A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood

Brain Structure and Function

Volumn 221, Issue 9, 2016, Pages 4691-4703

  Sakharkar, Amul J ^a,b   Vetreno, Ryan P ^c   Zhang, Huaibo ^a,b   Kokare, Dadasaheb M ^a   Crews, Fulton T ^c   Pandey, Subhash C ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Adolescent alcohol; Anxiety; Brain derived neurotrophic factor; Hippocampus; Histone H3 acetylation; Neurogenesis

Indexed keywords

ALCOHOL; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOUBLECORTIN; HISTONE DEACETYLASE; HISTONE H3; HISTONE H3K9; KI 67 ANTIGEN; MESSENGER RNA; SODIUM CHLORIDE; TRICHOSTATIN A; UNCLASSIFIED DRUG; CREBBP PROTEIN, MOUSE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HISTONE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID;

ADOLESCENCE; ADOLESCENT; ADULT; ADULTHOOD; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVITY; EXON; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTONE ACETYLATION; MALE; MOLECULAR BIOLOGY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; ACETYLATION; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENETIC EPIGENESIS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACETYLATION; ANIMALS; ANXIETY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CREB-BINDING PROTEIN; EPIGENESIS, GENETIC; ETHANOL; HIPPOCAMPUS; HISTONE DEACETYLASE INHIBITORS; HISTONES; HYDROXAMIC ACIDS; MALE; NEUROGENESIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84960098325     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-016-1196-y     Document Type: Article

References (68)

1. Alaux-Cantin S, Warnault V, Legastelois R, Botia B, Pierrefiche O, Vilpoux C, Naassila M (2013) Alcohol intoxications during adolescence increase motivation for alcohol in adult rats and induce neuroadaptations in the nucleus accumbens. Neuropharmacology 67:521–531
2. Alme MN, Wibrand K, Dagestad G, Bramham CR (2007) Chronic fluoxetine treatment induces brain region-specific upregulation of genes associated with BDNF-induced long-term potentiation. Neural Plast 2007:26496
3. Andero R, Choi DC, Ressler KJ (2014) BDNF-TrkB receptor regulation of distributed adult neural plasticity, memory formation, and psychiatric disorders. Prog Mol Biol Transl Sci 122:169–192
4. Barrett RM, Malvaez M, Kramar E, Matheos DP, Arrizon A, Cabrera SM, Lynch G, Greene RW, Wood MA (2011) Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory. Neuropsychopharmacology 36:1545–1556
5. Briones TL, Woods J (2013) Chronic binge-like alcohol consumption in adolescence causes depression-like symptoms possibly mediated by the effects of BDNF on neurogenesis. Neuroscience 254:324–334
6. Broadwater MA, Liu W, Crews FT, Spear LP (2014) Persistent loss of hippocampal neurogenesis and increased cell death following adolescent, but not adult, chronic ethanol exposure. Dev Neurosci 36:297–305
7. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10
8. Chambers RA (2013) Adult hippocampal neurogenesis in the pathogenesis of addiction and dual diagnosis disorders. Drug Alcohol Depend 130:1–12
9. Chatterjee S, Mizar P, Cassel R, Neidl R, Selvi BR, Mohankrishna DV, Vedamurthy BM, Schneider A, Bousiges O, Mathis C, Cassel JC, Eswaramoorthy M, Kundu TK, Boutillier AL (2013) A novel activator of CBP/p300 acetyltransferases promotes neurogenesis and extends memory duration in adult mice. J Neurosci 33:10698–10712
10. Crews FT, Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 44:115–127
11. Crews FT, Vetreno RP (2014) Neuroimmune basis of alcoholic brain damage. Int Rev Neurobiol 118:315–357
12. Crews FT, Nixon K, Wilkie ME (2004) Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol 33:63–71
13. Crews FT, Mdzinarishvili A, Kim D, He J, Nixon K (2006) Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 137:437–445
14. DeWit DJ, Adlaf EM, Offord DR, Ogborne AC (2000) Age at first alcohol use: a risk factor for the development of alcohol disorders. Am J Psychiatry 157:745–750
15. Donovan JE (2004) Adolescent alcohol initiation: a review of psychosocial risk factors. J Adolesc Health 35:529.e7–18
16. Duman RS (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromol Med 5:11–25
17. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127
18. Ehlers CL, Liu W, Wills DN, Crews FT (2013) Periadolescent ethanol vapor exposure persistently reduces measures of hippocampal neurogenesis that are associated with behavioral outcomes in adulthood. Neuroscience 244:1–15
19. Fuchikami M, Yamamoto S, Morinobu S, Takei S, Yamawaki S (2010) Epigenetic regulation of BDNF gene in response to stress. Psychiatry Investig 7:251–256
20. Grant BF, Dawson DA (1998) Age at onset of drug use and its association with DSM-IV drug abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 10:163–173
21. Gu Y, Janoschka S, Ge S (2013) Neurogenesis and hippocampal plasticity in adult brain. Curr Top Behav Neurosci 15:31–48
22. Hauser SR, Getachew B, Taylor RE, Tizabi Y (2011) Alcohol induced depressive-like behavior is associated with a reduction in hippocampal BDNF. Pharmacol Biochem Behav 100:253–258
23. Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 101:16659–16664
24. Ieraci A, Herrera DG (2007) Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiol Dis 26:597–605
25. Iwata M, Ota KT, Duman RS (2013) The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav Immun 31:105–114
26. Kalkhoven E (2004) CBP and p300: HATs for different occasions. Biochem Pharmacol 68:1145–1155
27. Keshvan MS, Giedd J, Lau JY, Lweis DA, Paus T (2014) Changes in the adolescent brain and the pathophysiology of psychotic disorders. Lancet Psychiatry 1:549–558
28. Kozisek ME, Middlemas D, Bylund DB (2008) Brain-derived neurotrophic factor and its receptor tropomyosin-related kinase B in the mechanism of action of antidepressant therapies. Pharmacol Ther 117:30–51
29. Krishnan HR, Sakharkar AJ, Teppen TL, Berkel TD, Pandey SC (2014) The epigenetic landscape of alcoholism. Int Rev Neurobiol 115:75–116
30. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, Neve RL, Self DW, Nestler EJ (2005) Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48:303–314
31. Leone L, Fusco S, Mastrodonato A, Piacentini R, Barbati SA, Zaffina S, Pani G, Podda MV, Grassi C (2014) Epigenetic modulation of adult hippocampal neurogenesis by extremely low-frequency electromagnetic fields. Mol Neurobiol 49:1472–1486
32. Lilja T, Heldring N, Hermanson O (2013) Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation. Biochim Biophys Acta 1830:2354–2360
33. Liu JX, Pinnock SB, Herbert J (2011) Novel control by the CA3 region of the hippocampus on neurogenesis in the dentate gyrus of the adult rat. PLoS One 6:e17562
34. Lubin FD, Roth TL, Sweatt JD (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28:10576–10586
35. McNaughton N, Gray JA (2000) Anxiolytic action on the behavioural system implies types of arousal contribute to anxiety. J Affect Disord 61:161–176
36. Medina KL, Schweinsburg AD, Cohen-Zion M, Nagel BJ, Tapert SF (2007) Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicol Teratol 29:141–152
37. Moonat S, Sakharkar AJ, Zhang H, Pandey SC (2011) The role of amygdaloid brain-derived neurotrophic factor, activity-regulated cytoskeleton-associated protein and dendritic spines in anxiety and alcoholism. Addict Biol 16:238–250
38. Moonat S, Sakharkar AJ, Zhang H, Tang L, Pandey SC (2013) Aberrant histone deacetylase2-mediated histone modifications and synaptic plasticity in the amygdala predisposes to anxiety and alcoholism. Biol Psychiatry 73:763–773
39. Nagel BJ, Schweinsburg AD, Phan V, Tapert SF (2005) Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res 139:181–190
40. Newton SS, Duman RS (2006) Chromatin remodeling: a novel mechanism of psychotropic drug action. Mol Pharmacol 70:440–443
41. Packard M (2009) Anxiety, cognition, and habit: a multiple memory systems perspective. Brain Res 1293:121–128
42. Pandey SC, Chartoff EH, Carlezon WA Jr, Zou J, Zhang H, Kreibich AS, Blendy JA, Crews FT (2005) CREB gene transcription factors: role in molecular mechanisms of alcohol and drug addiction. Alcohol Clin Exp Res 29:176–184
43. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A (2008) Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci 28:3729–3737
44. Pandey SC, Sakharkar AJ, Tang L, Zhang H (2015) Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood. Neurobiol Dis 82:607–619
45. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR 3rd, Lafaille JJ, Hempstead BL, Littman DR, Gan WB (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609
46. Pascual M, Boix J, Felipo V, Guerri C (2009) Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. J Neurochem 108:920–931
47. Pascual M, Do Couto BR, Alfonso-Loeches S, Aguilar MA, Rodriguez-Arias M, Guerri C (2012) Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rats are associated with ethanol-induced place conditioning. Neuropharmacology 62:2309–2319
48. Renthal W, Nestler EJ (2008) Epigenetic mechanisms in drug addiction. Trends Mol Med 14:341–350
49. Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV, Abrous DN (2009) Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 14:959–967
50. Roth TL, Lubin FD, Funk AJ, Sweatt JD (2009) Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65:760–769
51. Sakharkar AJ, Zhang H, Tang L, Shi G, Pandey SC (2012) Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol Clin Exp Res 36:61–71
52. Sakharkar AJ, Zhang H, Tang L, Baxstrom K, Shi G, Moonat S, Pandey SC (2014a) Effects of histone deacetylase inhibitors on amygdaloid histone acetylation and neuropeptide Y expression: a role in anxiety-like and alcohol-drinking behaviours. Int J Neuropsychopharmacol 17:1207–1220
53. Sakharkar AJ, Tang L, Zhang H, Chen Y, Grayson DR, Pandey SC (2014b) Effects of acute ethanol exposure on anxiety measures and epigenetic modifiers in the extended amygdala of adolescent rats. Int J Neuropsychopharmacol 17:2057–2067
54. Scharfman HE (2007) The CA3 “backprojection” to the dentate gyrus. Prog Brain Res 163:627–637
55. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108
56. Schoenfeld TJ, Cameron HA (2015) Adult neurogenesis and mental illness. Neuropsychopharmacology 40:113–128
57. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311–322
58. Sheikh BN (2014) Crafting the brain-role of histone acetyltransferases in neural development and disease. Cell Tissue Res 356:553–573
59. Swaminathan A, Kumar M, Halder Sinha S, Schneider-Anthony A, Boutillier AL, Kundu TK (2014) Modulation of neurogenesis by targeting epigenetic enzymes using small molecules: an overview. ACS Chem Neurosci 5:1164–1177
60. Taliaz D, Stall N, Dar DE, Zangen A (2010) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15:80–92
61. Tapia-Arancibia L, Rage F, Givalois L, Dingeon P, Arancibia S, Beaugé F (2001) Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J Neurosci Res 63:200–208
62. 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
63. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519–525
64. Valor LM, Viosca J, Lopez-Atalaya JP, Barco A (2013) Lysine acetyltransferases CBP and p300 as therapeutic targets in cognitive and neurodegenerative disorders. Curr Pharm Des 19:5051–5064
65. Vetreno RP, Crews FT (2015) Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning. Front Neurosci 9:35
66. Yoo DY, Kim DW, Kim MJ, Choi JH, Jung HY, Nam SM, Kim JW, Yoon YS, Choi SY, Hwang IK (2015) Sodium butyrate, a histone deacetylase Inhibitor, ameliorates SIRT2-induced memory impairment, reduction of cell proliferation, and neuroblast differentiation in the dentate gyrus. Neurol Res 37:69–76
67. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660
68. Zou J, Crews FT (2012) Inflammasome-IL-1β signaling mediates ethanol inhibition of hippocampal neurogenesis. Front Neurosci 6:77