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MicroRNAs in Opioid Pharmacology

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Journal of Neuroimmune Pharmacology Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNA), a class of ~22-nucleotide RNA molecules, are important gene regulators that bind to the target sites of mRNAs to inhibit the gene expressions either through translational inhibition or mRNA destabilization. There are growing evidences that miRNAs have played several regulatory roles in opioid pharmacology. Like other research fields such as cancer biology, the area where numerous miRNAs are found to be involved in gene regulation, we assume that in opioid studies including research fields of drug additions and opioid receptor regulation, there may be more miRNAs waiting to be discovered. This review will summarize our current knowledge of miRNA functions on opioids biology and briefly describe future research directions of miRNAs related to opioids.

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Abbreviations

Ago2:

Argonaute 2

BDNF:

Brain-derived neurotrophic factor

CNS:

Central nervous system

CREB:

cAMP-response element binding protein

CYP2D6:

cytochrome P450 2D6

Drd2:

Dopamine 2 receptor

Drd3:

dopamine D3 receptor

ERK:

Extracellular signal-regulated kinase

FGF-2:

Fibroblast growth factor-2

FosB:

FBJ murine osteosarcoma viral oncogene homolog B

GPCR:

G protein-coupled receptor

HEK:

Human embryonic kidney

HIV-1:

Human immunodeficiency virus type 1

MeCP2:

Methyl CpG binding protein 2

MOR:

Mu opioid receptor

NeuroD:

Neurogenic differentiation 1

PKA:

Protein kinase A

PKC:

Protein kinase C

References

  • Albulescu R, Neagu M, Albulescu L, Tanase C (2011) Tissular and soluble miRNAs for diagnostic and therapy improvement in digestive tract cancers. Expert Rev Mol Diagn 11(1):101–120. doi:10.1586/erm.10.106

    Article  PubMed  CAS  Google Scholar 

  • Ali S, Drendel AL, Kircher J, Beno S (2010) Pain management of musculoskeletal injuries in children: current state and future directions. Pediatr Emerg Care 26(7):518–524. doi:10.1097/PEC.0b013e3181e5c02b

    Article  PubMed  Google Scholar 

  • Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23(2):185–188. doi:10.1038/13810

    Article  PubMed  CAS  Google Scholar 

  • Amir RE, Sutton VR, Van den Veyver IB (2005) Newborn screening and prenatal diagnosis for Rett syndrome: implications for therapy. J Child Neurol 20(9):779–783

    Article  PubMed  Google Scholar 

  • Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770–776

    Article  PubMed  CAS  Google Scholar 

  • Azaryan AV, Clock BJ, Cox BM (1996a) Mu opioid receptor mRNA in nucleus accumbens is elevated following dopamine receptor activation. Neurochem Res 21(11):1411–1415

    Article  PubMed  CAS  Google Scholar 

  • Azaryan AV, Coughlin LJ, Buzas B, Clock BJ, Cox BM (1996b) Effect of chronic cocaine treatment on mu- and delta-opioid receptor mRNA levels in dopaminergically innervated brain regions. J Neurochem 66(2):443–448

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. doi:10.1016/S0092-8674(04)00045-5

    Article  PubMed  CAS  Google Scholar 

  • Bell JE, Arango JC, Anthony IC (2006) Neurobiology of multiple insults: HIV-1-associated brain disorders in those who use illicit drugs. J Neuroimmune Pharmacol 1(2):182–191. doi:10.1007/s11481-006-9018-2

    Article  PubMed  Google Scholar 

  • Brodsky M, Elliott K, Hynansky A, Jenab S, Inturrisi CE (1995) Quantitation of mu-opioid receptor (MOR-1) mRNA in selected regions of the rat CNS. Neuroreport 6(5):725–729

    Article  PubMed  CAS  Google Scholar 

  • Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320(5880):1224–1229. doi:10.1126/science.1153252

    Article  PubMed  CAS  Google Scholar 

  • Chen CZ, Li L, Lodish HF, Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303(5654):83–86. doi:10.1126/science.1091903

    Article  PubMed  CAS  Google Scholar 

  • Chhabra R, Adlakha YK, Hariharan M, Scaria V, Saini N (2009) Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and -independent apoptosis in human embryonic kidney cells. PLoS One 4(6):e5848. doi:10.1371/journal.pone.0005848

    Article  PubMed  CAS  Google Scholar 

  • Chhabra R, Dubey R, Saini N (2010) Cooperative and individualistic functions of the microRNAs in the miR-23a 27a 24–2 cluster and its implication in human diseases. Mol Cancer 9:232. doi:10.1186/1476-4598-9-232

    Article  PubMed  CAS  Google Scholar 

  • Dave RS, Khalili K (2010) Morphine treatment of human monocyte-derived macrophages induces differential miRNA and protein expression: impact on inflammation and oxidative stress in the central nervous system. J Cell Biochem 110(4):834–845. doi:10.1002/jcb.22592

    Article  PubMed  CAS  Google Scholar 

  • Deng JV, Rodriguiz RM, Hutchinson AN, Kim IH, Wetsel WC, West AE (2010) MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat Neurosci 13(9):1128–1136. doi:10.1038/nn.2614

    Article  PubMed  CAS  Google Scholar 

  • Donahoe RM, Vlahov D (1998) Opiates as potential cofactors in progression of HIV-1 infections to AIDS. J Neuroimmunol 83(1–2):77–87

    Article  PubMed  CAS  Google Scholar 

  • Dreyer JL (2010) New insights into the roles of microRNAs in drug addiction and neuroplasticity. Genome Med 2(12):92. doi:10.1186/gm213

    Article  PubMed  CAS  Google Scholar 

  • Drugs.com (2011) Codeine Information from Drugs.com. Web site from Drugs.com. http://www.drugs.com/monograph/codeine.html. Accessed October 18 2011

  • Duttaroy A, Yoburn BC (1995) The effect of intrinsic efficacy on opioid tolerance. Anesthesiology 82(5):1226–1236

    Article  PubMed  CAS  Google Scholar 

  • Duursma AM, Kedde M, Schrier M, le Sage C, Agami R (2008) miR-148 targets human DNMT3b protein coding region. RNA 14(5):872–877. doi:10.1261/rna.972008

    Article  PubMed  CAS  Google Scholar 

  • Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65(3):373–384. doi:10.1016/j.neuron.2010.01.005

    Article  PubMed  CAS  Google Scholar 

  • Feng J, Nestler EJ (2010) MeCP2 and drug addiction. Nat Neurosci 13(9):1039–1041. doi:10.1038/nn0910-1039

    Article  PubMed  CAS  Google Scholar 

  • Fitting S, Xu R, Bull C, Buch SK, El-Hage N, Nath A, Knapp PE, Hauser KF (2010) Interactive comorbidity between opioid drug abuse and HIV-1 Tat: chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. Am J Pathol 177(3):1397–1410. doi:10.2353/ajpath.2010.090945

    Article  PubMed  CAS  Google Scholar 

  • Flores CM, Mogil JS (2001) The pharmacogenetics of analgesia: toward a genetically-based approach to pain management. Pharmacogenomics 2(3):177–194. doi:10.1517/14622416.2.3.177

    Article  PubMed  CAS  Google Scholar 

  • Gao FB (2010) Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 5:25. doi:10.1186/1749-8104-5-25

    Article  PubMed  CAS  Google Scholar 

  • Gasche Y, Daali Y, Fathi M, Chiappe A, Cottini S, Dayer P, Desmeules J (2004) Codeine intoxication associated with ultrarapid CYP2D6 metabolism. N Engl J Med 351(27):2827–2831. doi:10.1056/NEJMoa041888

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5(1):69–81. doi:10.1038/nri1527

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb GS, Heath L, Nickle DC, Wong KG, Leach SE, Jacobs B, Gezahegne S, van’t Wout AB, Jacobson LP, Margolick JB, Mullins JI (2008) HIV-1 variation before seroconversion in men who have sex with men: analysis of acute/early HIV infection in the multicenter AIDS cohort study. J Infect Dis 197(7):1011–1015. doi:10.1086/529206

    Article  PubMed  Google Scholar 

  • Guo CJ, Li Y, Tian S, Wang X, Douglas SD, Ho WZ (2002) Morphine enhances HIV infection of human blood mononuclear phagocytes through modulation of beta-chemokines and CCR5 receptor. J Investig Med 50(6):435–442

    Article  PubMed  CAS  Google Scholar 

  • Hassan MQ, Gordon JA, Beloti MM, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2010) A network connecting Runx2, SATB2, and the miR-23a 27a 24–2 cluster regulates the osteoblast differentiation program. Proc Natl Acad Sci U S A 107(46):19879–19884. doi:10.1073/pnas.1007698107

    Article  PubMed  CAS  Google Scholar 

  • Hauser KF, El-Hage N, Stiene-Martin A, Maragos WF, Nath A, Persidsky Y, Volsky DJ, Knapp PE (2007) HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J Neurochem 100(3):567–586. doi:10.1111/j.1471-4159.2006.04227.x

    Article  PubMed  CAS  Google Scholar 

  • He Y, Yang C, Kirkmire CM, Wang ZJ (2010) Regulation of opioid tolerance by let-7 family microRNA targeting the mu opioid receptor. J Neurosci 30(30):10251–10258. doi:10.1523/JNEUROSCI.2419-10.2010

    Article  PubMed  CAS  Google Scholar 

  • Ho WZ, Guo CJ, Yuan CS, Douglas SD, Moss J (2003) Methylnaltrexone antagonizes opioid-mediated enhancement of HIV infection of human blood mononuclear phagocytes. J Pharmacol Exp Ther 307(3):1158–1162. doi:10.1124/jpet.103.056697

    Article  PubMed  CAS  Google Scholar 

  • Hollander JA, Im HI, Amelio AL, Kocerha J, Bali P, Lu Q, Willoughby D, Wahlestedt C, Conkright MD, Kenny PJ (2010) Striatal microRNA controls cocaine intake through CREB signalling. Nature 466(7303):197–202. doi:10.1038/nature09202

    Article  PubMed  CAS  Google Scholar 

  • Homan JW, Steele AD, Martinand-Mari C, Rogers TJ, Henderson EE, Charubala R, Pfleiderer W, Reichenbach NL, Suhadolnik RJ (2002) Inhibition of morphine-potentiated HIV-1 replication in peripheral blood mononuclear cells with the nuclease-resistant 2-5A agonist analog, 2-5A(N6B). J Acquir Immune Defic Syndr 30(1):9–20

    PubMed  CAS  Google Scholar 

  • Ingelman-Sundberg M (2005) Genetic polymorphisms of cytochrome P450 2D6 (CYP2D6): clinical consequences, evolutionary aspects and functional diversity. Pharmacogenomics J 5(1):6–13. doi:10.1038/sj.tpj.6500285

    Article  PubMed  CAS  Google Scholar 

  • Jeal W, Benfield P (1997) Transdermal fentanyl. A review of its pharmacological properties and therapeutic efficacy in pain control. Drugs 53(1):109–138

    Article  PubMed  CAS  Google Scholar 

  • Jeffrey GP, MacQuillan G, Chua F, Galhenage S, Bull J, Young E, Hulse G, O’Neil G (2007) Hepatitis C virus eradication in intravenous drug users maintained with subcutaneous naltrexone implants. Hepatology 45(1):111–117. doi:10.1002/hep. 21470

    Article  PubMed  CAS  Google Scholar 

  • Kalow W (2001) Pharmacogenetics, pharmacogenomics, and pharmacobiology. Clin Pharmacol Ther 70(1):1–4. doi:10.1067/mcp.2001.116714

    Article  PubMed  CAS  Google Scholar 

  • Kawashima H, Numakawa T, Kumamaru E, Adachi N, Mizuno H, Ninomiya M, Kunugi H, Hashido K (2010) Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 165(4):1301–1311. doi:10.1016/j.neuroscience.2009.11.057

    Article  PubMed  CAS  Google Scholar 

  • Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105(21):7552–7557. doi:10.1073/pnas.0802203105

    Article  PubMed  CAS  Google Scholar 

  • Kim E, Clark AL, Kiss A, Hahn JW, Wesselschmidt R, Coscia CJ, Belcheva MM (2006) Mu- and kappa-opioids induce the differentiation of embryonic stem cells to neural progenitors. J Biol Chem 281(44):33749–33760. doi:10.1074/jbc.M603862200

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G, Abeliovich A (2007) A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317(5842):1220–1224. doi:10.1126/science.1140481

    Article  PubMed  CAS  Google Scholar 

  • Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10(2):126–139. doi:10.1038/nrm2632

    Article  PubMed  CAS  Google Scholar 

  • Kimura H, Kawasaki H, Taira K (2004) Mouse microRNA-23b regulates expression of Hes1 gene in P19 cells. Nucleic Acids Symp Ser (Oxf) 48:213–214. doi:10.1093/nass/48.1.213

    Article  Google Scholar 

  • Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH (2007) Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci 10(12):1513–1514. doi:10.1038/nn2010

    Article  PubMed  CAS  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39(Database issue):D152–D157. doi:10.1093/nar/gkq1027

    Article  PubMed  Google Scholar 

  • Kusuda R, Cadetti F, Ravanelli MI, Sousa TA, Zanon S, De Lucca FL, Lucas G (2011) Differential expression of microRNAs in mouse pain models. Mol Pain 7:17. doi:10.1186/1744-8069-7-17

    Article  PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12(9):735–739. doi:10.1016/S0960-9822(02)00809-6

    Article  PubMed  CAS  Google Scholar 

  • Lai EC (2002) Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30(4):363–364. doi:10.1038/ng865

    Article  PubMed  CAS  Google Scholar 

  • Lai EC, Burks C, Posakony JW (1998) The K box, a conserved 3′ UTR sequence motif, negatively regulates accumulation of enhancer of split complex transcripts. Development 125(20):4077–4088

    PubMed  CAS  Google Scholar 

  • Lai EC, Tam B, Rubin GM (2005) Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs. Genes Dev 19(9):1067–1080. doi:10.1101/gad.1291905

    Article  PubMed  CAS  Google Scholar 

  • Law PY, Wong YH, Loh HH (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40:389–430

    Article  PubMed  CAS  Google Scholar 

  • Lee YS, Dutta A (2006) MicroRNAs: small but potent oncogenes or tumor suppressors. Curr Opin Investig Drugs 7(6):560–564

    PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854. doi:10.1016/0092-8674(93)90529-Y

    Article  PubMed  CAS  Google Scholar 

  • Lee HJ, Palkovits M, Young WS 3rd (2006) miR-7b, a microRNA up-regulated in the hypothalamus after chronic hyperosmolar stimulation, inhibits Fos translation. Proc Natl Acad Sci U S A 103(42):15669–15674. doi:10.1073/pnas.0605781103

    Article  PubMed  CAS  Google Scholar 

  • Lehmann U, Hasemeier B, Christgen M, Muller M, Romermann D, Langer F, Kreipe H (2008) Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J Pathol 214(1):17–24. doi:10.1002/path.2251

    Article  PubMed  CAS  Google Scholar 

  • Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69(6):905–914. doi:10.1016/0092-8674(92)90610-O

    Article  PubMed  CAS  Google Scholar 

  • Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1):15–20. doi:10.1016/j.cell.2004.12.035

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Wang X, Tian S, Guo CJ, Douglas SD, Ho WZ (2002) Methadone enhances human immunodeficiency virus infection of human immune cells. J Infect Dis 185(1):118–122. doi:10.1086/338011

    Article  PubMed  CAS  Google Scholar 

  • Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 276(8):2348–2358

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Kohane IS (2009) Tissue and process specific microRNA-mRNA co-expression in mammalian development and malignancy. PLoS One 4(5):e5436. doi:10.1371/journal.pone.0005436

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Walker EA, Kissane S, Khan I, Murray PI, Rauz S, Wallace GR (2011) Gene Expression and miR Profiles of Human Corneal Fibroblasts in Response to Dexamethasone. Invest Ophthalmol Vis Sci 52(10):7282–7288. doi:10.1007/s11033-010-0343-4

    Article  PubMed  CAS  Google Scholar 

  • Macey TA, Bobeck EN, Hegarty DM, Aicher SA, Ingram SL, Morgan MM (2009) Extracellular signal-regulated kinase 1/2 activation counteracts morphine tolerance in the periaqueductal gray of the rat. J Pharmacol Exp Ther 331(2):412–418. doi:10.1124/jpet.109.152157

    Article  PubMed  CAS  Google Scholar 

  • Madadi P, Ciszkowski C, Gaedigk A, Leeder JS, Teitelbaum R, Chitayat D, Koren G (2011) Genetic transmission of cytochrome P450 2D6 (CYP2D6) ultrarapid metabolism: implications for breastfeeding women taking codeine. Curr Drug Saf 6(1):36–39

    Article  PubMed  CAS  Google Scholar 

  • Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27(3):435–448. doi:10.1016/j.molcel.2007.07.015

    Article  PubMed  CAS  Google Scholar 

  • Mansour A, Fox CA, Akil H, Watson SJ (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18(1):22–29

    Article  PubMed  CAS  Google Scholar 

  • Mayes S, Ferrone M (2006) Fentanyl HCl patient-controlled iontophoretic transdermal system for the management of acute postoperative pain. Ann Pharmacother 40(12):2178–2186. doi:10.1345/aph.1H135

    Article  PubMed  CAS  Google Scholar 

  • McGregor RA, Choi MS (2011) microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med 11(4):304–316

    Article  PubMed  CAS  Google Scholar 

  • Mogensen TH, Melchjorsen J, Larsen CS, Paludan SR (2010) Innate immune recognition and activation during HIV infection. Retrovirology 7:54. doi:10.1186/1742-4690-7-54

    Article  PubMed  CAS  Google Scholar 

  • Nair MP, Schwartz SA, Polasani R, Hou J, Sweet A, Chadha KC (1997) Immunoregulatory effects of morphine on human lymphocytes. Clin Diagn Lab Immunol 4(2):127–132

    PubMed  CAS  Google Scholar 

  • Neves G, Cooke SF, Bliss TV (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9(1):65–75. doi:10.1038/nrn2303

    Article  PubMed  CAS  Google Scholar 

  • Nudelman AS, DiRocco DP, Lambert TJ, Garelick MG, Le J, Nathanson NM, Storm DR (2010) Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 20(4):492–498. doi:10.1002/hipo.20646

    PubMed  CAS  Google Scholar 

  • O’Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104(5):1604–1609. doi:10.1073/pnas.0610731104

    Article  PubMed  CAS  Google Scholar 

  • Ohno M, Natsume A, Kondo Y, Iwamizu H, Motomura K, Toda H, Ito M, Kato T, Wakabayashi T (2009) The modulation of microRNAs by type I IFN through the activation of signal transducers and activators of transcription 3 in human glioma. Mol Cancer Res 7(12):2022–2030. doi:10.1158/1541-7786.MCR-09-0319

    Article  PubMed  CAS  Google Scholar 

  • Pan YX, Xu J, Mahurter L, Bolan E, Xu M, Pasternak GW (2001) Generation of the mu opioid receptor (MOR-1) protein by three new splice variants of the Oprm gene. Proc Natl Acad Sci U S A 98(24):14084–14089

    Article  PubMed  CAS  Google Scholar 

  • Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M (2007) Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449(7164):919–922. doi:10.1038/nature06205

    Article  PubMed  CAS  Google Scholar 

  • Pergolizzi J, Boger RH, Budd K, Dahan A, Erdine S, Hans G, Kress HG, Langford R, Likar R, Raffa RB, Sacerdote P (2008) Opioids and the management of chronic severe pain in the elderly: consensus statement of an International Expert Panel with focus on the six clinically most often used World Health Organization Step III opioids (buprenorphine, fentanyl, hydromorphone, methadone, morphine, oxycodone). Pain Pract 8(4):287–313. doi:10.1111/j.1533-2500.2008.00204.x

    Article  PubMed  Google Scholar 

  • Perry AK, Chen G, Zheng D, Tang H, Cheng G (2005) The host type I interferon response to viral and bacterial infections. Cell Res 15(6):407–422. doi:10.1038/sj.cr.7290309

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues AC, Li X, Radecki L, Pan YZ, Winter JC, Huang M, Yu AM (2011) MicroRNA expression is differentially altered by xenobiotic drugs in different human cell lines. Biopharm Drug Dispos 32(6):355–367. doi:10.1002/bdd.764

    Article  PubMed  CAS  Google Scholar 

  • Rusinov V, Baev V, Minkov IN, Tabler M (2005) MicroInspector: a web tool for detection of miRNA binding sites in an RNA sequence. Nucleic Acids Res 33(Web Server issue):W696–W700. doi:10.1093/nar/gki364

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Simon FM, Zhang XX, Loh HH, Law PY, Rodriguez RE (2010) Morphine regulates dopaminergic neuron differentiation via miR-133b. Mol Pharmacol 78(5):935–942. doi:10.1124/mol.110.066837

    Article  PubMed  CAS  Google Scholar 

  • Sato F, Tsuchiya S, Meltzer SJ, Shimizu K (2011) MicroRNAs and epigenetics. FEBS J 278(10):1598–1609. doi:10.1111/j.1742-4658.2011.08089.x

    Article  PubMed  CAS  Google Scholar 

  • Schaefer A, Im HI, Veno MT, Fowler CD, Min A, Intrator A, Kjems J, Kenny PJ, O’Carroll D, Greengard P (2010) Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction. J Exp Med 207(9):1843–1851. doi:10.1084/jem.20100451

    Article  PubMed  CAS  Google Scholar 

  • 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(7074):283–289. doi:10.1038/nature04367

    Article  PubMed  CAS  Google Scholar 

  • Schwartz C, Catez P, Rohr O, Lecestre D, Aunis D, Schaeffer E (2000) Functional interactions between C/EBP, Sp1, and COUP-TF regulate human immunodeficiency virus type 1 gene transcription in human brain cells. J Virol 74(1):65–73

    Article  PubMed  CAS  Google Scholar 

  • Somel M, Guo S, Fu N, Yan Z, Hu HY, Xu Y, Yuan Y, Ning Z, Hu Y, Menzel C, Hu H, Lachmann M, Zeng R, Chen W, Khaitovich P (2010) MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 20(9):1207–1218. doi:10.1101/gr.106849.110

    Article  PubMed  CAS  Google Scholar 

  • Tuttle DL, Harrison JK, Anders C, Sleasman JW, Goodenow MM (1998) Expression of CCR5 increases during monocyte differentiation and directly mediates macrophage susceptibility to infection by human immunodeficiency virus type 1. J Virol 72(6):4962–4969

    PubMed  CAS  Google Scholar 

  • Unterwald EM, Horne-King J, Kreek MJ (1992) Chronic cocaine alters brain mu opioid receptors. Brain Res 584(1–2):314–318

    Article  PubMed  CAS  Google Scholar 

  • Unterwald EM, Rubenfeld JM, Kreek MJ (1994) Repeated cocaine administration upregulates kappa and mu, but not delta, opioid receptors. Neuroreport 5(13):1613–1616

    Article  PubMed  CAS  Google Scholar 

  • Unterwald EM, Rubenfeld JM, Imai Y, Wang JB, Uhl GR, Kreek MJ (1995) Chronic opioid antagonist administration upregulates mu opioid receptor binding without altering mu opioid receptor mRNA levels. Brain Res Mol Brain Res 33(2):351–355. doi:10.1016/0169-328X(95)00143-G

    Article  PubMed  CAS  Google Scholar 

  • Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20(5):515–524. doi:10.1101/gad.1399806

    Article  PubMed  CAS  Google Scholar 

  • Vallejo R, de Leon-Casasola O, Benyamin R (2004) Opioid therapy and immunosuppression: a review. Am J Ther 11(5):354–365

    Article  PubMed  Google Scholar 

  • van Jaarsveld MT, Helleman J, Berns EM, Wiemer EA (2010) MicroRNAs in ovarian cancer biology and therapy resistance. Int J Biochem Cell Biol 42(8):1282–1290. doi:10.1016/j.biocel.2010.01.014

    Article  PubMed  CAS  Google Scholar 

  • van Rooij E (2011) The art of microRNA research. Circ Res 108(2):219–234. doi:10.1161/circresaha.110.227496

    Article  PubMed  CAS  Google Scholar 

  • Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21(7):744–749. doi:10.1101/gad.1519107

    Article  PubMed  CAS  Google Scholar 

  • Wang X (2008) miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 14(6):1012–1017. doi:10.1261/rna.965408

    Article  PubMed  CAS  Google Scholar 

  • Wang X, El Naqa IM (2008) Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24(3):325–332. doi:10.1093/bioinformatics/btm595

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Gabuzda D (2006) Reconstitution of human immunodeficiency virus-induced neurodegeneration using isolated populations of human neurons, astrocytes, and microglia and neuroprotection mediated by insulin-like growth factors. J Neurovirol 12(6):472–491. doi:10.1080/13550280601039659

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Ye L, Hou W, Zhou Y, Wang YJ, Metzger DS, Ho WZ (2009) Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood 113(3):671–674. doi:10.1182/blood-2008-09-175000

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Li C, Ju S, Wang Y, Wang H, Zhong R (2011a) Myeloma cell adhesion to bone marrow stromal cells confers drug resistance by microRNA-21 up-regulation. Leuk Lymphoma 52(10):1991–1998. doi:10.3109/10428194.2011.591004

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Ye L, Zhou Y, Liu MQ, Zhou DJ, Ho WZ (2011b) Inhibition of anti-HIV microRNA expression: a mechanism for opioid-mediated enhancement of HIV infection of monocytes. Am J Pathol 178(1):41–47. doi:10.1016/j.ajpath.2010.11.042

    Article  PubMed  CAS  Google Scholar 

  • 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(26):9093–9098. doi:10.1073/pnas.0803072105

    Article  PubMed  CAS  Google Scholar 

  • Wibrand K, Panja D, Tiron A, Ofte ML, Skaftnesmo KO, Lee CS, Pena JT, Tuschl T, Bramham CR (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(4):636–645. doi:10.1111/j.1460-9568.2010.07112.x

    Article  PubMed  Google Scholar 

  • 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(12):4085–4095. doi:10.1096/fj.08-108175

    Article  PubMed  CAS  Google Scholar 

  • 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(4):744–750. doi:10.1124/mol.108.053462

    Article  PubMed  CAS  Google Scholar 

  • Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, Chen G, Wang Z (2007) The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 13(4):486–491. doi:10.1038/nm1569

    Article  PubMed  CAS  Google Scholar 

  • Yu JY, Chung KH, Deo M, Thompson RC, Turner DL (2008) MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 314(14):2618–2633. doi:10.1016/j.yexcr.2008.06.002

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Chu J, Zeng Y, Loh HH, Law PY (2010a) Yin Yang 1 phosphorylation contributes to the differential effects of mu-opioid receptor agonists on microRNA-190 expression. J Biol Chem 285(29):21994–22002. doi:10.1074/jbc.M110.112607

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Zeng Y, Chu J, Kam AY, Loh HH, Law PY (2010b) Modulations of NeuroD activity contribute to the differential effects of morphine and fentanyl on dendritic spine stability. J Neurosci 30(24):8102–8110. doi:10.1523/JNEUROSCI.6069-09.2010

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Zeng Y, Zhang X, Chu J, Loh HH, Law PY (2010c) mu-Opioid receptor agonists differentially regulate the expression of miR-190 and NeuroD. Mol Pharmacol 77(1):102–109. doi:10.1124/mol.109.060848

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Institutes of Health National Institutes of Drug Abuse [Grants DA000564, DA001583, DA011806, K05-DA070554, DA011190, DA013926]; and by the A & F Stark Fund of the Minnesota Medical Foundation. The authors declare no conflict of interest.

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Correspondence to Cheol Kyu Hwang.

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Hwang, C.K., Wagley, Y., Law, PY. et al. MicroRNAs in Opioid Pharmacology. J Neuroimmune Pharmacol 7, 808–819 (2012). https://doi.org/10.1007/s11481-011-9323-2

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