Identification of Highly Selective and Potent Histone Deacetylase 3 Inhibitors Using Click Chemistry-Based Combinatorial Fragment Assembly

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Suzuki, Takayoshi ^a,b   Kasuya, Yuki ^c   Itoh, Yukihiro ^a   Ota, Yosuke ^a   Zhan, Peng ^a   Asamitsu, Kaori ^d   Nakagawa, Hidehiko ^c   Okamoto, Takashi ^d   Miyata, Naoki ^c  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

^d NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYNE; AZIDE; COPPER; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 3 INHIBITOR; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P53; T 247; T 326; TRIAZOLE; UNCLASSIFIED DRUG; VORINOSTAT; ZINC;

ACETYLATION; ANTINEOPLASTIC ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CANCER CELL CULTURE; CLICK CHEMISTRY; CONCENTRATION RESPONSE; DRUG IDENTIFICATION; DRUG POTENCY; DRUG SELECTIVITY; DRUG STRUCTURE; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IC 50;

EID: 84880715554     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068669     Document Type: Article

References (55)

1. Glozak MA, Sengupta N, Zhang X, Seto E, (2005) Acetylation and deacetylation of non-histone proteins. Gene 7: 15-23.
2. Yoshida M, Shimazu T, Matsuyama A, (2003) Protein deacetylases: enzymes with functional diversity as novel therapeutic targets. Prog Cell Cycle Res 5: 269-278.
3. Sterner DE, Berger SL, (2000) Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64: 435-459.
4. Itoh Y, Suzuki T, Miyata N, (2008) Isoform-selective histone deacetylase inhibitors. Curr Pharm Des 14: 529-544.
5. Biel M, Wascholowski V, Giannis A, (2005) Epigenetics- An epicenter of gene regulation: Histones and histone-modifying enzymes. Angew Chem Int Ed 44: 3186-3216.
6. Mai A, Massa S, Rotili D, Cerbara I, Valente S, et al. (2005) Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med Res Rev 25: 261-309.
7. Suzuki T, Miyata N, (2006) Epigenetic control using natural products and synthetic molecules. Curr Med Chem 13: 935-958.
8. Schaefer S, Jung M, (2005) Chromatin modifications as targets for new anticancer drugs. Arch Pharm 338: 347-357.
9. Wen YD, Perissi V, Staszewski LM, Yang WM, Krones A, et al. (2000) The histone deacetylase-3 complex contains nuclear receptor corepressors. Proc Natl Acad Sci USA 97: 7202-7207.
10. Takami Y, Nakayama T, (2000) N-terminal region, C-terminal region, nuclear export signal, and deacetylation activity of histone deacetylase-3 are essential for the viability of the DT40 chicken B cell line. J Biol Chem 275: 16191-16201.
11. Longworth MS, Laimins LA, (2006) Histone deacetylase 3 localizes to the plasma membrane and is a substrate of Src. Oncogene 25: 4495-4500.
12. Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, et al. (2010) Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 18: 436-447.
13. Chen LF, Fischle W, Verdin E, Greene WC, (2001) Duration of nuclear NF-κB action regulated by reversible acetylation. Science 293: 1653-1657.
14. Hoberg JE, Popko AE, Ramsey CS, Mayo MW, (2006) IκB kinase α-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol Cell Biol 26: 457-471.
15. Grégoire S, Xiao L, Nie J, Zhang X, Xu M, et al. (2007) Histone deacetylase 3 interacts with and deacetylates myocyte enhancer factor 2. Mol Cell Biol 27: 1280-1295.
16. Karagianni P, Wong J, (2007) HDAC3: taking the SMRT-N-CoRrect road to repression. Oncogene 26: 5439-5449.
17. Mariadason JM, (2008) Dissecting HDAC3-mediated tumor progression. Cancer Biol Ther 7: 1581-1583.
18. Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, et al. (2012) Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci USA 109: E2865-2874.
19. Xu C, Soragni E, Chou CJ, Herman D, Plasterer HL, et al. (2009) Chemical probes identify a role for histone deacetylase 3 in Friedreich's ataxia gene silencing. Chem Biol 16: 980-989.
20. Jia H, Pallos J, Jacques V, Lau A, Tang B, et al. (2012) Histone deacetylase (HDAC) inhibitors targeting HDAC3 and HDAC1 ameliorate polyglutamine-elicited phenotypes in model systems of Huntington's disease. Neurobiol Dis 46: 351-361.
21. Miller TA, Witter DJ, Belvedere S, (2003) Histone deacetylase inhibitors. J Med Chem 46: 5097-5116.
22. Paris M, Porcelloni M, Binaschi M, Fattori D, (2008) Histone deacetylase inhibitors: From bench to clinic. J Med Chem 51: 1505-1529.
23. Suzuki T, Nagano Y, Kouketsu A, Matsuura A, Maruyama S, et al. (2005) Novel inhibitors of human histone deacetylases: Design, synthesis, enzyme inhibition, and cancer cell growth inhibition of SAHA-based non-hydroxamates. J Med Chem 48: 1019-1032.
24. Suzuki T, Kouketsu A, Itoh Y, Hisakawa S, Maeda S, et al. (2006) Highly potent and selective histone deacetylase 6 inhibitors designed based on a small-molecular substrate. J Med Chem 49: 4809-4812.
25. Itoh Y, Suzuki T, Kouketsu A, Suzuki N, Maeda S, et al. (2007) Design, synthesis, structure-selectivity relationship, and effect on human cancer cells of a novel series of histone deacetylase 6-selective inhibitors. J Med Chem 50: 5425-5438.
26. Suzuki N, Suzuki T, Ota Y, Nakano T, Kurihara M, et al. (2009) Design, synthesis, and biological activity of boronic acid-based histone deacetylase inhibitors. J Med Chem 52: 2909-2922.
27. Hu F, Chou CJ, Gottesfeld JM, (2009) Design and synthesis of novel hybrid benzamide-peptide histone deacetylase inhibitors. Bioorg Med Chem Lett 19: 3928-3931.
28. Chen Y, He R, Chen Y, D'Annibale MA, Langley B, et al. (2009) Studies of benzamide- and thiol-based histone deacetylase inhibitors in models of oxidative-stress-induced neuronal death: identification of some HDAC3-selective inhibitors. ChemMedChem 4: 842-852.
29. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, et al. (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci USA 110: 2647-2652.
30. Suzuki T, Ota Y, Ri M, Bando M, Gotoh A, et al. (2012) Rapid discovery of highly potent and selective inhibitors of histone deacetylase 8 using click chemistry to generate candidate libraries. J Med Chem 55: 9562-9575.
31. Kolb HC, Finn MG, Sharpless KB, (2001) Click chemistry: Diverse chemical function from a few good reactions. Angew Chem Int Ed 40: 2004-2021.
32. Rostovtsev VV, Green LG, Fokin VV, Sharpless KB, (2002) A stepwise Huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew Chem Int Ed 41: 2596-2599.
33. Tornøe CW, Christensen C, Meldal M, (2002) Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J Org Chem 67: 3057-3064.
34. Richon VM, Emiliani S, Verdin E, Webb Y, Breslow R, et al. (1998) A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci USA 95: 3003-3007.
35. Richon VM, Webb Y, Merger R, Sheppard T, Jursic B, et al. (1996) Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc Natl Acad Sci USA 93: 5705-5708.
36. Watson PJ, Fairall L, Santos GM, Schwabe JW, (2012) Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 481: 335-340.
37. Zhu W, Ma D (2004) Synthesis of aryl azides and vinyl azides via proline-promoted CuI-catalyzed coupling reactions. Chem Commun 888-889.
38. Suzuki T, Ota Y, Kasuya Y, Mutsuga M, Kawamura Y, et al. (2010) An unexpected example of protein-templated click chemistry. Angew Chem Int Ed 49: 6817-6820.
39. Lee LV, Mitchell ML, Huang SJ, Fokin VV, Sharpless KB, et al. (2003) A potent and highly selective inhibitor of human α-1,3-fucosyltransferase via click chemistry. J Am Chem Soc 125: 9588-9589.
40. Srinivasan R, Uttamchandani M, Yao SQ, (2006) Rapid assembly and in situ screening of bidentate inhibitors of protein tyrosine phosphatases. Org Lett 8: 713-716.
41. Wang J, Uttamchandani M, Li J, Hu M, Yao SQ, (2006) Rapid assembly of matrix metalloprotease inhibitors using click chemistry. Org Lett 8: 3821-3824.
42. Srinivasan R, Li J, Ng SL, Kalesh KA, Yao SQ, (2007) Methods of using click chemistry in the discovery of enzyme inhibitors. Nat Protoc 2: 2655-2664.
43. Hu M, Li J, Yao SQ, (2008) In situ "click" assembly of small molecule matrix metalloprotease inhibitors containing zinc-chelating groups. Org Lett 10: 5529-5531.
44. Tan LP, Wu H, Yang PY, Kalesh KA, Zhang X, et al. (2009) High-throughput discovery of Mycobacterium tuberculosis protein tyrosine phosphatase B (MptpB) inhibitors using click chemistry. Org Lett 11: 5102-5105.
45. Zhang J, Kalkum M, Chait BT, Roeder RG, (2002) The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell 9: 611-623.
46. Hassig CA, Tong JK, Fleischer TC, Owa T, Grable PG, et al. (1998) A role for histone deacetylase activity in HDAC1-mediated transcriptional repression. Proc Natl Acad Sci USA 95: 3519-3524.
47. Chen Y, Wang H, Yoon SO, Xu X, Hottiger MO, et al. (2011) HDAC-mediated deacetylation of NF-κB is critical for Schwann cell myelination. Nat Neurosci 14: 437-441.
48. Luo J, Su F, Chen D, Shiloh A, Gu W, (2000) Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408: 377-381.
49. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, et al. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458.
50. Thangaraju M, Carswell KN, Prasad PD, Ganapathy V, (2009) Colon cancer cells maintain low levels of pyruvate to avoid cell death caused by inhibition of HDAC1/HDAC3. Biochem J 417: 379-389.
51. Weichert W, Röske A, Gekeler V, Beckers T, Stephan C, et al. (2008) Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br J Cancer 98: 604-610.
52. Huber K, Doyon G, Plaks J, Fyne E, Mellors JW, et al. (2011) Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells. J Biol Chem 286: 22211-22218.
53. Frater J, (2011) New approaches in HIV eradication research. Curr Opin Infect Dis 24: 593-598.
54. Victoriano AF, Imai K, Togami H, Ueno T, Asamitsu K, et al. (2011) Novel histone deacetylase inhibitor NCH-51 activates latent HIV-1 gene expression. FEBS Lett 585: 1103-1111.
55. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, et al. (2012) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487: 482-485.