An Isochemogenic Set of Inhibitors to Define the Therapeutic Potential of Histone Deacetylases in β-Cell Protection

ACS Chemical Biology

Volumn 11, Issue 2, 2016, Pages 363-374

  Wagner, Florence F ^a   Lundh, Morten ^a,b   Kaya, Taner ^a   McCarren, Patrick ^a   Zhang, Yan Ling ^a   Chattopadhyay, Shrikanta ^a   Gale, Jennifer P ^a   Galbo, Thomas ^c   Fisher, Stewart L ^d   Meier, Bennett C ^a   Vetere, Amedeo ^a   Richardson, Sarah ^e   Morgan, Noel G ^e   Christensen, Dan Ploug ^b   Gilbert, Tamara J ^a   Hooker, Jacob M ^a,f   Leroy, Mélanie ^a   Walpita, Deepika ^a   Mandrup Poulsen, Thomas ^b,g   Wagner, Bridget K ^a   Holson, Edward B ^a,h   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SL Fisher Consulting   (United States)

^e UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g KAROLINSKA INSTITUTE   (Sweden)

^h 400 Technology Square   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRD 3308; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; INSULIN; UNCLASSIFIED DRUG; HISTONE DEACETYLASE; ISOPROTEIN;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOTOXICITY; HUMAN; HUMAN CELL; INSULIN RELEASE; LIPOTOXICITY; MEGAKARYOCYTE; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CELL PROTECTION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOLECULAR GENETICS; RAT;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL LINE; CYTOPROTECTION; DRUG DESIGN; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; INSULIN-SECRETING CELLS; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; RATS;

EID: 84959356933     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00640     Document Type: Article

References (50)

1. Khan, O. And La Thangue, N. B. (2012) HDAC inhibitors in cancer biology: Emerging mechanisms and clinical applications Immunol. Cell Biol. 90, 85-94 10.1038/icb.2011.100
2. Mahgoub, M. And Monteggia, L. M. (2013) Epigenetics and psychiatry Neurotherapeutics 10, 734-741 10.1007/s13311-013-0213-6
3. Chou, D. H., Holson, E. B., Wagner, F. F., Tang, A. J., Maglathlin, R. L., Lewis, T. A., Schreiber, S. L., and Wagner, B. K. (2012) Inhibition of histone deacetylase 3 protects beta cells from cytokine-induced apoptosis Chem. Biol. 19, 669-673 10.1016/j.chembiol.2012.05.010
4. Ferguson, B. S., Harrison, B. C., Jeong, M. Y., Reid, B. G., Wempe, M. F., Wagner, F. F., Holson, E. B., and McKinsey, T. A. (2013) Signal-dependent repression of DUSP5 by class I HDACs controls nuclear ERK activity and cardiomyocyte hypertrophy Proc. Natl. Acad. Sci. U. S. A. 110, 9806-9811 10.1073/pnas.1301509110
5. Andrews, K. T., Haque, A., and Jones, M. K. (2012) HDAC inhibitors in parasitic diseases Immunol. Cell Biol. 90, 66-77 10.1038/icb.2011.97
6. Rotili, D., Simonetti, G., Savarino, A., Palamara, A. T., Migliaccio, A. R., and Mai, A. (2009) Non-cancer uses of histone deacetylase inhibitors: Effects on infectious diseases and beta-hemoglobinopathies Curr. Top. Med. Chem. 9, 272-291 10.2174/156802609788085296
7. Richon, V. M. (2006) Cancer biology: Mechanism of antitumour action of vorinostat (suberoylanilide hydroxamic acid), a novel histone deacetylase inhibitor Br. J. Cancer 95, S2-S6 10.1038/sj.bjc.6603463
8. Bishton, M. J., Harrison, S. J., Martin, B. P., McLaughlin, N., James, C., Josefsson, E. C., Henley, K. J., Kile, B. T., Prince, H. M., and Johnstone, R. W. (2011) Deciphering the molecular and biologic processes that mediate histone deacetylase inhibitor-induced thrombocytopenia Blood 117, 3658-3668 10.1182/blood-2010-11-318055
9. Fraczek, J., Vanhaecke, T., and Rogiers, V. (2013) Toxicological and metabolic considerations for histone deacetylase inhibitors Expert Opin. Drug Metab. Toxicol. 9, 441-457 10.1517/17425255.2013.754011
10. Subramanian, S., Bates, S. E., Wright, J. J., Espinoza-Delgado, I., and Piekarz, R. L. (2010) Clinical Toxicities of Histone Deacetylase Inhibitors Pharmaceuticals 3, 2751-2767 10.3390/ph3092751
11. Wagner, F. F., Weïwer, M., Lewis, M. C., and Holson, E. B. (2013) Small Molecule Inhibitors of Zinc-dependent Histone Deacetylases Neurotherapeutics 10, 589-604 10.1007/s13311-013-0226-1
12. Malvaez, M., McQuown, S. C., Rogge, G. A., Astarabadi, M., Jacques, V., Carreiro, S., Rusche, J. R., and Wood, M. A. (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner Proc. Natl. Acad. Sci. U. S. A. 110, 2647-2652 10.1073/pnas.1213364110
13. Prakash, S., Foster, B. J., Meyer, M., Wozniak, A., Heilbrun, L. K., Flaherty, L., Zalupski, M., Radulovic, L., Valdivieso, M., and LoRusso, P. M. (2001) Chronic oral administration of CI-994: A phase 1 study Invest. New Drugs 19, 1-11 10.1023/A:1006489328324
14. Chou, C. J., Herman, D., and Gottesfeld, J. M. (2008) Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases J. Biol. Chem. 283, 35402-35409 10.1074/jbc.M807045200
15. Kral, A. M., Ozerova, N., Close, J., Jung, J., Chenard, M., Fleming, J., Haines, B. B., Harrington, P., Maclean, J., Miller, T. A., Secrist, P., Wang, H., and Heidebrecht, R. W., Jr. (2014) Divergent kinetics differentiate the mechanism of action of two HDAC inhibitors Biochemistry 53, 725-734 10.1021/bi400936h
16. Lauffer, B. E., Mintzer, R., Fong, R., Mukund, S., Tam, C., Zilberleyb, I., Flicke, B., Ritscher, A., Fedorowicz, G., Vallero, R., Ortwine, D. F., Gunzner, J., Modrusan, Z., Neumann, L., Koth, C. M., Lupardus, P. J., Kaminker, J. S., Heise, C. E., and Steiner, P. (2013) Histone deacetylase (HDAC) inhibitor kinetic rate constants correlate with cellular histone acetylation but not transcription and cell viability J. Biol. Chem. 288, 26926-26943 10.1074/jbc.M113.490706
17. Methot, J. L., Hoffman, D. M., Witter, D. J., Stanton, M. G., Harrington, P., Hamblett, C., Siliphaivanh, P., Wilson, K., Hubbs, J., Heidebrecht, R., Kral, A. M., Ozerova, N., Fleming, J. C., Wang, H., Szewczak, A. A., Middleton, R. E., Hughes, B., Cruz, J. C., Haines, B. B., Chenard, M., Kenific, C. M., Harsch, A., Secrist, J. P., and Miller, T. A. (2014) Delayed and Prolonged Histone Hyperacetylation with a Selective HDAC1/HDAC2 Inhibitor ACS Med. Chem. Lett. 5, 340-345 10.1021/ml4004233
18. Seo, Y. J., Kang, Y., Muench, L., Reid, A., Caesar, S., Jean, L., Wagner, F., Holson, E., Haggarty, S. J., Weiss, P., King, P., Carter, P., Volkow, N. D., Fowler, J. S., Hooker, J. M., and Kim, S. W. (2014) Image-guided synthesis reveals potent blood-brain barrier permeable histone deacetylase inhibitors ACS Chem. Neurosci. 5, 588-596 10.1021/cn500021p
19. Bressi, J. C., Jennings, A. J., Skene, R., Wu, Y., Melkus, R., De Jong, R., O'Connell, S., Grimshaw, C. E., Navre, M., and Gangloff, A. R. (2010) Exploration of the HDAC2 foot pocket: Synthesis and SAR of substituted N-(2-aminophenyl)benzamides Bioorg. Med. Chem. Lett. 20, 3142-3145 10.1016/j.bmcl.2010.03.091
20. Chen, Y., He, R., Chen, Y., D'Annibale, M. A., Langley, B., and Kozikowski, A. P. (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 10.1002/cmdc.200800461
21. Moradei, O. M., Mallais, T. C., Frechette, S., Paquin, I., Tessier, P. E., Leit, S. M., Fournel, M., Bonfils, C., Trachy-Bourget, M. C., Liu, J., Yan, T. P., Lu, A. H., Rahil, J., Wang, J., Lefebvre, S., Li, Z., Vaisburg, A. F., and Besterman, J. M. (2007) Novel aminophenyl benzamide-type histone deacetylase inhibitors with enhanced potency and selectivity J. Med. Chem. 50, 5543-5546 10.1021/jm701079h
22. Wagner, F. F., Zhang, Y. L., Fass, D. M., Joseph, N., Gale, J. P., Weiwer, M., McCarren, P., Fisher, S. L., Kaya, T., Zhao, W. N., Reis, S. A., Hennig, K. M., Thomas, M., Lemercier, B. C., Lewis, M. C., Guan, J. S., Moyer, M. P., Scolnick, E., Haggarty, S. J., Tsai, L. H., and Holson, E. B. (2015) Kinetically Selective Inhibitors of Histone Deacetylase 2 (HDAC2) as Cognition Enhancers Chem. Sci. 6, 804-815 10.1039/C4SC02130D
23. Vetere, A., Choudhary, A., Burns, S. M., and Wagner, B. K. (2014) Targeting the pancreatic beta-cell to treat diabetes Nat. Rev. Drug Discovery 13, 278-289 10.1038/nrd4231
24. Barton, K. M., Archin, N. M., Keedy, K. S., Espeseth, A. S., Zhang, Y. L., Gale, J., Wagner, F. F., Holson, E. B., and Margolis, D. M. (2014) Selective HDAC inhibition for the disruption of latent HIV-1 infection PLoS One 9, e102684 10.1371/journal.pone.0102684
25. Lundh, M., Galbo, T., Poulsen, S. S., and Mandrup-Poulsen, T. (2015) HDAC3 inhibition improves glycemia and insulin secretion in obese diabetic rats Diabetes, Obes. Metab. 17, 703 10.1111/dom.12470
26. Minucci, S. And Pelicci, P. G. (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer Nat. Rev. Cancer 6, 38-51 10.1038/nrc1779
27. Methot, J. L., Chakravarty, P. K., Chenard, M., Close, J., Cruz, J. C., Dahlberg, W. K., Fleming, J., Hamblett, C. L., Hamill, J. E., Harrington, P., Harsch, A., Heidebrecht, R., Hughes, B., Jung, J., Kenific, C. M., Kral, A. M., Meinke, P. T., Middleton, R. E., Ozerova, N., Sloman, D. L., Stanton, M. G., Szewczak, A. A., Tyagarajan, S., Witter, D. J., Secrist, J. P., and Miller, T. A. (2008) Exploration of the internal cavity of histone deacetylase (HDAC) with selective HDAC1/HDAC2 inhibitors (SHI-1:2) Bioorg. Med. Chem. Lett. 18, 973-978 10.1016/j.bmcl.2007.12.031
28. Rai, M., Soragni, E., Chou, C. J., Barnes, G., Jones, S., Rusche, J. R., Gottesfeld, J. M., and Pandolfo, M. (2010) Two new pimelic diphenylamide HDAC inhibitors induce sustained frataxin upregulation in cells from Friedreich's ataxia patients and in a mouse model PLoS One 5, e8825 10.1371/journal.pone.0008825
29. Liu, L., Chen, B., Qin, S., Li, S., He, X., Qiu, S., Zhao, W., and Zhao, H. (2010) A novel histone deacetylase inhibitor Chidamide induces apoptosis of human colon cancer cells Biochem. Biophys. Res. Commun. 392, 190-195 10.1016/j.bbrc.2010.01.011
30. Wagner, F. F., Zhang, Y.-L., Fass, D. M., Joseph, N., Gale, J. P., Weiwer, M., McCarren, P., Fisher, S. L., Kaya, T., Zhao, W.-N., Reis, S. A., Hennig, K. M., Thomas, M., Lemercier, B. C., Lewis, M. C., Guan, J.-S., Moyer, M. P., Scolnick, E. M., Haggarty, S. J., Tsai, L.-H., and Holson, E. B. (2015) Kinetically selective inhibitors of histone deacetylase 2 (HDAC2) as cognition enhancers Chemical Science 6, 804 10.1039/C4SC02130D
31. Dunbrack, R. L., Jr. And Cohen, F. E. (1997) Bayesian statistical analysis of protein side-chain rotamer preferences Protein Sci. 6, 1661-1681 10.1002/pro.5560060807
32. Lovell, S. C., Word, J. M., Richardson, J. S., and Richardson, D. C. (2000) The penultimate rotamer library Proteins: Struct., Funct., Genet. 40, 389-408 10.1002/1097-0134(20000815)40:3<389::AID-PROT50>3.3.CO;2-U
33. Scouras, A. D. And Daggett, V. (2011) The Dynameomics rotamer library: Amino acid side chain conformations and dynamics from comprehensive molecular dynamics simulations in water Protein science: A publication of the Protein Society 20, 341-352 10.1002/pro.565
34. Plevin, M. J., Bryce, D. L., and Boisbouvier, J. (2010) Direct detection of CH/pi interactions in proteins Nat. Chem. 2, 466-471 10.1038/nchem.650
35. Ringer, A. L., Figgs, M. S., Sinnokrot, M. O., and Sherrill, C. D. (2006) Aliphatic C-H/pi interactions: Methane-benzene, methane-phenol, and methane-indole complexes J. Phys. Chem. A 110, 10822-10828 10.1021/jp062740l
36. Walkup, G. K., You, Z., Ross, P. L., Allen, E. K., Daryaee, F., Hale, M. R., O'Donnell, J., Ehmann, D. E., Schuck, V. J., Buurman, E. T., Choy, A. L., Hajec, L., Murphy-Benenato, K., Marone, V., Patey, S. A., Grosser, L. A., Johnstone, M., Walker, S. G., Tonge, P. J., and Fisher, S. L. (2015) Translating slow-binding inhibition kinetics into cellular and in vivo effects Nat. Chem. Biol. 11, 416 10.1038/nchembio.1796
37. Lundh, M., Christensen, D. P., Damgaard Nielsen, M., Richardson, S. J., Dahllof, M. S., Skovgaard, T., Berthelsen, J., Dinarello, C. A., Stevenazzi, A., Mascagni, P., Grunnet, L. G., Morgan, N. G., and Mandrup-Poulsen, T. (2012) Histone deacetylases 1 and 3 but not 2 mediate cytokine-induced beta cell apoptosis in INS-1 cells and dispersed primary islets from rats and are differentially regulated in the islets of type 1 diabetic children Diabetologia 55, 2421-2431 10.1007/s00125-012-2615-0
38. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., and Butler, P. C. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes Diabetes 52, 102-110 10.2337/diabetes.52.1.102
39. Lenzen, S. (2008) Oxidative stress: The vulnerable beta-cell Biochem. Soc. Trans. 36, 343-347 10.1042/BST0360343
40. Maedler, K., Sergeev, P., Ris, F., Oberholzer, J., Joller-Jemelka, H. I., Spinas, G. A., Kaiser, N., Halban, P. A., and Donath, M. Y. (2002) Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets J. Clin. Invest. 110, 851-860 10.1172/JCI200215318
41. Cunha, D. A., Hekerman, P., Ladriere, L., Bazarra-Castro, A., Ortis, F., Wakeham, M. C., Moore, F., Rasschaert, J., Cardozo, A. K., Bellomo, E., Overbergh, L., Mathieu, C., Lupi, R., Hai, T., Herchuelz, A., Marchetti, P., Rutter, G. A., Eizirik, D. L., and Cnop, M. (2008) Initiation and execution of lipotoxic ER stress in pancreatic beta-cells J. Cell Sci. 121, 2308-2318 10.1242/jcs.026062
42. Tang, C., Koulajian, K., Schuiki, I., Zhang, L., Desai, T., Ivovic, A., Wang, P., Robson-Doucette, C., Wheeler, M. B., Minassian, B., Volchuk, A., and Giacca, A. (2012) Glucose-induced beta cell dysfunction in vivo in rats: Link between oxidative stress and endoplasmic reticulum stress Diabetologia 55, 1366-1379 10.1007/s00125-012-2474-8
43. Cunha, D. A., Igoillo-Esteve, M., Gurzov, E. N., Germano, C. M., Naamane, N., Marhfour, I., Fukaya, M., Vanderwinden, J. M., Gysemans, C., Mathieu, C., Marselli, L., Marchetti, P., Harding, H. P., Ron, D., Eizirik, D. L., and Cnop, M. (2012) Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human beta-cell apoptosis Diabetes 61, 2763-2775 10.2337/db12-0123
44. Wilting, R. H., Yanover, E., Heideman, M. R., Jacobs, H., Horner, J., van der Torre, J., DePinho, R. A., and Dannenberg, J. H. (2010) Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis EMBO J. 29, 2586-2597 10.1038/emboj.2010.136
45. Hogge, D., Fanning, S., Bockhold, K., Petzer, A., Lambie, K., Lansdorp, P., Eaves, A., and Eaves, C. (1997) Quantitation and characterization of human megakaryocyte colony-forming cells using a standardized serum-free agarose assay Br. J. Haematol. 96, 790-800 10.1046/j.1365-2141.1997.d01-2092.x
46. Parent-Massin, D. And Sibiril, Y. (2008) CFU-MK assay for acute thrombocytopenia Curr. Protoc. Toxicol. 37, 20.5.1 10.1002/0471140856.tx2005s37
47. Pessina, A., Parent-Massin, D., Albella, B., Van Den Heuvel, R., Casati, S., Croera, C., Malerba, I., Sibiril, Y., Gomez, S., de Smedt, A., and Gribaldo, L. (2009) Application of human CFU-Mk assay to predict potential thrombocytotoxicity of drugs Toxicol. In Vitro 23, 194-200 10.1016/j.tiv.2008.11.006
48. Knight, Z. A. And Shokat, K. M. (2007) Chemical genetics: Where genetics and pharmacology meet Cell 128, 425-430 10.1016/j.cell.2007.01.021
49. Volpe, D. A., LoRusso, P. M., Foster, B. J., and Parchment, R. E. (2004) In vitro and in vivo effects of acetyldinaline on murine megakaryocytopoiesis Cancer Chemother. Pharmacol. 54, 89-94 10.1007/s00280-004-0783-4
50. Zhang, Y.-L., Holson, E., and Wagner, F. F. (2013) Fluorescent substrates for determining lysine modifying enzyme activity, (The Broad Institute, Inc., USA). International Patent Application WO2013067391 A1.