Synaptic adaptations by alcohol and drugs of abuse: Changes in microRNA expression and mRNA regulation

Frontiers in Molecular Neuroscience

Volumn 7, Issue DEC, 2014, Pages

  Most, Dana ^a   Workman, Emily ^a   Adron Harris, R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cocaine; Ethanol; MiRNAs; MRNA targets; Stimulants; Synaptic translation; Synaptoneurosomes

Indexed keywords

ALCOHOL; ARGONAUTE 2 PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 1 RECEPTOR; FRAGILE X MENTAL RETARDATION PROTEIN; INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN; METHYL CPG BINDING PROTEIN 2; MICRORNA; MICRORNA 124; MICRORNA 125A; MICRORNA 181A; MICRORNA 206; MICRORNA 369; MICRORNA 382; MICRORNA 9; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RNA BINDING PROTEIN; RNA INDUCED SILENCING COMPLEX; S6 KINASE; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR DELTA FOSB; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ALCOHOL CONSUMPTION; AMYGDALOID NUCLEUS; ARTICLE; DOWN REGULATION; DRUG ABUSE; DRUG EXPOSURE; DRUG SEEKING BEHAVIOR; GENE EXPRESSION; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PLACE PREFERENCE; PREFRONTAL CORTEX; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RNA SEQUENCE; SYNAPTIC TRANSMISSION; TRANSLATION REGULATION; UPREGULATION; VENTRAL TEGMENTUM;

EID: 84918801417     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00085     Document Type: Article

References (109)

1. Aakalu, G., Smith, W. B., Nguyen, N., Jiang, C., and Schuman, E. M. (2001). Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron30, 489–502. doi: 10.1016/S0896-6273(01)00295-1
2. Ambros, V. (2001). microRNAs: tiny regulators with great potential. Cell 107, 823–826. doi: 10.1016/S0092-8674(01)00616-X
3. Banzhaf-Strathmann, J., Benito, E., May, S., Arzberger, T., Tahirovic, S., Kret-zschmar, H., et al. (2014). MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer’s disease. EMBO J. 33, 1667–1680. doi: 10.15252/embj.201387576
4. Barak, S., Liu, F., Ben Hamida, S., Yowell, Q. V., Neasta, J., Kharazia, V., et al. (2013). Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse. Nat. Neurosci.16, 1111–1117. doi: 10.1038/nn.3439
5. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell136, 215–233. doi: 10.1016/j.cell.2009.01.002
6. Bellone, C., and Luscher, C. (2006). Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat. Neurosci.9, 636–641. doi: 10.1038/nn1682
7. Berglind, W. J., Whitfield, T. W. Jr., LaLumiere, R. T., Kalivas, P. W., and McGinty, J. F. (2009). A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J. Neurosci.29, 3715–3719. doi: 10.1523/JNEUROSCI.5457-08.2009
8. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Fil-ipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell125, 1111–1124. doi: 10.1016/j.cell.2006.04.031
9. Blednov, Y. A., Benavidez, J. M., Geil, C., Perra, S., Morikawa, H., and Harris, R. A. (2011). Activation of inflammatory signaling by lipopolysaccharide produces a prolonged increase of voluntary alcohol intake in mice. Brain Behav. Immun.25(Suppl. 1), S92–S105. doi: 10.1016/j.bbi.2011.01.008
10. Cajigas, I. J., Tushev, G., Will, T. J., Tom Dieck, S., Fuerst, N., and Schu-man, E. M. (2012). The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron74, 453–466. doi: 10.1016/j.neuron.2012.02.036
11. Ceman, S., and Saugstad, J. (2011). MicroRNAs: meta-controllers of gene expression in synaptic activity emerge as genetic and diagnostic markers of human disease. Pharmacol. Ther.130, 26–37. doi: 10.1016/j.pharmthera.2011.01.004
12. Chandrasekar, V., and Dreyer, J. L. (2009). microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol. Cell. Neurosci. 42, 350–362. doi: 10.1016/j.mcn.2009.08.009
13. Chandrasekar, V., and Dreyer, J. L. (2011). Regulation of MiR-124, Let-7d, and MiR-181a in the accumbens affects the expression, extinction, and reinstatement of cocaine-induced conditioned place preference. Neuropsychopharmacology36, 1149–1164. doi: 10.1038/npp.2010.250
14. Cohen, J. E., Lee, P. R., Chen, S., Li, W., and Fields, R. D. (2011). MicroRNA regulation of homeostatic synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A.108, 11650–11655. doi: 10.1073/pnas.1017576108
15. Davies, A. G., Pierce-Shimomura, J. T., Kim, H., VanHoven, M. K., Thiele, T. R., Bonci, A., et al. (2003). A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell115, 655–666 doi: 10.1016/S0092-8674(03)00979-6
16. Di Chiara, G., and Imperato, A. (1988). Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. U.S.A.85, 5274-5278. doi: 10.1073/pnas.85.14.5274
17. Dopico, A. M., Anantharam, V., and Treistman, V. N. (1998). Ethanol increases the activity of Ca(++)-dependent K+ (mslo) channels: functional interaction with cytosolic Ca(++). J. Pharmacol. Exp. Ther.284, 258-268.
18. Duman, R. S., and Voleti, B. (2012). Signaling pathways underlying the pathophysiology and treatment of depression: novel mechanisms for rapid-acting agents. Trends Neurosci. 35,47-56. doi: 10.1016/j.tins.2011.11.004
19. Eipper-Mains, J. E., Kiraly, D. D., Palakodeti, D., Mains, R. E., Eipper, B. A., and Graveley, B. R. (2011). microRNA-Seq reveals cocaine-regulated expression of striatal microRNAs. RNA 17, 1529-1543. doi: 10.1261/rna.2775511
20. Eom, T., Antar, L. N., Singer, R. H., and Bassell, G. J. (2003). Localization of a beta-actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses. J. Neurosci.23, 10433-10444.
21. Farris, S.P., and Miles, M. F. (2012). Ethanol modulation of gene networks: implications for alcoholism. Neurobiol Dis. 45, 115-121. doi: 10.1016/j.nbd.2011.04.013
22. Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet.9,102-114. doi: 10.1038/nrg2290
23. Gibbings, D., Leblanc, P., Jay, F., Pontier, D., Michel, F., Schwab, Y., et al. (2012). Human prion protein binds Argonaute and promotes accumulation of microRNA effector complexes. Nat. Struct. Mol. Biol.19, 517-524. doi: 10.1038/nsmb.2273
24. Gibbings, D., Mostowy, S., andVoinnet, O. (2013). Autophagy selectively regulates miRNA homeostasis. Autophagy9, 781-783. doi: 10.4161/auto.23694
25. Goldie, B. J., and Cairns, M. J. (2012). Post-transcriptional trafficking and regulation of neuronal gene expression. Mol. Neurobiol.45, 99-108. doi: 10.1007/s12035-011-8222-0
26. Gong, R., Park, C. S., Abbassi, N. R., and Tang, S. J. (2006). Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J. Biol. Chem.281,18802-18815. doi: 10.1074/jbc.M512524200
27. Gorini, G., Harris, R. A., and Mayfield, R. D. (2014). Proteomic approaches and identification of novel therapeutic targets for alcoholism. Neuropsychopharmacology39, 104-130. doi: 10.1038/npp.2013.182
28. Gorini, G., Nunez, Y. O., and Mayfield, R. D. (2013). Integration of miRNA and protein profiling reveals coordinated neuroadaptations in the alcohol-dependent mouse brain. PLoS ONE8:e82565. doi: 10.1371/journal.pone.0082565
29. Graham, D. L., Edwards, S., Bachtell, R. K., DiLeone, R. J., Rios, M., and Self, D. W. (2007). Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat. Neurosci.10, 1029-1037. doi: 10.1038/nn1929
30. Grimm, J. W., Lu, L., Hayashi, T., Hope, B. T., Su, T. P., and Shaham, Y (2003). Time-dependent 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.
31. Heman-Ackah, S. M., Hallegger, M., Rao, M. S., and Wood, M. J. (2013). RISC in PD: the impact of microRNAs in Parkinson’s disease cellular and molecular pathogenesis. Front. Mol. Neurosci.6:40. doi: 10.3389/fnmol.2013.00040
32. Hengst, U., Cox, L. J., Macosko, E. Z., and Jaffrey, S. R. (2006). Functional and selective RNA interference in developing axons and growth cones. J. Neurosci.26, 5727-5732. doi: 10.1523/JNEUROSCI.5229-05.2006
33. Hensler, J. G., Ladenheim, E. E., and Lyons, W. E. (2003). Ethanol consumption and serotonin-1A (5-HT1A) receptor function in heterozygous BDNF (+/-) mice. J. Neurochem.85, 1139-1147. doi: 10.1046/j.1471-4159.2003.01748.x
34. Hollander, J. A., Im, H. I., Amelio, A. L., Kocerha, J., Bali, P., Lu, Q., et al. (2010). Striatal microRNA controls cocaine intake through CREB signalling. Nature466, 197-202. doi: 10.1038/nature09202
35. Hollingsworth, E. B., McNeal, E. T., Burton, J. L., Williams, R. J., Daly, J. W, and Creveling, C. R. (1985). Biochemical characterization of a filtered synap-toneurosome preparation from guinea pig cerebral cortex: cyclic adenosine 3:5'-monophosphate-generating systems, receptors, and enzymes. J. Neurosci.5, 2240-2253.
36. Holt, C. E., and Bullock, S. L. (2009). Subcellular mRNA localization in animal cells and why it matters. Science326, 1212–1216. doi: 10.1126/science.1176488
37. Im, H. I., Hollander, J. A., Bali, P., and Kenny, P. J. (2010). MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat. Neurosci.13, 1120–1127. doi: 10.1038/nn.2615
38. Iwasaki, S., Kobayashi, M., Yoda, M., Sakaguchi, Y., Katsuma, S., Suzuki, T., et al. (2010). Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell39, 292–299. doi: 10.1016/j.molcel.2010.05.015
39. Jambhekar, A., and Derisi, J. L. (2007). Cis-acting determinants of asymmetric, cytoplasmic RNA transport. RNA13, 625–642. doi: 10.1261/rna.262607
40. Jeanblanc, J., He, D. Y., Carnicella, S., Kharazia, V., Janak, P. H., and Ron, D. (2009). Endogenous BDNF in the dorsolateral striatum gates alcohol drinking. J. Neurosci.29, 13494–13502. doi: 10.1523/JNEUROSCI.2243-09.2009
41. Jimenez-Mateos, E. M., Engel, T., Merino-Serrais, P., McKiernan, R. C., Tanaka, K., and Mouri, G. (2012). Silencing microRNA-134 produces neuroprotec-tive and prolonged seizure-suppressive effects. Nat. Med.18, 1087–1094. doi: 10.1038/nm.2834
42. Jonkman, S., and Kenny, P. J. (2013). Molecular, cellular, and structural mechanisms of cocaine addiction: a key role for microRNAs. Neuropsychopharmacology38, 198–211. doi: 10.1038/npp.2012.120
43. Jung, H., Gkogkas, C. G., Sonenberg, N., and Holt, C. E. (2014). Remote control of gene function by local translation. Cell 157, 26–40. doi: 10.1016/j.cell.2014.03.005
44. Kauer, J. A., and Malenka, R. C. (2007). Synaptic plasticity and addiction. Nat. Rev. Neurosci.8, 844–858. doi: 10.1038/nrn2234
45. Kislauskis, E. H., and Singer, R. H. (1992). Determinants of mRNA localization. Curr. Opin. Cell Biol.4, 975–978. doi: 10.1016/0955-0674(92)90128-Y
46. Klein, M. E., Lioy, D. T., Ma, L., Impey, S., Mandel, G., and Goodman, R. H. (2007). Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci.10, 1513–1514. doi: 10.1038/nn2010
47. Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K., and Kosik, K. S. (2003). A microRNA array reveals extensive regulation of microRNAs during brain development. RNA9, 1274–1281. doi: 10.1261/rna.5980303
48. Kuo, Y. M., Liang, K. C., Chen, H. H., Cherng, C. G., Lee, H. T., Lin, Y., et al. (2007). Cocaine-but not methamphetamine-associated memory requires de novo protein synthesis. Neurobiol. Learn. Mem.87, 93–100. doi: 10.1016/j.nlm.2006.06.004
49. Kye, M. J., Neveu, P., Lee, Y. S., Zhou, M., Steen, J. A., Sahin, M., et al. (2011). NMDA mediated contextual conditioning changes miRNA expression. PLoS ONE6:e24682. doi: 10.1371/journal.pone.0024682
50. Laplante, M., and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274–293. doi: 10.1016/j.cell.2012.03.017
51. Lee, R. C., and Ambros, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science294, 862–864. doi: 10.1126/science.1065329
52. Lesscher, H. M., Wallace, M. J., Zeng, L., Wang, V., Deitchman, J. K., McMa-hon, T., et al. (2009). Amygdala protein kinase C epsilon controls alcohol consumption. Genes Brain Behav. 8, 493–499. doi: 10.1111/j.1601-183X.2009.00485.x
53. Lewohl, J. M., Nunez, Y. O., Dodd, P. R., Tiwari, G. R., Harris, R. A., and Mayfield, R. D. (2011). Up-regulation of microRNAs in brain of human alcoholics. Alcohol. Clin. Exp. Res.35, 1928–1937. doi: 10.1111/j.1530-0277.2011.01544.x
54. Li, J., Li, J., Liu, X., Qin, S., Guan, Y., Liu, Y., et al. (2013). MicroRNA expression profile and functional analysis reveal that miR-382 is a critical novel gene of alcohol addiction. EMBO Mol. Med.5, 1402–1414. doi: 10.1002/emmm.201201900
55. Li, M. D., and van der Vaart, A. D. (2011). MicroRNAs in addiction: adaptation’s middlemen? Mol. Psychiatry16, 1159–1168. doi: 10.1038/mp.2011.58
56. Li, X., and Wolf, M. E. (2011). Brain-derived neurotrophic factor rapidly increases AMPA receptor surface expression in rat nucleus accumbens. Eur. J. Neurosci.34, 190–198. doi: 10.1111/j.1460-9568.2011.07754.x
57. Lin, A. C., and Holt, C. E. (2007). Local translation and directional steering in axons. EMBO J. 26, 3729–3736. doi: 10.1038/sj.emboj.7601808
58. Lobo, M. K., Covington, H. E. III, Chaudhury, D., Friedman, A. K., Sun, H., Damez-Werno, D., et al. (2010). Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science330, 385–390. doi: 10.1126/science.1188472
59. Lu, L., Dempsey, J., Liu, S. Y., Bossert, J. M., and 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. Neurosci24, 1604-1611. doi: 10.1523/JNEUROSCI.5124-03.2004
60. Maciotta, S., Meregalli, M., and Torrente, Y (2013). The involvement of microRNAs in neurodegenerative diseases. Front Cell Neurosci. 7:265. doi: 10.3389/fncel.2013.00265
61. Malenka, R. C, and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron44, 5-21. doi: 10.1016/j.neuron.2004.09.012
62. Mameli, M., Balland, B., Lujan, R., and Luscher, C. (2007). Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science317, 530-533. doi: 10.1126/science.1142365
63. Martin, K. C, and Ephrussi, A. (2009). mRNA localization: gene expression in the spatial dimension. Cell 136, 719-730. doi: 10.1016/j.cell.2009.01.044
64. Mathonnet, G., Fabian, M. R., Svitkin, Y V., Parsyan, A., Huck, L., Murata, T., et al. (2007). MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science317, 1764-1767. doi: 10.1126/science.1146067
65. Mayfield, R. D., Harris, R. A., and Schuckit, M. A. (2008). Genetic factors influencing alcohol dependence. Br. J. Pharmacol.154, 275-287. doi: 10.1038/bjp.2008.88
66. Mayfield, R. D., and Nunez, Y O. (2012). Understanding alcoholism through microRNA signatures in brains of human alcoholics. Front. Genet.3:43. doi: 10.3389/fgene.2012.00043
67. Mayford, M., Baranes, D., Podsypanina, K., and Kandel, E. R. (1996). The 3'-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc. Natl. Acad. Sci. U.S.A.93, 13250-13255. doi: 10.1073/pnas.93.23.13250
68. Meer, E. J., Wang, D. O., Kim, S., Barr, I., Guo, F., and Martin, K. C. (2012). Identification of a cis-acting element that localizes mRNA to synapses. Proc. Natl. Acad. Sci. U.S.A.109, 4639-4644. doi: 10.1073/pnas.1116269109
69. Miller, S., Yasuda, M., Coats, J. K., Jones, Y, Martone, M. E., and Mayford, M. (2002). Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron36, 507-519. doi: 10.1016/S0896-6273(02)00978-9
70. Most, D., Ferguson, L. B., Blednov, Y A., Mayfield, R. D., and Harris, R. A. (2014). The synaptoneurosome transcriptome: a model for profiling the molecular effects of alcohol. Pharmacogenomics J. doi: 10.1038/tpj.2014.43 [Epub ahead of print].
71. Muddashetty, R. S., Nalavadi, V. C., Gross, C., Yao, X., Xing, L., Laur, O., et al. (2011). Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell42, 673-688. doi: 10.1016/j.molcel.2011.05.006
72. Mulligan, M. K., Ponomarev, I., Hitzemann, R. J., Belknap, J. K., Tabakoff, B., Harris, R. A., et al. (2006). Toward understanding the genetics of alcohol drinking through transcriptome meta-analysis. Proc. Natl. Acad. Sci. U.S.A.103, 6368-6373. doi: 10.1073/pnas.0510188103
73. Neasta, J., Ben Hamida, S., Yowell, Q., Carnicella, S., and Ron, D. (2010). Role for mammalian target of rapamycin complex 1 signaling in neuroadaptations underlying alcohol-related disorders. Proc. Natl. Acad. Sci. U.S.A.107, 20093-20098. doi: 10.1073/pnas.1005554107
74. Nestler, E. J. (2001). Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci.2,119-128. doi: 10.1038/35053570
75. Nielsen, C. B., Shomron, N., Sandberg, R., Hornstein, E., Kitzman, J., and Burge, C. B. (2007). Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA13, 1894-1910. doi: 10.1261/rna.768207
76. Niere, F., Wilkerson, J. R., and Huber, K. M. (2012). Evidence for a fragile X mental retardation protein-mediated translational switch in metabotropic glu-tamate receptor-triggered Arc translation and long-term depression. J. Neurosci.32, 5924-5936. doi: 10.1523/JNEUROSCI.4650-11.2012
77. Nunez, Y O., and Mayfield, R. D. (2012). Understanding alcoholism through microRNA signatures in brains of human alcoholics. Front. Genet.3:43. doi: 10.3389/fgene.2012.00043
78. Nunez, Y O., Truitt, J. M., Gorini, G., Ponomareva, O. N., Blednov, Y. A., Harris, R. A., et al. (2013). Positively correlated miRNA-mRNA regulatory networks in mouse frontal cortex during early stages of alcohol dependence. BMC Genomics14:725. doi: 10.1186/1471-2164-14-725
79. Parker, R., and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell25, 635–646. doi: 10.1016/j.molcel.2007.02.011
80. Penney, J., Tsurudome, K., Liao, E. H., Elazzouzi, F., Livingstone, M., Gonzalez, M., et al. (2012). TOR is required for the retrograde regulation of synaptic homeostasis at the Drosophila neuromuscular junction. Neuron74, 166–178. doi: 10.1016/j.neuron.2012.01.030
81. Pietrzykowski, A. Z., Friesen, R. M., Martin, G. E., Puig, S. I., Nowak, C. L., Wynne, P. M., et al. (2008). Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron59, 274–287. doi: 10.1016/j.neuron.2008.05.032
82. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., et al. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science309, 1573–1576. doi: 10.1126/science.1115079
83. Quinlan, E. M., Philpot, B. D., Huganir, R. L., and Bear, M. F. (1999). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci.2, 352–357. doi: 10.1038/7263
84. Raab-Graham, K. F., Haddick, P. C., Jan, Y. N., and Jan, L. Y. (2006). Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science314, 144–148. doi: 10.1126/science.1131693
85. Robison, A. J., and Nestler, E. J. (2011). Transcriptional and epigenetic mechanisms of addiction. Nat. Rev. Neurosci.12, 623–637. doi: 10.1038/nrn3111
86. Ron, D., and Messing, R. O. (2013). Signaling pathways mediating alcohol effects. Curr. Top. Behav. Neurosci. 13, 87–126. doi: 10.1007/978-3-642-28720-6_161
87. Saba, R., Storchel, P. H., Aksoy-Aksel, A., Kepura, F., Lippi, G., Plant, T. D., et al. (2012). Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons. Mol. Cell. Biol.32, 619–632. doi: 10.1128/MCB.05896-11
88. Sadri-Vakili, G., Kumaresan, V., Schmidt, H. D., Famous, K. R., Chawla, P., Vassoler, F. M., et al. (2010). Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine. J. Neurosci.30, 11735–11744. doi: 10.1523/JNEUROSCI.2328-10.2010
89. Sanna, P. P., Simpson, C., Lutjens, R., and Koob, G. (2002). ERK regulation in chronic ethanol exposure and withdrawal. Brain Res. 948, 186–191. doi: 10.1016/S0006-8993(02)03191-8
90. Schmidt, H. D., Sangrey, G. R., Darnell, S. B., Schassburger, R. L., Cha, J. H., Pierce, R. C., et al. (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. doi: 10.1111/j.1471-4159.2011.07571.x
91. Schratt, G. (2009). microRNAs at the synapse. Nat. Rev. Neurosci. 10, 842–849. doi: 10.1038/nrn2763
92. Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature439, 283–289. doi: 10.1038/nature04367
93. Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., et al. (2006). Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron52, 475–484. doi: 10.1016/j.neuron.2006.08.034
94. Smalheiser, N. R. (2008). Regulation of mammalian microRNA processing and function by cellular signaling and subcellular localization. Biochim. Biophys. Acta1779, 678–681. doi: 10.1016/j.bbagrm.2008.03.009
95. Smalheiser, N. R., and Lugli, G. (2009). microRNA regulation of synaptic plasticity. Neuromolecular Med. 11, 133–140. doi: 10.1007/s12017-009-8065-2
96. Smith, W. B., Starck, S. R., Roberts, R. W., and Schuman, E. M. (2005). Dopamin-ergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron45, 765–779. doi: 10.1016/j.neuron.2005.01.015
97. Soreq, H., and Wolf, Y. (2011). NeurimmiRs: microRNAs in the neuroim-mune interface. Trends Mol. Med. 17, 548–555. doi: 10.1016/j.molmed.2011.06.009
98. Sosanya, N. M., Huang, P. P., Cacheaux, L. P., Chen, C. J., Nguyen, K., Perrone-Bizzozero, N. I., et al. (2013). Degradation of high affinity HuD targets releases Kv1.1 mRNA from miR-129 repression by mTORC1. J. Cell Biol202, 53-69. doi: 10.1083/jcb.201212089
99. Stark, A., Brennecke, J., Bushati, N., Russell, R. B., and Cohen, S. M. (2005). Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell123, 1133-1146. doi: 10.1016/j.cell.2005.11.023
100. Steward, O., and Levy, W.B. (1982). Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci.2, 284-291. doi: 10.1126/science.1096202
101. Sutton, M. A., Wall, N. R., Aakalu, G. N., and Schuman, E. M. (2004). Regulation of dendritic protein synthesis by miniature synaptic events. Science 304,1979-1983. doi: 10.1126/science.1096202
102. Tapocik, J. D., Barbier, E., Flanigan, M., Solomon, M., Pincus, A., Pilling, A., et al. (2014). microRNA-206 in rat medial prefrontal cortex regulates BDNF expression and alcohol drinking. J. Neurosci. 34, 4581-4588. doi: 10.1523/JNEUROSCI.0445-14.2014
103. Tapocik, J. D., Solomon, M., Flanigan, M., Meinhardt, M., Barbier, E., Schank, J. R., et al. (2013). Coordinated dysregulation of mRNAs and microRNAs in the rat medial prefrontal cortex following a history of alcohol dependence. Pharmacogenomics J. 13,286-296. doi: 10.1038/tpj.2012.17
104. Taylor, A. M., Blurton-Jones, M., Rhee, S. W., Cribbs, D. H., Cotman, C. W., and Jeon, N. L. (2005). A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods2, 599-605. doi: 10.1038/nmeth777
105. Ule, J., and Darnell, R. B. (2006). RNA binding proteins and the regulation of neuronal synaptic plasticity. Curr. Opin. Neurobiol.16, 102-110. doi: 10.1016/j.conb.2006.01.003
106. Vasudevan, S., and Steitz, J. A. (2007). AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell128, 1105-1118. doi: 10.1016/j.cell.2007.01.038
107. Vasudevan, S., Tong, Y., and Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science318, 1931-1934. doi: 10.1126/science.1149460
108. Wang, D. O., Martin, K. C, and Zukin, R. S. (2010). Spatially restricting gene expression by local translation at synapses. Trends Neurosci. 33, 173-182. doi: 10.1016/j.tins.2010.01.005
109. Zhang, H. L., Singer, R. H., and Bassell, G. J. (1999). Neurotrophin regulation of beta-actin mRNA and protein localization within growth cones. J. Cell Biol.147, 59-70. doi: 10.1083/jcb.147.1.59