Indole-3-carbinol activates the ATM signaling pathway independent of DNA damage to stabilize p53 and induce G1 arrest of human mammary epithelial cells

International Journal of Cancer

Volumn 118, Issue 4, 2006, Pages 857-868

  Brew, Christine T ^a   Aronchik, Ida ^a   Hsu, Jocelyn C ^a   Sheen, Joon Ho ^b   Dickson, Robert B ^b   Bjeldanes, Leonar F ^a   Firestone, Gary L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

ATM; Breast cancer; Cell cycle arrest; Indole 3 carbinol; MDM2; p53

Indexed keywords

3 INDOLEMETHANOL; ATM PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DNA; HISTONE H2AX; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; UBIQUITIN PROTEIN LIGASE; WORTMANNIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; BROCCOLI; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL FRACTIONATION; CELL IMMORTALIZATION; CONTROLLED STUDY; CRUCIFERA; DNA DAMAGE; DNA STRAND BREAKAGE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ANTICARCINOGENIC AGENTS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA-BINDING PROTEINS; FEMALE; GENES, P53; HUMANS; INDOLES; MAMMARY GLANDS, HUMAN; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MDM2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 31544436372     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21445     Document Type: Article

References (62)

1. Grubbs CJ, Steele VE, Casebolt T, Juliana MM, Eto I, Whitaker LM, Dragnev KH, Kelloff GJ, Lubet RL. Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 1995;15:709-16.
2. Bradlow HL, Michnovicz J, Telang NT, Osborne MP. Effects of dietary indole-3- carbinol on estradiol metabolism and spontaneous mammary tumors in mice. Carcinogenesis 1991;12:1571-4.
3. Wattenberg LW, Loub WD. Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res 1978;38:1410-3.
4. Cover CM, Hsieh SJ, Tran SH, Hallden G, Kim GS, Bjeldanes LF, Firestone GL. Indole-3-carbinol inhibits the expression of cyclin-dependent kinase-6 and induces a G1 cell cycle arrest of human breast cancer cells independent of estrogen receptor signaling. J Biol Chem 1998;273:3838-47.
5. Cram EJ, Liu BD, Bjeldanes LF, Firestone GL. Indole-3-carbinol inhibits CDK6 expression in human MCF-7 breast cancer cells by disrupting Sp1 transcription factor interactions with a composite element in the CDK6 gene promoter. J Biol Chem 2001;276:22332-40.
6. Staub RE, Feng C, Onisko B, Bailey GS, Firestone GL, Bjeldanes LF. Fate of indole-3-carbinol in cultured human breast tumor cells. Chem Res Toxicol 2002;15:101-9.
7. Hong C, Kim HA, Firestone GL, Bjeldanes LF. 3,3′-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21 (WAF1/CIP1) expression. Carcinogenesis 2002;23:1297-305.
8. Ge X, Yannai S, Rennert G, Gruener N, Fares FA. 3,3′- Diindolylmethane induces apoptosis in human cancer cells. Biochem Biophys Res Commun 1996;228:153-8.
9. Hong C, Firestone GL, Bjeldanes LF. Bcl-2 family-mediated apoptotic effects of 3,3′-diindolylmethane (DIM) in human breast cancer cells. Biochem Pharmacol 2002;63:1085-97.
10. Rahman KM, Aranha O, Glazyrin A, Chinni SR, Sarkar FH. Translocation of Bax to mitochondria induces apoptotic cell death in indole-3-carbinol (I3C) treated breast cancer cells. Oncogene 2000;19:5764-71.
11. Rahman KM, Aranha O, Sarkar FH. Indole-3-carbinol (I3C) induces apoptosis in tumorigenic but not in nontumorigenic breast epithelial cells. Nutr Cancer 2003;45:101-12.
12. Balint EE, Vousden KH. Activation and activities of the p53 tumour suppressor protein. Br J Cancer 2001;85:1813-23.
13. Saito S, Yamaguchi H, Higashimoto Y, Chao C, Xu Y, Fornace AJ, Jr., Appella E, Anderson CW. Phosphorylation site interdependence of human p53 post-translational modifications in response to stress. J Biol Chem 2003;278:37536-44.
14. Shieh SY, Taya Y, Prives C. DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. EMBO J 1999;18:1815-23.
15. Damia G, Filiberti L, Vikhanskaya F, Carrassa L, Taya Y, D'Incalci M, Broggini M. Cisplatinum and taxol induce different patterns of p53 phosphorylation. Neoplasia 2001;3:10-6.
16. Baek SJ, Wilson LC, Eling TE. Resveratrol enhances the expression of non-steroidal anti-inflammatory drug-activated gene (NAG-1) by increasing the expression of p53. Carcinogenesis 2002;23:425-34.
17. Ye R, Bodero A, Zhou BB, Khanna KK, Lavin MF, Lees-Miller SP. The plant isoflavenoid genistein activates p53 and Chk2 in an ATM-dependent manner. J Biol Chem 2001;276:4828-33.
18. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res 2003;1:1001-8.
19. Appella E, Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 2001;268:2764-72.
20. Fukunaga-Takenaka R, Fukunaga K, Tatemichi M, Ohshima H. Nitric oxide prevents UV-induced phosphorylation of the p53 tumor-suppressor protein at serine 46: a possible role in inhibition of apoptosis. Biochem Biophys Res Commun 2003;308:966-74.
21. Kapoor M, Hamm R, Yan W, Taya Y, Lozano G. Cooperative phosphorylation at multiple sites is required to activate p53 in response to UV radiation. Oncogene 2000;19:358-64.
22. Yang Y, Li CC, Weissman AM. Regulating the p53 system through ubiquitination. Oncogene 2004;23:2096-106.
23. Stott FJ, Bates S, James MC, McConnell BB, Starborg M, Brookes S, Palmero I, Ryan K, Hara E, Vousden KH, Peters G. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J 1998;17: 5001-14.
24. Mayo LD, Dormer DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 2001;98:11598-603.
25. Hartmann A, Blaszyk H, Kovach JS, Sommer SS. The molecular epidemiology of p53 gene mutations in human breast cancer. Trends Genet 1997;13:27-33,
26. Pharoah PD, Day NE, Caldas C. Somatic mutations in the p53 gene and prognosis in breast cancer: a meta-analysis. Br J Cancer 1999; 80:1968-73.
27. Sutherland RL, Watts CKW, Lee CSL, Musgrove EA. Human cell culture. In: Masters JRW, Palsson B, eds. Cancer cell lines, vol. II. Great Britain: Kluwer, 1999.79-106.
28. Lacroix M, Leclercq G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat 2004; 83:249-89.
29. Merlo GR, Basolo F, Fiore L, Duboc L, Hynes NE. p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin. J Cell Biol 1995;128:1185-96.
30. Gudas J, Nguyen H, Li T, Hill D, Cowan KH. Effects of cell cycle, wild-type p53 and DNA damage on p21CIP1/Waf1 expression in human breast epithelial cells. Oncogene 1995;11:253-61.
31. Shaulian E, Zauberman A, Ginsberg D, Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol Cell Biol 1992;12:5581-92.
32. Sheen JH, Dickson RB. Overexpression of c-Myc alters G(1)/S arrest following ionizing radiation. Mol Cell Biol 2002;22:1819-33.
33. Chatterji U, Riby JE, Taniguchi T, Bjeldanes EL, Bjeldanes LF, Firestone GL. Indole-3- carbinol stimulates transcription of the interferon gamma receptor 1 gene and augments interferon responsiveness in human breast cancer cells. Carcinogenesis 2004;25:1119-28.
34. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993;75:817-25.
35. Firestone GL, Bjeldanes LF. Indole-3-carbinol and 3-3′- diindolylmethane antiproliferative signaling pathways control cell-cycle gene transcription in human breast cancer cells by regulating promoter-Sp1 transcription factor interactions. J Nutr 2003;133:2448S-55S.
36. el-Deiry WS, Harper JW, O'Connor PM, Velculescu VE, Canman CE, Jackman J, Pietenpol JA, Burrell M, Hill DE, Wang Y, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res 1994;54:1169-74.
37. Ko LJ, Prives C. p53: puzzle and paradigm. Genes Dev 1996;10: 1054-72.
38. el-Deiry WS, Tokino T, Waldman T, Oliner JD, Velculescu VE, Burrell M, Hill DE, Healy E, Rees JL, Hamilton SR, et al. Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues. Cancer Res 1995;55:2910-9.
39. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, Abraham RT. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 1998;58:4375-82.
40. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, Smorodinsky NI, Prives C, Reiss Y, Shiloh Y, Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998; 281:1674-7.
41. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004;64:2390-6.
42. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-506.
43. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia- mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA 2000;97:10389-94.
44. Gatei M, Scott SP, Filippovitch I, Soronika N, Lavin MF, Weber B, Khanna KK. Role for ATM in DNA damage-induced phosphorylation of BRCA1. Cancer Res 2000;60:3299-304.
45. Kreuzer KN. Bacteriophage T4, a model system for understanding the mechanism of type II topoisomerase inhibitors. Biochim Biophys Acta 1998;1400:339-47.
46. Ward IM, Minn K, Jorda KG, Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J Biol Chem 2003;278:19579-82.
47. Rahman KM, Li Y, Sarkar FH. Inactivation of akt and NF-kappaB play important roles during indole-3-carbinol-induced apoptosis in breast cancer cells. Nutr Cancer 2004;48:84-94.
48. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 2000;14:289-300.
49. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997;387:296-9.
50. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997;420:25-7.
51. Sakaguchi K, Saito S, Higashimoto Y, Roy S, Anderson CW, Appella E. Damage- mediated phosphorylation of human p53 threonine 18 through a cascade mediated by a casein 1-like kinase. Effect on Mdm2 binding. J Biol Chem 2000;275:9278-83.
52. Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 1997;91:325-34.
53. Momand J, Wu HH, Dasgupta G. MDM2-master regulator of the p53 tumor suppressor protein. Gene 2000;242:15-29.
54. Woods DB, Vousden KH. Regulation of p53 function. Exp Cell Res 2001;264:55-66.
55. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001;15:2177-96.
56. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000;408:433-9.
57. Jimenez GS, Bryntesson F, Torres-Arzayus MI, Priestley A, Beeche M, Saito S, Sakaguchi K, Appella E, Jeggo PA, Taccioli GE, Wahl GM, Hubank M. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 1999;400:81-3.
58. Meng Q, Yuan F, Goldberg ID, Rosen EM, Auborn K, Fan S. Indole-3-carbinol is a negative regulator of estrogen receptor-alpha signaling in human tumor cells. J Nutr 2000;130:2927-31.
59. Ye R, Goodarzi AA, Kurz EU, Saito S, Higashimoto Y, Lavin MF, Appella E, Anderson CW, Lees-Miller SP. The isoflavonoids genistein and quercetin activate different stress signaling pathways as shown by analysis of site-specific phosphorylation of ATM, p53 and histone H2AX. DNA Repair (Amst) 2004;3:235-44.
60. Mochan TA, Venere M, DiTullio RA, Jr., Halazonetis TD. 53BP1, an activator of ATM in response to DNA damage. DNA Repair (Amst) 2004;3:945-52.
61. Motoyama N, Naka K. DNA damage tumor suppressor genes and genomic instability. Curr Opin Genet Dev 2004;14:11-6.
62. Hastak K, Gupta S, Ahmad N, Agarwal MK, Agarwal ML, Mukhtar H. Role of p53 and NF-kappaB in epigallocatechin-3-gallate-induced apoptosis of LNCaP cells. Oncogene 2003;22:4851-9.