Long-term parental methamphetamine exposure of mice influences behavior and hippocampal DNA methylation of the offspring

Molecular Psychiatry

Volumn 20, Issue 2, 2015, Pages 252-262

  Itzhak, Y ^a   Ergui, I ^a   Young, J I ^a  

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

Author keywords

behavior; cross fostering; epigenetics; methamphetamine; prenatal exposure

Indexed keywords

COCAINE; METHAMPHETAMINE; CENTRAL STIMULANT AGENT; DOPAMINE; DOPAMINE UPTAKE INHIBITOR;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HYPERACTIVITY; LOCOMOTION; LONG TERM EXPOSURE; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MOTOR DYSFUNCTION; MOUSE; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PLACE PREFERENCE; PREGNANCY OUTCOME; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; SEX DIFFERENCE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED; CORPUS STRIATUM; DRUG EFFECTS; FEAR; INSTRUMENTAL CONDITIONING; METABOLISM; MOTOR ACTIVITY; NONPARAMETRIC TEST; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; PSYCHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; CONDITIONING, OPERANT; CORPUS STRIATUM; DNA METHYLATION; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; FEAR; FEMALE; HIPPOCAMPUS; MALE; MATERNAL BEHAVIOR; METHAMPHETAMINE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STATISTICS, NONPARAMETRIC;

EID: 84938550785     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2014.7     Document Type: Article

References (93)

1. Kuczenski R. Effects of phospholipases on the kinetic properties of rat striatal membrane-bound tyrosine hydroxylase. J Neurochem 1983; 40: 821-829.
2. Sulzer D, Chen TK, Lau YY, Kristensen H, Rayport S, Ewing A. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 1995; 15: 4102-4108.
3. Darke S, Kaye S, McKetin R, Duflou J. Major physical and psychological harms of methamphetamine use. Drug Alcohol Rev 2008; 27: 253-262.
4. Homer BD, Solomon TM, Moeller RW, Mascia A, DeRaleau L, Halkitis PN. Methamphetamine abuse and impairment of social functioning: a review of the underlying neurophysiological causes and behavioral implications. Psychol Bull 2008; 134: 301-310.
5. Pennay AE, Lee NK. Putting the call out for more research: the poor evidence base for treating methamphetamine withdrawal. Drug Alcohol Rev 2011; 30: 216-222.
6. Marshall BD, Werb D. Health outcomes associated with methamphetamine use among young people: a systematic review. Addiction 2010; 105: 991-1002.
7. Ellison G. Stimulant-induced psychosis, the dopamine theory of schizophrenia, and the habenula. Brain Res Brain Res Rev 1994; 19: 223-239.
8. Grant KM, LeVan TD, Wells SM, Li M, Stoltenberg SF, Gendelman HE et al. Methamphetamine-associated psychosis. J Neuroimmune Pharmacol 2012; 7: 113-139.
9. Grelotti DJ, Kanayama G, Pope HG Jr. Remission of persistent methamphetamineinduced psychosis after electroconvulsive therapy: presentation of a case and review of the literature. Am J Psychiatry 2010; 167: 17-23.
10. Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D et al. Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 2001; 158: 377-382.
11. Substance Abuse and Mental Health Services Administration (SAMHSA), Office of Applied Studies. Results from the 2007 National Survey on Drug Use and Health: National Findings (NSDUH Series H-34, DHHS Publication No. SMA 08-4343). Rockville, MD, USA, 2008.
12. American College of Obstetricians and Gynecologists Committee on Health Care for Underserved Women. Committee Opinion No. 479: Methamphetamine abuse in women of reproductive age. Obstet Gynecol 2011; 117: 751-755.
13. Lester BM, LaGasse LL. Children of addicted women. J Addict Dis 2010; 29: 259-276.
14. Chomchai C, Na Manorom N, Watanarungsan P, Yossuck P, Chomchai S. Methamphetamine abuse during pregnancy and its health impact on neonates born at Siriraj Hospital, Bangkok, Thailand. Southeast Asian J Trop Med Public Health 2004; 35: 228-231.
15. Dixon SD, Bejar R. Echoencephalographic findings in neonates associated with maternal cocaine and methamphetamine use: incidence and clinical correlates. J Pediatr 1989; 115: 770-778.
16. Little BB, Snell LM, Gilstrap LC3rd. Methamphetamine abuse during pregnancy: outcome and fetal effects. Obstet Gynecol 1988; 72: 541-544.
17. Smith LM, LaGasse LL, Derauf C, Grant P, Shah R, Arria A et al. Prenatal methamphetamine use and neonatal neurobehavioral outcome. Neurotoxicol Teratol 2008; 30: 20-28.
18. Eriksson M, Jonsson B, Steneroth G, Zetterström R. Cross-sectional growth of children whose mothers abused amphetamines during pregnancy. Acta Paediatr 1994; 83: 612-617.
19. Chang L, Alicata D, Ernst T, Volkow N. Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 2007; 102: 16-32.
20. Chang L, Smith LM, LoPresti C, Yonekura ML, Kuo J, Walot I et al. Smaller subcortical volumes and cognitive deficits in children with prenatal methamphetamine exposure. Psychiatry Res 2004; 132: 95-106.
21. Cloak CC, Ernst T, Fujii L, Hedemark B, Chang L. Lower diffusion in white matter of children with prenatal methamphetamine exposure. Neurology 2009; 72: 2068-2075.
22. Smith L, Yonekura ML, Wallace T, Berman N, Kuo J, Berkowitz C. Effects of prenatal methamphetamine exposure on fetal growth and drug withdrawal symptoms in infants born at term. J Dev Behav Pediatr 2003; 24: 17-23.
23. Struthers JM, Hansen RL. Visual recognition memory in drug-exposed infants. J Dev Behav Pediatr 1992; 13: 108-111.
24. Chang L, Cloak C, Jiang CS, Farnham S, Tokeshi B, Buchthal S et al. Altered neurometabolites and motor integration in children exposed to methamphetamine in utero. Neuroimage 2009; 48: 391-397.
25. Derauf C, LaGasse LL, Smith LM, Grant P, Shah R, Arria A et al. Demographic and psychosocial characteristics of mothers using meth-amphetamine during pregnancy: preliminary results of the infant development, environment, and lifestyle study (IDEAL). Am J Drug Alcohol Abuse 2007; 33: 281-289.
26. Shah R, Diaz SD, Arria A, LaGasse LL, Derauf C, Newman E et al. Prenatal methamphetamine exposure and short-term maternal and infant medical outcomes. Am J Perinatol 2012; 29: 391-400.
27. Good MM, Solt I, Acuna JG, Rotmensch S, Kim MJ.. Methamphetamine use during pregnancy: maternal and neonatal implications. Obstet Gynecol 2010; 116: 330-334.
28. Bubenikova-Valesova V, Kacer P, Syslova K, Rambousek L, Janovsky M, Schutova B et al. Prenatal methamphetamine exposure affects the mesolimbic dopaminergic system and behavior in adult offspring. Int J Dev Neurosci 2009; 27: 525-530.
29. Šlamberová R, Yamamotová A, Schutová B, Hrubá L, Pometlová M. Impact of prenatal methampheta-mine exposure on the sensitivity to the same drug in adult male rats. Prague Med Rep 2011; 112: 102-114.
30. Jeng W, Wong AW, Ting-A-Kee R, Wells PG. Methamphetamine-enhanced embryonic oxidative DNA damage and neurodevelopmental deficits. Free Radic Biol Med 2005; 39: 317-326.
31. Quinn R. Comparing rat's to human's age: How old is my rat in people years? Nutrition 2005; 21: 775-777.
32. Gentry WB, Ghafoor AU, Wessinger WD, Laurenzana EM, Hendrickson HP, Owens SM. (+)-Methamphetamine-induced spontaneous behavior in rats depends on route of (+)METH administration. Pharmacol Biochem Behav 2004; 79: 751-760.
33. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001; 24: 1161-1192.
34. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854.
35. Hickman DL, Swan MP.. Effects of age of pups and removal of existing litter on pup survival during cross-fostering between multiparous outbred mice. J Am Assoc Lab Anim Sci 2011; 50: 641-646.
36. Itzhak Y, Gandia C, Huang PL, Ali SF.. Resistance of neuronal nitric oxide synthasedeficient mice to methamphetamine-induced dopaminergic neurotoxicity. J Pharmacol Exp Ther 1998; 284: 1040-1047.
37. Itzhak Y, Martin JL. Cocaine-induced conditioned place preference in mice: Induction, extinction and reinstatement by related psychostimulants. Neuropsychopharmacology 2002; 26: 130-134.
38. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC. Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 2013; 16: 42-47.
39. Itzhak Y, Liddie S, Anderson KL. Sodium butyrate-induced histone acetylation strengthens the expression of cocaine-associated contextual memory. Neurobiol Learn Mem 2013; 102: 34-42.
40. Kelley JB, Balda MA, Anderson KL, Itzhak Y. Impairments in fear conditioning in mice lacking the nNOS gene. Learn Mem 2009; 16: 371-378.
41. Bourin M, Hascoët M. The mouse light/dark box test. Eur J Pharmacol 2003; 463: 55-65.
42. Crawley J, Goodwin FK. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 1980; 13: 167-170.
43. Onaivi ES, Martin BR. Neuropharmacological and physiological validation of a computer-controlled two-compartment black and white box for the assessment of anxiety. Prog Neuropsychopharmacol Biol Psychiatry 1989; 13: 963-976.
44. Tusnády GE, Simon I, Váradi A, Arányi T. BiSearch: primer-design and search tool for PCR on bisulfite-treated genomes. Nucleic Acids Res 2005; 33: e9.
45. Frantz KJ, O'Dell LE, Parsons LH. Behavioral and Neurochemical Responses to Cocaine in Periadolescent and Adult Rats. Neuropsychopharmacology 2007; 32: 625-637.
46. Cho AK, Melega WP, Kuczenski R, Segal DS. Relevance of pharmacokinetic parameters in animal models of methamphetamine abuse. Synapse 2011; 39: 161-166.
47. Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 2013; 14: 128-134.
48. Voigt P, Tee WW, Reinberg D. A double take on bivalent promoters. Genes Dev 2013; 27: 1318-1338.
49. United National Office on Drugs and Crime. World Drug Report, Analysis Vol. 1. United Nations Publication: Vienna, Austria, 2004.
50. Substance Abuse and Mental Health Services Administration. Treatment Episode Data Set (TEDS). 1999-2009. National Admissions to Substance Abuse Treatment Services, DASIS Series, S-56, HHS Publication No. (SMA) 11-4646, 2011.
51. LaGasse LL, Derauf C, Smith LM, Newman E, Shah R, Neal C et al. Prenatal methamphetamine exposure and childhood behavior problems at 3 and 5 years of age. Pediatrics 2012; 229: 681-688.
52. LaGasse LL, Wouldes T, Newman E, Smith LM, Shah RZ, Derauf C et al. Prenatal methamphetamine exposure and neonatal neurobehavioral outcome in the USA and New Zealand. Neurotoxicol Teratol 2011; 33: 166-175.
53. Johnson BA, Roache JD, Ait-Daoud N, Wells LT, Wallace CL, Dawes MA et al. Effects of acute topiramate dosing on methamphetamine-induced subjective mood. Int J Neuropsychopharmacol 2007; 10: 85-98.
54. Ghahremani DG, Tabibnia G, Monterosso J, Hellemann G, Poldrack RA, London ED. Effect of modafinil on learning and task-related brain activity in methamphetamine-dependent and healthy individuals. Neuropsychopharmacology 2011; 36: 950-959.
55. Alicata D, Chang L, Cloak C, Abe K, Ernst T. Higher diffusion in striatum and lower fractional anisotrophy in white matter of methamphetamine users. Psychiatry Res 2009; 174: 1-8.
56. Achat-Mendes C, Ali SF, Itzhak Y. Differential effects of amphetamines-induced neurotoxicity on appetitive and aversive Pavlovian conditioning in mice. Neuropsychopharmacology 2005; 30: 1128-1137.
57. Stephans S, Yamamoto B. Methamphetamines pretreatment and the vulnerability of the striatum to methamphetamine neurotoxicity. Neuroscience 1996; 72: 593-600.
58. Van der Veen R, Abrous DN, De Kloet ER, Piazza PV, Koehl M. Impact of intra- and interstrain cross-fostering on mouse maternal care. Genes Brain Behav 2008; 7: 184-192.
59. Curley JP, Rock V, Moynihan AM, Bateson P, Keverne EB, Champagne FA. Developmental shifts in the behavioral phenotypes of inbred mice: the role of postnatal and juvenile social experiences. Behav Genet 2010; 40: 220-232.
60. LaPlant Q, Vialou V, Covington HE3rd, Dumitriu D, Feng J, Warren BL et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010; 13: 1137-1143.
61. Torregrossa MM, Taylor JR. Learning to forget: manipulating extinction and reconsolidation processes to treat addiction. Psychopharmacology 2013; 226: 659-672.
62. Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 2010; 65: 7-19.
63. Swatt JD. Hippocampal function in cognition. Psychopharmacology 2004; 174: 99-110.
64. Meyers RA, Zavala AR, Neisewander JL. Dorsal, but not ventral, hippocampal lesions disrupt cocaine place conditioning. Neuroreport 2003; 14: 2127-2131.
65. Meyers RA, Zavala AR, Speer CM, Neisewander JL. Dorsal hippocampus inhibition disrupts acquisition and expression, but not consolidation, of cocaine conditioned place preference. Behav Neurosci 2006; 120: 401-412.
66. Shohamy D, Adcock RA. Dopamine and adaptive memory. Trends Cogn Sci 2010; 14: 464-472.
67. Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 2012; 76: 790-803.
68. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci USA 2009; 106: 11794-1179.
69. Yin H, Bardgett ME, Csernansky JG. Kainic acid lesions disrupt fear-mediated memory processing. Neurobiol Learn Mem 2002; 77: 389-401.
70. Bardgett ME, Boeckman R, Krochmal D, Fernando H, Ahrens R, Csernansky JG. NMDA receptor blockade and hippocampal neuronal loss impair fear conditioning and position habit reversal in C57Bl/6 mice. Brain Res Bull 2003; 60: 131-142.
71. Martin MV, Dong H, Bertchume A, Csernansky JG. Low dose quetiapine reverses deficits in contextual and cued fear conditioning in rats with excitotoxin-induced hippocampal neuropathy. Pharmacol Biochem Behav 2005; 82: 263-269.
72. Hunsaker MR, Kesner RP. Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol Learn Mem 2008; 89: 61-69.
73. Day JJ, Sweatt JD. DNA methylation and memory formation. Nat Neurosci 2010; 13: 1319-1323.
74. Suderman M, McGowan PO, Sasaki A, Huang TC, Hallett MT, Meaney MJ et al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc Natl Acad Sci USA 2012; 109: 17266-17272.
75. Novikova SI, He F, Bai J, Cutrufello NJ, Lidow MS, Undieh AS. Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS ONE 2008; 3: e1919.
76. Justinova Z, Ferre S, Segal PN, Antoniou K, Solinas M, Pappas LA et al. Involvement of adenosine A1 and A2A receptors in the adenosinergic modulation of the discriminative-stimulus effects of cocaine and methamphetamine in rats. J Pharmacol Exp Ther 2003; 307: 977-986.
77. Chen Q, Zhu X, Zhang Y, Wetsel WC, Lee TH, Zhang X. Integrin-linked kinase is involved in cocaine sensitization by regulating PSD-95 and synapsin I expression and GluR1 Ser845 phosphorylation. J Mol Neurosci 2010; 40: 284-294.
78. Reissner KJ, Uys JD, Schwacke JH, Comte-Walters S, Rutherford-Bethard JL, Dunn TE et al. AKAP signaling in reinstated cocaine seeking revealed by iTRAQ proteomic analysis. J Neurosci 2011; 31: 5648-5658.
79. Krasnova IN, Chiflikyan M, Justinova Z, McCoy MT, Ladenheim B, Jayanthi S et al. CREB phosphorylation regulates striatal transcriptional responses in the self-administration model of methamphetamine addiction in the rat. Neurobiol Dis 2013; 58: 132-1343.
80. Renthal W, Maze I, Krishnan V, Covington HE3rd, Xiao G, Kumar A et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007; 56: 517-529.
81. Niikura K, Zhou Y, Ho A, Kreek MJ. Proopiomelanocortin (POMC) expression and conditioned place aversion during protracted withdrawal from chronic intermittent escalating-dose heroin in POMC-EGFP promoter transgenic mice. Neuroscience 2013; 236: 220-232.
82. Robison AJ, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M et al. Behavioral and structural responses to chronic cocaine require a feedforward loop involving ΔFosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 2013; 33: 4295-4307.
83. Miller JS, Tallarida RJ, Unterwald EM. Cocaine-induced hyperactivity and sensitization are dependent on GSK3. Neuropharmacology 2009; 56: 1116-1123.
84. Xu CM, Wang J, Wu P, Zhu WL, Li QQ, Xue YX et al. Glycogen synthase kinase 3beta in the nucleus accumbens core mediates cocaine-induced behavioral sensitization. J Neurochem 2009; 111: 1357-1368.
85. Mash DC, ffrench-Mullen J, Adi N, Qin Y, Buck A, Pablo J. Gene expression in human hippocampus from cocaine abusers identifies genes which regulate extracellular matrix remodeling. PLoS ONE 2007; 2: e1187.
86. Shonesy BC, Thiruchelvam K, Parameshwaran K, Rahman EA, Karuppagounder SS, Huggins KW et al. Central insulin resistance and synaptic dysfunction in intracerebroventricular-streptozotocin injected rodents. Neurobiol Aging 2012; 33: e5-18.
87. Moita MA, Lamprecht R, Nader K, LeDoux JE. A-kinase anchoring proteins in amygdala are involved in auditory fear memory. Nat Neurosci 2002; 5: 837-838.
88. Govorko D, Bekdash RA, Zhang C, Sarkar DK. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol Psychiatry 2012; 72: 378-388.
89. West NA, Kechris K, Dabelea D. Exposure to maternal diabetes in utero and DNA methylation patterns in the offspring. Immunometabolism 2013; 1: 1-9.
90. Dowling AL, Iannacone EA, Zoeller RT. Maternal hypothyroidism selectively affects the expression of neuroendocrine-specific protein A messenger ribonucleic acid in the proliferative zone of the fetal rat brain cortex. Endocrinology 2001; 142: 390-399.
91. Bohuslavova R, Skvorova L, Sedmera D, Semenza GL, Pavlinkova G. Increased susceptibility of HIF-1α heterozygous-null mice to cardiovascular malformations associated with maternal diabetes. J Mol Cell Cardiol 2013; 60: 129-141.
92. Grisel JE, Bartels JL, Allen SA, Turgeon VL. Influence of beta-Endorphin on anxious behavior in mice: interaction with EtOH. Psychopharmacology 2008; 200: 105-115.
93. Nguyen AT, Marquez P, Hamid A, Kieffer B, Friedman TC, Lutfy K. The rewarding action of acute cocaine is reduced in β-endorphin deficient but not in μ opioid receptor knockout mice. Eur J Pharmacol 2012; 686: 50-54.