A novel small molecule hydroxamate preferentially inhibits HDAC6 activity and tumour growth

British Journal of Cancer

Volumn 108, Issue 2, 2013, Pages 342-350

  Kaliszczak, M ^a   Trousil, S ^a   Aberg O ^a   Perumal, M ^a   Nguyen, Q D ^a   Aboagye, E O ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Biomarkers; HDAC; PET; Pharmacology; Tumour

Indexed keywords

3' FLUOROTHYMIDINE F 18; ALPHA TUBULIN; ANTINEOPLASTIC AGENT; C 1A; CASPASE 3; CASPASE 7; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; UNCLASSIFIED DRUG; VORINOSTAT;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DNA ALKYLATION; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; GROWTH; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLID TUMOR; TREATMENT RESPONSE;

ACETYLATION; ANIMALS; APOPTOSIS; CASPASE 3; CELL CYCLE; CELL PROLIFERATION; FEMALE; GENE EXPRESSION; HCT116 CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROXAMIC ACIDS; KI-67 ANTIGEN; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; TUBULIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84873731735     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.576     Document Type: Article

References (45)

1. Balasubramanian S, Ramos J, Luo W, Sirisawad M, Verner E, Buggy JJ (2008) A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia 22(5): 1026-1034. (Pubitemid 351689885)
2. Bali P, Pranpat M, Bradner J, Balasis M, Fiskus W, Guo F, Rocha K, Kumaraswamy S, Boyapalle S, Atadja P, Seto E, Bhalla K (2005) 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 280(29): 26729-26734. (Pubitemid 41040705)
3. Banerji U, Walton M, Raynaud F, Grimshaw R, Kelland L, Valenti M, Judson I, Workman P (2005) Pharmacokinetic-pharmacodynamic relationships for the heat shock protein 90 molecular chaperone inhibitor 17-allylamino, 17-demethoxygeldanamycin in human ovarian cancer xenograft models. Clin Cancer Res 11(19 Pt 1): 7023-7032. (Pubitemid 41428762)
4. Boyault C, Sadoul K, Pabion M, Khochbin S (2007) HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 26(37): 5468-5476. (Pubitemid 47255928)
5. Bradner JE, West N, Grachan ML, Greenberg EF, Haggarty SJ, Warnow T, Mazitschek R (2010) Chemical phylogenetics of histone deacetylases. Nat Chem Biol 6(3): 238-243.
6. Bruserud O, Stapnes C, Ersvaer E, Gjertsen BT, Ryningen A (2007) Histone deacetylase inhibitors in cancer treatment: A review of the clinical toxicity and the modulation of gene expression in cancer cell. Curr Pharm Biotechnol 8(6): 388-400. (Pubitemid 350268198)
7. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, Kozikowski AP (2010) Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 132(31): 10842-10846.
8. Buyse M, Zeleniuch-Jacquotte A, Chalmers TC (1988) Adjuvant therapy of colorectal cancer. Why we still don't know. JAMA 259(24): 3571-3578.
9. Duvic M, VüJ (2007) Vorinostat: A new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 16(7): 1111-1120. (Pubitemid 47074165)
10. Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, Breslow R, Pavletich NP (1999) Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401(6749): 188-193. (Pubitemid 29436325)
11. Fotheringham S, Epping MT, Stimson L, Khan O, Wood V, Pezzella F, Bernards R, La Thangue NB (2009) Genome-wide loss-of-function screen reveals an important role for the proteasome in HDAC inhibitor-induced apoptosis. Cancer Cell 15(1): 57-66.
12. Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiology: Implications for disease and therapy. Nat Rev Genet 10(1): 32-42.
13. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL (2003) Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci USA 100(8): 4389-4394. (Pubitemid 36457739)
14. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417(6887): 455-458. (Pubitemid 34563539)
15. Janicke RÜ(2009) MCF-7 breast carcinoma cells do not express caspase-3. Breast Cancer Res Treat 117(1): 219-221.
16. Kaluza D, Kroll J, Gesierich S, Yao TP, Boon RA, Hergenreider E, Tjwa M, Rossig L, Seto E, Augustin HG, Zeiher AM, Dimmeler S, Urbich C (2011) Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin. EMBO J 30(20): 4142-4156.
17. Kawada J, ZoüP, Mazitschek R, Bradner JE, Cohen JI (2009) Tubacin kills Epstein-Barr virus (EBV)-Burkitt lymphoma cells by inducing reactive oxygen species and EBV lymphoblastoid cells by inducing apoptosis. J Biol Chem 284(25): 17102-17109.
18. Kazantsev AG, Thompson LM (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 7(10): 854-868.
19. LaBonte MJ, Wilson PM, Fazzone W, Groshen S, Lenz HJ, Ladner RD (2009) DNA microarray profiling of genes differentially regulated by the histone deacetylase inhibitors vorinostat and LBH589 in colon cancer cell lines. BMC Med Genomics 2: 67.
20. Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P, Sambucini S, Bottomley MJ, Lo Surdo P, Carfi A, Koch U, De Francesco R, Steinkuhler C, Gallinari P (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl Acad Sci USA 104(44): 17335-17340. (Pubitemid 350219843)
21. Lee YS, Lim KH, Guo X, Kawaguchi Y, Gao Y, Barrientos T, Ordentlich P, Wang XF, Counter CM, Yao TP (2008) The cytoplasmic deacetylase HDAC6 is required for efficient oncogenic tumorigenesis. Cancer Res 68(18): 7561-7569.
22. Leyton J, Alao JP, Da Costa M, StavropouloüAV, Latigo JR, Perumal M, Pillai R, He Q, Atadja P, Lam EW, Workman P, Vigushin DM, Aboagye EO (2006a) In vivo biological activity of the histone deacetylase inhibitor LAQ824 is detectable with 3'-deoxy-3'-[18F]fluorothymidine positron emission tomography. Cancer Res 66(15): 7621-7629. (Pubitemid 44289219)
23. Leyton J, Lockley M, Aerts JL, Baird SK, Aboagye EO, Lemoine NR, McNeish IA (2006b) Quantifying the activity of adenoviral E1A CR2 deletion mutants using renilla luciferase bioluminescence and 3'-deoxy-3'-[18F]fluorothymidine positron emission tomography imaging. Cancer Res 66(18): 9178-9185. (Pubitemid 44521138)
24. Leyton J, Smith G, Lees M, Perumal M, Nguyen QD, Aigbirhio FI, Golovko O, He Q, Workman P, Aboagye EO (2008) Noninvasive imaging of cell proliferation following mitogenic extracellular kinase inhibition by PD0325901. Mol Cancer Ther 7(9): 3112-3121.
25. Maloney A, Workman P (2002) HSP90 as a new therapeutic target for cancer therapy: The story unfolds. Expert Opin Biol Ther 2(1): 3-24. (Pubitemid 34462457)
26. Marks PA, XüWS (2009) Histone deacetylase inhibitors: Potential in cancer therapy. J Cell Biochem 107(4): 600-608.
27. Marsoni S, Damia G, Camboni G (2008) A work in progress: The clinical development of histone deacetylase inhibitors. Epigenetics 3(3): 164-171.
28. Matsuyama A, ShimazüT, Sumida Y, Saito A, YoshimatsüY, Seigneurin-Berny D, Osada H, KomatsüY, Nishino N, Khochbin S, Horinouchi S, Yoshida M (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21(24): 6820-6831. (Pubitemid 36014554)
29. Nguyen QD, Smith G, Glaser M, Perumal M, Arstad E, Aboagye EO (2009) Positron emission tomography imaging of drug-induced tumor apoptosis with a caspase-3/7 specific [18F]-labeled isatin sulfonamide. Proc Natl Acad Sci USA 106(38): 16375-16380.
30. Palijan A, Fernandes I, Bastien Y, Tang L, Verway M, Kourelis M, Tavera-Mendoza LE, Li Z, BourdeaüV, Mader S, Yang XJ, White JH (2009) Function of histone deacetylase 6 as a cofactor of nuclear receptor coregulator LCoR. J Biol Chem 284(44): 30264-30274.
31. Parmigiani RB, XüWS, Venta-Perez G, Erdjument-Bromage H, Yaneva M, Tempst P, Marks PA (2008) HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc Natl Acad Sci USA 105(28): 9633-9638. (Pubitemid 352031352)
32. Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, Zain J, Prince HM, Leonard JP, Geskin LJ, Reeder C, Joske D, Figg WD, Gardner ER, Steinberg SM, Jaffe ES, Stetler-Stevenson M, Lade S, Fojo AT, Bates SE (2009) Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol 27(32): 5410-5417.
33. Richon VM, Sandhoff TW, Rifkind RA, Marks PA (2000) Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci USA 97(18): 10014-10019.
34. Rivieccio MA, Brochier C, Willis DE, Walker BA, D'Annibale MA, McLaughlin K, Siddiq A, Kozikowski AP, Jaffrey SR, Twiss JL, Ratan RR, Langley B (2009) HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci USA 106(46): 19599-19604.
35. Santo L, Hideshima T, Kung AL, Tseng JC, Tamang D, Yang M, Jarpe M, van Duzer JH, Mazitschek R, Ogier WC, Cirstea D, Rodig S, Eda H, Scullen T, Canavese M, Bradner J, Anderson KC, Jones SS, Raje N (2012) Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood 119(11): 2579-2589.
36. Schultz BE, Misialek S, WüJ, Tang J, Conn MT, Tahilramani R, Wong L (2004) Kinetics and comparative reactivity of human class I and class IIb histone deacetylases. Biochemistry 43(34): 11083-11091. (Pubitemid 39433697)
37. Scroggins BT, Robzyk K, Wang D, MarcüMG, Tsutsumi S, Beebe K, Cotter RJ, Felts S, Toft D, Karnitz L, Rosen N, Neckers L (2007) An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 25(1): 151-159. (Pubitemid 46049066)
38. Shields AF, Grierson JR, Dohmen BM, Machulla HJ, Stayanoff JC, Lawhorn-Crews JM, Obradovich JE, Muzik O, Mangner TJ (1998) Imaging proliferation in vivo with [F-18]FLT and positron emission tomography. Nat Med 4(11): 1334-1336. (Pubitemid 28512118)
39. Vichai V, Kirtikara K (2006) Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc 1(3): 1112-1116.
40. Wilson AJ, Byun DS, Popova N, Murray LB, L'Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM (2006) 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 281(19): 13548-13558. (Pubitemid 43855268)
41. Witt O, Deubzer HE, Milde T, Oehme I (2009) HDAC family: What are the cancer relevant targets? Cancer Lett 277(1): 8-21.
42. Witter DJ, Harrington P, Wilson KJ, Chenard M, Fleming JC, Haines B, Kral AM, Secrist JP, Miller TA (2008) Optimization of biaryl Selective HDAC1&2 Inhibitors (SHI-1: 2). Bioorg Med Chem Lett 18(2): 726-731.
43. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, Eccles SA (2010) Guidelines for the welfare and use of animals in cancer research. Br J Cancer 102(11): 1555-1577.
44. XüWS, Parmigiani RB, Marks PA (2007) Histone deacetylase inhibitors: Molecular mechanisms of action. Oncogene 26(37): 5541-5552. (Pubitemid 47255934)
45. Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A, Koomen J, Olashaw N, Parsons JT, Yang XJ, Dent SR, Yao TP, Lane WS, Seto E (2007) HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell 27(2): 197-213. (Pubitemid 47058299)