A Selective HDAC 1/2 Inhibitor Modulates Chromatin and Gene Expression in Brain and Alters Mouse Behavior in Two Mood-Related Tests

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Schroeder, Frederick A ^a   Lewis, Michael C ^b   Fass, Daniel M ^a,b   Wagner, Florence F ^b   Zhang, Yan Ling ^b   Hennig, Krista M ^a,b   Gale, Jennifer ^b   Zhao, Wen Ning ^a   Reis, Surya ^a   Barker, Douglas D ^b   Berry Scott, Erin ^b   Kim, Sung Won ^c   Clore, Elizabeth L ^b   Hooker, Jacob M ^a,b   Holson, Edward B ^b   Haggarty, Stephen J ^a,b   Petryshen, Tracey L ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

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

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; VORINOSTAT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; BEHAVIOR DISORDER; BINDING AFFINITY; BIOCHEMISTRY; BRAIN REGION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG TARGETING; EMBRYO; ENZYME INHIBITION; EPIGENETICS; FEMALE; FORCED SWIMMING TEST; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HDAC1 GENE; HDAC2 GENE; HIPPOCAMPUS; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOOD DISORDER; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; TRANSCRIPTION REGULATION;

ACETYLATION; AFFECT; ANIMALS; BEHAVIOR, ANIMAL; BENZAMIDES; BRAIN; CHROMATIN; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HISTONES; LITHIUM; MALE; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICE, INBRED C57BL; NEURONS; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84881507348     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071323     Document Type: Article

References (58)

1. Nestler EJ, (2009) Epigenetic mechanisms in psychiatry. Biol Psychiatry 65: 189-190.
2. Verdone L, Caserta M, Di Mauro E, (2005) Role of histone acetylation in the control of gene expression. Biochem Cell Biol 83: 344-353.
3. Covington HE, (2009) Antidepressant actions of histone deacetylase inhibitors. J Neurosci 29: 11451-11460.
4. Hobara T, Uchida S, Otsuki K, Matsubara T, Funato H, et al. (2010) Altered gene expression of histone deacetylases in mood disorder patients. J Psychiatr Res 44: 263-270.
5. Benes FM, Lim B, Matzilevich D, Walsh JP, Subburaju S, et al. (2007) Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci U S A 104: 10164-10169.
6. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, et al. (2010) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35: 870-880.
7. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, et al. (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741.
8. Feng HL, Leng Y, Ma CH, Zhang J, Ren M, et al. (2008) Combined lithium and valproate treatment delays disease onset, reduces neurological deficits and prolongs survival in an amyotrophic lateral sclerosis mouse model. Neuroscience 155: 567-572.
9. Leng Y, Liang MH, Ren M, Marinova Z, Leeds P, et al. (2008) Synergistic neuroprotective effects of lithium and valproic acid or other histone deacetylase inhibitors in neurons: roles of glycogen synthase kinase-3 inhibition. J Neurosci 28: 2576-2588.
10. Bertran-Gonzalez J, Hakansson K, Borgkvist A, Irinopoulou T, Brami-Cherrier K, et al. (2009) Histone H3 phosphorylation is under the opposite tonic control of dopamine D2 and adenosine A2A receptors in striatopallidal neurons. Neuropsychopharmacology 34: 1710-1720.
11. Li J, Guo Y, Schroeder FA, Youngs RM, Schmidt TW, et al. (2004) Dopamine D2-like antagonists induce chromatin remodeling in striatal neurons through cyclic AMP-protein kinase A and NMDA receptor signaling. J Neurochem 90: 1117-1131.
12. Kurita M, Holloway T, Garcia-Bea A, Kozlenkov A, Friedman AK, et al. (2012) HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat Neurosci 15: 1245-1254.
13. Tsankova NM, Kumar A, Nestler EJ, (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24: 5603-5610.
14. Schroeder FA, Lin CL, Crusio WE, Akbarian S, (2007) Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 62: 55-64.
15. Arent CO, Valvassori SS, Fries GR, Stertz L, Ferreira CL, et al. (2011) Neuroanatomical profile of antimaniac effects of histone deacetylases inhibitors. Mol Neurobiol 43: 207-214.
16. Kim WY, Kim S, Kim JH, (2008) Chronic microinjection of valproic acid into the nucleus accumbens attenuates amphetamine-induced locomotor activity. Neurosci Lett 432: 54-57.
17. Methot JL, Chakravarty PK, Chenard M, Close J, Cruz JC, et al. (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.
18. Moradei OM, Mallais TC, Frechette S, Paquin I, Tessier PE, et al. (2007) Novel aminophenyl benzamide-type histone deacetylase inhibitors with enhanced potency and selectivity. J Med Chem 50: 5543-5546.
19. Covington HE, (2011) Hippocampal-dependent antidepressant-like activity of histone deacetylase inhibition. Neurosci Lett 493: 122-126.
20. Kilts CD, (2000) In vivo imaging of the pharmacodynamics and pharmacokinetics of lithium. J Clin Psychiatry 61Suppl 9: 41-46.
21. Breslow RU, Marks P, A.; (US)., Rifkind R, A.; (US) (1995) NOVEL POTENT INDUCERS OF TERMINAL DIFFERENTIATION AND METHODS OF USE THEREOF.
22. Stowell JC, Huot RI, Van Voast L, (1995) The synthesis of N-hydroxy-N'-phenyloctanediamide and its inhibitory effect on proliferation of AXC rat prostate cancer cells. J Med Chem 38: 1411-1413.
23. Fass DM, Reis SA, Ghosh B, Hennig KM, Joseph NF, et al. (2013) Crebinostat: A novel cognitive enhancer that inhibits histone deacetylase activity and modulates chromatin-mediated neuroplasticity. Neuropharmacology 64: 81-96.
24. Katragadda M, Magotti P, Sfyroera G, Lambris JD, (2006) Hydrophobic effect and hydrogen bonds account for the improved activity of a complement inhibitor, compstatin. J Med Chem 49: 4616-4622.
25. Chou CJ, Herman D, Gottesfeld JM, (2008) Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J Biol Chem 283: 35402-35409.
26. Pan JQ, Lewis MC, Ketterman JK, Clore EL, Riley M, et al. (2011) AKT kinase activity is required for lithium to modulate mood-related behaviors in mice. Neuropsychopharmacology 36: 1397-1411.
27. Huang HS, Matevossian A, Jiang Y, Akbarian S, (2006) Chromatin immunoprecipitation in postmortem brain. J Neurosci Methods 156: 284-292.
28. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, et al. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60.
29. Hooker JM, Kim SW, Alexoff D, Xu Y, Shea C, et al. (2010) Histone deacetylase inhibitor, MS-275, exhibits poor brain penetration: PK studies of [C]MS-275 using Positron Emission Tomography. ACS Chem Neurosci 1: 65-73.
30. Thompson C, (2002) Onset of action of antidepressants: results of different analyses. Hum Psychopharmacol 17Suppl 1: S27-32.
31. Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, et al. (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328: 753-756.
32. Gould TD, O'Donnell KC, Picchini AM, Manji HK, (2007) Strain differences in lithium attenuation of d-amphetamine-induced hyperlocomotion: a mouse model for the genetics of clinical response to lithium. Neuropsychopharmacology 32: 1321-1333.
33. Porsolt RD, Bertin A, Jalfre M, (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229: 327-336.
34. Porsolt RD, Deniel M, Jalfre M, (1979) Forced swimming in rats: hypothermia, immobility and the effects of imipramine. Eur J Pharmacol 57: 431-436.
35. Benjamini YHY, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society (Methodologial) 57: 289-300.
36. Nestler EJ, Carlezon WA Jr, (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
37. Obradovic T, Imel KM, White SR, (1996) Methylenedioxymethamphetamine-induced inhibition of neuronal firing in the nucleus accumbens is mediated by both serotonin and dopamine. Neuroscience 74: 469-481.
38. McQuillin A, Rizig M, Gurling HM, (2007) A microarray gene expression study of the molecular pharmacology of lithium carbonate on mouse brain mRNA to understand the neurobiology of mood stabilization and treatment of bipolar affective disorder. Pharmacogenet Genomics 17: 605-617.
39. Baltan S, Murphy SP, Danilov CA, Bachleda A, Morrison RS, (2011) Histone deacetylase inhibitors preserve white matter structure and function during ischemia by conserving ATP and reducing excitotoxicity. J Neurosci 31: 3990-3999.
40. MacDonald JL, Roskams AJ, (2008) Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev Dyn 237: 2256-2267.
41. Arnett MG, Kolber BJ, Boyle MP, Muglia LJ, (2011) Behavioral insights from mouse models of forebrain-and amygdala-specific glucocorticoid receptor genetic disruption. Mol Cell Endocrinol 336: 2-5.
42. Solomon MB, Furay AR, Jones K, Packard AE, Packard BA, et al. (2012) Deletion of forebrain glucocorticoid receptors impairs neuroendocrine stress responses and induces depression-like behavior in males but not females. Neuroscience 203: 135-143.
43. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
44. Fang HL, Shenoy S, Duanmu Z, Kocarek TA, Runge-Morris M, (2003) Transactivation of glucocorticoid-inducible rat aryl sulfotransferase (SULT1A1) gene transcription. Drug Metab Dispos 31: 1378-1381.
45. Kobayashi T, Cohen P, (1999) Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem J 339 (Pt 2): 319-328.
46. Conti M, Cavestri B, Benhamed L, Porte H, Wurtz A, (2007) [Malformations of the anterior chest wall]. Rev Mal Respir 24: 107-120.
47. Robbins MJ, Critchlow HM, Lloyd A, Cilia J, Clarke JD, et al. (2008) Differential expression of IEG mRNA in rat brain following acute treatment with clozapine or haloperidol: a semi-quantitative RT-PCR study. J Psychopharmacol 22: 536-542.
48. Sakoda H, Gotoh Y, Katagiri H, Kurokawa M, Ono H, et al. (2003) Differing roles of Akt and serum- and glucocorticoid-regulated kinase in glucose metabolism, DNA synthesis, and oncogenic activity. J Biol Chem 278: 25802-25807.
49. Weeks KR, Dwyer DS, Aamodt EJ, (2011) Clozapine and lithium require Caenorhabditis elegans beta-arrestin and serum- and glucocorticoid-inducible kinase to affect Daf-16 (FOXO) localization. J Neurosci Res 89: 1658-1665.
50. Hodes GE, Brookshire BR, Hill-Smith TE, Teegarden SL, Berton O, et al. (2012) Strain differences in the effects of chronic corticosterone exposure in the hippocampus. Neuroscience 222: 269-280.
51. Rane P, Shields J, Heffernan M, Guo Y, Akbarian S, et al. (2012) The histone deacetylase inhibitor, sodium butyrate, alleviates cognitive deficits in pre-motor stage PD. Neuropharmacology 62: 2409-2412.
52. Del Signore SJ, Amante DJ, Kim J, Stack EC, Goodrich S, et al. (2009) Combined riluzole and sodium phenylbutyrate therapy in transgenic amyotrophic lateral sclerosis mice. Amyotroph Lateral Scler 10: 85-94.
53. Hu Y, Chopra V, Chopra R, Locascio JJ, Liao Z, et al. (2011) Transcriptional modulator H2A histone family, member Y (H2AFY) marks Huntington disease activity in man and mouse. Proc Natl Acad Sci U S A 108: 17141-17146.
54. 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 U S A 110: 2647-2652.
55. Glozak MA, Sengupta N, Zhang X, Seto E, (2005) Acetylation and deacetylation of non-histone proteins. Gene 363: 15-23.
56. Espallergues J, Teegarden SL, Veerakumar A, Boulden J, Challis C, et al. (2012) HDAC6 regulates glucocorticoid receptor signaling in serotonin pathways with critical impact on stress resilience. J Neurosci 32: 4400-4416.
57. Fukada M, Hanai A, Nakayama A, Suzuki T, Miyata N, et al. (2012) Loss of deacetylation activity of Hdac6 affects emotional behavior in mice. PLoS One 7: e30924.
58. Renthal W, Maze I, Krishnan V, Covington HE, (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56: 517-529.