Neuroplasticity, axonal guidance and micro-RNA genes are associated with morphine self-administration behavior

Addiction Biology

Volumn 18, Issue 3, 2013, Pages 480-495

  Tapocik, Jenica D ^a,b   Luu, Truong V ^c   Mayo, Cheryl L ^a   Wang, Bi Dar ^c   Doyle, Erin ^c   Lee, Alec D ^c   Lee, Norman H ^c   Elmer, Greg I ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Addiction; H19; micro RNA; neuroadaptation; opioid; reward; vulnerability

Indexed keywords

MICRORNA; MICRORNA 154; MICRORNA 675; MORPHINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENOTYPE; MALE; MICROARRAY ANALYSIS; MORPHINE ADDICTION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OPIATE ADDICTION; PATHOGENESIS; POST HOC ANALYSIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REWARD; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; AXONS; INFUSIONS, INTRAVENOUS; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MICRORNAS; MORPHINE; MORPHINE DEPENDENCE; NARCOTICS; NEURONAL PLASTICITY; REINFORCEMENT (PSYCHOLOGY); REWARD; SELF ADMINISTRATION;

EID: 84876110303     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2012.00470.x     Document Type: Article

References (76)

1. Allen PB, Ouimet CC, Greengard P, (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci U S A 94: 9956-9961.
2. Allen PB, Zachariou V, Svenningsson P, Lepore AC, Centonze D, Costa C, Rossi S, Bender G, Chen G, Feng J, Snyder GL, Bernardi G, Nestler EJ, Yan Z, Calabresi P, Greengard P, (2006) Distinct roles for spinophilin and neurabin in dopamine-mediated plasticity. Neuroscience 140: 897-911.
3. Ambrosio E, Goldberg SR, Elmer GI, (1995) Behavior genetic investigation of the relationship between spontaneous locomotor activity and the acquisition of morphine self-administration behavior. Behav Pharmacol 6: 229-237.
4. Ammon S, Mayer P, Riechert U, Tischmeyer H, Hollt V, (2003) Microarray analysis of genes expressed in the frontal cortex of rats chronically treated with morphine and after naloxone precipitated withdrawal. Brain Res Mol Brain Res 112: 113-125.
5. Arguello AA, Harburg GC, Schonborn JR, Mandyam CD, Yamaguchi M, Eisch AJ, (2008) Time course of morphine's effects on adult hippocampal subgranular zone reveals preferential inhibition of cells in S phase of the cell cycle and a subpopulation of immature neurons. Neuroscience 157: 70-79.
6. Ayesh S, Matouk I, Schneider T, Ohana P, Laster M, Al-Sharef W, De-Groot N, Hochberg A, (2002) Possible physiological role of H19 RNA. Mol Carcinog 35: 63-74.
7. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I, (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.
8. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300.
9. Cai X, Cullen BR, (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13: 313-316.
10. Charlton JJ, Allen PB, Psifogeorgou K, Chakravarty S, Gomes I, Neve RL, Devi LA, Greengard P, Nestler EJ, Zachariou V, (2008) Multiple actions of spinophilin regulate mu opioid receptor function. Neuron 5: 238-247.
11. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K, (2007) MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 67: 8994-9000.
12. Cox PR, Fowler V, Xu B, Sweatt JD, Paylor R, Zoghbi HY, (2003) Mice lacking tropomodulin-2 show enhanced long-term potentiation, hyperactivity, and deficits in learning and memory. Mol Cell Neurosci 23: 1-12.
13. Crain SM, Shen K, (2000) Enhanced analgesic potency and reduced tolerance of morphine in 129/SvEv mice: evidence for a deficiency in GM1 ganglioside-regulated excitatory opioid receptor functions. Brain Res 856: 227-235.
14. Dumont EC, Rycroft BK, Maiz J, Williams JT, (2008) Morphine produces circuit-specific neuroplasticity in the bed nucleus of the stria terminalis. Neuroscience 153: 232-239.
15. Elmer GI, Evans JL, Goldberg SR, Epstein CJ, Cadet JL, (1996) Transgenic superoxide dismutase mice: increased mesolimbic micro-opioid receptors results in greater opioid-induced stimulation and opioid-reinforced behavior. Behav Pharmacol 7: 628-639.
16. Elmer GI, Pieper JO, Goldberg SR, George FR, (1995) Opioid operant self-administration, analgesia, stimulation and respiratory depression in mu-deficient mice. Psychopharmacology (Berl) 117: 23-31.
17. Elmer GI, Pieper JO, Hamilton LR, Wise RA, (2010) Qualitative differences between C57BL/6J and DBA/2J mice in morphine potentiation of brain stimulation reward and intravenous self-administration. Psychopharmacology (Berl) 208: 309-321.
18. Elmer GI, Pieper JO, Levy J, Rubinstein M, Low MJ, Grandy DK, Wise RA, (2005) Brain stimulation and morphine reward deficits in dopamine D2 receptor-deficient mice. Psychopharmacology (Berl) 182: 33-44.
19. Freed WJ, Chen J, Backman CM, Schwartz CM, Vazin T, Cai J, Spivak CE, Lupica CR, Rao MS, Zeng X, (2008) Gene expression profile of neuronal progenitor cells derived from hESCs: activation of chromosome 11p15.5 and comparison to human dopaminergic neurons. PLoS One 3: e1422.
20. Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM, (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26: 184-192.
21. Grice DE, Reelina I, Mannisto PT, Brooks AI, Smith GG, Golden GT, Buxbaum JD, Berrettini WD, (2007) Transcriptional profiling of C57 and DBA strains of mice in the absence and presence of morphine. BMC Genomics 8: 76.
22. Jacobs EH, de Vries TJ, Smit AB, Schoffelmeer AN, (2004) Gene transcripts selectively down-regulated in the shell of the nucleus accumbens long after heroin self-administration are up-regulated in the core independent of response contingency. FASEB J 18: 200-202.
23. Jacobs EH, Spijker S, Verhoog CW, Kamprath K, de, Vries TJ, Smit AB, Schoffelmeer AN, (2002) Active heroin administration induces specific genomic responses in the nucleus accumbens shell. FASEB J 16: 1961-1963.
24. Kalivas PW, O'Brien C, (2008) Drug addiction as a pathology of staged neuroplasticity. Neuropsychopharmacology 33: 166-180.
25. Kauer JA, Malenka RC, (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8: 844-858.
26. Kendler KS, Karkowski LM, Corey LA, Prescott CA, Neale MC, (1999) Genetic and environmental risk factors in the aetiology of illicit drug initiation and subsequent misuse in women. Br J Psychiatry 175: 351-356.
27. Kendler KS, Karkowski LM, Neale MC, Prescott CA, (2000) Illicit psychoactive substance use, heavy use, abuse, and dependence in a US population-based sample of male twins. Arch Gen Psychiatry 57: 261-269.
28. Kest B, Hopkins E, Palmese CA, Adler M, Mogil JS, (2002) Genetic variation in morphine analgesic tolerance: a survey of 11 inbred mouse strains. Pharmacol Biochem Behav 73: 821-828.
29. Kiyatkin EA, Wise RA, (2002) Brain and body hyperthermia associated with heroin self-administration in rats. J Neurosci 22: 1072-1080.
30. Kolesnikov Y, Jain S, Wilson R, Pasternak GW, (1998) Lack of morphine and enkephalin tolerance in 129/SvEv mice: evidence for a NMDA receptor defect. J Pharmacol Exp Ther 284: 455-459.
31. Korostynski M, Piechota M, Kaminski D, Solecki W, Przewlocki R, (2007) Morphine effects on striatal transcriptome in mice. Genome Biol 8: R128.
32. Kosik KS, (2006) The neuronal microRNA system. Nat Rev Neurosci 7: 911-920.
33. Kuntz KL, Patel KM, Grigson PS, Freeman WM, Vrana KE, (2008) Heroin self-administration: II. CNS gene expression following withdrawal and cue-induced drug-seeking behavior. Pharmacol Biochem Behav 90: 349-356.
34. LaLumiere RT, Kalivas PW, (2008) Glutamate release in the nucleus accumbens core is necessary for heroin seeking. J Neurosci 28: 3170-3177.
35. Lee NH, Saeed AI, (2007) Microarrays: an overview. Methods Mol Biol 353: 265-300.
36. Letwin NE, Kafkafi N, Benjamini Y, Mayo C, Frank BC, Luu T, Lee NH, Elmer GI, (2006) Combined application of behavior genetics and microarray analysis to identify regional expression themes and gene-behavior associations. J Neurosci 26: 5277-5287.
37. Liang M, Lee NH, Wang H, Greene AS, Kwitek AE, Kaldunski ML, Luu TV, Frank BC, Bugenhagen S, Jacob HJ, Cowley AW Jr, (2008) Molecular networks in Dahl salt-sensitive hypertension based on transcriptome analysis of a panel of consomic rats. Physiol Genomics 34: 54-64.
38. Liao D, Grigoriants OO, Wang W, Wiens K, Loh HH, Law PY, (2007) Distinct effects of individual opioids on the morphology of spines depend upon the internalization of mu opioid receptors. Mol Cell Neurosci 35: 456-469.
39. Liao D, Lin H, Law PY, Loh HH, (2005) Mu-opioid receptors modulate the stability of dendritic spines. Proc Natl Acad Sci U S A 102: 1725-1730.
40. Loguinov AV, Anderson LM, Crosby GJ, Yukhananov RY, (2001) Gene expression following acute morphine administration. Physiol Genomics 6: 169-181.
41. Lonart G, (2002) RIM1: an edge for presynaptic plasticity. Trends Neurosci 25: 329-332.
42. 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.
43. McClung CA, Nestler EJ, (2008) Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33: 3-17.
44. Merikangas KR, Stolar M, Stevens DE, Goulet J, Preisig MA, Fenton B, Zhang H, O'Malley SS, Rounsaville BJ, (1998) Familial transmission of substance use disorders. Arch Gen Psychiatry 55: 973-979.
45. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, (2011) A MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859.
46. Nestler EJ, (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2: 119-128.
47. Nestler EJ, Barrot M, Self DW, (2001) DeltaFosB: a sustained molecular switch for addiction. Proc Natl Acad Sci U S A 98: 11042-11046.
48. Papagiannakopoulos T, Kosik KS, (2008) MicroRNAs: regulators of oncogenesis and stemness. BMC Med 6: 15.
49. Pavlidis P, Noble WS, (2001) Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol 2: research0042.
50. Penzes P, Jones KA, (2008) Dendritic spine dynamics-a key role for kalirin-7. Trends Neurosci 31: 419-427.
51. Poschel B, Wroblewska B, Heinemann U, Manahan-Vaughan D, (2005) The metabotropic glutamate receptor mGluR3 is critically required for hippocampal long-term depression and modulates long-term potentiation in the dentate gyrus of freely moving rats. Cereb Cortex 15: 1414-1423.
52. Reiner-Benaim A, Yekutieli D, Letwin NE, Elmer GI, Lee NH, Kafkafi N, Benjamini Y, (2007) Associating quantitative behavioral traits with gene expression in the brain: searching for diamonds in the hay. Bioinformatics 23: 2239-2246.
53. Robinson TE, Gorny G, Savage VR, Kolb B, (2002) Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46: 271-279.
54. Robinson TE, Kolb B, (1999) Morphine alters the structure of neurons in the nucleus accumbens and neocortex of rats. Synapse 33: 160-162.
55. Rodriguez-Parkitna JM, Bilecki W, Mierzejewski P, Stefanski R, Ligeza A, Bargiela R, Ziolkowska B, Kostowski W, Przewlocki R, (2004) Effects of morphine on gene expression in the rat amygdala. J Neurochem 91: 38-48.
56. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC, (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375: 488-493.
57. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Sudhof TC, (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415: 321-326.
58. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME, (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439: 283-289.
59. Scott RE, Gao S, Kim CK, Cox R, (2005) De-differentiation-derived mesenchymal stem cells demonstrate selective repression in H19 bioregulatory RNA gene expression. Differentiation 73: 294-302.
60. Seitz H, Youngson N, Lin SP, Dalbert S, Paulsen M, Bachellerie JP, Ferguson-Smith AC, Cavaille J, (2003) Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat Genet 34: 261-262.
61. Sklair-Tavron L, Shi WX, Lane SB, Harris HW, Bunney BS, Nestler EJ, (1996) Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons. Proc Natl Acad Sci U S A 93: 11202-11207.
62. Slack JM, Tosh D, (2001) Transdifferentiation and metaplasia-switching cell types. Curr Opin Genet Dev 11: 581-586.
63. Tapocik JD, Letwin N, Mayo CL, Frank B, Luu T, Achinike O, House C, Williams R, Elmer GI, Lee NH, (2009) Identification of candidate genes and gene networks specifically associated with analgesic tolerance to morphine. J Neurosci 29: 5295-5307.
64. Tsuang MT, Bar JL, Harley RM, Lyons MJ, (2001) The Harvard Twin Study of Substance Abuse: what we have learned. Harv Rev Psychiatry 9: 267-279.
65. Tsuang MT, Lyons MJ, Harley RM, Xian H, Eisen S, Goldberg J, True WR, Faraone SV, (1999) Genetic and environmental influences on transitions in drug use. Behav Genet 29: 473-479.
66. van den Bree MB, Johnson EO, Neale MC, Pickens RW, (1998) Genetic and environmental influences on drug use and abuse/dependence in male and female twins. Drug Alcohol Depend 52: 231-241.
67. Vendruscolo LF, Schlosburg JE, Misra KK, Chen SA, Greenwell TN, Koob GF, (2011) Escalation patterns of varying periods of heroin access. Pharmacol Biochem Behav 98: 570-574.
68. Wayman GA, Davare M, Ando H, Fortin D, Varlamova O, Cheng HY, Marks D, Obrietan K, Soderling TR, Goodman RH, Impey S, (2008) An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci U S A 105: 9093-9098.
69. Weber RJ, Gomez-Flores R, Smith JE, Martin TJ, (2009) Neuronal adaptations, neuroendocrine and immune correlates of heroin self-administration. Brain Behav Immun 23: 993-1002.
70. Weise-Kelly L, Siegel S, (2001) Self-administration cues as signals: drug self-administration and tolerance. J Exp Psychol Anim Behav Process 27: 125-136.
71. Williams JT, Christie MJ, Manzoni O, (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81: 299-343.
72. Wu Q, Law PY, Wei LN, Loh HH, (2008) Post-transcriptional regulation of mouse mu opioid receptor (MOR1) via its 3' untranslated region: a role for microRNA23b. FASEB J 22: 4085-4095.
73. Wu Q, Zhang L, Law PY, Wei LN, Loh HH, (2009) Long-term morphine treatment decreases the association of mu-opioid receptor (MOR1) mRNA with polysomes through miRNA23b. Mol Pharmacol 75: 744-750.
74. Yang IV, Chen E, Hasseman JP, Liang W, Frank BC, Wang S, Sharov V, Saeed AI, White J, Li J, Lee NH, Yeatman TJ, Quackenbush J, (2002) Within the fold: assessing differential expression measures and reproducibility in microarray assays. Genome Biol 3: research0062.
75. Yeung KY, Haynor DR, Ruzzo WL, (2001) Validating clustering for gene expression data. Bioinformatics 17: 309-318.
76. Zhang B, Pan X, Cobb GP, Anderson TA, (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302: 1-12.