Epigenetic readers of lysine acetylation regulate cocaine-induced plasticity

Journal of Neuroscience

Volumn 35, Issue 45, 2015, Pages 15062-15072

  Sartor, Gregory C ^a   Powell, Samuel K ^a   Brothers, Shaun P ^a   Wahlestedt, Claes ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

BDNF; BET; BRD4; Bromodomain; Cocaine; Epigenetic

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BROMODOMAIN INHIBITOR; BROMODOMAIN PROTEIN; COCAINE; LYSINE; PEPTIDES AND PROTEINS; PROTEIN BRD2; PROTEIN BRD3; PROTEIN BRD4; PROTEIN BRDT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COCAINE DEPENDENCE; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; HISTOLOGY; HISTONE ACETYLATION; LOCOMOTION; MALE; MOUSE; NERVE CELL PLASTICITY; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ACETYLATION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETIC EPIGENESIS; HEK293 CELL LINE; HUMAN; INSTRUMENTAL CONDITIONING; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACETYLATION; ANIMALS; COCAINE; CONDITIONING, OPERANT; EPIGENESIS, GENETIC; HEK293 CELLS; HUMANS; LYSINE; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84946943935     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0826-15.2015     Document Type: Article

References (71)

1. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856–860. CrossRef Medline
2. Bahi A, Boyer F, Chandrasekar V, Dreyer JL (2008) Role of accumbens BDNF and TrkB in cocaine-induced psychomotor sensitization, conditioned-place preference, and reinstatement in rats. Psychopharmacology (Berl) 199:169–182. CrossRef Medline
3. Barrett E, Brothers S, Wahlestedt C, Beurel E (2014) I-BET151 selectively regulates IL-6 production. Biochim Biophys Acta 1842:1549–1555. CrossRef Medline
4. Belkina AC, Denis GV (2012) BET domain co-regulators in obesity, inflammation and cancer. Nat Rev Cancer 12:465–477. CrossRef Medline
5. Belkina AC, Nikolajczyk BS, Denis GV (2013) BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J Immunol 190: 3670–3678. CrossRef Medline
6. Brown JD, Lin CY, Duan Q, Griffin G, Federation AJ, Paranal RM, Bair S, Newton G, Lichtman AH, Kung AL, Yang T, Wang H, Luscinskas FW, Croce KJ, Bradner JE, Plutzky J (2014) NF-kappaB directs dynamic super enhancer formation in inflammation and atherogenesis. Mol Cell 56:219–231. CrossRef Medline
7. Cearley CN, Blindheim K, Sorg BA, Krueger JM, Churchill L (2011) Acute cocaine increases interleukin-1beta mRNA and immunoreactive cells in the cortex and nucleus accumbens. Neurochem Res 36:686–692. CrossRef Medline
8. Chung CW, Coste H, White JH, Mirguet O, Wilde J, Gosmini RL, Delves C, Magny SM, Woodward R, Hughes SA, Boursier EV, Flynn H, Bouillot AM, Bamborough P, Brusq JM, Gellibert FJ, Jones EJ, Riou AM, Homes P, Martin SL, et al. (2011) Discovery and characterization of smallmolecule inhibitors of the BET family bromodomains. J Med Chem 54: 3827–3838. CrossRef Medline
9. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM, Kastritis E, Gilpatrick T, Paranal RM, Qi J, Chesi M, Schinzel AC, McKeown MR, Heffernan TP, Vakoc CR, Bergsagel PL, Ghobrial IM, Richardson PG, Young RA, Hahn WC, et al. (2011) BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146:904–917. CrossRef Medline
10. Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K (2003) The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci U S A 100:8758–8763. CrossRef Medline
11. Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM (1999) Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491–496. CrossRef Medline
12. Elmér E, Kokaia Z, Kokaia M, Carnahan J, Nawa H, Lindvall O (1998) Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience 83:351–362. CrossRef Medline
13. Filip M, Faron-Górecka A, Kusmider M, Golda A, Frankowska M, Dziedzicka-Wasylewska M (2006) Alterations in BDNF and trkB mRNAs following acute or sensitizing cocaine treatments and withdrawal. Brain Res 1071:218–225. CrossRef Medline
14. Filippakopoulos P, Knapp S (2014) Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov 13:337–356. CrossRef Medline
15. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, Morse EM, Keates T, Hickman TT, Felletar I, Philpott M, Munro S, McKeown MR, Wang Y, Christie AL, West N, Cameron MJ, Schwartz B, Heightman TD, La Thangue N, et al. (2010) Selective inhibition of BET bromodomains. Nature 468:1067–1073. CrossRef Medline
16. Fumagalli F, Caffino L, Racagni G, Riva MA (2009) Repeated stress prevents cocaine-induced activation of BDNF signaling in rat prefrontal cortex. Eur Neuropsychopharmacol 19:402–408. CrossRef Medline
17. Graham DL, Edwards S, Bachtell RK, DiLeone RJ, Rios M, Self DW (2007) Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat Neurosci 10:1029–1037. CrossRef Medline
18. Graham DL, Krishnan V, Larson EB, Graham A, Edwards S, Bachtell RK, Simmons D, Gent LM, Berton O, Bolanos CA, DiLeone RJ, Parada LF, Nestler EJ, Self DW (2009) Tropomyosin-related kinase B in the mesolimbic dopamine system: region-specific effects on cocaine reward. Biol Psychiatry 65:696–701. CrossRef Medline
19. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003) Timedependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23:742–747. Medline
20. Harris GC, Hummel M, Wimmer M, Mague SD, Aston-Jones G (2007) Elevations of FosB in the nucleus accumbens during forced cocaine abstinence correlate with divergent changes in reward function. Neuroscience 147:583–591. CrossRef Medline
21. Hiroi N, Brown JR, Haile CN, Ye H, Greenberg ME, Nestler EJ (1997) FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine’s psychomotor and rewarding effects. Proc Natl Acad Sci U S A 94:10397–10402. CrossRef Medline
22. Horger BA, Iyasere CA, Berhow MT, Messer CJ, Nestler EJ, Taylor JR (1999) Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. J Neurosci 19:4110–4122. Medline
23. Im HI, Hollander JA, Bali P, Kenny PJ (2010) MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat Neurosci 13:1120–1127. CrossRef Medline
24. Jeanblanc J, He DY, Carnicella S, Kharazia V, Janak PH, Ron D (2009) Endogenous BDNF in the dorsolateral striatum gates alcohol drinking. J Neurosci 29:13494–13502. CrossRef Medline
25. Kennedy PJ, Feng J, Robison AJ, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han MH, Bassel-Duby R, Olson EN, Nestler EJ (2013) Class IHDACinhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 16:434–440. CrossRef Medline
26. Kerns RT, Ravindranathan A, Hassan S, Cage MP, York T, Sikela JM, Williams RW, Miles MF (2005) Ethanol-responsive brain region expression networks: implications for behavioral responses to acute ethanol in DBA/2J versus C57BL/6J mice. J Neurosci 25:2255–2266. CrossRef Medline
27. Korb E, Herre M, Zucker-Scharff I, Darnell RB, Allis CD (2015) BET protein Brd4 activates transcription in neurons and BET inhibitor Jq1 blocks memory in mice. Nat Neurosci 18:1464–1473. CrossRef Medline
28. 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 cocaineinduced plasticity in striatum. Neuron 48:303–314. CrossRef Medline
29. Kurita M, Holloway T, García-Bea A, Kozlenkov A, Friedman AK, Moreno JL, Heshmati M, Golden SA, Kennedy PJ, Takahashi N, Dietz DM, Mocci G, Gabilondo AM, Hanks J, Umali A, Callado LF, Gallitano AL, Neve RL, Shen L, Buxbaum JD, et al. (2012) HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat Neurosci 15:1245–1254. CrossRef Medline
30. LaPlant Q, Nestler EJ (2011) CRACKing the histone code: cocaine’s effects on chromatin structure and function. Horm Behav 59:321–330. CrossRef Medline
31. Le Foll B, Diaz J, Sokoloff P (2005) A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 16:175–178. CrossRef Medline
32. LeRoy G, Chepelev I, DiMaggio PA, Blanco MA, Zee BM, Zhao K, Garcia BA (2012) Proteogenomic characterization and mapping of nucleosomes decoded by Brd and HP1 proteins. Genome Biol 13:R68. CrossRef Medline
33. Liu QR, Lu L, Zhu XG, Gong JP, Shaham Y, Uhl GR (2006) Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res 1067:1–12. CrossRef Medline
34. Lu L, Dempsey J, Liu SY, Bossert JM, Shaham Y (2004) A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J Neurosci 24:1604–1611. CrossRef Medline
35. Malvaez M, Sanchis-Segura C, Vo D, Lattal KM, Wood MA (2010) Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biol Psychiatry 67:36–43. CrossRef Medline
36. Malvaez M, Mhillaj E, Matheos DP, Palmery M, Wood MA (2011) CBP in the nucleus accumbens regulates cocaine-induced histone acetylation and is critical for cocaine-associated behaviors. J Neurosci 31:16941–16948. CrossRef Medline
37. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, Carreiro S, Rusche JR, Wood MA (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci U S A 110:2647–2652. CrossRef Medline
38. Martin-Iverson MT, Todd KG, Altar CA (1994) Brain-derived neurotrophic factor and neurotrophin-3 activate striatal dopamine and serotonin metabolism and related behaviors: interactions with amphetamine. J Neurosci 14:1262–1270. Medline
39. Matzuk MM, McKeown MR, Filippakopoulos P, Li Q, Ma L, Agno JE, Lemieux ME, Picaud S, Yu RN, Qi J, Knapp S, Bradner JE (2012) Smallmolecule inhibition of BRDT for male contraception. Cell 150:673–684. CrossRef Medline
40. Maze I, Covington HE 3rd, Dietz DM, LaPlant Q, Renthal W, Russo SJ, Mechanic M, Mouzon E, Neve RL, Haggarty SJ, Ren Y, Sampath SC, Hurd YL, Greengard P, Tarakhovsky A, Schaefer A, Nestler EJ (2010) Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327:213–216. CrossRef Medline
41. Meng S, Zhang L, Tang Y, Tu Q, Zheng L, Yu L, Murray D, Cheng J, Kim SH, Zhou X, Chen J (2014) BET inhibitor JQ1 blocks inflammation and bone destruction. J Dent Res 93:657–662. CrossRef Medline
42. 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. CrossRef Medline
43. Morinière J, Rousseaux S, Steuerwald U, Soler-López M, Curtet S, Vitte AL, Govin J, Gaucher J, Sadoul K, Hart DJ, Krijgsveld J, Khochbin S, Müller CW, Petosa C (2009) Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461:664–668. CrossRef Medline
44. Narita M, Aoki K, Takagi M, Yajima Y, Suzuki T (2003) Implication of brain-derived neurotrophic factor in the release of dopamine and dopamine-related behaviors induced by methamphetamine. Neuroscience 119:767–775. CrossRef Medline
45. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, Chandwani R, Marazzi I, Wilson P, Coste H, White J, Kirilovsky J, Rice CM, Lora JM, Prinjha RK, Lee K, Tarakhovsky A (2010) Suppression of inflammation by a synthetic histone mimic. Nature 468:1119–1123. CrossRef Medline
46. Niwa M, Nitta A, Yamada K, Nabeshima T (2007) The roles of glial cell line-derived neurotrophic factor, tumor necrosis factor-alpha, and an inducer of these factors in drug dependence. J Pharmacol Sci 104: 116–121. CrossRef Medline
47. Owen DJ, Ornaghi P, Yang JC, Lowe N, Evans PR, Ballario P, Neuhaus D, Filetici P, Travers AA (2000) The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. EMBO J 19:6141–6149. CrossRef Medline
48. Pastori C, Kapranov P, Penas C, Peschansky V, Volmar CH, Sarkaria JN, Bregy A, Komotar R, St Laurent G, Ayad NG, Wahlestedt C (2015) The Bromodomain protein BRD4 controls HOTAIR, a long noncoding RNA essential for glioblastoma proliferation. Proc Natl Acad Sci U S A 112: 8326–8331. CrossRef Medline
49. Patel MC, Debrosse M, Smith M, Dey A, Huynh W, Sarai N, Heightman TD, Tamura T, Ozato K (2013) BRD4 coordinates recruitment of pause release factor P-TEFb and the pausing complex NELF/DSIF to regulate transcription elongation of interferon-stimulated genes. Mol Cell Biol 33:2497–2507. CrossRef Medline
50. Paxinos G, Watson C (1998) A stereotaxic atlas of the rat brain. San Diego: Academic.
51. Prinjha RK, Witherington J, Lee K (2012) Place your BETs: the therapeutic potential of bromodomains. Trends Pharmacol Sci 33:146–153. CrossRef Medline
52. Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517–529. CrossRef Medline
53. Renthal W, Kumar A, Xiao G, Wilkinson M, Covington HE 3rd, Maze I, Sikder D, Robison AJ, LaPlant Q, Dietz DM, Russo SJ, Vialou V, Chakravarty S, Kodadek TJ, Stack A, Kabbaj M, Nestler EJ (2009) Genomewide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62:335–348. CrossRef Medline
54. Rogge GA, Singh H, Dang R, Wood MA (2013) HDAC3 is a negative regulator of cocaine-context-associated memory formation. J Neurosci 33: 6623–6632. CrossRef Medline
55. Sadri-Vakili G, Kumaresan V, Schmidt HD, Famous KR, Chawla P, Vassoler FM, Overland RP, Xia E, Bass CE, Terwilliger EF, Pierce RC, Cha JH (2010) Cocaine-induced chromatin remodeling increases brainderived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine. J Neurosci 30: 11735–11744. CrossRef Medline
56. Saito M, O’Brien D, Kovacs KM, Wang R, Zavadil J, Vadasz C (2005) Nicotine-induced sensitization in mice: changes in locomotor activity and mesencephalic gene expression. Neurochem Res 30:1027–1035. CrossRef Medline
57. Sartor GC, Aston-Jones GS (2012) A septal-hypothalamic pathway drives orexin neurons, which is necessary for conditioned cocaine preference. J Neurosci 32:4623–4631. CrossRef Medline
58. Saylor AJ, McGinty JF (2008) Amphetamine-induced locomotion and gene expression are altered in BDNF heterozygous mice. Genes Brain Behav 7:906–914. CrossRef Medline
59. Schmidt HD, Sangrey GR, Darnell SB, Schassburger RL, Cha JH, Pierce RC, Sadri-Vakili G (2012) Increased brain-derived neurotrophic factor (BDNF) expression in the ventral tegmental area during cocaine abstinence is associated with increased histone acetylation at BDNF exon I-containing promoters. J Neurochem 120:202–209. CrossRef Medline
60. Shang E, Salazar G, Crowley TE, Wang X, Lopez RA, Wang X, Wolgemuth DJ (2004) Identification of unique, differentiation stage-specific patterns of expression of the bromodomain-containing genes Brd2, Brd3, Brd4, and Brdt in the mouse testis. Gene Expr Patterns 4:513–519. CrossRef Medline
61. Stafford JM, Raybuck JD, Ryabinin AE, Lattal KM (2012) Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biol Psychiatry 72:25–33. CrossRef Medline
62. Su D, Coudriet GM, Hyun Kim D, Lu Y, Perdomo G, Qu S, Slusher S, Tse HM, Piganelli J, Giannoukakis N, Zhang J, Dong HH (2009) FoxO1 links insulin resistance to proinflammatory cytokine IL-1beta production in macrophages. Diabetes 58:2624–2633. CrossRef Medline
63. Subramanian S, Bates SE, Wright JJ, Espinoza-Delgado I, Piekarz RI (2010) Clinical toxicities of histone deacetylase inhibitors. Pharmaceuticals 3:2751–2767. CrossRef
64. Sun J, Wang L, Jiang B, Hui B, Lv Z, Ma L (2008) The effects of sodium butyrate, an inhibitor of histone deacetylase, on the cocaine- and sucrosemaintained self-administration in rats. Neurosci Lett 441:72–76. CrossRef Medline
65. Tremolizzo L, Carboni G, Ruzicka WB, Mitchell CP, Sugaya I, Tueting P, Sharma R, Grayson DR, Costa E, Guidotti A (2002) An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci U S A 99:17095–17100. CrossRef Medline
66. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013) Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16: 42–47. CrossRef Medline
67. Wang L, Lv Z, Hu Z, Sheng J, Hui B, Sun J, Ma L (2010) Chronic cocaineinduced H3 acetylation and transcriptional activation of CaMKIIalpha in the nucleus accumbens is critical for motivation for drug reinforcement. Neuropsychopharmacology 35:913–928. CrossRef Medline
68. Winston F, Allis CD (1999) The bromodomain: a chromatin-targeting module? Nat Struct Biol 6:601–604. CrossRef Medline
69. Zeier Z, Esanov R, Belle KC, Volmar CH, Johnstone AL, Halley P, DeRosa BA, Khoury N, van Blitterswijk M, Rademakers R, Albert J, Brothers SP, Wuu J, Dykxhoorn DM, Benatar M, Wahlestedt C (2015) Bromodomain inhibitors regulate the C9ORF72 locus in ALS. Exp Neurol 271:241–250. CrossRef Medline
70. Zhang W, Prakash C, Sum C, Gong Y, Li Y, Kwok JJ, Thiessen N, Pettersson S, Jones SJ, Knapp S, Yang H, Chin KC (2012) Bromodomain-containing protein 4 (BRD4) regulates RNA polymerase II serine 2 phosphorylation in human CD4+ T cells. J Biol Chem 287:43137–43155. CrossRef Medline
71. Zuber J, Shi J, Wang E, Rappaport AR, Herrmann H, Sison EA, Magoon D, Qi J, Blatt K, Wunderlich M, Taylor MJ, Johns C, Chicas A, Mulloy JC, Kogan SC, Brown P, Valent P, Bradner JE, Lowe SW, Vakoc CR (2011) RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478:524–528. CrossRef Medline