The E2F1/Rb and p53/MDM2 pathways in DNA repair and apoptosis: Understanding the crosstalk to develop novel strategies for prostate cancer radiotherapy

Seminars in Radiation Oncology

Volumn 20, Issue 4, 2010, Pages 258-266

  Udayakumar, Thirupandiyur ^a   Shareef, Mohammed M ^a   Diaz, Dayssy A ^a   Ahmed, Mansoor M ^a   Pollack, Alan ^a  

^a UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MDM2; PROTEIN P53; TRANSCRIPTION FACTOR E2F;

APOPTOSIS; CANCER RADIOTHERAPY; DNA REPAIR; HUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; RADIOSENSITIVITY; RADIOSENSITIZATION; REVIEW;

APOPTOSIS; DNA REPAIR; E2F1 TRANSCRIPTION FACTOR; HUMANS; MALE; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MDM2; RADIATION ONCOLOGY; RADIATION TOLERANCE; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77956453807     PISSN: 10534296     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semradonc.2010.05.007     Document Type: Review

References (75)

1. Janicke R.U., Sohn D., Schulze-Osthoff K. The dark side of a tumor suppressor: Anti-apoptotic p53. Cell Death Differ 2008, 15:959-976.
2. Brooks C.L., Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006, 21:307-315.
3. Sherr C.J. Divorcing ARF and p53: An unsettled case. Nat Rev Cancer 2006, 6:663-673.
4. Vassilev L.T. Small-molecule antagonists of p53-MDM2 binding: Research tools and potential therapeutics. Cell Cycle 2004, 3:419-421.
5. Sherr C.J., McCormick F. The RB and p53 pathways in cancer. Cancer Cell 2002, 2:103-112.
6. 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.
7. Grignon D.J., Caplan R., Sarkar F.H. p53 status and prognosis of locally advanced prostatic adenocarcinoma: A study based on RTOG 8610. J Natl Cancer Inst 1997, 89:158-165. and others.
8. Khor L.Y., Desilvio M., Al-Saleem T., et al. MDM2 as a predictor of prostate carcinoma outcome: An analysis of Radiation Therapy Oncology Group protocol 8610. Cancer 2005, 104:962-967.
9. Chakravarti A., Heydon K., Wu C.L., et al. Loss of p16 expression is of prognostic significance in locally advanced prostate cancer: An analysis from the Radiation Therapy Oncology Group protocol 86-10. J Clin Oncol 2003, 21:3328-3334.
10. Chakravarti A., DeSilvio M., Zhang M., et al. Prognostic value of p16 in locally advanced prostate cancer: A study based on Radiation Therapy Oncology Group protocol 9202. J Clin Oncol 2007, 25:3082-3089.
11. Li R., Heydon K., Hammond M.E., et al. Ki-67 staining index predicts distant metastasis and survival in locally advanced prostate cancer treated with radiotherapy: An analysis of patients in Radiation Therapy Oncology Group protocol 86-10. Clin Cancer Res 2004, 10:4118-4124.
12. Pollack A., DeSilvio M., Khor L.Y., et al. Ki-67 staining is a strong predictor of distant metastasis and mortality for men with prostate cancer treated with radiotherapy plus androgen deprivation: Radiation Therapy Oncology Group trial 92-02. J Clin Oncol 2004, 22:2133-2140.
13. Pochampally R., Fodera B., Chen L., et al. A 60 Kd MDM2 isoform is produced by caspase cleavage in non-apoptotic tumor cells. Oncogene 1998, 17:2629-2636.
14. Meek D.W. Tumour suppression by p53: A role for the DNA damage response?. Nat Rev Cancer 2009, 9:714-723.
15. Zhang Z., Wang H., Li M., et al. Stabilization of E2F1 protein by MDM2 through the E2F1 ubiquitination pathway. Oncogene 2005, 24:7238-7247.
16. Seo Y.R., Fishel M.L., Amundson S., et al. Implication of p53 in base excision DNA repair: In vivo evidence. Oncogene 2002, 21:731-737.
17. Cohen H.Y., Lavu S., Bitterman K.J., et al. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol Cell 2004, 13:627-638.
18. Chen J., Sadowski I. Identification of the mismatch repair genes PMS2 and MLH1 as p53 target genes by using serial analysis of binding elements. Proc Natl Acad Sci U S A 2005, 102:4813-4818.
19. Warnick C.T., Dabbas B., Ford C.D., et al. Identification of a p53 response element in the promoter region of the hMSH2 gene required for expression in A2780 ovarian cancer cells. J Biol Chem 2001, 276:27363-27370.
20. Adimoolam S., Ford J.M. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc Natl Acad Sci U S A 2002, 99:12985-12990.
21. Ofir-Rosenfeld Y., Boggs K., Michael D., et al. Mdm2 Regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell 2008, 32:180-189.
22. Polager S., Ofir M., Ginsberg D. E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene 2008, 27:4860-4864.
23. Marti A., Wirbelauer C., Scheffner M., et al. Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat Cell Biol 1999, 1:14-19.
24. 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.
25. 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.
26. Maser R.S., Mirzoeva O.K., Wells J., et al. Mre11 Complex and DNA replication: Linkage to E2F and sites of DNA synthesis. Mol Cell Biol 2001, 21:6006-6016.
27. Liu K., Lin F.T., Ruppert J.M., et al. Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol Cell Biol 2003, 23:3287-3304.
28. Speidel D. Transcription-independent p53 apoptosis: An alternative route to death. Trends Cell Biol 2009, 20:14-24. Nos.
29. Polager S., Ginsberg D. p53 and E2F: Partners in life and death. Nat Rev Cancer 2009, 9:738-748.
30. Chipuk J.E., Kuwana T., Bouchier-Hayes L., et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
31. Leu J.I., Dumont P., Hafey M., et al. Mitochondrial p53 activates bak and causes disruption of a bak-Mcl1 complex. Nat Cell Biol 2004, 6:443-450.
32. Mihara M., Erster S., Zaika A., et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003, 11:577-590.
33. Bennett M., Macdonald K., Chan S.W., et al. Cell surface trafficking of Fas: A rapid mechanism of p53-mediated apoptosis. Science 1998, 282:290-293.
34. Bates S., Phillips A.C., Clark P.A., et al. p14ARF links the tumour suppressors RB and p53. Nature 1998, 395:124-125.
35. Mason S.L., Loughran O., La Thangue N.B. p14(ARF) regulates E2F activity. Oncogene 2002, 21:4220-4230.
36. 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., et al. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000, 407:645-648.
37. Hallstrom T.C., Nevins J.R. Specificity in the activation and control of transcription factor E2F-dependent apoptosis. Proc Natl Acad Sci U S A 2003, 100:10848-10853.
38. Zindy F., Eischen C.M., Randle D.H., et al. Myc Signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 1998, 12:2424-2433.
39. Tolbert D., Lu X., Yin C., et al. p19(ARF) is dispensable for oncogenic stress-induced p53-mediated apoptosis and tumor suppression in vivo. Mol Cell Biol 2002, 22:370-377.
40. Rogoff H.A., Pickering M.T., Debatis M.E., et al. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol Cell Biol 2002, 22:5308-5318.
41. Russell J.L., Powers J.T., Rounbehler R.J., et al. ARF differentially modulates apoptosis induced by E2F1 and Myc. Mol Cell Biol 2002, 22:1360-1368.
42. Tsai K.Y., MacPherson D., Rubinson D.A., et al. ARF is not required for apoptosis in Rb mutant mouse embryos. Curr Biol 2002, 12:159-163.
43. Nguyen K.H., Hachem P., Khor L.Y., et al. Adenoviral-E2F-1 radiosensitizes p53(wild-type) and p53(null) human prostate cancer cells. Int J Radiat Oncol Biol Phys 2005, 63:238-246.
44. Udayakumar T.S., Hachem P., Ahmed M.M., et al. MDM2 enhances E2F1-induced apoptosis and the combination sensitizes androgen-sensitive [corrected] and androgen-insensitive [corrected] prostate cancer cells to radiation. Mol Cancer Res 2008, 6:1742-1754.
45. Johnson D.G., Cress W.D., Jakoi L., et al. Oncogenic capacity of the E2F1 gene. Proc Natl Acad Sci U S A 1994, 91:12823-12827.
46. Hsieh J.K., Yap D., O'Connor D.J., et al. 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.
47. Xiao Z.X., Chen J., Levine A.J., et al. Interaction between the retinoblastoma protein and the oncoprotein MDM2. Nature 1995, 375:694-698.
48. Martin K., Trouche D., Hagemeier C., et al. Stimulation of E2F1/DP1 transcriptional activity by MDM2 oncoprotein. Nature 1995, 375:691-694.
49. Hsieh J.K., Chan F.S., O'Connor D.J., et al. RB regulates the stability and the apoptotic function of p53 via MDM2. Mol Cell 1999, 3:181-193.
50. Sdek P., Ying H., Chang D.L., et al. MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol Cell 2005, 20:699-708.
51. Sdek P., Ying H., Zheng H., et al. The central acidic domain of MDM2 is critical in inhibition of retinoblastoma-mediated suppression of E2F and cell growth. J Biol Chem 2004, 279:53317-53322.
52. Kowalik T.F., DeGregori J., Leone G., et al. E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ 1998, 9:113-118.
53. Yang H.L., Dong Y.B., Elliott M.J., et al. Adenovirus-mediated E2F-1 gene transfer inhibits MDM2 expression and efficiently induces apoptosis in MDM2-overexpressing tumor cells. Clin Cancer Res 1999, 5:2242-2250.
54. Zhang Z., Li M., Wang H., et al. Antisense therapy targeting MDM2 oncogene in prostate cancer: Effects on proliferation, apoptosis, multiple gene expression, and chemotherapy. Proc Natl Acad Sci U S A 2003, 100:11636-11641.
55. Wunderlich M., Berberich S.J. Mdm2 Inhibition of p53 induces E2F1 transactivation via p21. Oncogene 2002, 21:4414-4421.
56. Bottger A., Bottger V., Sparks A., et al. Design of a synthetic Mdm2-binding mini protein that activates the p53 response in vivo. Curr Biol 1997, 7:860-869.
57. Midgley C.A., Lane D.P. p53 protein stability in tumour cells is not determined by mutation but is dependent on Mdm2 binding. Oncogene 1997, 15:1179-1189.
58. Lehman J.A., Eitel J.A., Batuello C.N., et al. Therapeutic considerations for Mdm2: Not just a one trick pony. Expert Opin Drugs Discov 2008, 3:1309-1321.
59. Bouska A., Lushnikova T., Plaza S., et al. Mdm2 Promotes genetic instability and transformation independent of p53. Mol Cell Biol 2008, 28:4862-4874.
60. Mu Z., Hachem P., Agrawal S., et al. MDM2 sensitizes prostate cancer cells to androgen deprivation, radiation, and the combination. Int J Radiat Oncol Biol Phys 2004, 58:336-343.
61. Roach M., Waldman F., Pollack A. Predictive models in external beam radiotherapy for clinically localized prostate cancer. Cancer 2009, 115:3112-3120. (suppl).
62. Khor L.Y., Desilvio M., Li R., et al. Bcl-2 and Bax expression and prostate cancer outcome in men treated with radiotherapy in Radiation Therapy Oncology Group protocol 86-10. Int J Radiat Oncol Biol Phys 2006, 66:25-30.
63. Chakravarti A., Heydon K., Wu C.L., et al. Loss of p16 expression is of prognostic significance in locally advanced prostate cancer: An analysis from the Radiation Therapy Oncology Group protocol 86-10. J Clin Oncol 2003, 21:3328-3334.
64. Khor L.Y., Bae K., Al-Saleem T., et al. Protein kinase A RI-alpha predicts for prostate cancer outcome: Analysis of Radiation Therapy Oncology Group trial 86-10. Int J Radiat Oncol Biol Phys 2008, 71:1309-1315.
65. Zhang M., Ho A., Hammond E.H., et al. Prognostic value of survivin in locally advanced prostate cancer: Study based on RTOG 8610. Int J Radiat Oncol Biol Phys 2009, 73:1033-1042.
66. Khor L.Y., Bae K., Paulus R., et al. MDM2 and Ki-67 predict for distant metastasis and mortality in men treated with radiotherapy and androgen deprivation for prostate cancer RTOG, p 92, p 92. J Clin Oncol 2009, 27:3177-3184.
67. Che M., DeSilvio M., Pollack A., et al. Prognostic value of abnormal p53 expression in locally advanced prostate cancer treated with androgen deprivation and radiotherapy: A study based on RTOG 9202. Int J Radiat Oncol Biol Phys 2007, 69:1117-1123.
68. Khor L.Y., Moughan J., Al-Saleem T., et al. Bcl-2 and Bax expression predict prostate cancer outcome in men treated with androgen deprivation and radiotherapy on Radiation Therapy Oncology Group protocol 92-02. Clin Cancer Res 2007, 13:3585-3590.
69. Khor L.Y., Bae K., Pollack A., et al. Cox-2 expression predicts prostate-cancer outcome: Analysis of data from the RTOG 92-02 trial. Lancet Oncol 2007, 8:912-920.
70. Pollack A., Bae K., Khor L.Y., et al. The importance of protein kinase A in prostate cancer: Relationship to patient outcome in Radiation Therapy Oncology Group Trial 92-02. Clin Cancer Res 2009, 15:5478-5484.
71. Roach M., Bae K., Speight J., et al. Short-term neoadjuvant androgen deprivation therapy and external-beam radiotherapy for locally advanced prostate cancer: Long-term results of RTOG 8610. J Clin Oncol 2008, 26:585-591.
72. Horwitz E.M., Bae K., Hanks G.E., et al. Ten-year follow-up of Radiation Therapy Oncology Group protocol 92-02: A phase III trial of the duration of elective androgen deprivation in locally advanced prostate cancer. J Clin Oncol 2008, 26:2497-2504.
73. Hanks G.E., Pajak T.F., Porter A., et al. Phase III trial of long-term adjuvant androgen deprivation after neoadjuvant hormonal cytoreduction and radiotherapy in locally advanced carcinoma of the prostate: The Radiation Therapy Oncology Group Protocol 92-02. J Clin Oncol 2003, 21:3972-3978.
74. Pollack A., Bae K., Khor L.Y., et al. A model for distant metastasis incorporating tissue biomarkers from prostate cancer patients in Radiation Therapy Oncology Group (RTOG) 92-02. Boston 2008, S58. p Supplement.
75. Vergis R., Corbishley C.M., Thomas K., et al. Expression of Bcl-2, p 53 and MDM2, in Localized Prostate Cancer with Respect to the Outcome of Radical Radiotherapy Dose Escalation. Int J Radiat Oncol Biol Phys 2010, in press.