Valproate reverses mania-like behaviors in mice via preferential targeting of HDAC2.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
08 2021
Historique:
received: 22 07 2020
accepted: 06 11 2020
revised: 20 10 2020
pubmed: 26 11 2020
medline: 28 1 2022
entrez: 25 11 2020
Statut: ppublish

Résumé

Valproate (VPA) has been used in the treatment of bipolar disorder since the 1990s. However, the therapeutic targets of VPA have remained elusive. Here we employ a preclinical model to identify the therapeutic targets of VPA. We find compounds that inhibit histone deacetylase proteins (HDACs) are effective in normalizing manic-like behavior, and that class I HDACs (e.g., HDAC1 and HDAC2) are most important in this response. Using an RNAi approach, we find that HDAC2, but not HDAC1, inhibition in the ventral tegmental area (VTA) is sufficient to normalize behavior. Furthermore, HDAC2 overexpression in the VTA prevents the actions of VPA. We used RNA sequencing in both mice and human induced pluripotent stem cells (iPSCs) derived from bipolar patients to further identify important molecular targets. Together, these studies identify HDAC2 and downstream targets for the development of novel therapeutics for bipolar mania.

Identifiants

pubmed: 33235333
doi: 10.1038/s41380-020-00958-2
pii: 10.1038/s41380-020-00958-2
pmc: PMC8141541
mid: NIHMS1644759
doi:

Substances chimiques

Histone Deacetylase Inhibitors 0
Valproic Acid 614OI1Z5WI
HDAC2 protein, human EC 3.5.1.98
Hdac2 protein, mouse EC 3.5.1.98
Histone Deacetylase 2 EC 3.5.1.98

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4066-4084

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH111601
Pays : United States
Organisme : NIDA NIH HHS
ID : K01 DA038654
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH106460
Pays : United States
Organisme : NIMH NIH HHS
ID : R21 MH115241
Pays : United States

Informations de copyright

© 2020. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Lopez-Munoz F, Shen WW, D’Ocon P, Romero A, Alamo C. A history of the pharmacological treatment of bipolar disorder. Int J Mol Sci. 2018;19:2143.
pmcid: 6073684
Macdonald RL, Kelly KM. Antiepileptic drug mechanisms of action. Epilepsia. 1995;36:S2–12.
pubmed: 8784210
Gould TD, Quiroz JA, Singh J, Zarate CA, Manji HK. Emerging experimental therapeutics for bipolar disorder: insights from the molecular and cellular actions of current mood stabilizers. Mol Psychiatry. 2004;9:734–55.
pubmed: 15136794
Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem. 2001;276:36734–41.
pubmed: 11473107
Chiu CT, Wang Z, Hunsberger JG, Chuang DM. Therapeutic potential of mood stabilizers lithium and valproic acid: beyond bipolar disorder. Pharmacol Rev. 2013;65:105–42.
pubmed: 23300133 pmcid: 3565922
Nestler EJ, Pena CJ, Kundakovic M, Mitchell A, Akbarian S. Epigenetic basis of mental illness. Neuroscientist. 2016;22:447–63.
pubmed: 26450593
Morris MJ, Monteggia LM. Unique functional roles for class I and class II histone deacetylases in central nervous system development and function. Int J Dev Neurosci. 2013;31:370–81.
pubmed: 23466417 pmcid: 3726026
Dai Y, Faller DV. Transcription regulation by class III histone deacetylases (HDACs)-sirtuins. Transl Oncogenomics. 2008;3:53–65.
pubmed: 21566744 pmcid: 3022360
Baltan S, Bachleda A, Morrison RS, Murphy SP. Expression of histone deacetylases in cellular compartments of the mouse brain and the effects of ischemia. Transl Stroke Res. 2011;2:411–23.
pubmed: 21966324 pmcid: 3182145
Ryu H, Lee J, Olofsson BA, Mwidau A, Dedeoglu A, Escudero M, et al. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci USA. 2003;100:4281–6.
pubmed: 12640146 pmcid: 153084
Machado-Vieira R, Ibrahim L, Zarate CA Jr. Histone deacetylases and mood disorders: epigenetic programming in gene-environment interactions. CNS Neurosci Ther. 2011;17:699–704.
pubmed: 20961400
Benes FM, Lim B, Matzilevich D, Walsh JP, Subburaju S, Minns M. Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci USA. 2007;104:10164–9.
pubmed: 17553960 pmcid: 1888575
Tseng CJ, Gilbert TM, Catanese MC, Hightower BG, Peters AT, Parmar AJ, et al. In vivo human brain expression of histone deacetylases in bipolar disorder. Transl Psychiatry. 2020;10:224.
pubmed: 32641695 pmcid: 7343804
Arent CO, Valvassori SS, Fries GR, Stertz L, Ferreira CL, Lopes-Borges J, et al. Neuroanatomical profile of antimaniac effects of histone deacetylases inhibitors. Mol Neurobiol. 2011;43:207–14.
pubmed: 21424678
Varela RB, Resende WR, Dal-Pont GC, Gava FF, Tye SJ, Quevedo J, et al. HDAC inhibitors reverse mania-like behavior and modulate epigenetic regulatory enzymes in an animal model of mania induced by Ouabain. Pharmacol Biochem Behav. 2020;193:172917.
pubmed: 32222371
McClung CA, Sidiropoulou K, Vitaterna M, Takahashi JS, White FJ, Cooper DC, et al. Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc Natl Acad Sci USA. 2005;102:9377–81.
pubmed: 15967985 pmcid: 1166621
Roybal K, Theobold D, Graham A, DiNieri JA, Russo SJ, Krishnan V, et al. Mania-like behavior induced by disruption of CLOCK. Proc Natl Acad Sci USA. 2007;104:6406–11.
pubmed: 17379666 pmcid: 1851061
Arey R, McClung CA. An inhibitor of casein kinase 1 epsilon/delta partially normalizes the manic-like behaviors of the ClockDelta19 mouse. Behav= Pharmacol. 2012;23:392–6.
pubmed: 22743604 pmcid: 3673712
Arey RN, Enwright JF 3rd, Spencer SM, Falcon E, Ozburn AR, Ghose S, et al. An important role for cholecystokinin, a CLOCK target gene, in the development and treatment of manic-like behaviors. Mol Psychiatry. 2014;19:342–50.
pubmed: 23399917
Sidor MM, Spencer SM, Dzirasa K, Parekh PK, Tye KM, Warden MR, et al. Daytime spikes in dopaminergic activity drive rapid mood-cycling in mice. Mol Psychiatry. 2015;20:1406–19.
pubmed: 25560763 pmcid: 4492925
Logan RW, McClung CA. Animal models of bipolar mania: the past, present and future. Neuroscience. 2016;321:163–88.
pubmed: 26314632
Parekh PK, Sidor MM, Gillman A, Becker-Krail D, Bettelini L, Arban R, et al. Antimanic efficacy of a novel Kv3 potassium channel modulator. Neuropsychopharmacology. 2018;43:435–44.
pubmed: 28857068
King DP, Takahashi JS. Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci. 2000;23:713–42.
pubmed: 10845079
King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, et al. Positional cloning of the mouse circadian clock gene. Cell. 1997;89:641–53.
pubmed: 9160755 pmcid: 3815553
Naylor E, Bergmann BM, Krauski K, Zee PC, Takahashi JS, Vitaterna MH, et al. The circadian clock mutation alters sleep homeostasis in the mouse. J Neurosci. 2000;20:8138–43.
pubmed: 11050136 pmcid: 6772726
Easton A, Arbuzova J, Turek FW. The circadian Clock mutation increases exploratory activity and escape-seeking behavior. Genes Brain Behav. 2003;2:11–19.
pubmed: 12882315
Ozburn AR, Falcon E, Mukherjee S, Gillman A, Arey R, Spencer S, et al. The role of clock in ethanol-related behaviors. Neuropsychopharmacology. 2013;38:2393–2400.
pubmed: 23722243 pmcid: 3799058
Ozburn AR, Larson EB, Self DW, McClung CA. Cocaine self-administration behaviors in ClockDelta19 mice. Psychopharmacology. 2012;223:169–77.
pubmed: 22535308 pmcid: 3670183
van Enkhuizen J, Minassian A, Young JW. Further evidence for ClockDelta19 mice as a model for bipolar disorder mania using cross-species tests of exploration and sensorimotor gating. Behav Brain Res. 2013;249:44–54.
pubmed: 23623885 pmcid: 3672322
McClung CA, Nestler EJ, Zachariou V. Regulation of gene expression by chronic morphine and morphine withdrawal in the locus ceruleus and ventral tegmental area. J Neurosci. 2005;25:6005–15.
pubmed: 15976090 pmcid: 6724795
Coque L, Mukherjee S, Cao JL, Spencer S, Marvin M, Falcon E, et al. Specific role of VTA dopamine neuronal firing rates and morphology in the reversal of anxiety-related, but not depression-related behavior in the ClockDelta19 mouse model of mania. Neuropsychopharmacology. 2011;36:1478–88.
pubmed: 21430648 pmcid: 3096816
Mukherjee S, Coque L, Cao JL, Kumar J, Chakravarty S, Asaithamby A, et al. Knockdown of Clock in the ventral tegmental area through RNA interference results in a mixed state of mania and depression-like behavior. Biol Psychiatry. 2010;68:503–11.
pubmed: 20591414 pmcid: 2929276
Berk M, Dodd S, Kauer-Sant’anna M, Malhi GS, Bourin M, Kapczinski F, et al. Dopamine dysregulation syndrome: implications for a dopamine hypothesis of bipolar disorder. Acta Psychiatr Scand Supplementu. 2007;434:41–9.
Ashok AH, Marques TR, Jauhar S, Nour MM, Goodwin GM, Young AH, et al. The dopamine hypothesis of bipolar affective disorder: the state of the art and implications for treatment. Mol Psychiatry. 2017;22:666–79.
pubmed: 28289283 pmcid: 5401767
Abler B, Greenhouse I, Ongur D, Walter H, Heckers S. Abnormal reward system activation in mania. Neuropsychopharmacology. 2008;33:2217–27.
pubmed: 17987058
van Enkhuizen J, Geyer MA, Kooistra K, Young JW. Chronic valproate attenuates some, but not all, facets of mania-like behaviour in mice. Int J Neuropsychopharmacol. 2013;16:1021–31.
pubmed: 23164454
Simonini MV, Camargo LM, Dong E, Maloku E, Veldic M, Costa E, et al. The benzamide MS-275 is a potent, long-lasting brain region-selective inhibitor of histone deacetylases. Proc Natl Acad Sci USA. 2006;103:1587–92.
pubmed: 16432198 pmcid: 1360572
Kassis H, Shehadah A, Li C, Zhang Y, Cui Y, Roberts C, et al. Class IIa histone deacetylases affect neuronal remodeling and functional outcome after stroke. Neurochem Int. 2016;96:24–31.
pubmed: 27103167 pmcid: 4860113
Logan RW, Parekh PK, Kaplan GN, Becker-Krail DD, Williams WP 3rd, Yamaguchi S, et al. NAD+ cellular redox and SIRT1 regulate the diurnal rhythms of tyrosine hydroxylase and conditioned cocaine reward. Mol Psychiatry 2018;24:1668–84.
pubmed: 29728703 pmcid: 6215755
Ang SL. Transcriptional control of midbrain dopaminergic neuron development. Development. 2006;133:3499–506.
pubmed: 16899537
Lydall GJ, Bass NJ, McQuillin A, Lawrence J, Anjorin A, Kandaswamy R, et al. Confirmation of prior evidence of genetic susceptibility to alcoholism in a genome-wide association study of comorbid alcoholism and bipolar disorder. Psychiatr Genet. 2011;21:294–306.
pubmed: 21876473 pmcid: 3372889
McCarthy MJ, Nievergelt CM, Kelsoe JR, Welsh DK. A survey of genomic studies supports association of circadian clock genes with bipolar disorder spectrum illnesses and lithium response. PLoS ONE. 2012;7:e32091.
pubmed: 22384149 pmcid: 3285204
Langfelder P, Luo R, Oldham MC, Horvath S. Is my network module preserved and reproducible? PLoS Comput Biol. 2011;7:e1001057.
pubmed: 21283776 pmcid: 3024255
Stern S, Santos R, Marchetto MC, Mendes APD, Rouleau GA, Biesmans S, et al. Neurons derived from patients with bipolar disorder divide into intrinsically different sub-populations of neurons, predicting the patients’ responsiveness to lithium. Mol Psychiatry. 2018;23:1453–65.
pubmed: 28242870
Mertens J, Wang QW, Kim Y, Yu DX, Pham S, Yang B, et al. Differential responses to lithium in hyperexcitable neurons from patients with bipolar disorder. Nature. 2015;527:95–9.
pubmed: 26524527 pmcid: 4742055
Tobe BTD, Crain AM, Winquist AM, Calabrese B, Makihara H, Zhao WN, et al. Probing the lithium-response pathway in hiPSCs implicates the phosphoregulatory set-point for a cytoskeletal modulator in bipolar pathogenesis. Proc Natl Acad Sci USA. 2017;114:E4462–71.
pubmed: 28500272 pmcid: 5465887
Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10:1523.
pubmed: 30944313 pmcid: 6447622
Delcuve GP, Khan DH, Davie JR. Roles of histone deacetylases in epigenetic regulation: emerging paradigms from studies with inhibitors. Clin Epigenetics. 2012;4:5.
pubmed: 22414492 pmcid: 3320549
Marks PA, Dokmanovic M. Histone deacetylase inhibitors: discovery and development as anticancer agents. Expert Opin Investig Drugs. 2005;14:1497–511.
pubmed: 16307490
Bubna AK. Vorinostat—an overview. Indian J Dermatol. 2015;60:419.
pubmed: 26288427 pmcid: 4533557
Shearstone JR, Golonzhka O, Chonkar A, Tamang D, van Duzer JH, Jones SS, et al. Chemical inhibition of histone deacetylases 1 and 2 induces fetal hemoglobin through activation of GATA2. PloS ONE. 2016;11:e0153767.
pubmed: 27073918 pmcid: 4830539
Lima IVA, Almeida-Santos AF, Ferreira-Vieira TH, Aguiar DC, Ribeiro FM, Campos AC, et al. Antidepressant-like effect of valproic acid-Possible involvement of PI3K/Akt/mTOR pathway. Behav Brain Res. 2017;329:166–71.
pubmed: 28408298
Schroeder FA, Lewis MC, Fass DM, Wagner FF, Zhang YL, Hennig KM, et al. A selective HDAC 1/2 inhibitor modulates chromatin and gene expression in brain and alters mouse behavior in two mood-related tests. PLoS ONE. 2013;8:e71323.
pubmed: 23967191 pmcid: 3743770
Can A, Blackwell RA, Piantadosi SC, Dao DT, O’Donnell KC, Gould TD. Antidepressant-like responses to lithium in genetically diverse mouse strains. Genes Brain Behav. 2011;10:434–43.
pubmed: 21306560 pmcid: 3107888
White K, Bohart R, Whipple K, Boyd J. Lithium effects on normal subjects. Relationships to plasma and RBC lithium levels. Int Pharmacopsychiatry. 1979;14:176–83.
pubmed: 521242
Aldenkamp AP, Arends J, Bootsma HP, Diepman L, Hulsman J, Lambrechts D, et al. Randomized double-blind parallel-group study comparing cognitive effects of a low-dose lamotrigine with valproate and placebo in healthy volunteers. Epilepsia. 2002;43:19–26.
pubmed: 11879382
Cipriani A, Reid K, Young AH, Macritchie K, Geddes J. Valproic acid, valproate and divalproex in the maintenance treatment of bipolar disorder. Cochrane Database Syst Rev. 2013:CD003196.
Hallahan B, Newell J, Soares JC, Brambilla P, Strakowski SM, Fleck DE, et al. Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biol Psychiatry. 2011;69:326–35.
pubmed: 21030008
Hibar DP, Westlye LT, Doan NT, Jahanshad N, Cheung JW, Ching CRK, et al. Cortical abnormalities in bipolar disorder: an MRI analysis of 6503 individuals from the ENIGMA Bipolar Disorder Working Group. Mol Psychiatry. 2018;23:932–42.
pubmed: 28461699
Strakowski SM, Eliassen JC, Lamy M, Cerullo MA, Allendorfer JB, Madore M, et al. Functional magnetic resonance imaging brain activation in bipolar mania: evidence for disruption of the ventrolateral prefrontal-amygdala emotional pathway. Biol Psychiatry. 2011;69:381–8.
pubmed: 21051038
Milienne-Petiot M, Kesby JP, Graves M, van Enkhuizen J, Semenova S, Minassian A, et al. The effects of reduced dopamine transporter function and chronic lithium on motivation, probabilistic learning, and neurochemistry in mice: modeling bipolar mania. Neuropharmacology. 2017;113:260–70.
pubmed: 27732870
Young JW, Cope ZA, Romoli B, Schrurs E, Aniek J, van Enkhuizen J, et al. Mice with reduced DAT levels recreate seasonal-induced switching between states in bipolar disorder. Neuropsychopharmacology. 2018;43:1721–31.
pubmed: 29520059 pmcid: 6006292
Meylan EM, Halfon O, Magistretti PJ, Cardinaux JR. The HDAC inhibitor SAHA improves depressive-like behavior of CRTC1-deficient mice: possible relevance for treatment-resistant depression. Neuropharmacology. 2016;107:111–21.
pubmed: 26970016 pmcid: 5939991
Covington HE 3rd, Maze I, Vialou V, Nestler EJ. Antidepressant action of HDAC inhibition in the prefrontal cortex. Neuroscience. 2015;298:329–35.
pubmed: 25907440
Eom GH, Nam YS, Oh JG, Choe N, Min HK, Yoo EK, et al. Regulation of acetylation of histone deacetylase 2 by p300/CBP-associated factor/histone deacetylase 5 in the development of cardiac hypertrophy. Circ Res. 2014;114:1133–43.
pubmed: 24526703
Choubey SK, Jeyakanthan J. Molecular dynamics and quantum chemistry-based approaches to identify isoform selective HDAC2 inhibitor—a novel target to prevent Alzheimer’s disease. J Recept Signal Transduct Res. 2018;38:266–78.
pubmed: 29932788
Tan Y, Delvaux E, Nolz J, Coleman PD, Chen S, Mastroeni D. Upregulation of histone deacetylase 2 in laser capture nigral microglia in Parkinson’s disease. Neurobiol Aging. 2018;68:134–41.
pubmed: 29803514
Laugesen A, Helin K. Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell. 2014;14:735–51.
pubmed: 24905164
Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature. 2009;459:55–60.
pubmed: 19424149 pmcid: 3498958
Gonzalez-Zuniga M, Contreras PS, Estrada LD, Chamorro D, Villagra A, Zanlungo S, et al. c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer’s disease. Mol Cell. 2014;56:163–73.
pubmed: 25219501
Maletic V, Raison C. Integrated neurobiology of bipolar disorder. Front Psychiatry. 2014;5:98.
pubmed: 25202283 pmcid: 4142322
de la Fuente Revenga M, Ibi D, Saunders JM, Cuddy T, Ijaz MK, Toneatti R, et al. HDAC2-dependent antipsychotic-like effects of chronic treatment with the HDAC inhibitor SAHA in mice. Neuroscience. 2018;388:102–17.
pubmed: 30025863
Limanaqi F, Biagioni F, Busceti CL, Ryskalin L, Fornai F. The effects of proteasome on baseline and methamphetamine-dependent dopamine transmission. Neurosci Biobehav Rev. 2019;102:308–17.
pubmed: 31095962
Lauridsen JB, Johansen JL, Rekling JC, Thirstrup K, Moerk A, Sager TN. Regulation of the Bcas1 and Baiap3 transcripts in the subthalamic nucleus in mice recovering from MPTP toxicity. Neurosci Res. 2011;70:269–76.
pubmed: 21514331
Ishimoto T, Ninomiya K, Inoue R, Koike M, Uchiyama Y, Mori H. Mice lacking BCAS1, a novel myelin-associated protein, display hypomyelination, schizophrenia-like abnormal behaviors, and upregulation of inflammatory genes in the brain. Glia. 2017;65:727–39.
pubmed: 28230289
You C, Savarese A, Vandegrift BJ, He D, Pandey SC, Lasek AW, et al. Ethanol acts on KCNK13 potassium channels in the ventral tegmental area to increase firing rate and modulate binge-like drinking. Neuropharmacology. 2019;144:29–36.
pubmed: 30332606
Judy JT, Zandi PP. A review of potassium channels in bipolar disorder. Front Genet. 2013;4:105.
pubmed: 23781230 pmcid: 3678088
Avram S, Shaposhnikov S, Buiu C, Mernea M. Chondroitin sulfate proteoglycans: structure-function relationship with implication in neural development and brain disorders. Biomed Res Int. 2014;2014:642798.
pubmed: 24955366 pmcid: 4052930
Ganai SA, Ramadoss M, Mahadevan V. Histone deacetylase (HDAC) inhibitors—emerging roles in neuronal memory, learning, synaptic plasticity and neural regeneration. Curr Neuropharmacol. 2016;14:55–71.
pubmed: 26487502
Yamakawa H, Cheng J, Penney J, Gao F, Rueda R, Wang J, et al. The transcription factor Sp3 cooperates with HDAC2 to regulate synaptic function and plasticity in neurons. Cell Rep. 2017;20:1319–34.
pubmed: 28793257
Kramer OH, Zhu P, Ostendorff HP, Golebiewski M, Tiefenbach J, Peters MA, et al. The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J. 2003;22:3411–20.
pubmed: 12840003 pmcid: 165640
Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, et al. Core circadian protein CLOCK is a positive regulator of NF-kappaB-mediated transcription. Proc Natl Acad Sci USA. 2012;109:E2457–65.
pubmed: 22895791 pmcid: 3443185
Wagner T, Kiweler N, Wolff K, Knauer SK, Brandl A, Hemmerich P, et al. Sumoylation of HDAC2 promotes NF-kappaB-dependent gene expression. Oncotarget. 2015;6:7123–35.
pubmed: 25704882 pmcid: 4466673
Ashburner BP, Westerheide SD, Baldwin AS Jr. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol. 2001;21:7065–77.
pubmed: 11564889 pmcid: 99882
Howard AD, Wang R, Pong SS, Mellin TN, Strack A, Guan XM, et al. Identification of receptors for neuromedin U and its role in feeding. Nature. 2000;406:70–4.
pubmed: 10894543
Vallof D, Vestlund J, Engel JA, Jerlhag E. The anorexigenic peptide neuromedin U (NMU) attenuates amphetamine-induced locomotor stimulation, accumbal dopamine release and expression of conditioned place preference in mice. PloS ONE. 2016;11:e0154477.
pubmed: 27139195 pmcid: 4854378
Graham ES, Littlewood P, Turnbull Y, Mercer JG, Morgan PJ, Barrett P. Neuromedin-U is regulated by the circadian clock in the SCN of the mouse. Eur J Neurosci. 2005;21:814–9.
pubmed: 15733101
Lee IT, Chang AS, Manandhar M, Shan Y, Fan J, Izumo M, et al. Neuromedin s-producing neurons act as essential pacemakers in the suprachiasmatic nucleus to couple clock neurons and dictate circadian rhythms. Neuron. 2015;85:1086–102.
pubmed: 25741729 pmcid: 5811223
Harvey AG. Sleep and circadian rhythms in bipolar disorder: seeking synchrony, harmony, and regulation. Am J Psychiatry. 2008;165:820–9.
pubmed: 18519522
Landgraf D, Joiner WJ, McCarthy MJ, Kiessling S, Barandas R, Young JW, et al. The mood stabilizer valproic acid opposes the effects of dopamine on circadian rhythms. Neuropharmacology. 2016;107:262–70.
pubmed: 27033596
Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science. 1998;280:1564–9.
pubmed: 9616112
Hao Y, Creson T, Zhang L, Li P, Du F, Yuan P, et al. Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J Neurosci. 2004;24:6590–9.
pubmed: 15269271 pmcid: 6729884
Cui SS, Yang CP, Bowen RC, Bai O, Li XM, Jiang W, et al. Valproic acid enhances axonal regeneration and recovery of motor function after sciatic nerve axotomy in adult rats. Brain Res. 2003;975:229–36.
pubmed: 12763612
Hockly E, Richon VM, Woodman B, Smith DL, Zhou X, Rosa E, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington’s disease. Proc Natl Acad Sci USA. 2003;100:2041–6.
pubmed: 12576549 pmcid: 149955
Kurita M, Holloway T, Garcia-Bea A, Kozlenkov A, Friedman AK, Moreno JL, et al. HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat Neurosci. 2012;15:1245–54.
pubmed: 22864611 pmcid: 3431440
Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci. 2006;9:519–25.
pubmed: 16501568
Singec I, Crain AM, Hou J, Tobe BTD, Talantova M, Winquist AA, et al. Quantitative analysis of human pluripotency and neural specification by in-depth (Phospho)proteomic profiling. Stem Cell Rep. 2016;7:527–42.
Li W, Sun W, Zhang Y, Wei W, Ambasudhan R, Xia P, et al. Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc Natl Acad Sci USA. 2011;108:8299–304.
pubmed: 21525408 pmcid: 3100988
Madison JM, Zhou F, Nigam A, Hussain A, Barker DD, Nehme R, et al. Characterization of bipolar disorder patient-specific induced pluripotent stem cells from a family reveals neurodevelopmental and mRNA expression abnormalities. Mol Psychiatry. 2015;20:703–17.
pubmed: 25733313 pmcid: 4440839
Maroof AM, Keros S, Tyson JA, Ying SW, Ganat YM, Merkle FT. et al. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell. 2013;12:559–72.
pubmed: 23642365 pmcid: 3681523
Hunsberger JG, Austin DR, Chen G, Manji HK. Cellular mechanisms underlying affective resiliency: the role of glucocorticoid receptor- and mitochondrially-mediated plasticity. Brain Res. 2009;1293:76–84.
pubmed: 19595676 pmcid: 2804877
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.
pubmed: 23618408 pmcid: 4053844
Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9.
pubmed: 25260700
Volk DW, Matsubara T, Li S, Sengupta EJ, Georgiev D, Minabe Y, et al. Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia. Am J Psychiatry. 2012;169:1082–91.
pubmed: 22983435 pmcid: 3513625
Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016;11:1650–67.
pubmed: 27560171 pmcid: 5032908
Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH. Recovery of learning and memory is associated with chromatin remodelling. Nature. 2007;447:178–82.
pubmed: 17468743
Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Gen Mol Biol. 2005;4:Article17.
Langfelder P, Zhang B, Horvath S. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics. 2008;24:719–20.
pubmed: 18024473

Auteurs

Ryan W Logan (RW)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Angela R Ozburn (AR)

Department of Behavioral Neuroscience, Portland Alcohol Research Center, Oregon Health & Science University, Portland, OR, 97239, USA.
VA Portland Health Care System, Portland, OR, 97239, USA.

Rachel N Arey (RN)

Department of Molecular and Cellular Biology and Center for Precision Environmental Health, Baylor College of Medicine, Houston, TX, 77030, USA.

Kyle D Ketchesin (KD)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Alicia Winquist (A)

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, 92037, USA.
Sanford Consortium for Regenerative Medicine, La Jolla, CA, 92037, USA.

Andrew Crain (A)

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, 92037, USA.
Sanford Consortium for Regenerative Medicine, La Jolla, CA, 92037, USA.

Brian T D Tobe (BTD)

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, 92037, USA.
Sanford Consortium for Regenerative Medicine, La Jolla, CA, 92037, USA.
Department of Psychiatry, Veterans Administration Medical Center, La Jolla, CA, 92037, USA.

Darius Becker-Krail (D)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Matthew B Jarpe (MB)

Regenacy Pharmaceuticals, 303 Wyman St, Suite 300, Waltham, MA, 02451, USA.

Xiangning Xue (X)

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, 15261, USA.

Wei Zong (W)

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, 15261, USA.

Zhiguang Huo (Z)

Department of Biostatistics, University of Florida, Gainesville, FL, 32611, USA.

Puja K Parekh (PK)

Brain and Mind Research Institute, Department of Psychiatry, and Sackler Institute for Developmental Psychobiology, Weill Cornell Medicine, New York, NY, 10021, USA.

Xiyu Zhu (X)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.
Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Ethan Fitzgerald (E)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Hui Zhang (H)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.
Peking Union Medical College Hospital, 100730, Beijing, China.

Jeffrey Oliver-Smith (J)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Lauren M DePoy (LM)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Mariah A Hildebrand (MA)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA.

Evan Y Snyder (EY)

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, 92037, USA.
Sanford Consortium for Regenerative Medicine, La Jolla, CA, 92037, USA.
Department of Pediatrics, University of California San Diego, La Jolla, CA, 92037, USA.

George C Tseng (GC)

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, 15261, USA.
Department of Computational and Systems Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15213, USA.

Colleen A McClung (CA)

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219, USA. mcclungca@upmc.edu.

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