Histone deacetylase inhibitor-mediated cell death is distinct from its global effect on chromatin

Molecular Oncology

Volumn 8, Issue 8, 2014, Pages 1379-1392

  Luchenko, Victoria L ^a   Litman, Thomas ^b   Chakraborty, Arup R ^a   Heffner, Aaron ^a   Devor, Christopher ^a   Wilkerson, Julia ^a   Stein, Wilfred ^a,c   Robey, Robert W ^a   Bangiolo, Lois ^a   Levens, David ^a   Bates, Susan E ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Leo Pharma   (Denmark)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Apoptosis; Cell context; Cell cycle arrest; HDAC inhibitors; Histone modification

Indexed keywords

LYSINE; ROMIDEPSIN; VORINOSTAT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER INHIBITION; CELL SURVIVAL; CHROMATIN; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG EXPOSURE; DRUG HALF LIFE; DRUG POTENCY; DRUG SENSITIVITY; EPIGENETICS; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PHENOTYPE; PROTEIN MICROARRAY; PROTEOMICS;

EID: 84911967733     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.05.001     Document Type: Article

References (49)

1. Amiri-Kordestani L., Luchenko V., Peer C.J., Ghafourian K., Reynolds J., Draper D., Frye R., Woo S., Venzon D., Wright J., et al. Phase I trial of a new schedule of romidepsin in patients with advanced cancers. Clin. Cancer Res. 2013, 19:4499-4507.
2. Bali P., Pranpat M., Bradner J., Balasis M., Fiskus W., Guo F., Rocha K., Kumaraswamy S., Boyapalle S., Atadja P., et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J.Biol. Chem. 2005, 280:26729-26734.
3. Bates S., Zhan Z., Steadman K., Obrzut T., Luchenko V., Frye R., Robey R., Turner M., Gardner E., Figg W., et al. Laboratory correlates for a phase II trial of romidepsin in cutaneous and peripheral T-cell lymphoma. Br. J. Haematol. 2010, 148:256-267.
4. Baumann P., Junghanns C., Mandl-Weber S., Strobl S., Oduncu F., Schmidmaier R. The pan-histone deacetylase inhibitor CR2408 disrupts cell cycle progression, diminishes proliferation and causes apoptosis in multiple myeloma cells. Br. J. Haematol. 2012, 156:633-642.
5. Blagosklonny M.V., Robey R., Sackett D.L., Du L., Traganos F., Darzynkiewicz Z., Fojo T., Bates S.E. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol. Cancer Ther. 2002, 1:937-941.
6. Bradner J.E., West N., Grachan M.L., Greenberg E.F., Haggarty S.J., Warnow T., Mazitschek R. Chemical phylogenetics of histone deacetylases. Nat. Chem. Biol. 2010, 6:238-243.
7. Chakraborty A.R., Robey R.W., Luchenko V.L., Zhan Z., Piekarz R.L., Gillet J.P., Kossenkov A.V., Wilkerson J., Showe L.C., Gottesman M.M., et al. MAPK pathway activation leads to Bim loss and histone deacetylase inhibitor resistance: rationale to combine romidepsin with a MEK inhibitor. Blood 2013.
8. Chen S., Dai Y., Pei X.Y., Grant S. Bim upregulation by histone deacetylase inhibitors mediates interactions with the Bcl-2 antagonist ABT-737: evidence for distinct roles for Bcl-2, Bcl-xL, and Mcl-1. Mol. Cell Biol. 2009, 29:6149-6169.
9. Conti C., Leo E., Eichler G., Sordet O., Martin M., Fan A., Aladjem M., Pommier Y. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res. 2010, 70:4470-4480.
10. Crabb S.J., Howell M., Rogers H., Ishfaq M., Yurek-George A., Carey K., Pickering B.M., East P., Mitter R., Maeda S., et al. Characterisation of the invitro activity of the depsipeptide histone deacetylase inhibitor spiruchostatin A. Biochem. Pharmacol. 2008, 76:463-475.
11. Glaser K.B., Staver M.J., Waring J.F., Stender J., Ulrich R.G., Davidsen S.K. 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, 2:151-163.
12. Gravina G.L., Marampon F., Giusti I., Carosa E., Di Sante S., Ricevuto E., Dolo V., Tombolini V., Jannini E.A., Festuccia C. Differential effects of PXD101 (belinostat) on androgen-dependent and androgen-independent prostate cancer models. Int. J. Oncol. 2012, 40:711-720.
13. Gu W., Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997, 90:595-606.
14. Gupta M., Han J.J., Stenson M., Wellik L., Witzig T.E. Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia 2012, 26:1356-1364.
15. Ieranò C., Basseville A., To K.K., Zhan Z., Robey R.W., Wilkerson J., Bates S.E., Scala S. Histone deacetylase inhibitors induce CXCR4 mRNA but antagonize CXCR4 migration. Cancer Biol. Ther. 2012, 14.
16. Imre G., Gekeler V., Leja A., Beckers T., Boehm M. Histone deacetylase inhibitors suppress the inducibility of nuclear factor-kappaB by tumor necrosis factor-alpha receptor-1 down-regulation. Cancer Res. 2006, 66:5409-5418.
17. Jiang X., Tsang Y.H., Yu Q. c-Myc overexpression sensitizes Bim-mediated Bax activation for apoptosis induced by histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through regulating Bcl-2/Bcl-xL expression. Int. J. Biochem. Cell Biol. 2007, 39:1016-1025.
18. Kaminskyy V.O., Surova O.V., Vaculova A., Zhivotovsky B. Combined inhibition of DNA methyltransferase and histone deacetylase restores caspase-8 expression and sensitizes SCLC cells to TRAIL. Carcinogenesis 2011, 32:1450-1458.
19. Kastan M.B., Bartek J. Cell-cycle checkpoints and cancer. Nature 2004, 432:316-323.
20. Khan O., La Thangue N.B. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol. Cell Biol. 2012, 90:85-94.
21. Kitazono M., Robey R., Zhan Z., Sarlis N.J., Skarulis M.C., Aikou T., Bates S., Fojo T. Low concentrations of the histone deacetylase inhibitor, depsipeptide (FR901228), increase expression of the Na(+)/I(-) symporter and iodine accumulation in poorly differentiated thyroid carcinoma cells. J.Clin. Endocrinol. Metab. 2001, 86:3430-3435.
22. Lane A., Chabner B. Histone deacetylase inhibitors in cancer therapy. J.Clin. Oncol. 2009, 27:5459-5468.
23. Marrocco-Tallarigo D.L., Centenera M.M., Scher H.I., Tilley W.D., Butler L.M. Finding the place of histone deacetylase inhibitors in prostate cancer therapy. Expert Rev. Clin. Pharmacol. 2009, 2:619-630.
24. Mitić T., McKay J.S. Immunohistochemical analysis of acetylation, proliferation, mitosis, and apoptosis in tumor xenografts following administration of a histone deacetylase inhibitor-a pilot study. Toxicol. Pathol. 2005, 33:792-799.
25. Nebbioso A., Clarke N., Voltz E., Germain E., Ambrosino C., Bontempo P., Alvarez R., Schiavone E.M., Ferrara F., Bresciani F., et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat. Med. 2005, 11:77-84.
26. Newbold A., Lindemann R.K., Cluse L.A., Whitecross K.F., Dear A.E., Johnstone R.W. Characterisation of the novel apoptotic and therapeutic activities of the histone deacetylase inhibitor romidepsin. Mol. Cancer Ther. 2008, 7:1066-1079.
27. Olsen E.A., Kim Y.H., Kuzel T.M., Pacheco T.R., Foss F.M., Parker S., Frankel S.R., Chen C., Ricker J.L., Arduino J.M., Duvic M. 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.
28. Palmieri D., Lockman P.R., Thomas F.C., Hua E., Herring J., Hargrave E., Johnson M., Flores N., Qian Y., Vega-Valle E., et al. Vorinostat inhibits brain metastatic colonization in a model of triple-negative breast cancer and induces DNA double-strand breaks. Clin. Cancer Res. 2009, 15:6148-6157.
29. Peart M.J., Smyth G.K., van Laar R.K., Bowtell D.D., Richon V.M., Marks P.A., Holloway A.J., Johnstone R.W. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc. Natl. Acad. Sci. U S A 2005, 102:3697-3702.
30. Piekarz R., Bates S. Epigenetic modifiers: basic understanding and clinical development. Clin. Cancer Res. 2009, 15:3918-3926.
31. Piekarz R.L., Frye R., Prince H.M., Kirschbaum M.H., Zain J., Allen S.L., Jaffe E.S., Ling A., Turner M., Peer C.J., et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood 2011, 117:5827-5834.
32. Piekarz R.L., Frye R., Turner M., Wright J.J., Allen S.L., Kirschbaum M.H., Zain J., Prince H.M., Leonard J.P., Geskin L.J., et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J.Clin. Oncol. 2009, 27:5410-5417.
33. Piekarz R.L., Robey R., Sandor V., Bakke S., Wilson W.H., Dahmoush L., Kingma D.M., Turner M.L., Altemus R., Bates S.E. Inhibitor of histone deacetylation, depsipeptide (FR901228), in the treatment of peripheral and cutaneous T-cell lymphoma: a case report. Blood 2001, 98:2865-2868.
34. Richon V.M., Webb Y., Merger R., Sheppard T., Jursic B., Ngo L., Civoli F., Breslow R., Rifkind R.A., Marks P.A. Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc. Natl. Acad. Sci. U S A 1996, 93:5705-5708.
35. Robbins A.R., Jablonski S.A., Yen T.J., Yoda K., Robey R., Bates S.E., Sackett D.L. Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 2005, 4:717-726.
36. Robey R.W., Chakraborty A.R., Basseville A., Luchenko V., Bahr J., Zhan Z., Bates S.E. Histone deacetylase inhibitors: emerging mechanisms of resistance. Mol. Pharm. 2011, 8:2021-2031.
37. Robey R.W., Zhan Z., Piekarz R.L., Kayastha G.L., Fojo T., Bates S.E. Increased MDR1 expression in normal and malignant peripheral blood mononuclear cells obtained from patients receiving depsipeptide (FR901228, FK228, NSC630176). Clin. Cancer Res. 2006, 12:1547-1555.
38. Rosato R., Grant S. Histone deacetylase inhibitors in cancer therapy. Cancer Biol. Ther. 2003, 2:30-37.
39. Sandor V., Senderowicz A., Mertins S., Sackett D., Sausville E., Blagosklonny M.V., Bates S.E. P21-dependent g(1)arrest with downregulation of cyclin D1 and upregulation of cyclin E by the histone deacetylase inhibitor FR901228. Br. J. Cancer 2000, 83:817-825.
40. Shao W., Growney J.D., Feng Y., O'Connor G., Pu M., Zhu W., Yao Y.M., Kwon P., Fawell S., Atadja P. Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: defining molecular mechanisms of resistance. Int. J. Cancer 2010, 127:2199-2208.
41. Venugopal B., Evans T.R. Developing histone deacetylase inhibitors as anti-cancer therapeutics. Curr. Med. Chem. 2011, 18:1658-1671.
42. Xargay-Torrent S., López-Guerra M., Saborit-Villarroya I., Rosich L., Campo E., Roué G., Colomer D. Vorinostat-induced apoptosis in mantle cell lymphoma is mediated by acetylation of proapoptotic BH3-only gene promoters. Clin. Cancer Res. 2011, 17:3956-3968.
43. Xiao J.J., Huang Y., Dai Z., Sadée W., Chen J., Liu S., Marcucci G., Byrd J., Covey J.M., Wright J., et al. Chemoresistance to depsipeptide FK228 [(E)-(1S,4S,10S,21R)-7-[(Z)-ethylidene]-4,21-diisopropyl-2-oxa-12,13-dithia-5,8,20,23-tetraazabicyclo[8,7,6]-tricos-16-ene-3,6,9,22-pentanone] is mediated by reversible MDR1 induction in human cancer cell lines. J.Pharmacol. Exp. Ther. 2005, 314:467-475.
44. Xu W., Parmigiani R., Marks P. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007, 26:5541-5552.
45. Yang Y., Zhao Y., Liao W., Yang J., Wu L., Zheng Z., Yu Y., Zhou W., Li L., Feng J., et al. Acetylation of FoxO1 activates Bim expression to induce apoptosis in response to histone deacetylase inhibitor depsipeptide treatment. Neoplasia 2009, 11:313-324.
46. Yeh C.C., Deng Y.T., Sha D.Y., Hsiao M., Kuo M.Y. Suberoylanilide hydroxamic acid sensitizes human oral cancer cells to TRAIL-induced apoptosis through increase DR5 expression. Mol. Cancer Ther. 2009, 8:2718-2725.
47. Yu X.D., Wang S.Y., Chen G.A., Hou C.M., Zhao M., Hong J.A., Nguyen D.M., Schrump D.S. Apoptosis induced by depsipeptide FK228 coincides with inhibition of survival signaling in lung cancer cells. Cancer J. 2007, 13:105-113.
48. Zhang C., Richon V., Ni X., Talpur R., Duvic M. Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. J.Invest. Dermatol. 2005, 125:1045-1052.
49. Zhang Y., Li N., Caron C., Matthias G., Hess D., Khochbin S., Matthias P. HDAC-6 interacts with and deacetylates tubulin and microtubules invivo. EMBO J. 2003, 22:1168-1179.