Elevated methylation and decreased serum concentrations of BDNF in patients in levomethadone compared to diamorphine maintenance treatment

European Archives of Psychiatry and Clinical Neuroscience

Volumn 267, Issue 1, 2017, Pages 33-40

  Schuster, Rilana ^a,b   Kleimann, Alexandra ^b   Rehme, Marie Kathrin ^b   Taschner, Leonie ^b   Glahn, Alexander ^b   Groh, Adrian ^b   Frieling, Helge ^b   Lichtinghagen, Ralf ^b   Hillemacher, Thomas ^b   Bleich, Stefan ^b   Heberlein, Annemarie ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

BDNF; Brain derived neurotrophic factor; DNA methylation; Epigenetic regulation; Opiate dependence; Opiate maintenance

Indexed keywords

ALCOHOL; AMPHETAMINE DERIVATIVE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABIS; COCAINE; DIAMORPHINE; GENOMIC DNA; LEVOMETHADONE; MESSENGER RNA; METHAMPHETAMINE; MIDOMAFETAMINE; METHADONE; NARCOTIC ANALGESIC AGENT;

ADULT; ARTICLE; BECK DEPRESSION INVENTORY; CANNABIS USE; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; DRUG EFFICACY; DRUG USE; EPIGENETICS; EXON; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; MAINTENANCE THERAPY; MAJOR CLINICAL STUDY; MALE; METHADONE TREATMENT; OPIATE ADDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; SMOKING; TOBACCO USE; TREATMENT RESPONSE; BLOOD; CASE CONTROL STUDY; DEPRESSION; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; METHYLATION; MIDDLE AGED; NONPARAMETRIC TEST; OPIOID-RELATED DISORDERS; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; QUESTIONNAIRE; VISUAL ANALOG SCALE;

ADULT; ANALGESICS, OPIOID; BRAIN-DERIVED NEUROTROPHIC FACTOR; CASE-CONTROL STUDIES; DEPRESSION; EPIGENESIS, GENETIC; FEMALE; HEROIN; HUMANS; MALE; METHADONE; METHYLATION; MIDDLE AGED; OPIOID-RELATED DISORDERS; PROMOTER REGIONS, GENETIC; PROSPECTIVE STUDIES; PSYCHIATRIC STATUS RATING SCALES; STATISTICS, NONPARAMETRIC; SURVEYS AND QUESTIONNAIRES; VISUAL ANALOG SCALE;

EID: 84955243815     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-016-0668-7     Document Type: Article

References (51)

1. Autry AE, Monteggia LM (2012) Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev 64(2):238–258. doi:10.1124/pr.111.005108
2. Cowansage KK, LeDoux JE, Monfils MH (2010) Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3(1):12–29
3. Mitchelmore C, Gede L (2014) Brain derived neurotrophic factor: epigenetic regulation in psychiatric disorders. Brain Res 1586:162–172. doi:10.1016/j.brainres.2014.06.037
4. Huang Y, Doherty JJ, Dingledine R (2002) Altered histone acetylation at glutamate receptor 2 and brain-derived neurotrophic factor genes is an early event triggered by status epilepticus. J Neurosci 22(19):8422–8428
5. Lubin FD, Roth TL, Sweatt JD (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28(42):10576–10586. doi:10.1523/JNEUROSCI.1786-08.2008
6. Suri D, Veenit V, Sarkar A, Thiagarajan D, Kumar A, Nestler EJ, Galande S, Vaidya VA (2013) Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol Psychiatry 73(7):658–666. doi:10.1016/j.biopsych.2012.10.023
7. Tadic A, Muller-Engling L, Schlicht KF, Kotsiari A, Dreimuller N, Kleimann A, Bleich S, Lieb K, Frieling H (2014) Methylation of the promoter of brain-derived neurotrophic factor exon IV and antidepressant response in major depression. Mol Psychiatry 19(3):281–283. doi:10.1038/mp.2013.58
8. Kleimann A, Kotsiari A, Sperling W, Groschl M, Heberlein A, Kahl KG, Hillemacher T, Bleich S, Kornhuber J, Frieling H (2015) BDNF serum levels and promoter methylation of BDNF exon I, IV and VI in depressed patients receiving electroconvulsive therapy. J Neural Transm (Vienna) 122(6):925–928. doi:10.1007/s00702-014-1336-6
9. Bumb JM, Aksay SS, Janke C, Kranaster L, Geisel O, Gass P, Hellweg R, Sartorius A (2015) Focus on ECT seizure quality: serum BDNF as a peripheral biomarker in depressed patients. Eur Arch Psychiatry Clin Neurosci 265(3):227–232. doi:10.1007/s00406-014-0543-3
10. Koo JW, Mazei-Robison MS, LaPlant Q, Egervari G, Braunscheidel KM, Adank DN, Ferguson D, Feng J, Sun H, Scobie KN, Damez-Werno DM, Ribeiro E, Pena CJ, Walker D, Bagot RC, Cahill ME, Anderson SA, Labonte B, Hodes GE, Browne H, Chadwick B, Robison AJ, Vialou VF, Dias C, Lorsch Z, Mouzon E, Lobo MK, Dietz DM, Russo SJ, Neve RL, Hurd YL, Nestler EJ (2015) Epigenetic basis of opiate suppression of Bdnf gene expression in the ventral tegmental area. Nat Neurosci 18(3):415–422. doi:10.1038/nn.3932
11. Moonat S, Sakharkar AJ, Zhang H, Pandey SC (2011) The role of amygdaloid brain-derived neurotrophic factor, activity-regulated cytoskeleton-associated protein and dendritic spines in anxiety and alcoholism. Addict Biol 16(2):238–250. doi:10.1111/j.1369-1600.2010.00275.x
12. Roth TL, Sweatt JD (2011) Epigenetic marking of the BDNF gene by early-life adverse experiences. Horm Behav 59(3):315–320. doi:10.1016/j.yhbeh.2010.05.005
13. Gordon HW (2002) Early environmental stress and biological vulnerability to drug abuse. Psychoneuroendocrinology 27(1–2):115–126. doi:10.1016/S0306-4530(01)00039-7
14. Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130. doi:10.1196/annals.1441.030
15. Vargas-Perez H, Bahi A, Bufalino MR, Ting-A-Kee R, Maal-Bared G, Lam J, Fahmy A, Clarke L, Blanchard JK, Larsen BR, Steffensen S, Dreyer JL, van der Kooy D (2014) BDNF signaling in the VTA links the drug-dependent state to drug withdrawal aversions. J Neurosci 34(23):7899–7909. doi:10.1523/JNEUROSCI.3776-13.2014
16. Barker JM, Taylor JR, De Vries TJ, Peters J (2014) Brain-derived neurotrophic factor and addiction: pathological versus therapeutic effects on drug seeking. Brain Res. doi:10.1016/j.brainres.2014.10.058
17. Zilkha N, Feigin E, Barnea-Ygael N, Zangen A (2014) Induction of depressive-like effects by subchronic exposure to cocaine or heroin in laboratory rats. J Neurochem 130(4):575–582. doi:10.1111/jnc.12753
18. Theberge FR, Pickens CL, Goldart E, Fanous S, Hope BT, Liu QR, Shaham Y (2012) Association of time-dependent changes in mu opioid receptor mRNA, but not BDNF, TrkB, or MeCP2 mRNA and protein expression in the rat nucleus accumbens with incubation of heroin craving. Psychopharmacology 224(4):559–571. doi:10.1007/s00213-012-2784-z
19. Angelucci F, Ricci V, Pomponi M, Conte G, Mathe AA, Attilio Tonali P, Bria P (2007) Chronic heroin and cocaine abuse is associated with decreased serum concentrations of the nerve growth factor and brain-derived neurotrophic factor. J Psychopharmacol 21(8):820–825. doi:10.1177/0269881107078491
20. Zhang J, Zhang X, Su H, Tao J, Xie Y, Han B, Lu Y, Wei Y, Sun H, Wang Y, Wu W, Zou S, Liang H, Zoghbi AW, Tang W, He J (2014) Increased serum brain-derived neurotrophic factor levels during opiate withdrawal. Neurosci Lett 571:61–65. doi:10.1016/j.neulet.2014.04.048
21. Heberlein A, Dursteler-MacFarland KM, Lenz B, Frieling H, Grosch M, Bonsch D, Kornhuber J, Wiesbeck GA, Bleich S, Hillemacher T (2011) Serum levels of BDNF are associated with craving in opiate-dependent patients. J Psychopharmacol (Oxford, England) 25(11):1480–1484. doi:10.1177/0269881111411332
22. Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389
23. Kuhner C, Burger C, Keller F, Hautzinger M (2007) Reliability and validity of the Revised Beck Depression Inventory (BDI-II). Results from German samples. Der Nervenarzt 78(6):651–656. doi:10.1007/s00115-006-2098-7
24. Tiffany ST, Carter BL, Singleton EG (2000) Challenges in the manipulation, assessment and interpretation of craving relevant variables. Addiction (Abingdon, England) 95(Suppl 2):S177–S187
25. Gossop M (1990) The development of a Short Opiate Withdrawal Scale (SOWS). Addict Behav 15(5):487–490
26. Lewin J, Schmitt AO, Adorjan P, Hildmann T, Piepenbrock C (2004) Quantitative DNA methylation analysis based on four-dye trace data from direct sequencing of PCR amplificates (Oxford, England). Bioinformatics 20(17):3005–3012. doi:10.1093/bioinformatics/bth346
27. Fan G, Hutnick L (2005) Methyl-CpG binding proteins in the nervous system. Cell Res 15(4):255–261. doi:10.1038/sj.cr.7290294
28. Wade PA (2001) Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20(24):3166–3173. doi:10.1038/sj.onc.1204340
29. Casati A, Piontek D, Pfeiffer-Gerschel T (2014) Patterns of non-compliant buprenorphine, levomethadone, and methadone use among opioid dependent persons in treatment. Subst Abuse Treat Prev Policy 9:19-597X-599-519. doi:10.1186/1747-597X-9-19
30. Heberlein A, Buscher P, Schuster R, Kleimann A, Lichtinghagen R, Rhein M, Kornhuber J, Bleich S, Frieling H, Hillemacher T (2015) Do changes in the BDNF promoter methylation indicate the risk of alcohol relapse? Eur Neuropsychopharmacol. doi:10.1016/j.euroneuro.2015.08.018
31. Havassy BE, Alvidrez J, Owen KK (2004) Comparisons of patients with comorbid psychiatric and substance use disorders: implications for treatment and service delivery. Am J Psychiatry 161(1):139–145
32. Krausz M, Verthein U, Degkwitz P (1998) Prevalence of psychiatric disorders in opiate dependent patients in contact with the drug treatment system. Nervenarzt 69(7):557–567
33. Dixon L (1999) Dual diagnosis of substance abuse in schizophrenia: prevalence and impact on outcomes. Schizophr Res 35(Suppl):S93–100
34. Moller HJ (2005) Occurrence and treatment of depressive comorbidity/cosyndromality in schizophrenic psychoses: conceptual and treatment issues. World J Biol Psychiatry 6(4):247–263. doi:10.1080/15622970500316674
35. Fuchikami M, Morinobu S, Segawa M, Okamoto Y, Yamawaki S, Ozaki N, Inoue T, Kusumi I, Koyama T, Tsuchiyama K, Terao T (2011) DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLoS One 6(8):e23881. doi:10.1371/journal.pone.0023881
36. D’Addario C, Dell’Osso B, Galimberti D, Palazzo MC, Benatti B, Di Francesco A, Scarpini E, Altamura AC, Maccarrone M (2013) Epigenetic modulation of BDNF gene in patients with major depressive disorder. Biol Psychiatry 73(2):e6–e7. doi:10.1016/j.biopsych.2012.07.009
37. Kang HJ, Kim JM, Lee JY, Kim SY, Bae KY, Kim SW, Shin IS, Kim HR, Shin MG, Yoon JS (2013) BDNF promoter methylation and suicidal behavior in depressive patients. J Affect Disord 151(2):679–685. doi:10.1016/j.jad.2013.08.001
38. Verthein U, Ullmann R, Lachmann A, During A, Koch B, Meyer-Thompson HG, Schmidt R, Reimer J, Haasen C (2005) The effects of racemic d, l-methadone and l-methadone in substituted patients—a randomized controlled study. Drug Alcohol Depend 80(2):267–271. doi:10.1016/j.drugalcdep.2005.04.007
39. Soyka M, Zingg C (2009) Feasability and safety of transfer from racemic methadone to (R)-methadone in primary care: clinical results from an open study. J Biol Psychiatry 10(3):217–224. doi:10.1080/15622970802416057
40. Dwivedi Y (2009) Brain-derived neurotrophic factor: role in depression and suicide. Neuropsychiatr Dis Treat 5:433–449
41. Molendijk ML, Spinhoven P, Polak M, Bus BA, Penninx BW, Elzinga BM (2014) Serum BDNF concentrations as peripheral manifestations of depression: evidence from a systematic review and meta-analyses on 179 associations (N = 9484). Mol Psychiatry 19(7):791–800. doi:10.1038/mp.2013.105
42. Ricken R, Adli M, Lange C, Krusche E, Stamm TJ, Gaus S, Koehler S, Nase S, Bschor T, Richter C, Steinacher B, Heinz A, Rapp MA, Borgwardt S, Hellweg R, Lang UE (2013) Brain-derived neurotrophic factor serum concentrations in acute depressive patients increase during lithium augmentation of antidepressants. J Clin Psychopharmacol 33(6):806–809. doi:10.1097/JCP.0b013e3182a412b8
43. Seifert CL, Magon S, Sprenger T, Lang UE, Huber CG, Denier N, Vogel M, Schmidt A, Radue EW, Borgwardt S, Walter M (2015) Reduced volume of the nucleus accumbens in heroin addiction. Eur Arch Psychiatry Clin Neurosci 265(8):637–645. doi:10.1007/s00406-014-0564-y
44. Frischknecht U, Hermann D, Heinrich M, Hoerst M, Weber-Fahr W, Vollstadt-Klein S, Kiefer F, Mann K, Ende G (2013) Experience of social discrimination correlates with neurometabolism: a pilot study in heroin addicts. Eur Arch Psychiatry Clin Neurosci 263(3):197–203. doi:10.1007/s00406-012-0319-6
45. Man LH, Best D, Gossop M, Stillwell G, Strang J (2004) Relationship between prescribing and risk of opiate overdose among drug users in and out of maintenance treatment. Eur Addict Res 10(1):35–40. doi:10.1159/000073724
46. Specka M, Bonnet U, Heilmann M, Schifano F, Scherbaum N (2011) Longitudinal patterns of benzodiazepine consumption in a German cohort of methadone maintenance treatment patients. Hum Psychopharmacol 26(6):404–411. doi:10.1002/hup.1222
47. Angelucci F, Ricci V, Spalletta G, Pomponi M, Tonioni F, Caltagirone C, Bria P (2008) Reduced serum concentrations of nerve growth factor, but not brain-derived neurotrophic factor, in chronic cannabis abusers. Eur Neuropsychopharmacol 18(12):882–887. doi:10.1016/j.euroneuro.2008.07.008
48. Jockers-Scherubl MC, Danker-Hopfe H, Mahlberg R, Selig F, Rentzsch J, Schurer F, Lang UE, Hellweg R (2004) Brain-derived neurotrophic factor serum concentrations are increased in drug-naive schizophrenic patients with chronic cannabis abuse and multiple substance abuse. Neurosci Lett 371(1):79–83. doi:10.1016/j.neulet.2004.08.045
49. Jamal M, Van der Does W, Elzinga BM, Molendijk ML, Penninx BW (2015) Association between smoking, nicotine dependence, and BDNF Val66Met polymorphism with BDNF concentrations in serum. Nicotine Tob Res 17(3):323–329. doi:10.1093/ntr/ntu151
50. Angelucci F, Ricci V, Martinotti G, Palladino I, Spalletta G, Caltagirone C, Bria P (2010) Ecstasy (MDMA)-addicted subjects show increased serum levels of brain-derived neurotrophic factor, independently from a rise of drug-induced psychotic symptoms. Addict Biol 15(3):365–367. doi:10.1111/j.1369-1600.2010.00221.x
51. Chen PH, Huang MC, Lai YC, Chen PY, Liu HC (2014) Serum brain-derived neurotrophic factor levels were reduced during methamphetamine early withdrawal. Addict Biol 19(3):482–485. doi:10.1111/j.1369-1600.2012.00444.x