Molecular and biologic analysis of histone deacetylase inhibitors with diverse specificities

Molecular Cancer Therapeutics

Volumn 12, Issue 12, 2013, Pages 2709-2721

  Newbold, Andrea ^a   Matthews, Geoffrey M ^a   Bots, Michael ^a   Cluse, Leonie A ^a   Clarke, Christopher J P ^a   Banks, Kellie Marie ^a   Cullinane, Carleen ^b   Bolden, Jessica E ^a   Christiansen, Ailsa J ^a   Dickins, Ross A ^c   Miccolo, Claudia ^f   Chiocca, Susanna ^f   Kral, Astrid M ^e   Ozerova, Nicole D ^e   Miller, Thomas A ^e   Methot, Joey L ^e   Richon, Victoria M ^e   Secrist, J Paul ^e   Minucci, Saverio ^f,g   Johnstone, Ricky W ^a,d  

^a Gene Regulation Laboratory   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e MERCK RESEARCH LABORATORIES   (United States)

^f EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^g UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BREAKPOINT CLUSTER REGION PROTEIN; CASPASE; ENZYME INHIBITOR; HISTONE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE INHIBITOR; IMATINIB; MRLB 223; ROMIDEPSIN; UNCLASSIFIED DRUG; VORINOSTAT;

ACETYLATION; ANIMAL CELL; ARTICLE; CANCER CELL; DEGRADATION; DRUG BLOOD LEVEL; DRUG STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACETYLATION; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; FUSION PROTEINS, BCR-ABL; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROXAMIC ACIDS; LYMPHOMA; MICE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84890487090     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0626     Document Type: Article

References (52)

1. Johnstone RW. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 2002;1:287-99.
2. Marks PA, Miller T, Richon VM. Histone deacetylases. Curr Opin Pharmacol 2003;3:344-51.
3. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006;5:769-84.
4. Kouzarides T. Acetylation: A regulatory modification to rival phosphorylation? EMBO J 2000;19:1176-9.
5. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005;363:15-23.
6. Kim SC, 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.
7. 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;325:834-40.
8. Zhou Q, Chaerkady R, Shaw PG, Kensler TW, Pandey A, Davidson NE. Screening for therapeutic targets of vorinostat by SILAC-based proteomic analysis in human breast cancer cells. Proteomics 2010;10: 1029-39.
9. Spiegel S, Milstien S, Grant S. Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 2012;31:537-51.
10. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006;6:38-51.
11. Rasheed WK, Johnstone RW, Prince HM. Histone deacetylase inhibitors in cancer therapy. Expert Opin Investig Drugs 2007;16: 659-78.
12. Insinga A, Monestiroli S, Ronzoni S, Gelmetti V, Marchesi F, Viale A, et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med 2005;11:71-6.
13. Lindemann RK, Newbold A, Whitecross KF, Cluse LA, Frew AJ, Ellis L, et al. Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proc Natl Acad Sci U S A 2007;104:8071-6.
14. Johnstone RW, Licht JD. Histone deacetylase inhibitors in cancer therapy: is transcription the primary target? Cancer Cell 2003;4: 13-8.
15. Bantscheff M, Hopf C, Savitski MM, Dittmann A, Grandi P, MichonAM, et al. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat Biotechnol 2011;29:255-65.
16. Balasubramanian S, Verner E, Buggy JJ. Isoform-specific histone deacetylase inhibitors: the next step? Cancer Lett 2009;280:211-21.
17. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci U S A 2003;100:4389-94.
18. Inoue S, Mai A, Dyer MJ, Cohen GM. Inhibition of histone deacetylase class 1 but not class 2 is critical for the sensitization of leukemic cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Cancer Res 2006;66:6785-92.
19. Haberland M, Johnson A, Mokalled MH, Montgomery RL, Olson EN. Genetic dissection of histone deacetylase requirement in tumor cells. Proc Natl Acad Sci U S A 2009;106:7751-5.
20. Glaser KB, Li J, Staver MJ, Wei RQ, Albert DH, Davidsen SK. Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem Biophys Res Commun 2003;310:529-36.
21. Wilson AJ, Byun DS, Popova N, L'Italien K, Sowa Y, Arango D, et al. Histone Deacetylase 3 (HDAC3) and other Class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006;281:13548-58.
22. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer 2005;5:761-72.
23. Budillon A, Bruzzese F, Di Gennaro E, Caraglia M. Multiple-target drugs: inhibitors of heat shock protein 90 and of histone deacetylase. Curr Drug Targets 2005;6:337-51.
24. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005;18:601-7.
25. Fuino L, Bali P, Wittmann S, Donapaty S, Guo F, Yamaguchi H, et al. Histone deacetylase inhibitor LAQ824 down-regulates Her-2 and sensitizes human breast cancer cells to trastuzumab, taxotere, gemcitabine, and epothilone B. Mol Cancer Ther 2003;2:971-84.
26. 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.
27. Bali P, George P, Cohen P, Tao J,GuoF, Sigua C, et al. Superior activity of the combination of histone deacetylase inhibitor LAQ824 and the FLT-3 kinase inhibitor PKC412 against human acute myelogenous leukemia cells with mutant FLT-3. Clin Cancer Res 2004;10:4991-7.
28. Yu X, Guo ZS, Marcu MG, Neckers L, Nguyen DM, Chen GA, et al. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst 2002;94:504-13.
29. Bali P, Pranpat M, Bradner J, Balasis M, Fiskus W, Guo F, 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: 26729-34.
30. Dexter TM, Garland J, Scott D, Scolnick E, Metcalf D. Growth of factordependent hemopoietic precursor cell lines. J Exp Med 1980;152: 1036-47.
31. Vert JP, Foveau N, Lajaunie C, Vandenbrouck Y. An accurate and interpretable model for siRNA efficacy prediction. BMC Bioinformatics 2006;7:520.
32. Peart MJ, Tainton KM, Ruefli AA, Dear AE, Sedelies KA, O'Reilly LA, et al. Novel mechanisms of apoptosis induced by histone deacetylase inhibitors. Cancer Res 2003;63:4460-71.
33. Essmann F, Engels IH, Totzke G, Schulze-Osthoff K, Janicke RU. Apoptosis resistance of MCF-7 breast carcinoma cells to ionizing radiation is independent of p53 and cell cycle control but caused by the lack of caspase-3 and a caffeine-inhibitable event. Cancer Res 2004;64:7065-72.
34. Berk SC, Close J, Hamblett C, Heidebrecht RW, Kattar SD, Kliman LT, et al. inventors. Spirocyclic compounds. 7,544,695 U.S. Patent, 2009, June 9.
35. Ruefli AA, Ausserlechner MJ, Bernhard D, Sutton VR, Tainton KM, Kofler R, et al. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci U S A 2001;98:10833-8.
36. Whitecross KF, Alsop AE, Cluse LA, Wiegmans A, Banks KM, Coomans C, et al. Defining the target specificity of ABT-737 and synergistic antitumor activities in combination with histone deacetylase inhibitors. Blood 2009;113:1982-91.
37. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002;417: 455-8.
38. Zhang Y, Li N, Caron C, Matthias G, Hess D, Khochbin S, et al. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 2003;22:1168-79.
39. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001;293:876-80.
40. Rao R, Nalluri S, Kolhe R, Yang Y, Fiskus W, Chen J, et al. Treatment with panobinostat induces glucose-regulated protein 78 acetylation and endoplasmic reticulum stress in breast cancer cells. Mol Cancer Ther 2010;9:942-52.
41. Kekatpure VD, Dannenberg AJ, Subbaramaiah K. HDAC6 modulates Hsp90 chaperone activity and regulates activation of aryl hydrocarbon receptor signaling. J Biol Chem 2009;284:7436-45.
42. Rasheed W, Bishton M, Johnstone RW, Prince HM. Histone deacetylase inhibitors in lymphoma and solid malignancies. Expert Rev Anticancer Ther 2008;8:413-32.
43. Vrana JA, Decker RH, Johnson CR, Wang Z, Jarvis WD, Richon VM, et al. Induction of apoptosis in U937 human leukemia cells by suberoylanilide hydroxamic acid (SAHA) proceeds through pathways that are regulated by Bcl-2/Bcl-XL, c-Jun, and p21CIP1, but independent of p53. Oncogene 1999;18:7016-25.
44. Singh TR, Shankar S, Srivastava RK. HDAC inhibitors enhance the apoptosis-inducing potential of TRAIL in breast carcinoma. Oncogene 2005;24:4609-23.
45. Bernhard D, Ausserlechner MJ, Tonko M, L€offler M, Hartmann BL Csordas A, et al. Apoptosis induced by the histone deacetylase inhibitor sodium butyrate in human leukemic lymphoblasts. FASEB J 1999;13:1991-2001.
46. Rosato RR, Almenara JA, Dai Y, Grant S. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2003;2: 1273-84.
47. Mitsiades N, Mitsiades CS, Richardson PG, McMullan C, Poulaki V, Fanourakis G, et al. Molecular sequelae of histone deacetylase inhibition in human malignant B cells. Blood 2003;101:4055-62.
48. Zhang XD, Gillespie SK, Borrow JM, Hersey P. The histone deacetylase inhibitor suberic bishydroxamate regulates the expression of multiple apoptotic mediators and induces mitochondria-dependent apoptosis of melanoma cells. Mol Cancer Ther 2004;3:425-35.
49. Newbold A, Lindemann RK, Cluse LA, Whitecross KF, Dear AE, Johnstone RW. Characterisation of the novel apoptotic and therapeutic activities of the histone deacetylase inhibitor romidepsin. Mol Cancer Ther 2008;7:1066-79.
50. Ellis L, Bots M, Lindemann RK, Bolden JE, Newbold A, Cluse LA, et al. The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood 2009;114:380-93.
51. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun ZW, et al. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 2008;30:61-72.
52. Nishioka C, Ikezoe T, Yang J, Takeuchi S, Koeffler HP, Yokoyama A. MS-275, a novel histone deacetylase inhibitor with selectivity against HDAC1, induces degradation of FLT3 via inhibition of chaperone function of heat shock protein 90 in AML cells. Leuk Res 2008;32: 1382-92.