Apigenin induces DNA damage through the PKCδ-dependent activation of ATM and H2AX causing down-regulation of genes involved in cell cycle control and DNA repair

Biochemical Pharmacology

Volumn 84, Issue 12, 2012, Pages 1571-1580

  Arango, Daniel ^a   Parihar, Arti ^a   Villamena, Frederick A ^a   Wang, Liwen ^a   Freitas, Michael A ^a   Grotewold, Erich ^a   Doseff, Andrea I ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; DNA damage; Flavonoids; PKC delta

Indexed keywords

APIGENIN; ATM PROTEIN; ATR PROTEIN; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C DELTA;

APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; ENZYME INHIBITION; G1 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LEUKEMIA CELL; MONOCYTIC LEUKEMIA; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA ANALYSIS;

APIGENIN; CASPASE 3; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DOWN-REGULATION; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS;

EID: 84869205521     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.09.005     Document Type: Article

References (63)

1. J.A. Ross, and C.M. Kasum Dietary flavonoids: bioavailability, metabolic effects, and safety Annu Rev Nutr 22 2002 19 34
2. E. Middleton Jr., C. Kandaswami, and T.C. Theoharides The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer Pharmacol Rev 52 2000 673 751
3. C. Rice-Evans, J.P. Spencer, H. Schroeter, and A.R. Rechner Bioavailability of flavonoids and potential bioactive forms in vivo Drug Metab Drug Interact 17 2000 291 310
4. B.H. Havsteen The biochemistry and medical significance of the flavonoids Pharmacol Ther 96 2002 67 202
5. S.E. Nielsen, J.F. Young, B. Daneshvar, S.T. Lauridsen, P. Knuthsen, and B. Sandstrom Effect of parsley (Petroselinum crispum) intake on urinary apigenin excretion, blood antioxidant enzymes and biomarkers for oxidative stress in human subjects Br J Nutr 81 1999 447 455
6. Y. Yao, W. Sang, M. Zhou, and G. Ren Phenolic composition and antioxidant activities of 11 celery cultivars J Food Sci 75 2010 C9 C13
7. K. Esposito, M. Ciotola, F. Giugliano, M. De Sio, G. Giugliano, and M. D'Armiento Mediterranean diet improves erectile function in subjects with the metabolic syndrome Int J Impot Res 18 2006 405 410
8. L. Skoldstam, L. Hagfors, and G. Johansson An experimental study of a Mediterranean diet intervention for patients with rheumatoid arthritis Ann Rheum Dis 62 2003 208 214
9. M.A. Gates, A.F. Vitonis, S.S. Tworoger, B. Rosner, L. Titus-Ernstoff, and S.E. Hankinson Flavonoid intake and ovarian cancer risk in a population-based case-control study Int J Cancer 124 2009 1918 1925
10. M.A. Vargo, O.H. Voss, F. Poustka, A.J. Cardounel, E. Grotewold, and A.I. Doseff Apigenin-induced-apoptosis is mediated by the activation of PKCδ and caspases in leukemia cells Biochem Pharmacol 72 2006 681 692
11. S. Shukla, and S. Gupta Apigenin-induced cell cycle arrest is mediated by modulation of MAPK, PI3K-Akt, and loss of cyclin D1 associated retinoblastoma dephosphorylation in human prostate cancer cells Cell Cycle 6 2007 1102 1114
12. F. Yin, A.E. Giuliano, R.E. Law, and A.J. Van Herle Apigenin inhibits growth and induces G2/M arrest by modulating cyclin-CDK regulators and ERK MAP kinase activation in breast carcinoma cells Anticancer Res 21 2001 413 420
13. M.E. Gonzalez-Mejia, O.H. Voss, E.J. Murnan, and A.I. Doseff Apigenin-induced apoptosis of leukemia cells is mediated by a bimodal and differentially regulated residue-specific phosphorylation of heat-shock protein-27 Cell Death Dis 1 2010 e64
14. R. Van Dross, Y. Xue, A. Knudson, and J.C. Pelling The chemopreventive bioflavonoid apigenin modulates signal transduction pathways in keratinocyte and colon carcinoma cell lines J Nutr 133 2003 3800S 3804S
15. S. Shukla, and S. Gupta Apigenin: a promising molecule for cancer prevention Pharm Res 27 2010 962 978
16. C.J. Lord, and A. Ashworth The DNA damage response and cancer therapy Nature 481 2012 287 294
17. J.L. Nitiss Targeting DNA topoisomerase II in cancer chemotherapy Nat Rev Cancer 9 2009 338 350
18. Y. Pommier Topoisomerase I inhibitors: camptothecins and beyond Nat Rev Cancer 6 2006 789 802
19. E.P. Rogakou, D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139 J Biol Chem 273 1998 5858 5868
20. C.E. Helt, W.A. Cliby, P.C. Keng, R.A. Bambara, and M.A. O'Reilly Ataxia telangiectasia mutated (ATM) and ATM and Rad3-related protein exhibit selective target specificities in response to different forms of DNA damage J Biol Chem 280 2005 1186 1192
21. C.J. Bakkenist, and M.B. Kastan DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation Nature 421 2003 499 506
22. M.B. Kastan, and D.S. Lim The many substrates and functions of ATM Nat Rev Mol Cell Biol 1 2000 179 186
23. K.A. Cimprich, and D. Cortez ATR: an essential regulator of genome integrity Nat Rev Mol Cell Biol 9 2008 616 627
24. B.B. Zhou, and S.J. Elledge The DNA damage response: putting checkpoints in perspective Nature 408 2000 433 439
25. A. Kinner, W. Wu, C. Staudt, and G. Iliakis Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin Nucleic Acids Res 36 2008 5678 5694
26. M.F. Lavin, G. Birrell, P. Chen, S. Kozlov, S. Scott, and N. Gueven ATM signaling and genomic stability in response to DNA damage Mutat Res 569 2005 123 132
27. C. Brodie, and P.M. Blumberg Regulation of cell apoptosis by protein kinase cδ Apoptosis 8 2003 19 27
28. M.E. Reyland, S.M. Anderson, A.A. Matassa, K.A. Barzen, and D.O. Quissell Protein kinase Cδ is essential for etoposide-induced apoptosis in salivary gland acinar cells J Biol Chem 274 1999 19115 19123
29. C. Clavijo, J.L. Chen, K.J. Kim, M.E. Reyland, and D.K. Ann Protein kinase Cδ-dependent and -independent signaling in genotoxic response to treatment of desferroxamine, a hypoxia-mimetic agent Am J Physiol Cell Physiol 292 2007 C2150 C2160
30. D.V. Bulavin, S. Saito, M.C. Hollander, K. Sakaguchi, C.W. Anderson, and E. Appella Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation EMBO J 18 1999 6845 6854
31. N.P. Singh, M.T. McCoy, R.R. Tice, and E.L. Schneider A simple technique for quantitation of low levels of DNA damage in individual cells Exp Cell Res 175 1988 184 191
32. K. Konca, A. Lankoff, A. Banasik, H. Lisowska, T. Kuszewski, and S. Gozdz A cross-platform public domain PC image-analysis program for the comet assay Mutat Res 534 2003 15 20
33. A.I. Doseff, J.H. Baker Jr., T.A. Bourgeois, and M.D. Wewers Interleukin-4-induced apoptosis entails caspase activation and suppression of extracellular signal-regulated kinase phosphorylation Am J Respir Cell Mol Biol 29 2003 367 374
34. C. Ren, L. Zhang, M.A. Freitas, K. Ghoshal, M.R. Parthun, and S.T. Jacob Peptide mass mapping of acetylated isoforms of histone H4 from mouse lymphosarcoma cells treated with histone deacetylase (HDACs) inhibitors J Am Soc Mass Spectrom 16 2005 1641 1653
35. G.K. Smyth Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat Appl Genet Mol Biol 3 2004 Article3
36. 2 and γ-irradiation with the alkaline comet assay Mutat Res 383 1997 71 80
37. K. Matkovic, V. Lukinovic-Skudar, H. Banfic, and D. Visnjic The activity of extracellular signal-regulated kinase is required during G2/M phase before metaphase-anaphase transition in synchronized leukemia cell lines Int J Hematol 89 2009 159 166
38. F. Boege, T. Straub, A. Kehr, C. Boesenberg, K. Christiansen, and A. Andersen Selected novel flavones inhibit the DNA binding or the DNA religation step of eukaryotic topoisomerase I J Biol Chem 271 1996 2262 2270
39. O.J. Bandele, and N. Osheroff Bioflavonoids as poisons of human topoisomerase II alpha and II beta Biochemistry 46 2007 6097 6108
40. I.K. Wang, S.Y. Lin-Shiau, and J.K. Lin Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells Eur J Cancer 35 1999 1517 1525
41. R.U. Janicke, M.L. Sprengart, M.R. Wati, and A.G. Porter Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis J Biol Chem 273 1998 9357 9360
42. N. Yamashita, and S. Kawanishi Distinct mechanisms of DNA damage in apoptosis induced by quercetin and luteolin Free Radic Res 33 2000 623 633
43. Y. Liu, K. Deng, J. Li, S. Liu, and S. Yao Investigation of double stranded DNA damage induced by quercetin-copper(II) using piezoelectric quartz crystal impedance technique and potentiometric stripping analysis Biophys Chem 112 2004 69 76
44. A. Rahman, F. Fazal, J. Greensill, K. Ainley, J.H. Parish, and S.M. Hadi Strand scission in DNA induced by dietary flavonoids: role of Cu(I) and oxygen free radicals and biological consequences of scission Mol Cell Biochem 111 1992 3 9
45. F. Fazal, A. Rahman, J. Greensill, K. Ainley, S.M. Hadi, and J.H. Parish Strand scission in DNA by quercetin and Cu(II): identification of free radical intermediates and biological consequences of scission Carcinogenesis 11 1990 2005 2008
46. K. Yoshida, T. Yamaguchi, H. Shinagawa, N. Taira, K.I. Nakayama, and Y. Miki Protein kinase Cδ activates topoisomerase IIα to induce apoptotic cell death in response to DNA damage Mol Cell Biol 26 2006 3414 3431
47. C. Lu, Y. Shi, Z. Wang, Z. Song, M. Zhu, and Q. Cai Serum starvation induces H2AX phosphorylation to regulate apoptosis via p38 MAPK pathway FEBS Lett 582 2008 2703 2708
48. K.E. Rakkestad, I. Skaar, V.E. Ansteinsson, A. Solhaug, J.A. Holme, and J.J. Pestka DNA damage and DNA damage responses in THP-1 monocytes after exposure to spores of either Stachybotrys chartarum or Aspergillus versicolor or to T-2 toxin Toxicol Sci 115 2010 140 155
49. T. Kobayashi, J. Kuroda, E. Ashihara, S. Oomizu, Y. Terui, and A. Taniyama Galectin-9 exhibits anti-myeloma activity through JNK and p38 MAP kinase pathways Leukemia 24 2010 843 850
50. P.W. Hsiao, C.C. Chang, H.F. Liu, C.M. Tsai, T.H. Chiu, and J.I. Chao Activation of p38 mitogen-activated protein kinase by celecoxib oppositely regulates survivin and (H2AX in human colorectal cancer cells Toxicol Appl Pharmacol 222 2007 97 104
51. H.C. Reinhardt, A.S. Aslanian, J.A. Lees, and M.B. Yaffe p53-Deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage Cancer Cell 11 2007 175 189
52. A. Bharti, S.K. Kraeft, M. Gounder, P. Pandey, S. Jin, and Z.M. Yuan Inactivation of DNA-dependent protein kinase by protein kinase Cδ: implications for apoptosis Mol Cell Biol 18 1998 6719 6728
53. Y. Emoto, Y. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, and M. Robertson Proteolytic activation of protein kinase Cδ by an ICE-like protease in apoptotic cells EMBO J 14 1995 6148 6156
54. S. Matsuoka, B.A. Ballif, A. Smogorzewska, E.R. McDonald 3rd, K.E. Hurov, and J. Luo ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 316 2007 1160 1166
55. P.W. Zheng, L.C. Chiang, and C.C. Lin Apigenin induced apoptosis through p53-dependent pathway in human cervical carcinoma cells Life Sci 76 2005 1367 1379
56. N. Takagaki, Y. Sowa, T. Oki, R. Nakanishi, S. Yogosawa, and T. Sakai Apigenin induces cell cycle arrest and p21/WAF1 expression in a p53-independent pathway Int J Oncol 26 2005 185 189
57. D.M. Lepley, and J.C. Pelling Induction of p21/WAF1 and G1 cell-cycle arrest by the chemopreventive agent apigenin Mol Carcinog 19 1997 74 82
58. M. McVean, W.C. Weinberg, and J.C. Pelling A p21(waf1)-independent pathway for inhibitory phosphorylation of cyclin-dependent kinase p34(cdc2) and concomitant G(2)/M arrest by the chemopreventive flavonoid apigenin Mol Carcinog 33 2002 36 43
59. D.M. Lepley, B. Li, D.F. Birt, and J.C. Pelling The chemopreventive flavonoid apigenin induces G2/M arrest in keratinocytes Carcinogenesis 17 1996 2367 2375
60. M. Shiohara, M. Akashi, A.F. Gombart, R. Yang, and H.P. Koeffler Tumor necrosis factor alpha: posttranscriptional stabilization of WAF1 mRNA in p53-deficient human leukemic cells J Cell Physiol 166 1996 568 576
61. K. Shoulars, M.A. Rodriguez, T. Thompson, and B.M. Markaverich Regulation of cell cycle and RNA transcription genes identified by microarray analysis of PC-3 human prostate cancer cells treated with luteolin J Steroid Biochem Mol Biol 118 2010 41 50
62. D. Cobrinik Regulatory interactions among E2Fs and cell cycle control proteins Curr Top Microbiol Immunol 208 1996 31 61
63. M. Malumbres, and M. Barbacid Cell cycle, CDKs and cancer: a changing paradigm Nat Rev Cancer 9 2009 153 166