The emerging role of non-coding RNAs in drug addiction

Frontiers in Genetics

Volumn 3, Issue JUN, 2012, Pages

  Sartor, Gregory C ^a   St Laurent III, Georges ^b,c   Wahlestedt, Claes ^a  

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

^b St Laurent Institute   (United States)

^c UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

Addiction; Epigenetic; IncRNA; Long non coding RNA; MicroRNA; MiRNA

Indexed keywords

EID: 84867591497     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00106     Document Type: Article

References (84)

1. Alvarez-Saavedra, M., Antoun, G., Yanagiya, A., Oliva-Hernandez, R., Cornejo-Palma, D., Perez-Iratxeta, C., Sonenberg, N., and Cheng, H. Y. (2011). miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum. Mol. Genet. 20, 731-751.
2. Baek, M. N., Jung, K. H., Halder, D., Choi, M. R., Lee, B. H., Lee, B. C., Jung, M. H., Choi, I. G., Chung, M. K., Oh, D. Y., and Chai, Y. G. (2010). Artificial microRNA-based neurokinin-1 receptor gene silencing reduces alcohol consumption in mice. Neurosci. Lett. 475,124-128.
3. Belgard, T. G., Marques, A. C., Oliver, P. L., Abaan, H. O., Sirey, T. M., Hoerder-Suabedissen, A., Garcia-Moreno, F., Molnar, Z., Margulies, E. H., and Ponting, C. P. (2011). A transcriptomic atlas of mouse neo-cortical layers. Neuron 71, 605-616.
4. Berezikov, E. (2011). Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet. 12, 846-860.
5. Bernard, D., Prasanth, K. V., Tripathi, V., Colasse, S., Nakamura, T., Xuan, Z., Zhang, M. Q., Sedel, F., Jourdren, L., Coulpier, F., Triller, A., Spector, D. L., and Bessis, A. (2010). A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 29, 3082-3093.
6. Bitko, V., and Barik, S. (2007). Intranasal antisense therapy: pre-clinical models with a clinical future? Curr. Opin. Mol. Ther. 9, 119-125.
7. Carlezon, W. A. Jr., Thome, J., Olson, V. G., Lane-Ladd, S. B., Brodkin, E. S., Hiroi, N., Duman, R. S., Neve, R. L., and Nestler, E. J. (1998). Regulation of cocaine reward by CREB. Science 282,2272-2275.
8. 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.
9. Chandrasekar, V., and Dreyer, J. L. (2011). Regulation of MiR-124, Let-7d, and MiR-181a in the accum-bens affects the expression, extinction, and reinstatement of cocaine-induced conditioned place preference. Neuropsychopharmacology 36, 1149-1164.
10. Chen, J. F., Mandel, E. M., Thomson, J. M., Wu, Q., Callis, T. E., Hammond, S. M., Conlon, F. L., and Wang, D. Z. (2006). The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38, 228-233.
11. Cheng, H. Y., Papp, J. W., Varlamova, O., Dziema, H., Russell, B., Curf-man, J. P., Nakazawa, T., Shimizu, K., Okamura, H., Impey, S., and Obri-etan, K. (2007). microRNA modulation of circadian-clock period and entrainment. Neuron 54, 813-829.
12. Chu, C., Qu, K., Zhong, F. L., Artandi, S. E., and Chang, H. Y (2011). Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell 44, 667-678.
13. Cuellar, T. L., Davis, T. H., Nelson, P. T., Loeb, G. B., Harfe, B. D., Ullian, E., and McManus, M. T. (2008). Dicer loss in stri-atal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 105, 5614-5619.
14. Dinger, M. E., Mercer, T. R., and Mattick, J. S. (2008). RNAs as extracellular signaling molecules. J. Mol. Endocrinol. 40, 151-159.
15. Edbauer, D., Neilson, J. R., Foster, K. A., Wang, C. F., Seeburg, D. P., Batterton, M. N., Tada, T., Dolan, B. M., Sharp, P. A., and Sheng, M. (2010). Regulation of synaptic structure and function by FMRP-associated microR-NAs miR-125b and miR-132. Neuron 65, 373-384.
16. 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.
17. Fabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N., Callegari, E., Liu, S., Alder, H., Costinean, S., Fernandez-Cymering, C., Volinia, S., Guler, G., Morrison, C. D., Chan, K. K., Marcucci, G., Calin, G. A., Hueb-ner, K., and Croce, C. M. (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc. Natl. Acad. Sci. U.S.A. 104, 15805-15810.
18. French, P. J., Bliss, T. V., and O'Connor, V. (2001). Ntab, a novel non-coding RNA abundantly expressed in rat brain. Neuroscience 108, 207-215.
19. Gao, J., Wang, W. Y., Mao, Y. W., Graff, J., Guan, J. S., Pan, L., Mak, G., Kim, D., Su, S. C., and Tsai, L. H. (2010). A novel pathway regulates memory and plasticity via SIRT 1 and miR-134. Nature 466, 1105-1109.
20. Ghitza, U. E.,Zhai, H., Wu, P., Airavaara, M., Shaham, Y., and Lu, L. (2010). Role of BDNF and GDNF in drug reward and relapse: a review. Neu-rosci. Biobehav. Rev. 35, 157-171.
21. Guo, Y., Chen, Y., Carreon, S., and Qiang, M. (2011). Chronic intermittent ethanol exposure and its removal induce a different mirna expression pattern in primary cortical neuronal cultures. Alcohol. Clin. Exp. Res. doi: 10.1111/j.1530-0277.2011.01689.x. [Epub ahead of print].
22. He, Y., Yang, C., Kirkmire, C. M., and Wang, Z. J. (2010). Regulation of opioid tolerance by let-7 family microRNA targeting the mu opioid receptor. J. Neurosci. 30, 10251-10258.
23. Hiroi, N., Brown, J. R., Haile, C. N., Ye, H., Greenberg, M. E., and Nestler, E. J. (1997). FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psy-chomotor and rewarding effects. Proc. Natl. Acad. Sci. U.S.A. 94, 10397-10402.
24. Hollander, J. A., Im, H. I., Amelio, A. L., Kocerha, J., Bali, P., Lu, Q., Willoughby, D., Wahlestedt, C., Conkright, M. D., and Kenny, P. J. (2010). Striatal microRNA controls cocaine intake through CREB signalling. Nature 466, 197-202.
25. Houseley, J., Rubbi, L., Grunstein, M., Tollervey, D., and Vogelauer, M. (2008). A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol. Cell 32, 685-695.
26. Huang, W., and Li, M. D. (2009a). Differential allelic expression of dopamine D1 receptor gene (DRD1) is modulated by microRNA miR-504. Biol. Psychiatry 65, 702-705.
27. Huang, W., and Li, M. D. (2009b). Nicotine modulates expression of miR-140, which targets the 3'-untranslated region of dynamin 1 gene (Dnm1). Int. J. Neuropsy-chopharmacol. 12, 537-546.
28. Hung, G., Mazur, C., Wancewicz, E., Norris, D., and Bennet, F. (2011). Second Generation Oligonucleotide CNS Delivery via IT Administration inMice, Rats and Monkey. Societyfor Neuroscience, Washington, 557.06.
29. Hwang, Y Y., and Li, M. D. (2006). Proteins differentially expressed in response to nicotine in five rat brain regions: identification using a 2-DE/MS-based proteomics approach. Proteomics 6, 3138-3153.
30. 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.
31. Jia, H., Osak, M., Bogu, G. K., Stan-ton, L. W.,Johnson, R., and Lipovich, L. (2010). Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA 16, 1478-1487.
32. Johnson, R., Teh, C. H., Jia, H., Vanisri, R. R., Pandey, T., Lu, Z. H., Buckley, N. J., Stanton, L. W., and Lipovich, L. (2009). Regulation of neural macroRNAs by the transcriptional repressor REST. RNA 15, 85-96.
33. Kapranov, P., St Laurent, G., Raz, T., Ozsolak, F., Reynolds, C. P., Sorensen, P. H., Reaman, G., Milos, P., Arceci, R. J., Thompson, J. F., and Triche, T. J. (2010). The majority of total nuclear-encoded non-ribosomal RNA in a human cell is dark matter un-annotated RNA. BMC Biol. 8, 149. doi:10.1186/1741-7007-8-149
34. Khalil, A. M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B. E., van Oudenaarden, A., Regev, A., Lander, E. S., and Rinn, J. L. (2009). Many human large inter-genic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. U.S.A. 106, 11667-11672.
35. Konopka, W., Kiryk, A., Novak, M., Her-werth, M., Parkitna, J. R., Wawrzy-niak, M., Kowarsch, A., Michaluk, P., Dzwonek, J., Arnsperger, T., Wilczynski, G., Merkenschlager, M., Theis, E J., Kohr, G., Kaczmarek, L., and Schutz, G. (2010). MicroRNA loss enhances learning and memory in mice. J. Neurosci. 30, 14835-14842.
36. Lagos-Quintana, M., Rauhut, R., Yal-cin, A., Meyer, J., Lendeckel, W., and Tuschl, T. (2002). Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739.
37. LaPlant, Q., Vialou, V., Covington, H. E. III, Dumitriu, D., Feng, J., Warren, B. L., Maze, I., Dietz, D. M., Watts, E. L., Iniguez, S. D., Koo, J. W., Mouzon, E., Renthal, W., Hollis, F., Wang, H., Noonan, M. A., Ren, Y., Eisch, A. J., Bolaños, C. A., Kabbaj, M., Xiao, G., Neve, R. L., Hurd, Y L., Oosting, R. S., Fan, G., Morrison, J. H., and Nestler, E. J. (2010). Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci. 13, 1137-1143.
38. Lewohl, J. M., Nunez, Y O., Dodd, P. R., Tiwari, G. R., Harris, R. A., and May-field, R. D. (2011). Up-regulation of MicroRNAs in brain of human alcoholics. Alcohol. Clin. Exp. Res. 35, 1928-1937.
39. Lin, D., Pestova, T. V., Hellen, C. U., and Tiedge, H. (2008). Transla-tional control by a small RNA: dendritic BC1 RNA targets the eukary-otic initiation factor 4A helicase mechanism. Mol. Cell. Biol. 28, 3008-3019.
40. Lippi, G., Steinert, J. R., Marczylo, E. L., D'Oro, S., Fiore, R., Forsythe, I. D., Schratt, G., Zoli, M., Nicotera, P., and Young, K. W. (2011). Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology. J. Cell Biol. 194, 889-904.
41. Lugli, G., Torvik, V. I., Larson, J., and Smalheiser, N. R. (2008). Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J. Neurochem. 106, 650-661.
42. Makeyev, E. V., Zhang, J., Carrasco, M. A., and Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448.
43. Mattick, J. S. (2007). A new paradigm for developmental biology. J. Exp. Biol. 210, 1526-1547.
44. Maze, I., Covington, H. E. III, Dietz, D. M., LaPlant, Q., Renthal, W., Russo, S. J., Mechanic, M., Mouzon, E., Neve, R. L., Haggarty, S. J., Ren, Y., Sampath, S. C., Hurd, Y L., Green-gard, P., Tarakhovsky, A., Schaefer, A., and Nestler, E. J. (2010). Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327,213-216.
45. Maze, I., and Nestler, E. J. (2011). The epigenetic landscape of addiction. Ann. N. Y. Acad. Sci. 1216, 99-113.
46. Mercer, T. R., Dinger, M. E., Sunkin, S. M., Mehler, M. F., and Mattick, J. S. (2008). Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. U.S.A. 105,716-721.
47. Mercer, T. R., Qureshi, I. A., Gokhan, S., Dinger, M. E., Li, G., Mattick, J. S., and Mehler, M. F. (2010). Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci. 11, 14. doi:10.1186/1471-2202-11-14
48. Michelhaugh, S. K., Lipovich, L., Blythe, J., Jia, H., Kapatos, G., and Ban-non, M. J. (2011). MiningAffymetrix microarray data for long non-coding RNAs: altered expression in the nucleus accumbens of heroin abusers.J. Neurochem. 116,459-466.
49. Modarresi, F., Faghihi, M. A., Lopez-Toledano, M. A., Fatemi, R. P., Mag-istri, M., Brothers, S. P., van der Brug, M. P., and Wahlestedt, C. (2012). Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation. Nat. Biotechnol. 30, 453-459.
50. Nagano, T., Mitchell, J. A., Sanz, L. A., Pauler, F. M., Ferguson-Smith, A. C., Feil, R., and Fraser, P. (2008). The Air noncoding RNA epigeneti-cally silences transcription by targeting G9a to chromatin. Science 322, 1717-1720.
51. Nudelman, A. S., DiRocco, D. P., Lambert, T. J., Garelick, M. G., Le, J., Nathanson, N. M., and Storm, D. R. (2010). Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 20, 492-498.
52. Pandey, R. R., Mondal, T., Mohammad, F., Enroth, S., Redrup, L., Komorowski, J., Nagano, T., Mancini-Dinardo, D., and Kanduri, C. (2008). Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32, 232-246.
53. Pietrzykowski, A. Z., Friesen, R. M., Martin, G. E., Puig, S. I., Nowak, C. L., Wynne, P. M., Siegelmann, H. T., and Treistman, S. N. (2008). Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59, 274-287.
54. Ponjavic, J., Oliver, P. L., Lunter, G., and Ponting, C. P. (2009). Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet. 5, e1000617. doi:10.1371/journal.pgen.1000617
55. Pulipparacharuvil, S., Renthal, W., Hale, C. F., Taniguchi, M., Xiao, G., Kumar, A., Russo, S. J., Sikder, D., Dewey, C. M., Davis, M. M., Greengard, P., Nairn, A. C., Nestler, E. J., and Cowan, C. W. (2008). Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59, 621-633.
56. Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S. V., Russo, J. J., Sander, C., Tuschl, T., and Kandel, E. (2009). Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817.
57. Rinn, J. L., Kertesz, M., Wang, J. K., Squazzo, S. L., Xu, X., Brugmann, S. A., Goodnough, L. H., Helms, J. A., Farnham, P. J., Segal, E., and Chang, H. Y. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323.
58. Robison, A. J., and Nestler, E. J. (2011). Transcriptional and epige-netic mechanisms of addiction. Nat. Rev. Neurosci. 12, 623-637.
59. Saba,R.,Storchel,P.H.,Aksoy-Aksel,A., Kepura, F., Lippi, G., Plant, T. D., and Schratt, G. M. (2012). Dopamine-regulated MicroRNA MiR-18 1a controls GluA2 surface expression in hippocampal neurons. Mol. Cell. Biol. 32, 619-632.
60. Salmena, L., Poliseno, L., Tay, Y., Kats, L., and Pandolfi, P. P. (2011). A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146, 353-358.
61. Sanchez-Simon, F. M., Zhang, X. X., Loh, H. H., Law, P. Y., and Rodriguez, R. E. (2010). Morphine regulates dopaminergic neuron differentiation via miR-133b. Mol. Pharmacol. 78, 935-942.
62. Schaefer, A., Im, H. I., Veno, M. T., Fowler, C. D., Min, A., Intrator, A., Kjems, J., Kenny, P. J., O'Carroll, D., and Greengard, P. (2010).Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction. J. Exp. Med. 207, 1843-1851.
63. Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., and Greenberg, M. E. (2006). A brain-specific microRNA regulates dendritic spine development. Nature 439,283-289.
64. Sempere, L. F., Cole, C. N., McPeek, M. A., and Peterson, K. J. (2006). The phylogenetic distribution of meta-zoan microRNAs: insights into evolutionary complexity and constraint. J. Exp. Zool. B Mol. Dev. Evol. 306, 575-588.
65. Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P. E., Busch, C. J., Kane, C., Hiibel, K., Dekker, F., Hedberg, C., Rengarajan, B., Drepper, C., Waldmann, H., Kauppinen, S., Greenberg, M. E., Draguhn, A., Rehmsmeier, M., Martinez, J., and Schratt, G. M. (2009). A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 11, 705-716.
66. Siegel, G., Saba, R., and Schratt, G. (2011). microRNAs in neurons: manifold regulatory roles at the synapse. Curr. Opin. Genet. Dev. 21, 491-497.
67. Simon, M. D., Wang, C. I., Kharchenko, P. V., West, J. A., Chapman, B. A., Alekseyenko, A. A., Borowsky, M. L., Kuroda, M. I., and Kingston, R. E. (2011). The genomic binding sites of a noncoding RNA. Proc. Natl. Acad. Sci. U.S.A. 108,20497-20502.
68. Smalheiser, N. R. (2007). Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol. Direct 2, 35.
69. Taft, R. J., Pheasant, M., and Mattick, J. S. (2007). The relationship between non-protein-coding DNA and eukaryotic complexity. Bioessays 29,288-299.
70. Tay, Y., Kats, L., Salmena, L., Weiss, D., Tan, S. M., Ala, U., Karreth, E, Poliseno, L., Provero, P., Di Cunto, F., Lieberman, J., Rigout-sos, I., and Pandolfi, P. P. (2011). Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147, 344-357.
71. Tilley, M. R., O'Neill, B., Han, D. D., and Gu, H. H. (2009). Cocaine does not produce reward in absence of dopamine transporter inhibition. Neuroreport 20, 9-12.
72. Treistman, S. N., and Martin, G. E. (2009). BK Channels: mediators and models for alcohol tolerance. Trends Neurosci. 32, 629-637.
73. Wang, K. C., and Chang, H. Y (2011). Molecular mechanisms of long non-coding RNAs. Mol. Cell 43,904-914.
74. Wang, L., Lv, Z., Hu, Z., Sheng, J., Hui, B., Sun, J., and Ma, L. (2010). Chronic cocaine-induced H3 acety-lation and transcriptional activation of CaMKIIalpha in the nucleus accumbens is critical for motivation for drug reinforcement. Neuropsy-chopharmacology 35, 913-928.
75. Wayman, G. A., Davare, M., Ando, H., Fortin, D., Varlamova, O., Cheng, H. Y., Marks, D., Obrietan, K., Soderling, T. R., Goodman, R. H., and Impey, S. (2008). An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl. Acad. Sci. U.S.A. 105, 9093-9098.
76. Wibrand, K., Panja, D., Tiron, A., Ofte, M. L., Skaftnesmo, K. O., Lee, C. S., Pena, J. T., Tuschl, T., and Bramham, C. R. (2010). Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. Eur. J. Neurosci. 31,636-645.
77. Wood, M., Yin, H., and McClorey, G. (2007). Modulating the expression of disease genes with RNA-based therapy. PLoS Genet. 3, e109. doi:10.1371/journal.pgen.0030109
78. Wu, Q., Zhang, L., Law, P. Y., Wei, L. N., and Loh, H. H. (2009). Long-term morphine treatment decreases the association of mu-opioid receptor (MOR1) mRNA with polysomes through miRNA23b. Mol. Pharmacol. 75, 744-750.
79. Yadav, S., Pandey, A., Shukla, A., Tal-welkar, S. S., Kumar, A., Pant, A. B., and Parmar, D. (2011). miR-497 and miR-302b regulate ethanol-induced neuronal cell death through BCL2 protein and cyclin D2. J. Biol. Chem. 286,37347-37357.
80. Yap, K. L., Li, S., Munoz-Cabello, A. M., Raguz, S., Zeng, L., Mujtaba, S., Gil, J., Walsh, M. J., and Zhou, M. M. (2010). Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38, 662-674.
81. Yu, W., Gius, D., Onyango, P., Muldoon-Jacobs, K., Karp, J., Feinberg, A. P., and Cui, H. (2008). Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451,202-206.
82. Zhang, Y., Li, J., Kong, L., Gao, G., Liu, Q. R., and Wei, L. (2007). NATsDB: natural antisense transcripts DataBase. Nucleic Acids Res. 35, D156-D161.
83. Zhao, J., Zhang, X., Zhou, Y., Ansell, P. J., and Klibanski, A. (2006). Cyclic AMP stimulates MEG3 gene expression in cells through a cAMP-response element (CRE) in the MEG3 proximal promoter region. Int. J. Biochem. Cell Biol. 38, 1808-1820.
84. Zheng, H., Zeng, Y., Zhang, X., Chu, J., Loh, H. H., and Law, P. Y (2010). mu-Opioid receptor agonists differentially regulate the expression of miR-190 andNeuroD. Mol. Pharmacol. 77, 102-109.