Discovery of an orally active subtype-selective HDAC inhibitor, chidamide, as an epigenetic modulator for cancer treatment

MedChemComm

Volumn 5, Issue 12, 2014, Pages 1789-1796

  Pan, De Si ^a   Yang, Qian Jiao ^a   Fu, Xin ^a   Shan, Song ^a   Zhu, Jing Zhong ^a   Zhang, Kun ^a   Li, Zhi Bin ^a   Ning, Zhi Qiang ^a   Lu, Xian Ping ^a  

^a Shenzhen High Tech Industrial Park   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BENZAMIDE; CARBOPLATIN; CHIDAMIDE; ENTINOSTAT; FLUOROURACIL; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; ROMIDEPSIN; TRICHOSTATIN A; UNCLASSIFIED DRUG; VORINOSTAT;

ADENOID CYSTIC CARCINOMA; ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG STRUCTURE; ENZYME INHIBITION; EPIGENETICS; GENETIC REGULATION; HISTONE ACETYLATION; HUMAN; IN VIVO STUDY; NEUTROPENIA; PERIPHERAL T CELL LYMPHOMA; PHASE 1 CLINICAL TRIAL (TOPIC); REVIEW; SINGLE DRUG DOSE; THROMBOCYTOPENIA;

EID: 84911933639     PISSN: 20402503     EISSN: 20402511     Source Type: Journal    
DOI: 10.1039/c4md00350k     Document Type: Review

References (51)

1. S. B. Baylin P. A. Jones A decade of exploring the cancer epigenome - biological and translational implications Nat. Rev. Cancer 2011 11 10 726 734
2. J. S. You P. A. Jones Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell 2012 22 1 9 20
3. M. A. Dawson T. Kouzarides Cancer epigenetics: from mechanism to therapy Cell 2012 150 1 12 27
4. M. Haberland R. L. Montgomery E. N. Olson The many roles of histone deacetylases in development and physiology: implications for disease and therapy Nat. Rev. Genet. 2009 10 1 32 42
5. S. Minucci P. G. Pelicci Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer Nat. Rev. Cancer 2006 6 1 38 51
6. J. H. Dannenberg A. Berns Drugging Drug Resistance Cell 2010 141 1 18 20
7. N. Azad C. A. Zahnow C. M. Rudin S. B. Baylin The future of epigenetic therapy in solid tumours-lessons from the past Nat. Rev. Clin. Oncol. 2013 10 5 256 266
8. O. Witt H. E. Deubzer T. Milde I. Oehme HDAC family: What are the cancer relevant targets? Cancer Lett. 2009 277 1 8 21
9. F. M. Foss P. L. Zinzani J. M. Vose R. D. Gascoyne S. T. Rosen K. Tobinai Peripheral T-cell lymphoma Blood 2011 117 25 6756 6767
10. J. Vose J. Armitage D. Weisenburger International T-Cell Lymphoma Project. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes J. Clin. Oncol. 2008 26 25 4124 4130
11. Y. K. Shi X. N. Hong W. J. Zhang J. F. Feng J. Zhu L. Yu X. Y. Ke H. Q. Huang Z. X. Shen Y. Fan W. Li X. L. Zhao L. G. Qiu H. Huang Phase II study of chidamide (CS055), a new subtype-selective oral histone deacetylase inhibitor, in patients with relapsed or refractory peripheral T-cell lymphoma J. Clin. Oncol. 2013 31 15-suppl 8525
12. A. H. Xie B. Y. Li C. Z. Liao Z. B. Li X. P. Lu L. M. Shi J. J. Zhou Docking Study of HDAC Implication for Benzamide Inhibitors Binding Mode Acta Phys.-Chim. Sin. 2004 20 6 569 572
13. A. H. Xie C. Z. Liao Z. B. Li Z. Q. Ning W. M. Hu X. Lu L. M. Shi J. J. Zhou Quantitative Structure-Activity Relationship Study of Histone Deacetylase I inhibitors Curr. Med. Chem.: Anti-Cancer Agents 2004 4 3 273 299
14. Z. Q. Ning Z. B. Li M. J. Newman S. Shan X. H. Wang D. S. Pan J. Zhang M. Dong X. Du X. P. Lu 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 4 901 909
15. R. D. Kelly S. M. Cowley The physiological roles of histone deacetylase (HDAC) 1 and 2: complex co-stars with multiple leading parts Biochem. Soc. Trans. 2013 41 3 741 749
16. M. Bantscheff C. Hopf M. M. Savitski A. Dittmann P. Grandi A. M. Michon J. Schlegl Y. Abraham I. Becher G. Bergamini M. Boesche M. Delling B. Dümpelfeld D. Eberhard C. Huthmacher T. Mathieson D. Poeckel V. Reader K. Strunk G. Sweetman U. Kruse G. Neubauer N. G. Ramsden G. Drewes Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes Nat. Biotechnol. 2011 29 3 255 265
17. K. B. Glaser M. J. Staver J. F. Waring J. Stender R. G. Ulrich S. K. Davidsen Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines Mol. Cancer Ther. 2003 2 2 151 163
18. M. Dong Z. Q. Ning P. Y. Xing J. L. Xu H. X. Cao G. F. Dou Z. Y. Meng Y. K. Shi X. P. Lu F. Y. Feng Phase I study of chidamide (CS055/HBI-8000), a new histone deacetylase inhibitor, in patients with advanced solid tumors and lymphomas Cancer Chemother. Pharmacol. 2012 69 6 1413 1422
19. B. E. Lauffer R. Mintzer R. Fong S. Mukund C. Tam I. Zilberleyb B. Flicke A. Ritscher G. Fedorowicz R. Vallero D. F. Ortwine J. Gunzner Z. Modrusan L. Neumann C. M. Koth P. J. Lupardus J. S. Kaminker C. E. Heise P. Steiner Histone deacetylase (HDAC) inhibitor kinetic rate constants correlate with cellular histone acetylation but not transcription and cell viability J. Biol. Chem. 2013 288 37 26926 26943
20. T. Beckers C. Burkhardt H. Wieland P. Gimmnich T. Ciossek T. Maier K. Sanders Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group Int. J. Cancer 2007 121 5 1138 1148
21. C. J. Chou D. Herman J. M. Gottesfeld Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases J. Biol. Chem. 2008 283 51 35402 35409
22. W. K. Kelly O. A. O'Connor L. M. Krug J. H. Chiao M. Heaney T. Curley B. MacGregore-Cortelli W. Tong J. P. Secrist L. Schwartz S. Richardson E. Chu S. Olgac P. A. Marks H. Scher V. M. Richon Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer J. Clin. Oncol. 2005 23 17 3923 3931
23. ZOLINZA® (vorinostat) Prescribing information, https://www.merck.com/product/usa/pi-circulars/z/zolinza/zolinza-pi.pdf, accessed April 2013
24. ISTODAX (Romidepsin) Package Insert, http://www.istodax.com/pdfs/ISTODAX-PackageInsert.pdf, accessed June 2013
25. DACOGEN® (decitabine) Prescribing information, http://www.dacogen.com/content/documents/Dacogen-PI.pdf, accessed February 2014
26. K. Gong J. Xie H. Yi W. Li 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 3 735 746
27. S. S. Ramalingam S. Kummar J. Sarantopoulos S. Shibata P. LoRusso M. Yerk J. Holleran Y. Lin J. H. Beumer R. D. Harvey S. P. Ivy C. P. Belani M. J. Egorin Phase I study of vorinostat in patients with advanced solid tumors and hepatic dysfunction: a National Cancer Institute Organ Dysfunction Working Group study J. Clin. Oncol. 2010 28 29 4507 4512
28. A. S. Ho K. Kannan D. M. Roy L. G. Morris I. Ganly N. Katabi D. Ramaswami L. A. Walsh S. Eng J. T. Huse J. Zhang I. Dolgalev K. Huberman A. Heguy A. Viale M. Drobnjak M. A. Leversha C. E. Rice B. Singh N. G. Iyer C. R. Leemans E. Bloemena R. L. Ferris R. R. Seethala B. E. Gross Y. Liang R. Sinha L. Peng B. J. Raphael S. Turcan Y. Gong N. Schultz S. Kim S. Chiosea J. P. Shah C. Sander W. Lee T. A. Chan The mutational landscape of adenoid cystic carcinoma Nat. Genet. 2013 45 7 791 798
29. H. F. Frierson Jr C. A. Moskaluk Mutation signature of adenoid cystic carcinoma: evidence for transcriptional and epigenetic reprogramming J. Clin. Invest. 2013 123 7 2783 2785
30. V. Gelmetti J. Zhang M. Fanelli S. Minucci P. G. Pelicci M. A. Lazar Aberrant Recruitment of the Nuclear Receptor Corepressor-Histone Deacetylase Complex by the Acute Myeloid Leukemia Fusion Partner ETO Mol. Cell. Biol. 1998 18 12 7185 7191
31. S. Minucci C. Nervi F. Lo Coco P. G. Pelicci Histone deacetylases: a common molecular target for differentiation treatment of acute myeloid leukemias? Oncogene 2001 20 24 3110 3115
32. S. Liu L. C. Wu J. Pang R. Santhanam S. Schwind Y. Z. Wu C. J. Hickey J. Yu H. Becker K. Maharry M. D. Radmacher C. Li S. P. Whitman A. Mishra N. Stauffer A. M. Eiring R. Briesewitz R. A. Baiocchi K. K. Chan P. Paschka M. A. Caligiuri J. C. Byrd C. M. Croce C. D. Bloomfield D. Perrotti R. Garzon G. Marcucci Sp1/NFκB/HDAC/miR-29b Regulatory Network in KIT-driven Myeloid Leukemia Cancer Cell 2010 17 4 333 347
33. M. Schmudde A. Braun D. Pende J. Sonnemann U. Klier J. F. Beck L. Moretta B. M. Bröker Histone deacetylase inhibitors sensitize tumour cells for cytotoxic effects of natural killer cells Cancer Lett. 2008 272 1 110 121
34. Y. Yao J. Zhou L. Wang X. Gao Q. Ning M. Jiang J. Wang L. Wang L. Yu 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 8 e70522
35. U. H. Beier L. Wang R. Han T. Akimova Y. Liu W. W. Hancock Histone deacetylases 6 and 9 and sirtuin-1 control Foxp3+ regulatory T cell function through shared and isoform-specific mechanisms Sci. Signaling 2012 5 229 ra45
36. L. Wang R. Tao W. W. Hancock Using histone deacetylase inhibitors to enhance Foxp3(+) regulatory T-cell function and induce allograft tolerance Immunol. Cell Biol. 2009 87 3 195 202
37. L. Shen R. Pili Class I histone deacetylase inhibition is a novel mechanism to target regulatory T cells in immunotherapy OncoImmunology 2012 1 6 948 950
38. O. A. Botrugno T. Robert F. Vanoli M. Foiani S. Minucci Molecular pathways: old drugs define new pathways: non-histone acetylation at the crossroads of the DNA damage response and autophagy Clin. Cancer Res. 2012 18 9 2436 2442
39. T. Robert F. Vanoli I. Chiolo G. Shubassi K. A. Bernstein R. Rothstein O. A. Botrugno D. Parazzoli A. Oldani S. Minucci M. Foiani HDACs link the DNA damage response, processing of double-strand breaks and autophagy Nature 2011 471 7336 74 79
40. Y. Zhou D. S. Pan S. Shan J. Z. Zhu K. Zhang X. P. Yue L. P. Nie J. Wan X. P. Lu W. Zhang Z. Q. Ning Non-toxic dose chidamide synergistically enhances platinum-induced DNA damage responses and apoptosis in non-small-cell lung cancer cells Biomed. Pharmacother. 2014 68 4 483 491
41. T. Kiesslich M. Pichler D. Neureiter Epigenetic control of epithelial-mesenchymal-transition in human cancer Mol. Clin. Oncol. 2013 1 1 3 11
42. T. Braletz To differentiate or not-routes towards metastasis Nat. Rev. Cancer 2012 12 425 436
43. D. R. Pattabiraman R. A. Weinberg Tackling the cancer stem cells-what challenges do they pose? Nat. Rev. Drug Discovery 2014 13 7 497 512
44. Y. Shintani A. Okimura K. Sato T. Nakagiri Y. Kadota M. Inoue N. Sawabata M. Minami N. Ikeda K. Kawahara T. Matsumoto N. Matsuura M. Ohta M. Okumura Epithelial to mesenchymal transition is a determinant of sensitivity to chemoradiotherapy in non-small cell lung cancer Ann. Thorac. Surg. 2011 92 5 1794 1804
45. R. H. Wilting E. Yanover M. R. Heideman H. Jacobs J. Horner J. van der Torre R. A. DePinho J. H. Dannenberg Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis EMBO J. 2010 29 15 2586 2597
46. M. R. Heideman C. Lancini N. Proost E. Yanover H. Jacobs J. H. Dannenberg Sin3a associated Hdac1 and Hdac2 are essential for hematopoietic stem cell homeostasis and contribute differentially to hematopoiesis Haematologica 2014 99 8 1292 1303
47. B. Zhang A. C. Strauss S. Chu M. Li Y. Ho K. D. Shiang D. S. Snyder C. S. Huettner L. Shultz T. Holyoake R. Bhatia Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate Cancer Cell 2010 17 5 427 442
48. R. A. Juergens J. Wrangle F. P. Vendetti S. C. Murphy M. Zhao B. Coleman R. Sebree K. Rodgers C. M. Hooker N. Franco B. Lee S. Tsai I. E. Delgado M. A. Rudek S. A. Belinsky J. G. Herman S. B. Baylin M. V. Brock C. M. Rudin Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer Cancer Discovery 2011 1 7 598 607
49. S. E. Witta R. M. Jotte K. Konduri M. A. Neubauer A. I. Spira R. L. Ruxer M. Varella-Garcia P. A. Bunn Jr F. R. Hirsch 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 2255
50. D. A. Yardley R. R. Ismail-Khan B. Melichar M. Lichinitser P. N. Munster P. M. Klein S. Cruickshank K. D. Miller M. J. Lee J. B. Trepel Randomized phase II, double-blind, placebo-controlled study of exemestane with or without entinostat in postmenopausal women with locally recurrent or metastatic estrogen receptor-positive breast cancer progressing on treatment with a nonsteroidal aromatase inhibitor J. Clin. Oncol. 2013 31 17 2128 2135
51. T. Prebet T. Braun O. Beyne-Rauzy F. Dreyfus A. Stammatoullas E. Wattel S. Ame E. Raffoux J. Delaunay A. Charbonnier L. Adès P. Fenaux N. Vey Combination of vorinostat and low dose cytarabine for patients with azacitidine-refractory/relapsed high risk myelodysplastic syndromes Leuk. Res. 2014 38 1 29 33