Non-toxic dose chidamide synergistically enhances platinum-induced DNA damage responses and apoptosis in Non-Small-Cell lung cancer cells

Biomedicine and Pharmacotherapy

Volumn 68, Issue 4, 2014, Pages 483-491

  Zhou, You ^a,b   Pan, De Si ^b   Shan, Song ^b   Zhu, Jing Zhong ^b   Zhang, Kun ^b   Yue, Xu Peng ^b   Nie, Li Ping ^c   Wan, Jun ^a   Lu, Xian Ping ^b   Zhang, Wei ^a   Ning, Zhi Qiang ^b  

^a Biomedical Research Institute   (China)

^b Chipscreen Biosciences Ltd   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

Carboplatin; Cisplatin; DNA damage; HDAC inhibitor; Non small cell lung cancer; Oxaliplatin

Indexed keywords

BIOLOGICAL MARKER; CARBOPLATIN; CHIDAMIDE; CISPLATIN; HISTONE DEACETYLASE INHIBITOR; HISTONE H2AX; HISTONE H3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OXALIPLATIN; UNCLASSIFIED DRUG; AMINOPYRIDINE DERIVATIVE; ANTINEOPLASTIC AGENT; BENZAMIDE DERIVATIVE; N-(2-AMINO-5-FLUOROBENZYL)-4-(N-(PYRIDINE-3-ACRYLYL)AMINOMETHYL)BENZAMIDE; PLATINUM COMPLEX;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL CYCLE ARREST; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG POTENTIATION; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; LUNG NON SMALL CELL CANCER; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; CARCINOMA, NON-SMALL-CELL LUNG; DOSE RESPONSE; DRUG EFFECTS; LUNG NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

AMINOPYRIDINES; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BENZAMIDES; CARBOPLATIN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FLOW CYTOMETRY; HUMANS; LUNG NEOPLASMS; ORGANOPLATINUM COMPOUNDS;

EID: 84901626822     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2014.03.011     Document Type: Article

References (61)

1. Jakopovic M., Thomas A., Lopez-Chavez A. From platinum compounds to targeted therapies in advanced thoracic malignancies. Anticancer Res 2014, 34:477-482.
2. Kobayashi K., Hagiwara K. Epidermal growth factor receptor (EGFR) mutation and personalized therapy in advanced nonsmall cell lung cancer (NSCLC). Target Oncol 2013, 8:27-33.
3. Fu S., Li Y., Huang J., Liu T., Hong Z., Chen A., et al. Aurora kinase inhibitor VE 465 synergistically enhances cytotoxicity of carboplatin in ovarian cancer cells through induction of apoptosis and downregulation of histone 3. Cancer Biol Ther 2012, 13:1034-1041.
4. Sun Y., Zhang T., Wang B., Li H., Li P. Tannic acid, an inhibitor of poly(ADP-ribose) glycohydrolase, sensitizes ovarian carcinoma cells to cisplatin. Anticancer Drugs 2012, 23:979-990.
5. Ercoli A., Scambia G., De Vincenzo R., Alimonti A., Petrucci F., Fattorossi A., et al. Tamoxifen synergizes the antiproliferative effect of cisplatin in human ovarian cancer cells: enhancement of DNA platination as a possible mechanism. Cancer Lett 1996, 108:7-14.
6. Stiborova M., Eckschlager T., Poljakova J., Hrabeta J., Adam V., Kizek R., et al. The synergistic effects of DNA-targeted chemotherapeutics and histone deacetylase inhibitors as therapeutic strategies for cancer treatment. Curr Med Chem 2012, 19:4218-4238.
7. Diyabalanage H.V., Granda M.L., Hooker J.M. Combination therapy: histone deacetylase inhibitors and platinum-based chemotherapeutics for cancer. Cancer Lett 2013, 329:1-8.
8. Knox R.J., Friedlos F., Lydall D.A., Roberts J.J. Mechanism of cytotoxicity of anticancer platinum drugs: evidence that cis-diamminedichloroplatinum(II) and cis-diammine-(1,1-cyclobutanedicarboxylato)platinum(II) differ only in the kinetics of their interaction with DNA. Cancer Res 1986, 46:1972-1979.
9. Florea A.M., Busselberg D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers (Basel) 2011, 3:1351-1371.
10. Glozak M.A., Seto E. Histone deacetylases and cancer. Oncogene 2007, 26:5420-5432.
11. Sharma S., Kelly T.K., Jones P.A. Epigenetics in cancer. Carcinogenesis 2010, 31:27-36.
12. Maeda T., Nagaoka Y., Kawai Y., Takagaki N., Yasuda C., Yogosawa S., et al. Inhibitory effects of cancer cell proliferation by novel histone deacetylase inhibitors involve p21/WAF1 induction and G2/M arrest. Biol Pharm Bull 2005, 28:849-853.
13. Wu Y., Guo S.W. Histone deacetylase inhibitors trichostatin A and valproic acid induce cell cycle arrest and p21 expression in immortalized human endometrial stromal cells. Eur J Obstet Gynecol Reprod Biol 2008, 137:198-203.
14. Hrabeta J., Stiborova M., Adam V., Kizek R., Eckschlager T. Histone deacetylase inhibitors in cancer therapy. A review. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2013, [Epub ahead of print]. 10.5507/bp.2013.085.
15. Duvic M., Talpur R., Ni X., Zhang C., Hazarika P., Kelly C., et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 2007, 109:31-39.
16. Olsen E.A., Kim Y.H., Kuzel T.M., Pacheco T.R., Foss F.M., Parker S., et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol 2007, 25:3109-3115.
17. Mackay H.J., Hirte H., Colgan T., Covens A., MacAlpine K., Grenci P., et al. Phase II trial of the histone deacetylase inhibitor belinostat in women with platinum resistant epithelial ovarian cancer and micropapillary (LMP) ovarian tumours. Eur J Cancer 2010, 46:1573-1579.
18. de Marinis F., Atmaca A., Tiseo M., Giuffreda L., Rossi A., Gebbia V., et al. A phase II study of the histone deacetylase inhibitor panobinostat (LBH589) in pretreated patients with small-cell lung cancer. J Thorac Oncol 2013, 8:1091-1094.
19. Graff J., Tsai L.H. Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 2013, 14:97-111.
20. Ning Z.Q., Li Z.B., Newman M.J., Shan S., Wang X.H., Pan D.S., et al. Chidamide (CS055/HBI-8000): a new histone deacetylase inhibitor of the benzamide class with antitumor activity and the ability to enhance immune cell-mediated tumor cell cytotoxicity. Cancer Chemother Pharmacol 2012, 69:901-909.
21. Gong K., Xie J., Yi H., Li W. CS055 (Chidamide/HBI-8000), a novel histone deacetylase inhibitor, induces G1 arrest, ROS-dependent apoptosis and differentiation in human leukaemia cells. Biochem J 2012, 443:735-746.
22. Liu L., Chen B., Qin S., Li S., He X., Qiu S., et al. A novel histone deacetylase inhibitor Chidamide induces apoptosis of human colon cancer cells. Biochem Biophys Res Commun 2010, 392:190-195.
23. Wang H., Guo Y., Fu M., Liang X., Zhang X., Wang R., et al. Antitumor activity of Chidamide in hepatocellular carcinoma cell lines. Mol Med Rep 2012, 5:1503-1508.
24. Li Y.Y., Wang Y.F., Wang J., Ke X.Y. [Effect of chidamide on human B lymphoma cell lines and its mechanisms]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2012, 20:893-899.
25. Qiao Z., Ren S., Li W., Wang X., He M., Guo Y., et al. Chidamide, a novel histone deacetylase inhibitor, synergistically enhances gemcitabine cytotoxicity in pancreatic cancer cells. Biochem Biophys Res Commun 2013, 434:95-101.
26. Yao Y., Zhou J., Wang L., Gao X., Ning Q., Jiang M., et al. Increased PRAME-specific CTL killing of acute myeloid leukemia cells by either a novel histone deacetylase inhibitor chidamide alone or combined treatment with decitabine. PLoS One 2013, 8:e70522.
27. Chou T.C., Talaly P. A simple generalized equation for the analysis of multiple inhibitions of Michaelis-Menten kinetic systems. J Biol Chem 1977, 252:6438-6442.
28. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
29. Xie H., Wise S.S., Holmes A.L., Xu B., Wakeman T.P., Pelsue S.C., et al. Carcinogenic lead chromate induces DNA double-strand breaks in human lung cells. Mutat Res 2005, 586:160-172.
30. Qi X., Zhang D., Xu X., Feng F., Ren G., Chu Q., et al. Oridonin nanosuspension was more effective than free oridonin on G2/M cell cycle arrest and apoptosis in the human pancreatic cancer PANC-1 cell line. Int J Nanomedicine 2012, 7:1793-1804.
31. + transport, and cisplatin-induced apoptosis in renal cells. J Biol Chem 2002, 277:43377-43388.
32. Cossarizza A., Salvioli S. Flow cytometric analysis of mitochondrial membrane potential using JC-1. Curr Protoc Cytom 2001, Chapter9:9-14.
33. Cepeda V., Fuertes M.A., Castilla J., Alonso C., Quevedo C., Perez J.M. Biochemical mechanisms of cisplatin cytotoxicity. Anticancer Agents Med Chem 2007, 7:3-18.
34. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998, 273:5858-5868.
35. Sedelnikova O.A., Rogakou E.P., Panyutin I.G., Bonner W.M. Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 2002, 158:486-492.
36. Trask B.J., Allen S., Massa H., Fertitta A., Sachs R., van den Engh G., et al. Studies of metaphase and interphase chromosomes using fluorescence in situ hybridization. Cold Spring Harb Symp Quant Biol 1993, 58:767-775.
37. Heck M.M. Condensins, cohesins, and chromosome architecture: how to make and break a mitotic chromosome. Cell 1997, 91:5-8.
38. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssiere J.L., Petit P.X., et al. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 1995, 181:1661-1672.
39. Reers M., Smiley S.T., Mottola-Hartshorn C., Chen A., Lin M., Chen L.B. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol 1995, 260:406-417.
40. Touma S.E., Goldberg J.S., Moench P., Guo X., Tickoo S.K., Gudas L.J., et al. Retinoic acid and the histone deacetylase inhibitor trichostatin a inhibit the proliferation of human renal cell carcinoma in a xenograft tumor model. Clin Cancer Res 2005, 11:3558-3566.
41. Kwa F.A., Balcerczyk A., Licciardi P., El-Osta A., Karagiannis T.C. Chromatin modifying agents - the cutting edge of anticancer therapy. Drug Discov Today 2011, 16:543-547.
42. Bots M., Johnstone R.W. Rational combinations using HDAC inhibitors. Clin Cancer Res 2009, 15:3970-3977.
43. Sawyers C. Targeted cancer therapy. Nature 2004, 432:294-297.
44. Kim M.S., Kwon H.J., Lee Y.M., Baek J.H., Jang J.E., Lee S.W., et al. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 2001, 7:437-443.
45. Ozaki K., Kishikawa F., Tanaka M., Sakamoto T., Tanimura S., Kohno M. Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Sci 2008, 99:376-384.
46. Sato T., Suzuki M., Sato Y., Echigo S., Rikiishi H. Sequence-dependent interaction between cisplatin and histone deacetylase inhibitors in human oral squamous cell carcinoma cells. Int J Oncol 2006, 28:1233-1241.
47. Yoon C.Y., Park M.J., Lee J.S., Lee S.C., Oh J.J., Park H., et al. The histone deacetylase inhibitor trichostatin A synergistically resensitizes a cisplatin resistant human bladder cancer cell line. J Urol 2011, 185:1102-1111.
48. Wang L.E., Yin M., Dong Q., Stewart D.J., Merriman K.W., Amos C.I., et al. DNA repair capacity in peripheral lymphocytes predicts survival of patients with non-small-cell lung cancer treated with first-line platinum-based chemotherapy. J Clin Oncol 2011, 29:4121-4128.
49. Matsuoka S., Rotman G., Ogawa A., Shiloh Y., Tamai K., Elledge S.J. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A 2000, 97:10389-10394.
50. Nur-E-Kamal A., Li T.K., Zhang A., Qi H., Hars E.S., Liu L.F. Single-stranded DNA induces ataxia telangiectasia mutant (ATM)/p53-dependent DNA damage and apoptotic signals. J Biol Chem 2003, 278:12475-12481.
51. Cortez D., Wang Y., Qin J., Elledge S.J. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 1999, 286:1162-1166.
52. Thurn K.T., Thomas S., Raha P., Qureshi I., Munster P.N. Histone deacetylase regulation of ATM-mediated DNA damage signaling. Mol Cancer Ther 2013, 12:2078-2087.
53. Miller K.M., Tjeertes J.V., Coates J., Legube G., Polo S.E., Britton S., et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 2010, 17:1144-1151.
54. Davis A.J., Chen D.J. DNA double strand break repair via non-homologous end-joining. Transl Cancer Res 2013, 2:130-143.
55. Van Lint C., Emiliani S., Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr 1996, 5:245-253.
56. Kim Y.B., Ki S.W., Yoshida M., Horinouchi S. Mechanism of cell cycle arrest caused by histone deacetylase inhibitors in human carcinoma cells. J Antibiot (Tokyo) 2000, 53:1191-1200.
57. Rosato R.R., Grant S. Histone deacetylase inhibitors in cancer therapy. Cancer Biol Ther 2003, 2:30-37.
58. Richon V.M., Sandhoff T.W., Rifkind R.A., Marks P.A. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci U S A 2000, 97:10014-10019.
59. Chen J., Lan T., Hou J., Zhang J., An Y., Tie L., et al. Atorvastatin sensitizes human non-small cell lung carcinomas to carboplatin via suppression of AKT activation and upregulation of TIMP-1. Int J Biochem Cell Biol 2012, 44:759-769.
60. Wang R.H., Liu C.W., Avramis V.I., Berndt N. Protein phosphatase 1alpha-mediated stimulation of apoptosis is associated with dephosphorylation of the retinoblastoma protein. Oncogene 2001, 20:6111-6122.
61. Suzuki M.M., Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008, 9:465-476.