The emerging role of E2F-1 in the DNA damage response and checkpoint control

DNA Repair

Volumn 3, Issue 8-9, 2004, Pages 1071-1079

  Stevens, Craig ^a   La Thangue, Nicholas B ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

DNA damage; DNA repair; E2F 1

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; ARF PROTEIN; BETA LAPACHONE; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DNA TOPOISOMERASE (ATP HYDROLYSING); IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN MDM2; PROTEIN P53; PROTEIN P68; PROTEIN P73; PROTEIN TYROSINE PHOSPHATASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F4; TRANSCRIPTION FACTOR E2F5;

AMINO TERMINAL SEQUENCE; APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA SYNTHESIS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENOTOXICITY; HUMAN; MITOSIS INHIBITION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; DIMERIZATION; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; GENOME; HUMANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 3242880237     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.03.034     Document Type: Review

References (88)

1. De Bruin A., Maiti B., Jakoi L., Timmers C., Buerki R., Leone G. Identification and characterization of E2F7, a novel mammalian E2F family member capable of blocking cellular proliferation. J. Biol. Chem. 24:2003;42041-42049
2. L. Delavaine, N. Logan, C. Reilly, J. Wilson, T.R. Brummelkamp, E.M. Hijmans, R. Bernards, N.B. La Thangue, E2F-7: a distinctive E2F family member with an unusual organization of DNA binding domains, in press.
3. Leone G., DeGregori J., Yan Z., Jakoi L., Ishida S., Williams R.S., Nevins J.R. E2F3 activity is regulated during the cell cycle and is required for the induction of S phase. Genes Dev. 12:1998;2120-2130
4. Humbert P.O., Verona R., Trimarchi J.M., Rogers C., Dandapani S., Lees J.A. E2F3 is critical for normal cellular proliferation. Genes Dev. 14:2000;690-703
5. Bruce J.L., Hurford R.K. Jr., Classon M., Koh J., Dyson N. Requirements for cell cycle arrest by p16INK4a. Mol. Cell. 6:2000;737-742
6. Gaubatz S., Lindeman G.J., Ishida S., Jakoi L., Nevins J.R., Livingston D.M., Rempel R.E. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol. Cell. 6:2000;729-735
7. Rempel R.E., Saenz-Robles M.T., Storms R., Morham S., Ishida S., Engel A., Jakoi L., Melhem M.F., Pipas J.M., Smith C., Nevins J.R. Loss of E2F4 activity leads to abnormal development of multiple cellular lineages. Mol. Cell. 6:2000;293-306
8. Lindeman G.J., Dagnino I., Gaubatz S., Xu Y., Bronson R.T., Warren H.B., Livingston D.M. A specific, nonproliferative role for E2F-5 in choroid plexus function revealed by gene targetting. Genes Dev. 12:1998;1092-1098
9. Trimarchi J., Lees J.A. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell. Biol. 3:2001;11-20
10. La Thangue N.B. The yin and yang of E2F-1: balancing life and death. Nat. Cell. Biol. 5:2003;587-589
11. Johnson D.G., Schwarz J.K., Cress W.D., Nevins J.R. Expression of transcription factor E2F-1 induces quiescent cells to enter S phase. Nature. 365:1993;349-352
12. Johnson D.G., Cress W.D., Jakoi L., Nevins J.R. Oncogenic capacity of the E2F-1 gene. Proc. Natl. Acad. Sci. U.S.A. 91:1994;12823-12827
13. Lukas J., Petersen B.O., Holm K., Bartek J., Helin K. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4a mediated growth suppression. Mol. Cell. Biol. 16:1996;1047-1057
14. +/- mice. Nat. Genet. 18:1998;360-364
15. 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. U.S.A. 94:1997;7245-7250
16. Wu L., Timmers C., Maiti B., Saavedra H.I., Sang L., Chong G.T., Nuckolls F., Giangrande P., Wright F.A., Field S.J., Greenberg M.E., Orkin S., Nevins J.R., Robinson M.L., Leone G. The E2F1-3 transcription factors are essential for cellular proliferation. Nature. 414:2001;457-462
17. Wikonkal N.M., Remenyik E., Knezveic D., Zhang W., Liu M., Zhao H., Berton T.R., Johnson D.G., Brash D.E. Inactivating E2F-1 reverts apoptosis resistance and cancer sensitivity in Trp53-deficient mice. Nat. Cell. Biol. 5:2003;655-6660
18. 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. U.S.A. 91:1994;10918-10922
19. Shan B., Lee W.H. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:1994;8166-8173
20. Wu X., Levine A.J. p53 and E2F-1 co-operate to mediate apoptosis. Proc. Natl. Acad. Sci. U.S.A. 91:1994;3602-3606
21. 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. 85:1996;549-561
22. Yamasaki L., Jacks T., Bronson R., Goillot E., Harlow E., Dyson N. Tumour induction and tissue atrophy in mice lacking E2F-1. Cell. 85:1996;537-547
23. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., Weinberg R.A. Effects of an Rb mutation in the mouse. Nature. 359:1992;295-300
24. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., Lee W.H., Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 359:1992;288-294
25. 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. 2:1998;293-304
26. 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. 15:2001;386-391
27. Saavedra H.I., Maiti B., Timmers C., Altura R., Tokuyama K., Fukasawa K., Leone G. Inactivation of E2F3 results in centrosome amplification. Cancer Cell. 3:2003;333-346
28. Leone G., Sears R., Huang E., Rempel R., Nuckolls F., Park C-H., Giangrande P., Wu L., Saavedra H.I., Field S.J., Thompson M.A., Yang H., Fujiwara Y., Greenberg M.E., Orkin S., Smith C., Nevins J.R. Myc requires distinct E2F activities to induce S phase and apoptosis. Mol. Cell. 8:2001;105-113
29. Hsieh J.K., Fredersdorf S., Kouzarides T., Martin K., Lu X. E2F1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev. 11:1997;1840-1852
30. Phillips A.C., Bates S., Ryan K.M., Helin K., Vousden K.H. Induction of DNA synthesis and apoptosis are separable functions of E2F1. Genes Dev. 11:1997;1853-1863
31. Phillips A.C., Ernst M.K., Bates S., Rice N.R., Vousden K.H. E2F1 potentiates cell death by blocking anti-apoptotic signalling pathways. Mol. Cell. 4:1999;771-781
32. ARF links the tumour suppressor RB and p53. Nature. 395:1998;124-125
33. 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. 1:1999;20-26
34. Zindy F., Eischen C.M., Randle D.H., Kamijo T., Cleveland J.L., Sherr C.-J., Roussel M.F. Myc signalling via the ARF tumour suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:1998;2424-2433
35. 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. 22:2002;1360-1368
36. ARF is dispensable for oncogenic stress-induced p53-mediated apoptosis and tumor suppression in vivo. Mol. Cell. Biol. 22:2002;370-377
37. 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. 12:2002;159-163
38. Rogoff H.A., Pickering M.T., Debatis M.E., Jones S., Kowalik T.F. E2F-1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol. Cell. Biol. 22:2002;5308-5318
39. ARF targets certain E2F species for degradation. Proc. Natl. Acad. Sci. U.S.A. 98:2001;4455-4460
40. ARF regulates E2F activity. Oncogene. 21:2002;4220-4230
41. Berkovich E., Ginsberg D. ATM is a target for positive regulation by E2F-1. Oncogene. 22:2003;161-167
42. Irwin M., Martin 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. 407:2000;645-648
43. Stiewe T., Putzer B.M. Role of the p53-homologue p73 in E2F1-induced apoptosis. Nat. Genet. 26:2000;464-469
44. Lissy N.A., Davis P.K., Irwin M., Kaelin W.G., Dowdy S.F. A common E2F-1 and p73 pathway mediates cell death induced by TCR activation. Nature. 407:2000;642-644
45. Moroni M.C., Hickman E.S., Denchi E.L., Caprara G., Colli E., Cecconi F., Müller F., Helin K. Apaf-1 is a transcriptional target for E2F and p53. Nat. Cell. Biol. 3:2001;552-558
46. 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. 277:2002;39760-39768
47. Nahle Z., Polakoff J., Davuluri R.V., McCurrach M.E., Jacobson M.D., Narita M., Zhang M.Q., Lazebnik Y., Bar-Sagi D., Lowe S.W. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell. Biol. 4:2002;859-864
48. Guo Z., Yikang S., Yoshida H., Mak T.W., Zacksenhaus E. Inactivation of the retinoblastoma tumor suppressor induces apoptosis protease activating factor-1 dependent and independent apoptotic pathways during embryogenesis. Cancer Res. 61:2001;8395-8400
49. Karin M., Lin A. NF-κB at the crossroads of life and death. Nat. Immunol. 3:2002;221-227
50. Tanaka H., Matsumura I., Ezoe S., Satoh Y., Sakamaki T., Albanese C., Machii T., Pestell R.G., Kanakura Y. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-κB activity that facilitates MnSOD-mediated ROS elimination. Mol. Cell. 9:2002;1017-1029
51. 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. 19:1999;3704-3713
52. Hofferer M., Wirbelauer C., Humar B., Krek W. Increased levels of E2F1-dependent DNA binding activity after UV- or γ-irradiation. Nucleic Acid. Res. 27:1999;491-495
53. O'Connor D.J., Lu X. Stress signals induce transcriptionally inactive E2F-1 independently of p53 and Rb. Oncogene. 19:2000;2369-2376
54. 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. 15:2001;1833-1844
55. Stevens C., La Thangue N.B. Checkpoint kinase activates E2F-1 in response to DNA damage. Nat. Cell. Biol. 5:2003;401-409
56. Bartek J., Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell. 3:2003;21-429
57. Canman C.E., Lim D., Cimprich K.A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M.B., Siliciano J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science. 281:1998;1677-1679
58. Hirao A., Kong Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S.J., Mak T.W. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science. 287:2000;1824-1827
59. 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. 404:2000;201-204
60. Cortez D., Wang Y., Qin J., Elledge S.J. Requirement of ATM-dependent phosphorylation of BRCA1 in the DNA damage response to double strand breaks. Science. 286:1999;162-166
61. Chehab N.H., Malikzay A., Appel M., Halazonetis T.D. Chk2/hCds1 functions as a DNA damage checkpoint in G1 by stabilizing p53. Genes Dev. 14:2000;278-288
62. Shieh S., Ahn J., Tamai K., Taya Y., Prives C. The human homologues of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:2000;289-300
63. Maya R., Balass M., Kim S.T., Shkedy D., Leal J.M., Shifman O., Moas M., Buschmann T., Ronai Z., Shiloh Y., Kastan M.B., Katzir E., Oren M. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev. 15:2001;1067-1077
64. Li S., Ting N.S.Y., Zheng L., Chen P.L., Ziv Y., Shiloh Y., Lee E.Y.P., Lee W.H. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature. 406:2000;210-215
65. Hsiao K.M., McMahon S.L., Farnham P.J. Multiple DNA elements are required for the growth regulation of the mouse E2F-1 promoter. Genes Dev. 8:1994;1526-1537
66. Sellers W.R., Rodgers J.W., Kaelin W.G. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. U.S.A. 92:1995;11544-11548
67. Krek W., Ewen M.E., Shirodkar S., Arany Z., Kaelin W.G., Livingston D.M. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclinA-dependent protein kinase. Cell. 78:1994;161-172
68. Hateboer G., Kerkhoven R.M., Shvarts A., Bernards R., Beijerbergen R.L. Deregulation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev. 10:1996;2960-2970
69. Hofmann F., Martelli F., Livingston D.M., Wang Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev. 10:1996;2949-2959
70. SKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat. Cell. Biol. 1:1999;14-19
71. Martin K., Trouche D., Hagemeier C., Sorenson T.S., La Thangue N.B., Kouzarides T. Stimulation of E2F1/DP1 transcriptional activity by MDM2 oncoprotein. Nature. 375:1995;691-698
72. Loughran O., La Thangue N.B. Apoptotic and growth-promoting activity of E2F modulated by MDM2. Mol. Cell. Biol. 20:2000;2186-2197
73. Sakaguchi K., Herrera J.E., Saito S., Miki T., Bustin M., Vassilev A., Anderson C.W., Appella E. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 12:1998;2831-2841
74. 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. 5:2003;552-558
75. Ciechanover A., Orian A., Schwartz A.L. Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays. 22:2000;442-451
76. Takahashi Y., Rayman J.B., Dynlacht B.D. Analysis of promoter binding by the E2F and pRb families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:2000;804-816
77. Schlisio S., Halperin T., Vidal M., Nevins J.R. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. EMBO J. 21:2002;5775-5786
78. Giangrande P.H., Hallstrom T.C., Tunyaplin C., Calame K., Nevins J.R. Identification of the E-box factor TFE3 as a functional partner for the E2F-3 transcription factor. Mol. Cell. Biol. 23:2003;3707-3720
79. Rouse J., Jackson S.P. Interfaces between the detection. Signaling, and repair of DNA damage. Science. 297:2002;547-551
80. D'Amours D., Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell. Biol. 3:2002;317-327
81. 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 of E2F and sites of DNA synthesis. Mol. Cell. Biol. 21:2001;6006-6016
82. Bosco G., Du W., Orr-Weaver T.L. DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell. Biol. 3:2001;289-295
83. Liu K., Lin F.T., Ruppert M.J., Lin W.C. Regulation of E2F-1 by BRCT domain-containing protein TopBP1. Mol. Cell. Biol. 23:2003;3287-3304
84. Ren B., Cam H., Takahashi Y., Volkert T., Terragni J., Young R.A., Dynlacht B.D. E2F integrates cell cycle progression with DNA repair, replication, and G2/M checkpoints. Genes Dev. 16:2002;245-256
85. Polager S., Kalma Y., Berkovich E., Ginsberg D. E2Fs up-regulate expression of genes involved in DNA replication. Oncogene. 21:2002;437-446
86. Gottifredi V., Karni-Schmidt O., Shieh S.Y., Prives C. p53 downregulates Chk1 through p21 and the retinoblastoma protein. Mol. Cell. Biol. 21:2001;1066-1076
87. Carrassa L., Broggini M., Vikhanskaya F., Dam G. Characterisation of the 5′ flanking region of the human Chk1 gene: identification of E2F-1 functional sites. Cell Cycle. 2:2003;604-609
88. Li Y., Sun X., LaMont J.T., Pardee A.B., Li C.J. Selective killing of cancer cells by β-lapachone: Direct checkpoint activation as a strategy against cancer. Proc. Natl. Acad. Sci. U.S.A. 100:2003;2674-2678