Pre-clinical studies of epigenetic therapies targeting histone modifiers in lung cancer

Frontiers in Oncology

Volumn 3 SEP, Issue , 2013, Pages

  Huffman, Kenneth ^a   Martinez, Elisabeth D ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

BRD4; Epigenetic therapeutics; EZH2 inhibitors; HDAC inhibitors; Jumonji demethylases; Jumonji inhibitors; Lung cancer; Pre clinical studies

Indexed keywords

3 DEAZANEPLANOCIN A; BIM PROTEIN; CUDC 101; ENTINOSTAT; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; HISTONE; HISTONE DEACETYLASE INHIBITOR; HISTONE DEMETHYLASE; JIB 04; JQ 1; LSD 1; MATRIX METALLOPROTEINASE; PROTEIN KINASE C; PROTEIN P53; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; UVOMORULIN; VORINOSTAT;

CANCER GROWTH; CELL VIABILITY; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; LUNG CANCER; LUNG NON SMALL CELL CANCER; MOLECULARLY TARGETED THERAPY; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHORT SURVEY;

EID: 84891098436     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00235     Document Type: Short Survey

References (64)

1. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet (2002) 3(6):415-28.
2. Jones PA, Baylin SB. The epigenomics of cancer. Cell (2007) 128(4):683-92. doi:10.1016/j.cell.2007.01.029
3. Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med (2011) 17(3):330-9. doi:10.1038/nm.2305
4. Waldmann T, Schneider R. Targeting histone modifications-epigenetics in cancer. Curr Opin Cell Biol (2013) 25(2):184-9. doi:10.1016/j.ceb.2013.01.001
5. Ohashi K, Maruvka YE, Michor F, Pao W. Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J Clin Oncol (2013) 31(8):1070-80. doi:10.1200/JCO.2012.43.3912
6. Federico M, Bagella L. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J Biomed Biotechnol (2011) 2011:475641. doi:10.1155/2011/475641
7. Johnstone RW, Licht JD. Histone deacetylase inhibitors in cancer therapy: is transcription the primary target? Cancer Cell (2003) 4(1):13-8. doi:10.1016/S1535-6108(03)00165-X
8. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nat Rev Cancer (2006) 6(2):107-16. doi:10.1038/nrc1799
9. Pao W, Hutchinson KE. Chipping away at the lung cancer genome. Nat Med (2012) 18(3):349-51. doi:10.1038/nm.2697
10. Weinstein IB. Cancer. Addiction to oncogenes-the Achilles heal of cancer. Science (2002) 297(5578):63-4. doi:10.1126/science.1073096
11. Schrump DS. Targeting epigenetic mediators of gene expression in thoracic malignancies. Biochim Biophys Acta (2012) 1819(7):836-45. doi:10.1016/j.bbagrm.2012.03.009
12. Juergens RA, Wrangle J, Vendetti FP, Murphy SC, Zhao M, Coleman B, et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov (2011) 1(7):598-607. doi:10.1158/2159-8290.CD-11-0214
13. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science (2009) 325(5942):834-40. doi:10.1126/science.1175371
14. Azad N, Zahnow CA, Rudin CM, Baylin SB. The future of epigenetic therapy in solid tumours-lessons from the past. Nat Rev Clin Oncol (2013) 10(5):256-66. doi:10.1038/nrclinonc.2013.42
15. Witt O, Deubzer HE, Milde T, Oehme I. HDAC family: what are the cancer relevant targets? Cancer Lett (2009) 277(1):8-21. doi:10.1016/j.canlet.2008.08.016
16. Hassler MR, Egger G. Epigenomics of cancer-emerging new concepts. Biochimie (2012) 94(11):2219-30. doi:10.1016/j.biochi.2012.05.007
17. Song JS, Kim YS, Kim DK, Park SI, Jang SJ. Global histone modification pattern associated with recurrence and disease-free survival in non-small cell lung cancer patients. Pathol Int (2012) 62(3):182-90. doi:10.1111/j.1440-1827.2011.02776.x
18. Minamiya Y, Ono T, Saito H, Takahashi N, Ito M, Mitsui M, et al. Expression of histone deacetylase 1 correlates with a poor prognosis in patients with adenocarcinoma of the lung. Lung Cancer (2011) 74(2):300-4. doi:10.1016/j.lungcan.2011.02.019
19. Osada H, Tatematsu Y, Saito H, Yatabe Y, Mitsudomi T, Takahashi T. Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int J Cancer (2004) 112(1):26-32. doi:10.1002/ijc.20395
20. Liu F, Killian JK, Yang M, Walker RL, Hong JA, Zhang M, et al. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene (2010) 29(25):3650-64. doi:10.1038/onc.2010.129
21. Nagathihalli NS, Massion PP, Gonzalez AL, Lu P, Datta PK. Smoking induces epithelial-to-mesenchymal transition in non-small cell lung cancer through HDAC-mediated downregulation of E-cadherin. Mol Cancer Ther (2012) 11(11):2362-72. doi:10.1158/1535-7163.MCT-12-0107
22. O'Connor OA, Heaney ML, Schwartz L, Richardson S, Willim R, MacGregor-Cortelli B, et al. Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol (2006) 24(1):166-73. doi:10.1200/JCO.2005.01.9679
23. Miyanaga A, Gemma A, Noro R, Kataoka K, Matsuda K, Nara M, et al. Antitumor activity of histone deacetylase inhibitors in non-small cell lung cancer cells: development of a molecular predictive model. Mol Cancer Ther (2008) 7(7):1923-30. doi:10.1158/1535-7163.MCT-07-2140
24. Traynor AM, Dubey S, Eickhoff JC, Kolesar JM, Schell K, Huie MS, et al. Vorinostat (NSC# 701852) in patients with relapsed non-small cell lung cancer: a Wisconsin Oncology Network phase II study. J Thorac Oncol (2009) 4(4):522-6. doi:10.1097/JTO.0b013e3181952478
25. Li CT, Hsiao YM, Wu TC, Lin YW, Yeh KT, Ko JL. Vorinostat, SAHA, represses telomerase activity via epigenetic regulation of telomerase reverse transcriptase in non-small cell lung cancer cells. J Cell Biochem (2011) 112(10):3044-53. doi:10.1002/jcb.23229
26. Lin KT, Wang YW, Chen CT, Ho CM, Su WH, Jou YS. HDAC inhibitors augmented cell migration and metastasis through induction of PKCs leading to identification of low toxicity modalities for combination cancer therapy. Clin Cancer Res (2012) 18(17):4691-701. doi:10.1158/1078-0432.CCR-12-0633
27. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science (2004) 304(5676):1497-500. doi:10.1126/science.1099314
28. Witta SE, Dziadziuszko R, Yoshida K, Hedman K, Varella-Garcia M, Bunn PA Jr, et al. ErbB-3 expression is associated with E-cadherin and their coexpression restores response to gefitinib in non-small-cell lung cancer (NSCLC). Ann Oncol (2009) 20(4):689-95. doi:10.1093/annonc/mdn703
29. Witta SE, Gemmill RM, Hirsch FR, Coldren CD, Hedman K, Ravdel L, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res (2006) 66(2):944-50. doi:10.1158/0008-5472.CAN-05-1988
30. Witta SE, Jotte RM, Konduri K, Neubauer MA, Spira AI, Ruxer RL, et al. Randomized phase II trial of erlotinib with and without entinostat in patients with advanced non-small-cell lung cancer who progressed on prior chemotherapy. J Clin Oncol (2012) 30(18):2248-55. doi:10.1200/JCO.2011.38.9411
31. Nakagawa T, Takeuchi S, Yamada T, Ebi H, Sano T, Nanjo S, et al. EGFR-TKI resistance due to BIM polymorphism can be circumvented in combination with HDAC inhibition. Cancer Res (2013) 73(8):2428-34. doi:10.1158/0008-5472.CAN-12-3479
32. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, et al. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med (2007) 4(10):e315. doi:10.1371/journal.pmed.0040315 discussion 80
33. Liu JW, Chandra D, Tang SH, Chopra D, Tang DG. Identification and characterization of Bimgamma, a novel proapoptotic BH3-only splice variant of Bim. Cancer Res (2002) 62(10):2976-81.
34. Seo SK, Jin HO, Woo SH, Kim YS, An S, Lee JH, et al. Histone deacetylase inhibitors sensitize human non-small cell lung cancer cells to ionizing radiation through acetyl p53-mediated c-myc down-regulation. J Thorac Oncol (2011) 6(8):1313-9. doi:10.1097/JTO.0b013e318220caff
35. Cai X, Zhai HX, Wang J, Forrester J, Qu H, Yin L, et al. Discovery of 7-(4-(3-ethynylphenylamino)-7-methoxyquinazolin-6-yloxy)-N-hydroxyheptanamide (CUDc-101) as a potent multi-acting HDAC, EGFR, and HER2 inhibitor for the treatment of cancer. J Med Chem (2010) 53(5):2000-9. doi:10.1021/jm901453q
36. Lai CJ, Bao R, Tao X, Wang J, Atoyan R, Qu H, et al. CUDC-101, a multitargeted inhibitor of histone deacetylase, epidermal growth factor receptor, and human epidermal growth factor receptor 2, exerts potent anticancer activity. Cancer Res (2010) 70(9):3647-56. doi:10.1158/0008-5472.CAN-09-3360
37. Wang J, Pursell NW, Samson ME, Atoyan R, Ma AW, Selmi A, et al. Potential advantages of CUDC-101, a multitargeted HDAC, EGFR, and HER2 inhibitor, in treating drug resistance and preventing cancer cell migration and invasion. Mol Cancer Ther (2013) 12(6):925-36. doi:10.1158/1535-7163.MCT-12-1045
38. Qian C, Lai CJ, Bao R, Wang DG, Wang J, Xu GX, et al. Cancer network disruption by a single molecule inhibitor targeting both histone deacetylase activity and phosphatidylinositol 3-kinase signaling. Clin Cancer Res (2012) 18(15):4104-13. doi:10.1158/1078-0432.CCR-12-0055
39. Breuer RH, Snijders PJ, Smit EF, Sutedja TG, Sewalt RG, Otte AP, et al. Increased expression of the EZH2 polycomb group gene in BMI-1-positive neoplastic cells during bronchial carcinogenesis. Neoplasia (2004) 6(6):736-43. doi:10.1593/neo.04160
40. Byers LA, Wang J, Nilsson MB, Fujimoto J, Saintigny P, Yordy J, et al. Proteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1. Cancer Discov (2012) 2(9):798-811. doi:10.1158/2159-8290.CD-12-0112
41. Findeis-Hosey JJ, Huang J, Li F, Yang Q, McMahon LA, Xu H. High-grade neuroendocrine carcinomas of the lung highly express enhancer of zeste homolog 2, but carcinoids do not. Hum Pathol (2011) 42(6):867-72. doi:10.1016/j.humpath.2010.09.019
42. Wan L, Li X, Shen H, Bai X. Quantitative analysis of EZH2 expression and its correlations with lung cancer patients' clinical pathological characteristics. Clin Transl Oncol (2013) 15(2):132-8. doi:10.1007/s12094-012-0897-9
43. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev (2007) 21(9):1050-63. doi:10.1101/gad.1524107
44. Kikuchi J, Takashina T, Kinoshita I, Kikuchi E, Shimizu Y, Sakakibara-Konishi J, et al. Epigenetic therapy with 3-deazaneplanocin A, an inhibitor of the histone methyltransferase EZH2, inhibits growth of non-small cell lung cancer cells. Lung Cancer (2012) 78(2):138-43. doi:10.1016/j.lungcan.2012.08.003
45. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet (2008) 40(6):741-50. doi:10.1038/ng.159
46. Chen Y, Jie W, Yan W, Zhou K, Xiao Y. Lysine-specific histone demethylase 1 (LSD1): a potential molecular target for tumor therapy. Crit Rev Eukaryot Gene Expr (2012) 22(1):53-9. doi:10.1615/CritRevEukarGeneExpr.v22.i1.40
47. Yang M, Culhane JC, Szewczuk LM, Gocke CB, Brautigam CA, Tomchick DR, et al. Structural basis of histone demethylation by LSD1 revealed by suicide inactivation. Nat Struct Mol Biol (2007) 14(6):535-9. doi:10.1038/nsmb1255
48. Hayami S, Kelly JD, Cho HS, Yoshimatsu M, Unoki M, Tsunoda T, et al. Overexpression of LSD1 contributes to human carcinogenesis through chromatin regulation in various cancers. Int J Cancer (2011) 128(3):574-86. doi:10.1002/ijc.25349
49. Lv T, Yuan D, Miao X, Lv Y, Zhan P, Shen X, et al. Over-expression of LSD1 promotes proliferation, migration and invasion in non-small cell lung cancer. PLoS ONE (2012) 7(4):e35065. doi:10.1371/journal.pone.0035065
50. Hazeldine S, Pachaiyappan B, Steinbergs N, Nowotarski S, Hanson AS, Casero RA Jr, et al. Low molecular weight amidoximes that act as potent inhibitors of lysine-specific demethylase 1. J Med Chem (2012) 55(17):7378-91. doi:10.1021/jm3002845
51. Best AM, Chang J, Dull AB, Beutler JA, Martinez ED. Identification of four potential epigenetic modulators from the NCI structural diversity library using a cell-based assay. J Biomed Biotechnol (2011) 2011:868095. doi:10.1155/2011/868095
52. Johnson RL, Huang W, Jadhav A, Austin CP, Inglese J, Martinez ED. A quantitative high-throughput screen identifies potential epigenetic modulators of gene expression. Anal Biochem (2008) 375(2):237-48. doi:10.1016/j.ab.2007.12.028
53. King ON, Li XS, Sakurai M, Kawamura A, Rose NR, Ng SS, et al. Quantitative high-throughput screening identifies 8-hydroxyquinolines as cell-active histone demethylase inhibitors. PLoS ONE (2010) 5(11):e15535. doi:10.1371/journal.pone.0015535
54. Sayegh J, Cao J, Zou MR, Morales A, Blair LP, Norcia M, et al. Identification of small molecule inhibitors of Jumonji AT-rich interactive domain 1B (JARID1B) histone demethylase by a sensitive high throughput screen. J Biol Chem (2013) 288(13):9408-17. doi:10.1074/jbc.M112.419861
55. Wang L, Chang J, Varghese D, Dellinger M, Kumar S, Best AM, et al. A small molecule modulates Jumonji histone demethylase activity and selectively inhibits cancer growth. Nat Commun (2013) 4:2035. doi:10.1038/ncomms3035
56. Kogure M, Takawa M, Cho HS, Toyokawa G, Hayashi K, Tsunoda T, et al. Deregulation of the histone demethylase JMJD2A is involved in human carcinogenesis through regulation of the G1/S transition. Cancer Lett (2013) 336(1):76-84. doi:10.1016/j.canlet.2013.04.009
57. Wang Z, Wang C, Huang X, Shen Y, Shen J, Ying K. Differential proteome profiling of pleural effusions from lung cancer and benign inflammatory disease patients. Biochim Biophys Acta (2012) 1824(4):692-700. doi:10.1016/j.bbapap.2012.01.016
58. Toyokawa G, Cho HS, Iwai Y, Yoshimatsu M, Takawa M, Hayami S, et al. The histone demethylase JMJD2B plays an essential role in human carcinogenesis through positive regulation of cyclin-dependent kinase 6. Cancer Prev Res (Phila) (2011) 4(12):2051-61. doi:10.1158/1940-6207.CAPR-11-0290
59. Lu Y, Chang Q, Zhang Y, Beezhold K, Rojanasakul Y, Zhao H, et al. Lung cancer-associated JmjC domain protein mdig suppresses formation of tri-methyl lysine 9 of histone H3. Cell Cycle (2009) 8(13):2101-9. doi:10.4161/cc.8.13.8927
60. Teng YC, Lee CF, Li YS, Chen YR, Hsiao PW, Chan MY, et al. Histone demethylase RBP2 promotes lung tumorigenesis and cancer metastasis. Cancer Res (2013) 73(15):4711-21. doi:10.1158/0008-5472.CAN-12-3165
61. Zhang J, Ni SS, Zhao WL, Dong XC, Wang JL. High expression of JMJD6 predicts unfavorable survival in lung adenocarcinoma. Tumour Biol (2013) 34(4):2397-401. doi:10.1007/s13277-013-0789-9
62. Ott CJ, Kopp N, Bird L, Paranal RM, Qi J, Bowman T, et al. BET bromodomain inhibition targets both c-Myc and IL7R in high-risk acute lymphoblastic leukemia. Blood (2012) 120(14):2843-52. doi:10.1182/blood-2012-02-413021
63. Lockwood WW, Zejnullahu K, Bradner JE, Varmus H. Sensitivity of human lung adenocarcinoma cell lines to targeted inhibition of BET epigenetic signaling proteins. Proc Natl Acad Sci USA (2012) 109(47):19408-13. doi:10.1073/pnas.1216363109
64. Lu Q, Quinn AM, Patel MP, Semus SF, Graves AP, Bandyopadhyay D, et al. Perspectives on the discovery of small-molecule modulators for epigenetic processes. J Biomol Screen (2012) 17(5):555-71. doi:10.1177/1087057112437763