Genetic-epigenetic interaction modulates μ-opioid receptor regulation

Human Molecular Genetics

Volumn 21, Issue 21, 2012, Pages 4751-4760

  Oertel, Bruno G ^a   Doehring, Alexandra ^a   Roskam, Bianca ^a   Kettner, Mattias ^b   Hackmann, Nadja ^a   Ferreirós, Nerea ^a   Schmidt, Peter H ^b   Lötsch, Jörn ^a  

^a GOETHE UNIVERSITY   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MU OPIATE RECEPTOR; NUCLEOTIDE;

ADULT; ARTICLE; AUTOPSY; BRAIN TISSUE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWNSTREAM PROCESSING; EPIGENETICS; FEMALE; GENETIC VARIABILITY; GENOTYPE; HEROIN DEPENDENCE; HUMAN; HUMAN TISSUE; MALE; OPIATE ADDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION;

ADULT; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; HEROIN DEPENDENCE; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, OPIOID, MU; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84867822943     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds314     Document Type: Article

References (48)

1. Bird, A. (2007) Perceptions of epigenetics. Nature, 447, 396-398.
2. Zhang, D., Cheng, L., Badner, J.A., Chen, C., Chen, Q., Luo, W., Craig, D.W., Redman, M., Gershon, E.S. and Liu, C. (2010) Genetic control of individual differences in gene-specific methylation in human brain. Am. J. Hum. Genet., 86, 411-419.
3. Gibbs, J.R., van der Brug, M.P., Hernandez, D.G., Traynor, B.J., Nalls, M.A., Lai, S.L., Arepalli, S., Dillman, A., Rafferty, I.P., Troncoso, J. et al. (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet., 6, e1000952.
4. Lötsch, J. and Geisslinger, G. (2005) Are mu-opioid receptor polymorphisms important for clinical opioid therapy? Trends Mol. Med., 11, 82-89.
5. Bond, C., LaForge, K.S., Tian, M., Melia, D., Zhang, S., Borg, L., Gong, J., Schluger, J., Strong, J.A., Leal, S.M. et al. (1998) Single-nucleotide polymorphism in the human mu opioid receptor gene alters beta-endorphin binding and activity: possible implications for opiate addiction. Proc. Natl Acad. Sci. USA, 95, 9608-9613.
6. Lötsch, J., Skarke, C., Grosch, S., Darimont, J., Schmidt, H. and Geisslinger, G. (2002) The polymorphism A118G of the human mu-opioid receptor gene decreases the pupil constrictory effect of morphine-6-glucuronide but not that of morphine. Pharmacogenetics, 12, 3-9.
7. Oertel, B.G., Preibisch, C., Wallenhorst, T., Hummel, T., Geisslinger, G., Lanfermann, H. and Lötsch, J. (2008) Differential opioid action on sensory and affective cerebral pain processing. Clin. Pharmacol. Ther., 83, 577-588.
8. Oertel, B.G., Schmidt, R., Schneider, A., Geisslinger, G. and Lötsch, J. (2006) The mu-opioid receptor gene polymorphism 118A.G depletes alfentanil-induced analgesia and protects against respiratory depression in homozygous carriers. Pharmacogenet. Genomics, 16, 625-636.
9. Shi, J., Hui, L., Xu, Y., Wang, F., Huang, W. and Hu, G. (2002) Sequence variations in the mu-opioid receptor gene (OPRM1) associated with human addiction to heroin. Hum. Mutat., 19, 459-460.
10. Szeto, C.Y., Tang, N.L., Lee, D.T. and Stadlin, A. (2001) Association between mu opioid receptor gene polymorphisms and Chinese heroin addicts. Neuroreport, 12, 1103-1106.
11. Chou, W.Y., Wang, C.H., Liu, P.H., Liu, C.C., Tseng, C.C. and Jawan, B. (2006) Human opioid receptor A118G polymorphism affects intravenous patient-controlled analgesia morphine consumption after total abdominal hysterectomy. Anesthesiology, 105, 334-337.
12. Sia, A.T., Lim, Y., Lim, E.C., Goh, R.W., Law, H.Y., Landau, R., Teo, Y.Y. and Tan, E.C. (2008) A118G single nucleotide polymorphism of human mu-opioid receptor gene influences pain perception and patient-controlled intravenous morphine consumption after intrathecal morphine for postcesarean analgesia. Anesthesiology, 109, 520-526.
13. Klepstad, P., Rakvag, T.T., Kaasa, S., Holthe, M., Dale, O., Borchgrevink, P.C., Baar, C., Vikan, T., Krokan, H.E. and Skorpen, F. (2004) The 118 A.G polymorphism in the human mu-opioid receptor gene may increase morphine requirements in patients with pain caused by malignant disease. Acta Anaesthesiol. Scand., 48, 1232-1239.
14. Bart, G., Heilig, M., LaForge, K.S., Pollak, L., Leal, S.M., Ott, J. and Kreek, M.J. (2004) Substantial attributable risk related to a functional mu-opioid receptor gene polymorphism in association with heroin addiction in central Sweden. Mol. Psychiatry, 9, 547-549.
15. Drakenberg, K., Nikoshkov, A., Horvath, M.C., Fagergren, P., Gharibyan, A., Saarelainen, K., Rahman, S., Nylander, I., Bakalkin, G., Rajs, J. et al. (2006) Mu opioid receptor A118G polymorphism in association with striatal opioid neuropeptide gene expression in heroin abusers. Proc. Natl Acad. Sci. USA, 103, 7883-7888.
16. Oertel, B.G., Kettner, M., Scholich, K., Renne, C., Roskam, B., Geisslinger, G., Schmidt, P.H. and Lotsch, J. (2009) A common human micro-opioid receptor genetic variant diminishes the receptor signaling efficacy in brain regions processing the sensory information of pain. J. Biol. Chem., 284, 6530-6535.
17. Zhang, Y., Wang, D., Johnson, A.D., Papp, A.C. and Sadee, W. (2005) Allelic expression imbalance of human mu opioid receptor (OPRM1) caused by variant A118G. J. Biol. Chem., 280, 32618-32624.
18. Mague, S.D., Isiegas, C., Huang, P., Liu-Chen, L.Y., Lerman, C. and Blendy, J.A. (2009) Mouse model of OPRM1 (A118G) polymorphism has sex-specific effects on drug-mediated behavior. Proc. Natl Acad. Sci. USA, 106, 10847-10852.
19. Huang, P., Chen, C., Mague, S.D., Blendy, J.A. and Liu-Chen, L.Y. (2011) A common single nucleotide polymorphism A118G of the mu opioid receptor alters its N-glycosylation and protein stability. Biochem. J., 44, 379-386.
20. Ramchandani, V.A., Umhau, J., Pavon, F.J., Ruiz-Velasco, V., Margas, W., Sun, H., Damadzic, R., Eskay, R., Schoor, M., Thorsell, A. et al. (2011) A genetic determinant of the striatal dopamine response to alcohol in men. Mol. Psychiatry, 16, 809-817.
21. Wang, Y.J., Huang, P., Ung, A., Blendy, J.A. and Liu-Chen, L.Y. (2012) Reduced expression of the mu opioid receptor in some, but not all, brain regions in mice with Oprm1 A112G. Neuroscience, 205, 178-184.
22. Nielsen, D.A., Yuferov, V., Hamon, S., Jackson, C., Ho, A., Ott, J. and Kreek, M.J. (2009) Increased OPRM1 DNA methylation in lymphocytes of methadone-maintained former heroin addicts. Neuropsychopharmacology, 34, 867-873.
23. Oertel, B.G., Preibisch, C., Martin, T., Walter, C., Gamer, M., Deichmann, R. and Lötsch, J. (2011) Separating brain processing of pain from that of stimulus intensity. Hum. Brain Mapp., 33, 883-894.
24. Stefanidou, M., Athanaselis, S., Spiliopoulou, C., Dona, A. and Maravelias, C. (2010) Biomarkers of opiate use. Int. J. Clin. Pract., 64, 1712-1718.
25. Bird, A.P. (1986) CpG-rich islands and the function of DNA methylation. Nature, 321, 209-213.
26. Hsieh, C.L. (1994) Dependence of transcriptional repression on CpG methylation density. Mol. Cell Biol., 14, 5487-5494.
27. Hwang, C.K., Song, K.Y., Kim, C.S., Choi, H.S., Guo, X.H., Law, P.Y., Wei, L.N. and Loh, H.H. (2007) Evidence of endogenous mu opioid receptor regulation by epigenetic control of the promoters. Mol. Cell Biol., 27, 4720-4736.
28. Vucetic, Z., Kimmel, J. and Reyes, T.M. (2011) Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology, 36, 1199-1206.
29. Hao, Y., Huang, W., Nielsen, D.A. and Kosten, T.A. (2011) Litter gender composition and sex affect maternal behavior and DNA methylation levels of the oprm1 gene in rat offspring. Front Psychiatry, 2, 21.
30. Chorbov, V.M., Todorov, A.A., Lynskey, M.T. and Cicero, T.J. (2011) Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. J. Opioid Manag., 7, 258-264.
31. Jurkowska, R.Z., Anspach, N., Urbanke, C., Jia, D., Reinhardt, R., Nellen, W., Cheng, X. and Jeltsch, A. (2008) Formation of nucleoprotein filaments by mammalian DNA methyltransferase Dnmt3a in complex with regulator Dnmt3L. Nucleic Acids Res., 36, 6656-6663.
32. Jia, D., Jurkowska, R.Z., Zhang, X., Jeltsch, A. and Cheng, X. (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature, 449, 248-251.
33. Zhang, Y., Rohde, C., Tierling, S., Jurkowski, T.P., Bock, C., Santacruz, D., Ragozin, S., Reinhardt, R., Groth, M., Walter, J. et al. (2009) DNA methylation analysis of chromosome 21 gene promoters at single base pair and single allele resolution. PLoS Genet., 5, e1000438.
34. Tegeder, I., Adolph, J., Schmidt, H., Woolf, C.J., Geisslinger, G. and Lötsch, J. (2008) Reduced hyperalgesia in homozygous carriers of a GTP cyclohydrolase 1 haplotype. Eur. J. Pain, 12, 1069-1077.
35. Tegeder, I., Costigan, M., Griffin, R.S., Abele, A., Belfer, I., Schmidt, H., Ehnert, C., Nejim, J., Marian, C., Scholz, J. et al. (2006) GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat. Med., 12, 1269-1277.
36. Hay, J.L., White, J.M., Bochner, F. and Somogyi, A.A. (2008) Antinociceptive effects of high-dose remifentanil in male methadone-maintained patients. Eur. J. Pain, 12, 926-933.
37. Peles, E., Schreiber, S., Gordon, J. and Adelson, M. (2005) Significantly higher methadone dose for methadone maintenance treatment (MMT) patients with chronic pain. Pain, 113, 340-346.
38. Law, P.Y., Hom, D.S. and Loh, H.H. (1983) Opiate receptor down-regulation and desensitization in neuroblastoma X glioma NG108-15 hybrid cells are two separate cellular adaptation processes. Mol. Pharmacol., 24, 413-424.
39. Yabaluri, N. and Medzihradsky, F. (1997) Down-regulation of mu-opioid receptor by full but not partial agonists is independent of G protein coupling. Mol. Pharmacol., 52, 896-902.
40. Zhang, L., Yu, Y., Mackin, S., Weight, F.F., Uhl, G.R. and Wang, J.B. (1996) Differential mu opiate receptor phosphorylation and desensitization induced by agonists and phorbol esters. J. Biol. Chem., 271, 11449-11454.
41. Schulz, S., Mayer, D., Pfeiffer, M., Stumm, R., Koch, T. and Hollt, V. (2004) Morphine induces terminal micro-opioid receptor desensitization by sustained phosphorylation of serine-375. EMBO J., 23, 3282-3289.
42. Gabilondo, A.M., Meana, J.J., Barturen, F., Sastre, M. and Garcia-Sevilla, J.A. (1994) mu-Opioid receptor and alpha 2-adrenoceptor agonist binding sites in the postmortem brain of heroin addicts. Psychopharmacology, 115, 135-140.
43. Meana, J.J., Gonzalez-Maeso, J., Garcia-Sevilla, J.A. and Guimon, J. (2000) mu-opioid receptor and alpha2-adrenoceptor agonist stimulation of [35S]GTPgammaS binding to G-proteins in postmortem brains of opioid addicts. Mol. Psychiatry, 5, 308-315.
44. Noble, F. and Cox, B.M. (1996) Differential desensitization of mu- and delta- opioid receptors in selected neural pathways following chronic morphine treatment. Br. J. Pharmacol., 117, 161-169.
45. Skarke, C., Kirchhof, A., Geisslinger, G. and Lötsch, J. (2004) Comprehensive mu-opioid-receptor genotyping by pyrosequencing. Clin. Chem., 50, 640-644.
46. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
47. Wang, Y. and Leung, F.C. (2004) An evaluation of new criteria for CpG islands in the human genome as gene markers. Bioinformatics, 20, 1170-1177.
48. Hardy, G.H. (1908) Mendelian proportions in a mixed population. Science, 28, 49-50.