Resveratrol induces DNA damage in colon cancer cells by poisoning topoisomerase II and activates the ATM kinase to trigger p53-dependent apoptosis

Toxicology in Vitro

Volumn 29, Issue 5, 2015, Pages 1156-1165

  Demoulin, Benjamin ^a   Hermant, Maryse ^a,b   Castrogiovanni, Cédric ^a   Staudt, Catherine ^a,b   Dumont, Patrick ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b Facultes Universitaires Notre Dame de la Paix Faculte de Medicine   (Belgium)

Author keywords

Apoptosis; Colon cancer; DNA damage; P53; Resveratrol; Topoisomerase II

Indexed keywords

ACETYLCYSTEINE; ATM PROTEIN; DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); DOUBLE STRANDED DNA; DOXORUBICIN; ETOPOSIDE; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUTLIN 3; PROTEIN P53; RESVERATROL; SERINE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; STILBENE DERIVATIVE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CHEMOSENSITIVITY; CHROMATIN CONDENSATION; COLON CANCER; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; HCT116 CELL LINE; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; WILD TYPE; COLON TUMOR; DRUG EFFECTS; HUMAN; METABOLISM;

RICE STRIPE VIRUS; VITACEAE;

APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; COLONIC NEOPLASMS; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II; HCT116 CELLS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; STILBENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84929993798     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.04.015     Document Type: Article

References (50)

1. Athar M., Back J.H., Tang X., Kim K.H., Kopelovich L., Bickers D.R., Kim A.L. Resveratrol: a review of pre-clinical studies for human cancer prevention. Toxicol. Appl. Pharmacol. 2007, 224:274-283.
2. Bishayee A. Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev. Res. (Phila) 2009, 2:409-418.
3. Brosh R., Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat. Rev. Cancer 2009, 9:701-713.
4. Brown C.J., Lain S., Verma C.S., Fersht A.R., Lane D.P. Awakening guardian angels: drugging the p53 pathway. Nat. Rev. Cancer 2009, 9:862-873.
5. Bunz F., Hwang P.M., Torrance C., Waldman T., Zhang Y., Dillehay L., Williams J., Lengauer C., Kinzler K.W., Vogelstein B. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J. Clin. Invest. 1999, 104:263-269.
6. Carter L.G., D'Orazio J.A., Pearson K.J. Resveratrol and cancer: focus on in vivo evidence. Endocr. Relat. Cancer 2014, 21:R209-R225.
7. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., Green D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
8. Cuenda A., Rouse J., Doza Y.N., Meier R., Cohen P., Gallagher T.F., Young P.R., Lee J.C. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 1995, 364:229-233.
9. Donehower L.A., Lozano G. 20 years studying p53 functions in genetically engineered mice. Nat. Rev. Cancer 2009, 9:831-841.
10. Dudley D.T., Pang L., Decker S.J., Bridges A.J., Saltiel A.R. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 1995, 92:7686-7689.
11. Dumont P., Burton M., Chen Q.M., Gonos E.S., Frippiat C., Mazarati J.-B., Eliaers F., Remacle J., Toussaint O. Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic. Biol. Med. 2000, 28:361-373.
12. Dumont P., Leu J.I.-J., Della Pietra A.C., George D.L., Murphy M. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat. Genet. 2003, 33:357-365.
13. Fukuhara K., Miyata N. Resveratrol as a new type of DNA-cleaving agent. Bioorg. Med. Chem. 1998, 8:3187-3192.
14. Fukuhara K., Nagakawa M., Nakanishi I., Ohkubo K., Imai K., Urano S., Fukuzumi S., Ozawa T., Ikota N., Mochizuki M., Miyata N., Okuda H. Structural basis for DNA-cleaving activity of resveratrol in the presence of Cu(II). Bioorg. Med. Chem. 2006, 14:1437-1444.
15. Fulda S. Resveratrol and derivatives for the prevention and treatment of cancer. Drug Discov. Today 2010, 15:757-765.
16. Gu B., Zhu W.G. Surf the post-translational modification network of p53 regulation. Int. J. Biol. Sci. 2012, 8:672-684.
17. Gusman J., Malonne H., Atassi G. A reappraisal of the potential chemopreventive and chemotherapeutic properties of resveratrol. Carcinogenesis 2001, 22:1111-1117.
18. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
19. Heiss E.H., Schilder Y.D.C., Dirsch V. Chronic treatment with resveratrol induces redox stress- and Ataxia Telangiectasia-mutated (ATM)-dependent senescence in p53-positive cancer cells. J. Biol. Chem. 2007, 282:26759-26766.
20. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 2004, 64:9152-9159.
21. Jang M., Cai L., Udeani G.O., Slowing K.V., Thomas C.F., Beecher C.W., Fong H.H., Farnsworth N.R., Kinghorn A.D., et al. Cancer Chemopreventive activity of resveratrol, a natural products derived from grapes. Science 1997, 275:218-220.
22. Jo J.Y., Gonzalez de Mejia E., Lila M.A. Effects of grape cell culture extracts on human topoisomerase II catalytic activity and characterization of active fractions. J. Agric. Food Chem. 2005, 53:2489-2498.
23. Jo J.Y., Gonzalez de Mejia E., Lila M.A. Catalytic inhibition of human DNA topoisomerase II by interactions of grape cell culture polyphenols. J. Agric. Food Chem. 2006, 54:2083-2087.
24. Kinner A., Wu W., Staudt C., Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucl. Acids Res. 2008, 36:5678-5694.
25. Laptenko O., Prives C. Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ. 2006, 13:951-961.
26. Leone S., Cornetta T., Basso E., Cozzi R. Resveratrol induces DNA double-strand-breaks through human topoisomerase II interaction. Cancer Lett. 2010, 295:167-172.
27. Leu J.I.-J., Dumont P., Hafey M., Murphy M.E., George D.L. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat. Cell Biol. 2004, 6:443-450.
28. Li X., Dumont P., Della Pietra A., Shetler C., Murphy M.E. The codon 47 polymorphism in p53 is functionally significant. J. Biol. Chem. 2005, 280:24245-24251.
29. Luo H., Yang A., Schulte B.A., Wargovich M.J., Wan G.Y. Resveratrol induces premature senescence in lung cancer cells via ROS-mediated DNA damage. PLoS One 2013, 8:e60065.
30. Marchenko N.D., Zaika A., Moll U.M. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem. 2000, 275:16202-16212.
31. Mihara M., Erster S., Zaika A., Petrenko O., Chittenden T., Pancoska P., Moll U.M. P53 has a direct apoptogenic role at the mitochondria. Mol. Cell 2003, 11:577-590.
32. Murray-Zmijewski F., Slee E.A., Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat. Rev. Mol. Cell Biol. 2008, 9:702-712.
33. Park J.W., Choi Y.J., Suh S.I., Baek W.K., Suh M.H., Jin I.N., Min D.S., Woo J.H., Chang J.S., Passaniti A., et al. Bcl-2 overexpression attenuates resveratrol-induced apoptosis in U937 cells by inhibition of caspase-3 activity. Carcinogenesis 2001, 22:1633-1639.
34. Patel K.R., Brown V.A., Jones D.J., Britton R.G., Hemingway D., Miller A.S., West K.P., Ooth T.D., Perloff M., Crowell J.A., et al. Pharmacology of resveratrol and its metabolites in colorectal cancer patients. Cancer Res. 2010, 70:7392-7399.
35. Pervaiz S., Holme A.L. Resveratrol: its biological targets and functional activity. Antioxid. Redox Signal. 2009, 11:2851-2897.
36. Pietsch E.C., Perchiniak E., Canutescu A.A., Wang G., Dunbrack R.L., Murphy M.E. Oligomerization of BAK by p53 utilizes conserved residues of the p53 DNA binding domain. J. Biol. Chem. 2008, 283:21294-21304.
37. Pommier Y., Leo E., Zhang H.L., Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 2010, 17:421-433.
38. Sarkaria J.N., Eshleman J.S. ATM as a target for novel radiosensitizers. Semin. Radiat. Oncol. 2001, 4:316-327.
39. Schroeter A., Marko D. Resveratrol modulates the topoisomerase inhibitory potential of doxorubicin in human colon carcinoma cells. Molecules 2014, 19:20054-20072.
40. Scully R., Xie A. Double strand break repair functions of histone H2AX. Mutat. Res. 2013, 750:5-14.
41. Shakibaei M., Harikumar K.B., Aggarwal B.B. Resveratrol addiction: to die or not to die. Mol. Nutr. Food Res. 2009, 53:115-128.
42. Shankar S., Singh G., Srivastava R.K. Chemoprevention by resveratrol: molecular mechanisms and therapeutic potential. Front. Biosci. 2007, 12:4839-4854.
43. She Q.-B., Bode A.M., Ma W.-Y., Chen N.-Y., Dong Z. Resveratrol-induced activation of p53 and apoptosis is mediated by extracellular-signal-regulated protein kinases and p38 kinase. Cancer Res. 2001, 61:1604-1610.
44. Toledo F., Wahl G.M. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 2006, 6:909-923.
45. Valdiglesias V., Giunta S., Fenech M., Neri M., Bonassi S. ΓH2AX as a marker of DNA double strand breaks and genomic instability in human population studies. Mutat. Res. 2013, 753:24-40.
46. Van Quaquebeke E., Mahieu T., Dumont P., Dewelle J., Ribaucour F., Simon G., Sauvage S., Gaussin J.-F., Tuti J., El Yazidi M., et al. 2,2,2-Trichloro-N-({2-[2-(dimethylamino)ethyl]-1,3-dioxo-2,3-dihydro-1H-benzo[de]isoquinolin- 5-yl}carbamoyl) acetamide (UNBS3157), a novel non hematotoxic naphthalimide derivative with potent antitumor activity. J. Med. Chem. 2007, 50:4122-4134.
47. Vang O., Ahmad N., Baile C.A., Baur J.A., Brown K., Csiszar A., Das D.K., Delmas D., Gottfried C., Lin H.-U., et al. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS ONE 2011, 6:e19881.
48. Vousden K.H., Lane D.P. P53 in health and disease. Nat. Rev. Mol. Cell Biol. 2007, 8:275-283.
49. Yamada M., Hayashi K., Hayashi H., Ikeda S., Hoshino T., Tsutsui K., Tsutsui K., Iinuma M., Nozaki H. Stilbenoids of Kobresia nepalensis (Cyperaceae) exhibiting DNA topoisomerase II inhibition. Phytochem 2006, 67:307-313.
50. Yang F., Teves S.S., Kemp C.J., Henikoff S. Doxorubicin, DNA torsion, and chromatin dynamics. Biochim. Biophys. Acta 2014, 1845:84-89.