2,638
Views
91
CrossRef citations to date
0
Altmetric
Research Paper

HDAC turnover, CtIP acetylation and dysregulated DNA damage signaling in colon cancer cells treated with sulforaphane and related dietary isothiocyanates

, , , , , , , & show all
Pages 612-623 | Received 20 Dec 2012, Accepted 15 Apr 2013, Published online: 26 Apr 2013

References

  • American Cancer Society. Cancer Facts & Figures 2012. Atlanta: American Cancer Society, 2013.
  • Herr I, Büchler MW. Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev 2010; 36:377 - 83; http://dx.doi.org/10.1016/j.ctrv.2010.01.002; PMID: 20172656
  • Higdon JV, Delage B, Williams DE, Dashwood RH. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res 2007; 55:224 - 36; http://dx.doi.org/10.1016/j.phrs.2007.01.009; PMID: 17317210
  • Keum YS, Jeong WS, Kong ANT. Chemoprevention by isothiocyanates and their underlying molecular signaling mechanisms. Mutat Res 2004; 555:191 - 202; http://dx.doi.org/10.1016/j.mrfmmm.2004.05.024; PMID: 15476860
  • Rajendran P, Williams DE, Ho E, Dashwood RH. Metabolism as a key to histone deacetylase inhibition. Crit Rev Biochem Mol Biol 2011; 46:181 - 99; http://dx.doi.org/10.3109/10409238.2011.557713; PMID: 21599534
  • Hsu A, Wong CP, Yu Z, Williams DE, Dashwood RH, Ho E. Promoter de-methylation of cyclin D2 by sulforaphane in prostate cancer cells. Clin Epigenetics 2011; 3:3; http://dx.doi.org/10.1186/1868-7083-3-3; PMID: 22303414
  • Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, et al. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 2011; 471:74 - 9; http://dx.doi.org/10.1038/nature09803; PMID: 21368826
  • Rajendran P, Ho E, Williams DE, Dashwood RH. Dietary phytochemicals, HDAC inhibition, and DNA damage/repair defects in cancer cells. Clin Epigenetics 2011; 3:4; http://dx.doi.org/10.1186/1868-7083-3-4; PMID: 22247744
  • Kaidi A, Weinert BT, Choudhary C, Jackson SP. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 2010; 329:1348 - 53; http://dx.doi.org/10.1126/science.1192049; PMID: 20829486
  • Marks PA, Xu WS. Histone deacetylase inhibitors: Potential in cancer therapy. J Cell Biochem 2009; 107:600 - 8; http://dx.doi.org/10.1002/jcb.22185; PMID: 19459166
  • Kachhap SK, Rosmus N, Collis SJ, Kortenhorst MS, Wissing MD, Hedayati M, et al. Downregulation of homologous recombination DNA repair genes by HDAC inhibition in prostate cancer is mediated through the E2F1 transcription factor. PLoS One 2010; 5:e11208; http://dx.doi.org/10.1371/journal.pone.0011208; PMID: 20585447
  • Rosato RR, Almenara JA, Maggio SC, Coe S, Atadja P, Dent P, et al. Role of histone deacetylase inhibitor-induced reactive oxygen species and DNA damage in LAQ-824/fludarabine antileukemic interactions. Mol Cancer Ther 2008; 7:3285 - 97; http://dx.doi.org/10.1158/1535-7163.MCT-08-0385; PMID: 18852132
  • Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, Yang CC, et al. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 2007; 67:5318 - 27; http://dx.doi.org/10.1158/0008-5472.CAN-06-3996; PMID: 17545612
  • Myzak MC, Karplus PA, Chung FL, Dashwood RH. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 2004; 64:5767 - 74; http://dx.doi.org/10.1158/0008-5472.CAN-04-1326; PMID: 15313918
  • Batra S, Sahu RP, Kandala PK, Srivastava SK. Benzyl isothiocyanate-mediated inhibition of histone deacetylase leads to NF-kappaB turnoff in human pancreatic carcinoma cells. Mol Cancer Ther 2010; 9:1596 - 608; http://dx.doi.org/10.1158/1535-7163.MCT-09-1146; PMID: 20484017
  • Lea MA, Randolph VM, Lee JE, desBordes C. Induction of histone acetylation in mouse erythroleukemia cells by some organosulfur compounds including allyl isothiocyanate. Int J Cancer 2001; 92:784 - 9; http://dx.doi.org/10.1002/ijc.1277; PMID: 11351296
  • Ma X, Fang Y, Beklemisheva A, Dai W, Feng J, Ahmed T, et al. Phenylhexyl isothiocyanate inhibits histone deacetylases and remodels chromatins to induce growth arrest in human leukemia cells. Int J Oncol 2006; 28:1287 - 93; PMID: 16596246
  • Wang LG, Liu XM, Fang Y, Dai W, Chiao FB, Puccio GM, et al. De-repression of the p21 promoter in prostate cancer cells by an isothiocyanate via inhibition of HDACs and c-Myc. Int J Oncol 2008; 33:375 - 80; PMID: 18636159
  • Dashwood RH, Myzak MC, Ho E. Dietary HDAC inhibitors: time to rethink weak ligands in cancer chemoprevention?. Carcinogenesis 2006; 27:344 - 9; http://dx.doi.org/10.1093/carcin/bgi253; PMID: 16267097
  • Rajendran P, Delage B, Dashwood WM, Yu TW, Wuth B, Williams DE, et al. Histone deacetylase turnover and recovery in sulforaphane-treated colon cancer cells: competing actions of 14-3-3 and Pin1 in HDAC3/SMRT corepressor complex dissociation/reassembly. Mol Cancer 2011; 10:68; http://dx.doi.org/10.1186/1476-4598-10-68; PMID: 21624135
  • Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461:1071 - 8; http://dx.doi.org/10.1038/nature08467; PMID: 19847258
  • Nakamura K, Kogame T, Oshiumi H, Shinohara A, Sumitomo Y, Agama K, et al. Collaborative action of Brca1 and CtIP in elimination of covalent modifications from double-strand breaks to facilitate subsequent break repair. PLoS Genet 2010; 6:e1000828; http://dx.doi.org/10.1371/journal.pgen.1000828; PMID: 20107609
  • Wilson AJ, Byun DS, Popova N, Murray LB, L’Italien K, Sowa Y, et al. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006; 281:13548 - 58; http://dx.doi.org/10.1074/jbc.M510023200; PMID: 16533812
  • Godman CA, Joshi R, Tierney BR, Greenspan E, Rasmussen TP, Wang HW, et al. HDAC3 impacts multiple oncogenic pathways in colon cancer cells with effects on Wnt and vitamin D signaling. Cancer Biol Ther 2008; 7:1570 - 80; http://dx.doi.org/10.4161/cbt.7.10.6561; PMID: 18769117
  • Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, Zheng S, et al. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 2010; 18:436 - 47; http://dx.doi.org/10.1016/j.ccr.2010.10.022; PMID: 21075309
  • Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun ZW, et al. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 2008; 30:61 - 72; http://dx.doi.org/10.1016/j.molcel.2008.02.030; PMID: 18406327
  • Conti C, Leo E, Eichler GS, Sordet O, Martin MM, Fan A, et al. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 2010; 70:4470 - 80; http://dx.doi.org/10.1158/0008-5472.CAN-09-3028; PMID: 20460513
  • Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858 - 68; http://dx.doi.org/10.1074/jbc.273.10.5858; PMID: 9488723
  • Pappa G, Bartsch H, Gerhäuser C. Biphasic modulation of cell proliferation by sulforaphane at physiologically relevant exposure times in a human colon cancer cell line. Mol Nutr Food Res 2007; 51:977 - 84; http://dx.doi.org/10.1002/mnfr.200700115; PMID: 17628879
  • Herman-Antosiewicz A, Johnson DE, Singh SV. Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res 2006; 66:5828 - 35; http://dx.doi.org/10.1158/0008-5472.CAN-06-0139; PMID: 16740722
  • Namdar M, Perez G, Ngo L, Marks PA. Selective inhibition of histone deacetylase 6 (HDAC6) induces DNA damage and sensitizes transformed cells to anticancer agents. Proc Natl Acad Sci U S A 2010; 107:20003 - 8; http://dx.doi.org/10.1073/pnas.1013754107; PMID: 21037108
  • Fimognari C, Turrini E, Ferruzzi L, Lenzi M, Hrelia P. Natural isothiocyanates: genotoxic potential versus chemoprevention. Mutat Res 2012; 750:107 - 31; http://dx.doi.org/10.1016/j.mrrev.2011.12.001; PMID: 22178957
  • Sharma R, Sharma A, Chaudhary P, Pearce V, Vatsyayan R, Singh SV, et al. Role of lipid peroxidation in cellular responses to D,L-sulforaphane, a promising cancer chemopreventive agent. Biochemistry 2010; 49:3191 - 202; http://dx.doi.org/10.1021/bi100104e; PMID: 20205397
  • Maynard S, Schurman SH, Harboe C, de Souza-Pinto NC, Bohr VA. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2009; 30:2 - 10; http://dx.doi.org/10.1093/carcin/bgn250; PMID: 18978338
  • Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase inhibitors and genomic instability. Cancer Lett 2009; 274:169 - 76; http://dx.doi.org/10.1016/j.canlet.2008.06.005; PMID: 18635312
  • Doyle K, Fitzpatrick FA. Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptional repressor function. J Biol Chem 2010; 285:17417 - 24; http://dx.doi.org/10.1074/jbc.M109.089250; PMID: 20385560
  • Rossetto D, Truman AW, Kron SJ, Côté J. Epigenetic modifications in double-strand break DNA damage signaling and repair. Clin Cancer Res 2010; 16:4543 - 52; http://dx.doi.org/10.1158/1078-0432.CCR-10-0513; PMID: 20823147
  • Subramanian C, Opipari AW Jr., Bian X, Castle VP, Kwok RPS. Ku70 acetylation mediates neuroblastoma cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2005; 102:4842 - 7; http://dx.doi.org/10.1073/pnas.0408351102; PMID: 15778293
  • Zhang JX, Li DQ, He AR, Motwani M, Vasiliou V, Eswaran J, et al. Synergistic inhibition of hepatocellular carcinoma growth by cotargeting chromatin modifying enzymes and poly (ADP-ribose) polymerases. Hepatology 2012; 55:1840 - 51; http://dx.doi.org/10.1002/hep.25566; PMID: 22223166
  • Sekine-Suzuki E, Yu D, Kubota N, Okayasu R, Anzai K. Sulforaphane induces DNA double strand breaks predominantly repaired by homologous recombination pathway in human cancer cells. Biochem Biophys Res Commun 2008; 377:341 - 5; http://dx.doi.org/10.1016/j.bbrc.2008.09.150; PMID: 18854174
  • Chernikova SB, Game JC, Brown JM. Inhibiting homologous recombination for cancer therapy. Cancer Biol Ther 2012; 13:61 - 8; http://dx.doi.org/10.4161/cbt.13.2.18872; PMID: 22336907
  • Cazaux C. [Genetic instability as a driver for oncogenesis]. Bull Cancer 2010; 97:1241 - 51; PMID: 21084240
  • Spurling CC, Godman CA, Noonan EJ, Rasmussen TP, Rosenberg DW, Giardina C. HDAC3 overexpression and colon cancer cell proliferation and differentiation. Mol Carcinog 2008; 47:137 - 47; http://dx.doi.org/10.1002/mc.20373; PMID: 17849419
  • Wang W, Jariyasopit N, Schrlau J, Jia Y, Tao S, Yu TW, et al. Concentration and photochemistry of PAHs, NPAHs, and OPAHs and toxicity of PM2.5 during the Beijing Olympic Games. Environ Sci Technol 2011; 45:6887 - 95; http://dx.doi.org/10.1021/es201443z; PMID: 21766847
  • Watson PJ, Fairall L, Santos GM, Schwabe JWR. Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 2012; 481:335 - 40; PMID: 22230954
  • Cardozo T, Totrov M, Abagyan R. Homology modeling by the ICM method. Proteins 1995; 23:403 - 14; http://dx.doi.org/10.1002/prot.340230314; PMID: 8710833
  • Totrov M, Abagyan R. Protein-Ligand Docking as an Energy Optimization Problem. In: Raffa RB, ed(s). Drug-Receptor Thermodynamics: Introduction and Experimental Applications. Vol 1, New York: John Wiley & Sons, 2001:603–24.
  • Abagyan R, Totrov M, Kuznetsov D. ICM—A new method for protein modeling and design: Applications to docking and structure prediction from the distorted native conformation. J Comput Chem 1994; 15:488 - 506; http://dx.doi.org/10.1002/jcc.540150503
  • Totrov M, Abagyan R. Flexible protein-ligand docking by global energy optimization in internal coordinates. Proteins 1997; Suppl 1 215 - 20; http://dx.doi.org/10.1002/(SICI)1097-0134(1997)1+<215::AID-PROT29>3.0.CO;2-Q; PMID: 9485515
  • Bisson WH, Koch DC, O’Donnell EF, Khalil SM, Kerkvliet NI, Tanguay RL, et al. Modeling of the aryl hydrocarbon receptor (AhR) ligand binding domain and its utility in virtual ligand screening to predict new AhR ligands. J Med Chem 2009; 52:5635 - 41; http://dx.doi.org/10.1021/jm900199u; PMID: 19719119