Epigenetic landscape of amphetamine and methamphetamine addiction in rodents

Epigenetics

Volumn 10, Issue 7, 2015, Pages 574-580

  Godino, A ^a   Jayanthi, S ^b   Cadet, Jean Lud ^b  

^a UNIVERSITÉ DE LYON   (France)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Amphetamine; DNA methylation; Histone acetylation; Histone methylation; Methamphetamine

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; METHAMPHETAMINE; CENTRAL STIMULANT AGENT; HISTONE;

BEHAVIOR; BEHAVIOR CHANGE; BEHAVIOR DISORDER; DNA METHYLATION; DRUG DEPENDENCE; DRUG EXPOSURE; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; HISTONE ACETYLATION; HISTONE METHYLATION; LOCOMOTION; MICROARRAY ANALYSIS; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; RODENT; TRANSCRIPTION INITIATION; ACETYLATION; AMPHETAMINE DEPENDENCE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; METHYLATION; MOUSE; PATHOPHYSIOLOGY; RAT;

ACETYLATION; AMPHETAMINE; AMPHETAMINE-RELATED DISORDERS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; GENE EXPRESSION; HISTONE DEACETYLASES; HISTONES; HUMANS; METHAMPHETAMINE; METHYLATION; MICE; NEURONAL PLASTICITY; RATS;

EID: 84940901751     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2015.1055441     Document Type: Review

References (57)

1. Howell LL, Kimmel HL. Monoamine transporters and psychostimulant addiction. Biochem Pharmacol 2008; 75: 196-217; PMID: 17825265; http://dx. doi. org/10. 1016/j. bcp. 2007. 08. 003.
2. Schultz W. Multiple reward signals in the brain. Nat Rev Neurosci 2000; 1: 199-207; PMID: 11257908; http://dx. doi. org/10. 1038/35044563.
3. Goodwin JS, Larson GA, Swant J, Sen N, Javitch JA, Zahniser NR, Felice LJD, Khoshbouei H. Amphetamine and methamphetamine differentially affect dopamine transporters in vitro and in vivo. J Biol Chem 2009; 284: 2978-89; PMID: 19047053; http://dx. doi. org/10. 1074/jbc. M805298200.
4. Cadet JL, Krasnova IN, Jayanthi S, Lyles J. Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotox Res 2007; 11: 183-202; PMID: 17449459; http://dx. doi. org/10. 1007/BF03033567.
5. Bird A. Perceptions of epigenetics. Nature 2007; 447: 396-8; PMID: 17522671; http://dx. doi. org/10. 1038/nature05913.
6. Nestler EJ. Epigenetic mechanisms of drug addiction. Neuropharmacology 2014; 76 Pt B: 259-68; PMID: 23643695; http://dx. doi. org/10. 1016/j. neuropharm. 2013. 04. 004.
7. Rogge GA, Wood MA. The role of histone acetylation in cocaine-induced neural plasticity and behavior. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2013; 38: 94-110; http://dx. doi. org/10. 1038/npp. 2012. 154.
8. ShibasakiM, Mizuno K, Kurokawa K, Ohkuma S. L-type voltage-dependent calcium channels facilitate acetylation of histone H3 through PKCg phosphorylation in mice with methamphetamine-induced place preference. J Neurochem2011; 118: 1056-66; PMID: 21781114; http://dx. doi. org/10. 1111/j. 1471-4159. 2011. 07387. x.
9. Jing L, Zhang M, Li J-X, Huang P, Liu Q, Li Y-L, Liang H, Liang J-H. Comparison of single versus repeated methamphetamine injection induced behavioral sensitization in mice. Neurosci Lett 2014; 560: 103-6; PMID: 24361545; http://dx. doi. org/10. 1016/j. neulet. 2013. 12. 024.
10. Frey BN, Andreazza AC, Ceresér KMM, Martins MR, Valvassori SS, Réus GZ, Quevedo J, Kapczinski F. Effects of mood stabilizers on hippocampus BDNF levels in an animal model of mania. Life Sci 2006; 79: 281-6; PMID: 16460767; http://dx. doi. org/10. 1016/j. lfs. 2006. 01. 002.
11. Moretti M, Valvassori SS, Varela RB, Ferreira CL, Rochi N, Benedet J, Scaini G, Kapczinski F, Streck EL, Zugno AI, et al. Behavioral and neurochemical effects of sodium butyrate in an animal model of mania. Behav Pharmacol 2011; 22: 766-72; PMID: 21989497; http://dx. doi. org/10. 1097/FBP. 0b013e32834d0f1b.
12. Arent CO, Valvassori SS, Fries GR, Stertz L, Ferreira CL, Lopes-Borges J, Mariot E, Varela RB, Ornell F, Kapczinski F, et al. Neuroanatomical profile of antimaniac effects of histone deacetylases inhibitors. Mol Neurobiol 2011; 43: 207-14; PMID: 21424678; http://dx. doi. org/10. 1007/s12035-011-8178-0.
13. Kim WY, Kim S, Kim J-H. Chronic microinjection of valproic acid into the nucleus accumbens attenuates amphetamine-induced locomotor activity. Neurosci Lett 2008; 432: 54-7; PMID: 18164815; http://dx. doi. org/10. 1016/j. neulet. 2007. 12. 005.
14. Schroeder FA, Lewis MC, Fass DM, Wagner FF, Zhang Y-L, Hennig KM, Gale J, Zhao W-N, Reis S, Barker DD, 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; PMID: 23967191; http://dx. doi. org/10. 1371/journal. pone. 0071323.
15. Kalda A, Heidmets L-T, Shen H-Y, Zharkovsky A, Chen J-F. Histone deacetylase inhibitors modulates the induction and expression of amphetamine-induced behavioral sensitization partially through an associated learning of the environment in mice. Behav Brain Res 2007; 181: 76-84; PMID: 17477979; http://dx. doi. org/10. 1016/j. bbr. 2007. 03. 027.
16. Coccurello R, Caprioli A, Ghirardi O, Virmani A. Valproate and acetyl-L-carnitine prevent methamphetamine-induced behavioral sensitization in mice. Ann N Y Acad Sci 2007; 1122: 260-75; PMID: 18077579; http://dx. doi. org/10. 1196/annals. 1403. 019.
17. Shen H-Y, Kalda A, Yu L, Ferrara J, Zhu J, Chen J-F. Additive effects of histone deacetylase inhibitors and amphetamine on histone H4 acetylation, cAMP responsive element binding protein phosphorylation and DeltaFosB expression in the striatum and locomotor sensitization in mice. Neuroscience 2008; 157: 644-55; PMID: 18848971; http://dx. doi. org/10. 1016/j. neuroscience. 2008. 09. 019.
18. Harkness JH, Hitzemann RJ, Edmunds S, Phillips TJ. Effects of sodium butyrate on methamphetamine-sensitized locomotor activity. Behav Brain Res 2013; 239: 139-47; PMID: 23137698; http://dx. doi. org/10. 1016/j. bbr. 2012. 10. 046.
19. Li J-X, Han R, Deng Y-P, Chen S-Q, Liang J-H. Different effects of valproate on methamphetamine-and cocaine-induced behavioral sensitization in mice. Behav Brain Res 2005; 161: 125-32; PMID: 15904719; http://dx. doi. org/10. 1016/j. bbr. 2005. 01. 015.
20. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rumbaugh G. Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2010; 35: 870-80; http://dx. doi. org/10. 1038/npp. 2009. 197.
21. Owens MJ, Nemeroff CB. Pharmacology of valproate. Psychopharmacol Bull 2003; 37 Suppl 2: 17-24; PMID: 14624230.
22. Cadet JL, Jayanthi S, McCoy MT, Ladenheim B, Saint-Preux F, Lehrmann E, De S, Becker KG, Brannock C. Genome-wide profiling identifies a subset of methamphetamine (METH)-induced genes associated with METH-induced increased H4K5Ac binding in the rat striatum. BMC Genomics 2013; 14: 545; PMID: 23937714; http://dx. doi. org/10. 1186/1471-2164-14-545.
23. Martin TA, Jayanthi S, McCoy MT, Brannock C, Ladenheim B, Garrett T, Lehrmann E, Becker KG, Cadet JL. Methamphetamine causes differential alterations in gene expression and patterns of histone acetylation/hypoacetylation in the rat nucleus accumbens. PloS One 2012; 7: e34236; PMID: 22470541; http://dx. doi. org/10. 1371/journal. pone. 0034236.
24. Ma P, Schultz RM. Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 2008; 319: 110-20; PMID: 18501342; http://dx. doi. org/10. 1016/j. ydbio. 2008. 04. 011.
25. Li H, Li F, Wu N, Su R-B, Li J. Methamphetamine induces dynamic changes of histone deacetylases in different phases of behavioral sensitization. CNS Neurosci Ther 2014; 20: 874-6; PMID: 24954603; http://dx. doi. org/10. 1111/cns. 12301.
26. Kennedy PJ, Feng J, Robison AJ, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han M-H, et al. Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 2013; 16: 434-40; PMID: 23475113; http://dx. doi. org/10. 1038/nn. 3354.
27. Renthal W, Maze I, Krishnan V, Covington HE, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007; 56: 517-29; PMID: 17988634; http://dx. doi. org/10. 1016/j. neuron. 2007. 09. 032.
28. Cadet JL, Brannock C, Jayanthi S, Krasnova IN. Transcriptional and Epigenetic Substrates of Methamphetamine Addiction and Withdrawal: Evidence from a Long-Access Self-Administration Model in the Rat. Mol Neurobiol 2014; http://dx. doi. org/10. 1007/s12035-014-9040-y.
29. Toska E, Campbell HA, Shandilya J, Goodfellow SJ, Shore P, Medler KF, Roberts SGE. Repression of transcription by WT1-BASP1 requires the myristoylation of BASP1 and the PIP2-dependent recruitment of histone deacetylase. Cell Rep 2012; 2: 462-9; PMID: 22939983; http://dx. doi. org/10. 1016/j. celrep. 2012. 08. 005.
30. Zhang JS, Moncrieffe MC, Kaczynski J, Ellenrieder V, Prendergast FG, Urrutia R. A conserved alpha-helical motif mediates the interaction of Sp1-like transcriptional repressors with the corepressor mSin3A. Mol Cell Biol 2001; 21: 5041-9; PMID: 11438660; http://dx. doi. org/10. 1128/MCB. 21. 15. 5041-5049. 2001.
31. Hess J, Angel P, Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 2004; 117: 5965-73; PMID: 15564374; http://dx. doi. org/10. 1242/jcs. 01589.
32. Pitchers KK, Vialou V, Nestler EJ, Laviolette SR, Lehman MN, Coolen LM. Natural and Drug Rewards Act on Common Neural Plasticity Mechanisms with DFosB as a Key Mediator. J Neurosci 2013; 33: 3434-42; PMID: 23426671; http://dx. doi. org/10. 1523/JNEUROSCI. 4881-12. 2013.
33. Nestler EJ, Barrot M, Self DW. DFosB: A sustained molecular switch for addiction. Proc Natl Acad Sci 2001; 98: 11042-6; PMID: 11572966; http://dx. doi. org/10. 1073/pnas. 191352698.
34. McCoy MT, Jayanthi S, Wulu JA, Beauvais G, Ladenheim B, Martin TA, Krasnova IN, Hodges AB, Cadet JL. Chronic methamphetamine exposure suppresses the striatal expression of members of multiple families of immediate early genes (IEGs) in the rat: normalization by an acute methamphetamine injection. Psychopharmacology (Berl) 2011; 215: 353-65; PMID: 21229349; http://dx. doi. org/10. 1007/s00213-010-2146-7.
35. Cornish JL, Hunt GE, Robins L, McGregor IS. Regional c-Fos and FosB/DFosB expression associated with chronic methamphetamine self-administration and methamphetamine-seeking behavior in rats. Neuroscience 2012; 206: 100-14; PMID: 22266344; http://dx. doi. org/10. 1016/j. neuroscience. 2012. 01. 004.
36. Renthal W, Carle TL, Maze I, Covington HE, Truong H-T, Alibhai I, Kumar A, Montgomery RL, Olson EN, Nestler EJ. Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J Neurosci Off J Soc Neurosci 2008; 28: 7344-9; http://dx. doi. org/10. 1523/JNEUROSCI. 1043-08. 2008.
37. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293: 1074-80; PMID: 11498575; http://dx. doi. org/10. 1126/science. 1063127.
38. Ikegami D, Narita M, Imai S, Miyashita K, Tamura R, Narita M, Takagi S, Yokomizo A, Takeshima H, Ando T, et al. Epigenetic modulation at the CCR2 gene correlates with the maintenance of behavioral sensitization to methamphetamine. Addict Biol 2010; 15: 358-61; PMID: 20624155; http://dx. doi. org/10. 1111/j. 1369-1600. 2010. 00219. x.
39. Aguilar-Valles A, Vaissiére T, Griggs EM, Mikaelsson MA, Takács IF, Young EJ, Rumbaugh G, Miller CA. Methamphetamine-associated memory is regulated by a writer and an eraser of permissive histone methylation. Biol Psychiatry 2014; 76: 57-65; PMID: 24183790; http://dx. doi. org/10. 1016/j. biopsych. 2013. 09. 014.
40. Krasnova IN, Chiflikyan M, Justinova Z, McCoy MT, Ladenheim B, Jayanthi S, Quintero C, Brannock C, Barnes C, Adair JE, et al. CREB phosphorylation regulates striatal transcriptional responses in the self-administration model of methamphetamine addiction in the rat. Neurobiol Dis 2013; 58: 132-43; PMID: 23726845; http://dx. doi. org/10. 1016/j. nbd. 2013. 05. 009.
41. Kim J, Shin S, Subramaniam M, Bruinsma E, Kim TD, Hawse JR, Spelsberg TC, Janknecht R. Histone demethylase JARID1B/KDM5B is a corepressor of TIEG1/KLF10. Biochem Biophys Res Commun 2010; 401: 412-6; PMID: 20863814; http://dx. doi. org/10. 1016/j. bbrc. 2010. 09. 068.
42. Goto K, Numata M, Komura JI, Ono T, Bestor TH, Kondo H. Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differ Res Biol Divers 1994; 56: 39-44; http://dx. doi. org/10. 1046/j. 1432-0436. 1994. 56120039. x.
43. Numachi Y, Shen H, Yoshida S, Fujiyama K, Toda S, Matsuoka H, Sora I, Sato M. Methamphetamine alters expression of DNA methyltransferase 1 mRNA in rat brain. Neurosci Lett 2007; 414: 213-7; PMID: 17254711; http://dx. doi. org/10. 1016/j. neulet. 2006. 12. 052.
44. Mychasiuk R, Muhammad A, Ilnytskyy S, Kolb B. Persistent gene expression changes in NAc, mPFC, and OFC associated with previous nicotine or amphetamine exposure. Behav Brain Res 2013; 256: 655-61; PMID: 24021241; http://dx. doi. org/10. 1016/j. bbr. 2013. 09. 006.
45. Robinson TE, Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 2004; 47, Supplement 1: 33-46; PMID: 15464124; http://dx. doi. org/10. 1016/j. neuropharm. 2004. 06. 025.
46. Pol Bodetto S, Carouge D, Fonteneau M, Dietrich J-B, Zwiller J, Anglard P. Cocaine represses protein phosphatase-1Cb through DNA methylation and Methyl-CpG Binding Protein-2 recruitment in adult rat brain. Neuropharmacology 2013; 73: 31-40; PMID: 23688924; http://dx. doi. org/10. 1016/j. neuropharm. 2013. 05. 005.
47. Pol Bodetto S, Romieu P, Sartori M, Tesone-Coelho C, Majchrzak M, Barbelivien A, Zwiller J, Anglard P. Differential regulation of MeCP2 and PP1 in passive or voluntary administration of cocaine or food. Int J Neuropsychopharmacol Off Sci J Coll Int Neuropsychopharmacol CINP 2014; 17: 2031-44.
48. Deng JV, Rodriguiz RM, Hutchinson AN, Kim I-H, Wetsel WC, West AE. MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat Neurosci 2010; 13: 1128-36; PMID: 20711186; http://dx. doi. org/10. 1038/nn. 2614.
49. Deng JV, Wan Y, Wang X, Cohen S, Wetsel WC, Greenberg ME, Kenny PJ, Calakos N, West AE. MeCP2 Phosphorylation Limits Psychostimulant-Induced Behavioral and Neuronal Plasticity. J Neurosci 2014; 34: 4519-27; PMID: 24671997; http://dx. doi. org/10. 1523/JNEUROSCI. 2821-13. 2014.
50. Zhou Z, Hong EJ, Cohen S, Zhao W-N, Ho H-YH, Schmidt L, Chen WG, Lin Y, Savner E, Griffith EC, et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 2006; 52: 255-69; PMID: 17046689; http://dx. doi. org/10. 1016/j. neuron. 2006. 09. 037.
51. McFadden LM, Vieira-Brock PL, Hanson GR, Fleckenstein AE. Methamphetamine self-administration attenuates hippocampal serotonergic deficits: role of brain-derived neurotrophic factor. Int J Neuropsychopharmacol Off Sci J Coll Int Neuropsychopharmacol CINP 2014; 17: 1315-20.
52. Kim D-J, Roh S, Kim Y, Yoon S-J, Lee H-K, Han C-S, Kim Y-K. High concentrations of plasma brain-derived neurotrophic factor in methamphetamine users. Neurosci Lett 2005; 388: 112-5; PMID: 16039058; http://dx. doi. org/10. 1016/j. neulet. 2005. 06. 042.
53. Itzhak Y, Ergui I, Young JI. Long-term parental methamphetamine exposure of mice influences behavior and hippocampal DNA methylation of the offspring. Mol Psychiatry 2014; 20: 232-9; PMID: 24535458.
54. Cantone I, Fisher AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol 2013; 20: 282-9; PMID: 23463313; http://dx. doi. org/10. 1038/nsmb. 2489.
55. Jayanthi S, McCoy MT, Chen B, Britt JP, Kourrich S, Yau H-J, Ladenheim B, Krasnova IN, Bonci A, Cadet JL. Methamphetamine downregulates striatal glutamate receptors via diverse epigenetic mechanisms. Biol Psychiatry 2014; 76: 47-56; PMID: 24239129; http://dx. doi. org/10. 1016/j. biopsych. 2013. 09. 034.
56. Cadet JL, Jayanthi S. Epigenetics of methamphetamine-induced changes in glutamate function. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2013; 38: 248-9; http://dx. doi. org/10. 1038/npp. 2012. 169.
57. Wolf ME, Ferrario CR. AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev 2010; 35: 185-211; PMID: 20109488; http://dx. doi. org/10. 1016/j. neubiorev. 2010. 01. 013.