Combination of HDAC and topoisomerase inhibitors in small cell lung cancer

Cancer Biology and Therapy

Volumn 13, Issue 8, 2012, Pages 614-622

  Gray, Jhanelle ^a   Cubitt, Christopher L ^a   Zhang, Shumin ^a   Chiappori, Alberto ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Combination therapy; HDAC; SCLC; Survival; Topoisomerase inhibitors

Indexed keywords

AMRUBICIN; CASPASE; CISPLATIN; DNA TOPOISOMERASE INHIBITOR; EPIRUBICIN; ETOPOSIDE; FLUOROURACIL; HISTONE DEACETYLASE INHIBITOR; MOCETINOSTAT; TOPOTECAN; VORINOSTAT; BENZAMIDE DERIVATIVE; CASPASE 3; HYDROXAMIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PYRIMIDINE DERIVATIVE;

ADD ON THERAPY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL VIABILITY; CLINICAL TRIAL; CUTANEOUS T CELL LYMPHOMA; DRUG CYTOTOXICITY; DRUG POTENTIATION; ENZYME ACTIVATION; HUMAN; IC 50; LUNG SMALL CELL CANCER; SOLID TUMOR; TREATMENT FAILURE; UNSPECIFIED SIDE EFFECT; DRUG EFFECTS; IC50; LUNG TUMOR; METABOLISM; SMALL CELL LUNG CANCER; TUMOR CELL LINE;

APOPTOSIS; BENZAMIDES; CASPASE 3; CELL LINE, TUMOR; DRUG SYNERGISM; ENZYME ACTIVATION; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; INHIBITORY CONCENTRATION 50; LUNG NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES; PYRIMIDINES; SMALL CELL LUNG CARCINOMA; TOPOISOMERASE INHIBITORS;

EID: 85047686704     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.19848     Document Type: Article

References (43)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics. CA Cancer J Clin 2010; 60:277-300; PMID:20610543; http://dx.doi.org/10.3322/caac.20073.
2. Jänne PA, Freidlin B, Saxman S, Johnson DH, Livingston RB, Shepherd FA, et al. Twenty-five years of clinical research for patients with limited-stage small cell lung carcinoma in North America. Cancer 2002; 95:1528-38; PMID:12237922; http://dx.doi.org/10.1002/cncr.10841.
3. Simon GR, Wagner H; American College of Chest Physicians. Small cell lung cancer. Chest 2003; 123:259-71; PMID:12527584; http://dx.doi.org/10.1378/chest. 123.1-suppl.259S.
4. Davies AM, Lara PN, Lau DH, Gandara DR. Treatment of extensive small cell lung cancer. Hematol Oncol Clin North Am 2004; 18:373-85; PMID:15094177; http://dx.doi.org/10.1016/j.hoc.2003.12.012.
5. Ardizzoni A, Hansen H, Dombernowsky P, Gamucci T, Kaplan S, Postmus P, et al. Topotecan, a new active drug in the second-line treatment of small-cell lung cancer: a phase II study in patients with refractory and sensitive disease. The European Organization for Research and Treatment of Cancer Early Clinical Studies Group and New Drug Development Office, and the Lung Cancer Cooperative Group. J Clin Oncol 1997; 15:2090-6; PMID:9164222.
6. von Pawel J, Schiller JH, Shepherd FA, Fields SZ, Kleisbauer JP, Chrysson NG, et al. Topotecan versus cyclophosphamide, doxorubicin and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol 1999; 17:658-67; PMID:10080612.
7. O'Brien ME, Ciuleanu TE, Tsekov H, Shparyk Y, Cuceviá B, Juhasz G, et al. Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J Clin Oncol 2006; 24:5441-7; PMID:17135646; http://dx.doi.org/10.1200/JCO.2006.06. 5821.
8. Onoda S, Masuda N, Seto T, Eguchi K, Takiguchi Y, Isobe H, et al.; Thoracic Oncology Research Group Study 0301. Phase II trial of amrubicin for treatment of refractory or relapsed small-cell lung cancer: Thoracic Oncology Research Group Study 0301. J Clin Oncol 2006; 24:5448-53; PMID:17135647; http://dx.doi.org/10.1200/JCO.2006.08.4145.
9. Ettinger DS, Jotte R, Lorigan P, Gupta V, Garbo L, Alemany C, et al. Phase II study of amrubicin as second-line therapy in patients with platinum-refractory small-cell lung cancer. J Clin Oncol 2010; 28:2598-603; PMID:20385980; http://dx.doi.org/10.1200/JCO.2009.26.7682.
10. Jotte R, Conkling P, Reynolds C, Galsky MD, Klein L, Fitzgibbons JF, et al. Randomized phase II trial of single-agent amrubicin or topotecan as second-line treatment in patients with small-cell lung cancer sensitive to first-line platinum-based chemotherapy. J Clin Oncol 2011; 29:287-93; PMID:21135284; http://dx.doi.org/10.1200/JCO.2010.29.8851.
11. Inoue A, Sugawara S, Yamazaki K, Maemondo M, Suzuki T, Gomi K, et al. Randomized phase II trial comparing amrubicin with topotecan in patients with previously treated small-cell lung cancer: North Japan Lung Cancer Study Group Trial 0402. J Clin Oncol 2008; 26:5401-6; PMID:18854562; http://dx.doi.org/10. 1200/JCO.2008.18.1974.
12. Pommier Y. DNA topoisomerase I inhibitors: chemistry, biology and interfacial inhibition. Chem Rev 2009; 109:2894-902; PMID:19476377; http://dx.doi.org/10.1021/cr900097c.
13. Pommier Y, Pourquier P, Urasaki Y, Wu J, Laco GS. Topoisomerase I inhibitors: selectivity and cellular resistance. Drug Resist Updat 1999; 2:307-18; PMID:11504505; http://dx.doi.org/10.1054/drup.1999.0102.
14. Brangi M, Litman T, Ciotti M, Nishiyama K, Kohlhagen G, Takimoto C, et al. Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR) and potential for glucuronidation in MXR-expressing cells. Cancer Res 1999; 59:5938-46; PMID:10606239.
15. Bates SE, Medina-Pérez WY, Kohlhagen G, Antony S, Nadjem T, Robey RW, et al. ABCG2 mediates differential resistance to SN-38 (7-ethyl-10- hydroxycamptothecin) and homocamptothecins. J Pharmacol Exp Ther 2004; 310:836-42; PMID:15075385; http://dx.doi.org/10.1124/jpet.103.063149.
16. Liao Z, Robey RW, Guirouilh-Barbat J, To KK, Polgar O, Bates SE, et al. Reduced expression of DNA topoisomerase I in SF295 human glioblastoma cells selected for resistance to homocamptothecin and diflomotecan. Mol Pharmacol 2008; 73:490-7; PMID:17984197; http://dx.doi.org/10.1124/mol.107.041178.
17. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005; 363:15-23; PMID:16289629; http://dx.doi.org/10. 1016/j.gene.2005.09.010.
18. Kim SC Sr, Sprung R, Chen Y, Xu Y, Ball H, Pei J, et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 2006; 23:607-18; PMID:16916647; http://dx.doi.org/10.1016/j.molcel.2006.06. 026.
19. Nimmanapalli R, Fuino L, Bali P, Gasparetto M, Glozak M, Tao J, et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res 2003; 63:5126-35; PMID:12941844.
20. Garcia-Manero G, Assouline S, Cortes J, Estrov Z, Kantarjian H, Yang H, et al. Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood 2008; 112:981-9; PMID:18495956; http://dx.doi.org/ 10.1182/blood-2007-10-115873.
21. Stimson L, Wood V, Khan O, Fotheringham S, La Thangue NB. HDAC inhibitor-based therapies and haematological malignancy. Ann Oncol 2009; 20:1293-302; PMID:19515748; http://dx.doi.org/10.1093/annonc/mdn792.
22. Fazzone W, Wilson PM, Labonte MJ, Lenz HJ, Ladner RD. Histone deacetylase inhibitors suppress thymidylate synthase gene expression and synergize with the fluoropyrimidines in colon cancer cells. Int J Cancer 2009; 125:463-73; PMID:19384949.
23. Li Z, Zhou N, Fournel M, et al. Antitumor Activities of MGCD0103, a novel and isotype-selective histone deacetylase inhibitor. Eur J Cancer Supp Mol Targets Cancer Ther 2004; 2:83.
24. Moradei O, Leit S, Zhou N, Fréchette S, Paquin I, Raeppel S, et al. Substituted N-(2-aminophenyl)-benzamides, (E)-N-(2-aminophenyl)-acrylamides and their analogues: novel classes of histone deacetylase inhibitors. Bioorg Med Chem Lett 2006; 16:4048-52; PMID:16713259; http://dx.doi.org/10.1016/j.bmcl. 2006.05.005.
25. Siu LL, Pili R, Duran I, Messersmith WA, Chen EX, Sullivan R, et al. Phase I study of MGCD0103 given as a three-times-per-week oral dose in patients with advanced solid tumors. J Clin Oncol 2008; 26:1940-7; PMID:18421048; http://dx.doi.org/10.1200/JCO.2007.14.5730.
26. Marchion DC, Bicaku E, Turner JG, Daud AI, Sullivan DM, Munster PN. Synergistic interaction between histone deacetylase and topoisomerase II inhibitors is mediated through topoisomerase IIbeta. Clin Cancer Res 2005; 11:8467-75; PMID:16322310; http://dx.doi.org/10.1158/1078-0432.CCR-05-1073.
27. Münster P, Marchion D, Bicaku E, Schmitt M, Lee JH, DeConti R, et al. Phase I trial of histone deacetylase inhibition by valproic acid followed by the topoisomerase II inhibitor epirubicin in advanced solid tumors: a clinical and translational study. J Clin Oncol 2007; 25:1979-85; PMID:17513804; http://dx.doi.org/10.1200/JCO.2006.08.6165.
28. Yoshida M, Kijima M, Akita M, Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem 1990; 265:17174-9; PMID:2211619.
29. Johnson CA, Padget K, Austin CA, Turner BM. Deacetylase activity associates with topoisomerase II and is necessary for etoposide-induced apoptosis. J Biol Chem 2001; 276:4539-42; PMID:11136718; http://dx.doi.org/10. 1074/jbc.C000824200.
30. Bevins RL, Zimmer SG. It's about time: scheduling alters effect of histone deacetylase inhibitors on camptothecin-treated cells. Cancer Res 2005; 65:6957-66; PMID:16061681; http://dx.doi.org/10.1158/0008-5472.CAN-05-0836.
31. Tsai SC, Valkov N, Yang WM, Gump J, Sullivan D, Seto E. Histone deacetylase interacts directly with DNA topoisomerase II. Nat Genet 2000; 26:349-53; PMID:11062478; http://dx.doi.org/10.1038/81671.
32. Catalano MG, Fortunati N, Pugliese M, Poli R, Bosco O, Mastrocola R, et al. Valproic acid, a histone deacetylase inhibitor, enhances sensitivity to doxorubicin in anaplastic thyroid cancer cells. J Endocrinol 2006; 191:465-72; PMID:17088416; http://dx.doi.org/10.1677/joe.1.06970.
33. Marchion DC, Bicaku E, Daud AI, Richon V, Sullivan DM, Munster PN. Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. J Cell Biochem 2004; 92:223-37; PMID:15108350; http://dx.doi.org/10.1002/jcb.20045.
34. Marchion DC, Bicaku E, Turner JG, Schmitt ML, Morelli DR, Munster PN. HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Mol Cancer Ther 2009; 8:794-801; PMID:19372552; http://dx.doi.org/10.1158/1535-7163.MCT-08- 0985.
35. Bruzzese F, Rocco M, Castelli S, Di Gennaro E, Desideri A, Budillon A. Synergistic antitumor effect between vorinostat and topotecan in small cell lung cancer cells is mediated by generation of reactive oxygen species and DNA damage-induced apoptosis. Mol Cancer Ther 2009; 8:3075-87; PMID:19887547; http://dx.doi.org/10.1158/1535-7163.MCT-09-0254.
36. Dedes KJ, Dedes I, Imesch P, von Bueren AO, Fink D, Fedier A. Acquired vorinostat resistance shows partial cross-resistance to 'second-generation' HDAC inhibitors and correlates with loss of histone acetylation and apoptosis but not with altered HDAC and HAT activities. Anticancer Drugs 2009; 20:321-33; PMID:19322073; http://dx.doi.org/10.1097/CAD.0b013e3283262a32.
37. Bhalla KN. Epigenetic and chromatin modifiers as targeted therapy of hematologic malignancies. J Clin Oncol 2005; 23:3971-93; PMID:15897549; http://dx.doi.org/10.1200/JCO.2005.16.600.
38. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997; 90:595-606; PMID:9288740.
39. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, Carrier F. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res 2003; 63:7291-300; PMID:14612526.
40. Piacentini P, Donadelli M, Costanzo C, Moore PS, Palmieri M, Scarpa A. Trichostatin A enhances the response of chemotherapeutic agents in inhibiting pancreatic cancer cell proliferation. Virchows Arch 2006; 448:797-804; PMID:16568310; http://dx.doi.org/10.1007/s00428-006-0173-x.
41. Nolan L, Johnson PW, Ganesan A, Packham G, Crabb SJ. Will histone deacetylase inhibitors require combination with other agents to fulfil their therapeutic potential? Br J Cancer 2008; 99:689-94; PMID:18728657; http://dx.doi.org/10.1038/sj.bjc.6604557.
42. Chou T, Ed. The median-effect principle and the combination index for quantitation of synergism and antagonism. San Diego: Academic Press 1991.
43. Chou TC. Theoretical basis, experimental design and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58:621-81; PMID:16968952; http://dx.doi.org/10.1124/pr.58.3.10.