53 are transcriptionally upregulated by E2F. Cell Death Differ. 2005, 12, 377-383.
69. Fogal, V.; Kartasheva, N. N.; Trigiante, G.; Llanos, S.; Yap, D.; Vousden, K. H.; Lu, X. ASPP1 and ASPP2 are new transcriptional targets of E2F. Cell Death Differ. 2005, 12, 369-376.
70. Samuels-Lev, Y.; O'Connor, D. J.; Bergamaschi, D.; Trigiante, G.; Hsieh, J. K.; Zhong, S.; Campargue, I.; Naumovski, L.; Crook, T.; Lu, X. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 2001, 8, 781-794.
71. Fueyo, J.; Gomez-Manzano, C.; Yung, W. K.; Liu, T. J.; Alemany, R.; McDonnell, T. J.; Shi, X.; Rao, J. S.; Levin, V. A.; Kyritsis, A. P. Overexpression of E2F-1 in glioma triggers apoptosis and suppresses tumor growth in vitro and in vivo. Nat. Med. 1998, 4, 685-690.
72. Hunt, K. K.; Deng, J.; Liu, T. J.; Wilson-Heiner, M.; Swisher, S. G.; Clayman, G.; Hung, M. C. Adenovirus-mediated overexpression of the transcription factor E2F-1 induces apoptosis in human breast and ovarian carcinoma cell lines and does not require p53. Cancer Res. 1997, 57, 4722-4726.
73. Irwin, M.; Marin, M. C.; Phillips, A. C.; Seelan, R. S.; Smith, D. I.; Liu, W.; Flores, E. R.; Tsai, K. Y.; Jacks, T.; Vousden, K. H.; Kaelin, W. G., Jr. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000, 407, 645-648.
74. Phillips, A. C.; Bates, S.; Ryan, K. M.; Helin, K.; Vousden, K. H. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev. 1997, 11, 1853-1863.
75. Macleod, K. F.; Hu, Y.; Jacks, T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 1996, 15, 6178-6188.
76. Krek, W.; Xu, G.; Livingston, D. M. Cyclin A-kinase regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint. Cell 1995, 83, 1149-1158.
77. Stiewe, T.; Putzer, B. M. Role of the p53-homologue p73 in E2F1-induced apoptosis. Nat. Genet. 2000, 26, 464-469.
78. Ng, S. W.; Yiu, G. K.; Liu, Y.; Huang, L. W.; Palnati, M.; Jun, S. H.; Berkowitz, R. S.; Mok, S. C. Analysis of p73 in human borderline and invasive ovarian tumor. Oncogene 2000, 19, 1885-1890.
79. Yokomizo, A.; Mai, M.; Tindall, D. J.; Cheng, L.; Bostwick, D. G.; Naito, S.; Smith, D. I.; Liu, W. Overexpression of the wild type p73 gene in human bladder cancer. Oncogene 1999, 18, 1629-1633.
80. Urist, M.; Tanaka, T.; Poyurovsky, M. V.; Prives, C. p73 induction after DNA damage is regulated by checkpoint kinases Chk1 and Chk2. Genes Dev. 2004, 18, 3041-3054.
81. Marabese, M.; Vikhanskaya, F.; Rainelli, C.; Sakai, T.; Broggini, M. DNA damage induces transcriptional activation of p73 by removing C-EBPalpha repression on E2F1. Nucleic Acids Res. 2003, 31, 6624-6632.
82. Moroni, M. C.; Hickman, E. S.; Lazzerini Denchi, E.; Caprara, G.; Colli, E.; Cecconi, F.; Muller, H.; Helin, K. Apaf-1 is a transcriptional target for E2F and p53. Nat. Cell Biol. 2001, 3, 552-558.
83. Furukawa, Y.; Nishimura, N.; Furukawa, Y.; Satoh, M.; Endo, H.; Iwase, S.; Yamada, H.; Matsuda, M.; Kano, Y.; Nakamura, M. Apaf-1 is a mediator of E2F-1-induced apoptosis. J. Biol. Chem. 2002, 277, 39760-39768.
84. Nahle, Z.; Polakoff, J.; Davuluri, R. V.; McCurrach, M. E.; Jacobson, M. D.; Narita, M.; Zhang, M. Q.; Lazebnik, Y.; Barsagi, D.; Lowe, S. W. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol. 2002, 4, 859-864.
85. Routes, J. M.; Ryan, S.; Clase, A.; Miura, T.; Kuhl, A.; Potter, T. A.; Cook, J. L. Adenovirus E1A oncogene expression in tumor cells enhances killing by TNF-related apoptosis-inducing ligand (TRAIL). J. Immunol. 2000, 165, 4522-4527.
86. Xie, W.; Jiang, P.; Miao, L.; Zhao, Y.; Zhimin, Z.; Qing, L.; Zhu, W. G.; Wu, M. Novel link between E2F1 and Smac/DIABLO: proapoptotic Smac/DIABLO is transcriptionally upregulated by E2F1. Nucleic Acids Res. 2006, 34, 2046-2055.
87. Stanelle, J.; Tu-Rapp, H.; Putzer, B. M. A novel mitochondrial protein DIP mediates E2F1-induced apoptosis independently of p53. Cell Death Differ. 2005, 12, 347-357.
88. Prasad, K. V.; Ao, Z.; Yoon, Y.; Wu, M. X.; Rizk, M.; Jacquot, S.; Schlossman, S. F. CD27, a member of the tumor necrosis factor receptor family, induces apoptosis and binds to Siva, a proapoptotic protein. Proc. Natl. Acad. Sci. USA 1997, 94, 6346-6351.
89. Xue, L.; Chu, F.; Cheng, Y.; Sun, X.; Borthakur, A.; Ramarao, M.; Pandey, P.; Wu, M.; Schlossman, S. F.; Prasad, K. V. Siva-1 binds to and inhibits BCL-X(L)-mediated protection against UV radia-tion-induced apoptosis. Proc. Natl. Acad. Sci. USA 2002, 99, 6925-6930.
90. Fortin, A.; MacLaurin, J. G.; Arbour, N.; Cregan, S. P.; Kushwaha, N.; Callaghan, S. M.; Park, D. S.; Albert, P. R.; Slack, R. S. The proapoptotic gene SIVA is a direct transcriptional target for the tumor suppressors p53 and E2F1. J. Biol. Chem. 2004, 279, 28706-28714.
91. Qin, L. F.; Lee, T. K.; Ng, I. O. Gene expression profiling by cDNA array in human hepatoma cell line in response to cisplatin treatment. Life Sci. 2002, 70, 1677-1690.
92. Chen, L.; Willis, S. N.; Wei, A.; Smith, B. J.; Fletcher, J. I.; Hinds, M. G.; Colman, P. M.; Day, C. L.; Adams, J. M.; Huang, D. C. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell 2005, 17, 393-403.
93. Yu, J.; Zhang, L.; Hwang, P. M.; Kinzler, K. W.; Vogelstein, B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 2001, 7, 673-682.
94. Oda, E.; Ohki, R.; Murasawa, H.; Nemoto, J.; Shibue, T.; Yamashita, T.; Tokino, T.; Taniguchi, T.; Tanaka, N. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000, 288, 1053-1058.
95. O'Connor, L.; Strasser, A.; O'Reilly, L. A.; Hausmann, G.; Adams, J. M.; Cory, S.; Huang, D. C. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 1998, 17, 384-395.
96. Han, J.; Flemington, C.; Houghton, A. B.; Gu, Z.; Zambetti, G. P.; Lutz, R. J.; Zhu, L.; Chittenden, T. Expression of bbc3, a proapoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc. Natl. Acad. Sci. USA 2001, 98, 11318-11323.
97. Han, J.; Sabbatini, P.; White, E. Induction of apoptosis by human Nbk/Bik, a BH3-containing protein that interacts with E1B 19K. Mol. Cell Biol. 1996, 16, 5857-5864.
98. Hershko, T.; Ginsberg, D. Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F1 mediates apoptosis. J. Biol. Chem. 2004, 279, 8627-8634.
99. Real, P. J.; Sanz, C.; Gutierrez, O.; Pipaon, C.; Zubiaga, A. M.; Fernandez-Luna, J. L. Transcriptional activation of the proapoptotic bik gene by E2F proteins in cancer cells. FEBS Lett. 2006, 580, 5905-5909.
100. Rodriguez, J. M.; Glozak, M. A.; Ma, Y.; Cress, W. D. Bok, Bcl-2-related ovarian killer, is cell cycle-regulated and sensitizes to stress-induced apoptosis. J. Biol. Chem. 2006, 281, 22729-22735.
101. Croxton, R.; Ma, Y.; Song, L.; Haura, E. B.; Cress, W. D. Direct repression of the Mcl-1 promoter by E2F1. Oncogene 2002, 21, 1359-1369.
102. Zhou, P.; Qian, L.; Bieszczad, C. K.; Noelle, R.; Binder, M.; Levy, N. B.; Craig, R. W. Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage. Blood 1998, 92, 3226-3239.
103. Zhou, P.; Qian, L.; Kozopas, K. M.; Craig, R. W. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 1997, 89, 630-643.
104. Lomo, J.; Smeland, E. B.; Krajewski, S.; Reed, J. C.; Blomhoff, H. K. Expression of the Bcl-2 homologue Mcl-1 correlates with survival of peripheral blood B lymphocytes. Cancer Res. 1996, 56, 40-43.
105. Reynolds, J. E.; Yang, T.; Qian, L.; Jenkinson, J. D.; Zhou, P.; Eastman, A.; Craig, R. W. Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res. 1994, 54, 6348-6352.
106. Beg, A. A.; Baltimore, D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 1996, 274, 782-784.
107. Phillips, A. C.; Ernst, M. K.; Bates, S.; Rice, N. R.; Vousden, K. H. E2F-1 potentiates cell death by blocking antiapoptotic signaling pathways. Mol. Cell 1999, 4, 771-781.
108. Tanaka, H.; Matsumura, I.; Ezoe, S.; Satoh, Y.; Sakamaki, T.; Albanese, C.; Machii, T.; Pestell, R. G.; Kanakura, Y. E2F1 and cmyc potentiate apoptosis through inhibition of NF-kappa B activity that facilitates MnSOD-mediated ROS elimination. Mol. Cell 2002, 9, 1017-1029.
109. Salon, C.; Eymin, B.; Micheau, O.; Chaperot, L.; Plumas, J.; Brambilla, C.; Brambilla, E.; Gazzeri, S. E2F1 induces apoptosis and sensitizes human lung adenocarcinoma cells to death-receptor-mediated apoptosis through specific downregulation of c-FLIP(short). Cell Death Differ. 2006, 13, 260-272.
110. Wang, J.; Shen, W. H.; Jin, Y. J.; Brandt-Rauf, P. W.; Yin, Y. A molecular link between E2F-1 and the MAPK cascade. J. Biol. Chem. 2007, 282, 18521-18531.
111. Wu, J.; Jin, Y. J.; Calaf, G. M.; Huang, W. L.; Yin, Y. PAC1 is a direct transcription target of E2F-1 in apoptotic signaling. Oncogene 2007, 26, 6526-6535.
112. Sancar, A.; Lindsey-Boltz, L. A.; Unsal-Kacmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73, 39-85.
113. Blattner, C.; Sparks, A.; Lane, D. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol. Cell Biol. 1999, 19, 3704-3713.
114. Lin, W. C.; Lin, F. T.; Nevins, J. R. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 2001, 15, 1833-1844.
115. Huang, Y.; Ishiko, T.; Nakada, S.; Utsugisawa, T.; Kato, T.; Yuan, Z. M. Role for E2F in DNA damage-induced entry of cells into S phase. Cancer Res. 1997, 57, 3640-3643.
116. Stevens, C.; Smith, L.; La Thangue, N. B. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 2003, 5, 401-409.
117. Pommier, Y.; Sordet, O.; Rao, V. A.; Zhang, H.; Kohn, K. W. Targeting chk2 kinase: molecular interaction maps and therapeutic rationale. Curr. Pharm. Des. 2005, 11, 2855-2872.
118. Lee, J. S.; Collins, K. M.; Brown, A. L.; Lee, C. H.; Chung, J. H. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 2000, 404, 201-204.
119. Chehab, N. H.; Malikzay, A.; Appel, M.; Halazonetis, T. D. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 2000, 14, 278-288.
120. Berkovich, E.; Ginsberg, D. ATM is a target for positive regulation by E2F-1. Oncogene 2003, 22, 161-167.
121. Ianari, A.; Gallo, R.; Palma, M.; Alesse, E.; Gulino, A. Specific role for p300/CREB-binding protein-associated factor activity in E2F1 stabilization in response to DNA damage. J. Biol. Chem. 2004, 279, 30830-30835.
122. Markham, D.; Munro, S.; Soloway, J.; O'Connor, D. P.; La Thangue, N. B. DNA-damage-responsive acetylation of pRb regulates binding to E2F-1. EMBO Rep. 2006, 7, 192-198.
123. Banerjee, D.; Schnieders, B.; Fu, J. Z.; Adhikari, D.; Zhao, S. C.; Bertino, J. R. Role of E2F-1 in chemosensitivity. Cancer Res. 1998, 58, 4292-4296.
124. Meng, R. D.; Phillips, P.; El-Deiry, W. S. p53-independent increase in E2F-1 expression enhances the cytotoxic effects of etoposide and of adriamycin. Int. J. Oncol. 1999, 14, 5-14.
125. Pruschy, M.; Wirbelauer, C.; Glanzmann, C.; Bodis, S.; Krek, W. E2F-1 has properties of a radiosensitizer and its regulation by cyclin A kinase is required for cell survival of fibrosarcoma cells lacking p53. Cell Growth Differ. 1999, 10, 141-146.
126. Wang, B.; Liu, K.; Lin, F. T.; Lin, W. C. A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J. Biol. Chem. 2004, 279, 54140-54152.
127. Maser, R. S.; Mirzoeva, O. K.; Wells, J.; Olivares, H.; Williams, B. R.; Zinkel, R. A.; Farnham, P. J.; Petrini, J. H. Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell Biol. 2001, 21, 6006-6016.
128. Hallstrom, T. C.; Mori, S.; Nevins, J. R. An E2F1-dependent gene expression program that determines the balance between proliferation and cell death. Cancer Cell 2008, 13, 11-22.
129. Zhou, B. P.; Liao, Y.; Xia, W.; Zou, Y.; Spohn, B.; Hung, M. C. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat. Cell Biol. 2001, 3, 973-982.
130. Chaussepied, M.; Ginsberg, D. Transcriptional regulation of AKT activation by E2F. Mol. Cell 2004, 16, 831-837.
131. Nip, J.; Strom, D. K.; Fee, B. E.; Zambetti, G.; Cleveland, J. L.; Hiebert, S. W. E2F-1 cooperates with topoisomerase II inhibition and DNA damage to selectively augment p53-independent apoptosis. Mol. Cell Biol. 1997, 17, 1049-1056.
132. Dong, Y. B.; Yang, H. L.; Elliott, M. J.; McMasters, K. M. Adeno-virus-mediated E2F-1 gene transfer sensitizes melanoma cells to apoptosis induced by topoisomerase II inhibitors. Cancer Res. 2002, 62, 1776-1783.
133. Li, Y.; Sun, X.; LaMont, J. T.; Pardee, A. B.; Li, C. J. Selective killing of cancer cells by beta -lapachone: direct checkpoint activation as a strategy against cancer. Proc. Natl. Acad. Sci. USA 2003, 100, 2674-2678.
134. Vassilev, L. T.; Vu, B. T.; Graves, B.; Carvajal, D.; Podlaski, F.; Filipovic, Z.; Kong, N.; Kammlott, U.; Lukacs, C.; Klein, C.; Fotouhi, N.; Liu, E. A. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004, 303, 844-848.
135. Carvajal, D.; Tovar, C.; Yang, H.; Vu, B. T.; Heimbrook, D. C.; Vassilev, L. T. Activation of p53 by MDM2 antagonists can protect proliferating cells from mitotic inhibitors. Cancer Res. 2005, 65, 1918-1924.
136. Ambrosini, G.; Sambol, E. B.; Carvajal, D.; Vassilev, L. T.; Singer, S.; Schwartz, G. K. Mouse double minute antagonist Nutlin-3a enhances chemotherapy-induced apoptosis in cancer cells with mutant p53 by activating E2F1. Oncogene 2007, 26, 3473-3481.
137. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer. Cell 2000, 100, 57-70.
138. Hahn, W. C.; Counter, C. M.; Lundberg, A. S.; Beijersbergen, R. L.; Brooks, M. W.; Weinberg, R. A. Creation of human tumour cells with defined genetic elements. Nature 1999, 400, 464-468.
139. Baylin, S. B.; Ohm, J. E. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 2006, 6, 107-116.
140. Roy, S.; Packman, K.; Jeffrey, R.; Tenniswood, M. Histone deacetylase inhibitors differentially stabilize acetylated p53 and induce cell cycle arrest or apoptosis in prostate cancer cells. Cell Death Differ. 2005, 12, 482-491.
141. Zhao, Y.; Tan, J.; Zhuang, L.; Jiang, X.; Liu, E. T.; Yu, Q. Inhibitors of histone deacetylases target the Rb-E2F1 pathway for apoptosis induction through activation of proapoptotic protein Bim. Proc. Natl. Acad. Sci. USA 2005, 102, 16090-16095.
142. Tan, J.; Zhuang, L.; Jiang, X.; Yang, K. K.; Karuturi, K. M.; Yu, Q. Apoptosis signal-regulating kinase 1 is a direct target of E2F1 and contributes to histone deacetylase inhibitor-induced apoptosis through positive feedback regulation of E2F1 apoptotic activity. J. Biol. Chem. 2006, 281, 10508-10515.
143. Wang, C.; Chen, L.; Hou, X.; Li, Z.; Kabra, N.; Ma, Y.; Nemoto, S.; Finkel, T.; Gu, W.; Cress, W. D.; Chen, J. Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage. Nat. Cell Biol. 2006, 8, 1025-1031.