Epigenetically modified nucleotides in chronic heroin and cocaine treated mice

Toxicology Letters

Volumn 229, Issue 3, 2014, Pages 451-457

  Chao, Mu Rong ^a,b   Fragou, Domniki ^c   Zanos, Panos ^d   Hu, Chiung Wen ^a   Bailey, Alexis ^d   Kouidou, Sofia ^c   Kovatsi, Leda ^c  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^d UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

5 Hydroxymethylcytosine; 5 Methylcytosine; Addiction; Cocaine; Epigenetics; Heroin

Indexed keywords

5-HYDROXYMETHYLCYTOSINE; 5-METHYLCYTOSINE; ADDICTION; COCAINE; EPIGENETICS; HEROIN;

5-METHYLCYTOSINE; ANIMALS; BRAIN; BRAIN CHEMISTRY; COCAINE; CYTOSINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPIGENESIS, GENETIC; HEROIN; LIVER; MALE; MICE; MICE, INBRED C57BL;

EID: 84905394260     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.07.023     Document Type: Article

References (60)

1. Anier K., Zharkovsky A., Kalda A. S-adenosylmethionine modifies cocaine-induced DNA methylation and increases locomotor sensitization in mice. Int. J. Neuropsychopharmacol. 2013, 16:2053-2066.
2. Bailey A., Gianotti R., Ho A., Kreek M.J. Persistent upregulation of mu-opioid, but not adenosine, receptors in brains of long-term withdrawn escalating dose binge cocaine-treated rats. Synapse 2005, 57:160-166.
3. Bailey A., Yuferov V., Bendor J., Schlussman S.D., Zhou Y., Ho A., Kreek M.J. Immediate withdrawal from chronic binge cocaine administration increases mu-opioid receptor mRNA levels in rat frontal cortex. Brain Res. Mol. Brain Res. 2005, 137:258-262.
4. Bailey A., Gianotti R., Ho A., Kreek M.J. Downregulation of kappa-opioid receptors in basolateral amygdala and septum of rats withdrawn for 14 days from an escalating dose binge cocaine administration paradigm. Synapse 2007, 61:820-826.
5. Bailey A., Metaxas A., Yoo J.H., McGee T., Kitchen I. Decrease of D2 receptor binding but increase in D2-stimulated G-protein activation dopamine transporter binding and behavioural sensitization in brains of mice treated with a chronic escalating dose 'binge' cocaine administration paradigm. Eur. J. Neurosci. 2008, 28:759-770.
6. Bailey A., Metaxas A., Al-Hasani R., Keyworth H.L., Forster D.M., Kitchen I. Mouse strain differences in locomotor sensitisation and rewarding effect of heroin; association with alterations in MOP-r activation and dopamine transporter binding. Eur. J. Neurosci. 2010, 31:742-753.
7. Barros M., Dempster E.L., Illott N., Chabrawi S., Maior R.S., Tomaz C., Silva M.A., Huston J.P., Mill J., Muller C.P. Decreased methylation of the NK3 receptor coding gene (TACR3) after cocaine-induced place preference in marmoset monkeys. Addict. Biol. 2013, 18:452-454.
8. Bart G., Heilig M., LaForge K.S., Pollak L., Leal S.M., Ott J., Kreek M.J. Substantial attributable risk related to a functional mu-opioid receptor gene polymorphism in association with heroin addiction in central Sweden. Mol. Psychiatry 2004, 9:547-549.
9. Carouge D., Host L., Aunis D., Zwiller J., Anglard P. CDKL5 is a brain MeCP2 target gene regulated by DNA methylation. Neurobiol. Dis. 2010, 38:414-424.
10. Chia N., Wang L., Lu X., Senut M.C., Brenner C., Ruden D.M. Hypothesis: environmental regulation of 5-hydroxymethylcytosine by oxidative stress. Epigenetics 2011, 6:853-856.
11. Chorbov V.M., Todorov A.A., Lynskey M.T., Cicero T.J. Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. J. Opioid Manag. 2011, 7:258-264.
12. Fragou A., Kovatsi L., Kouidou S. DNA methylation and specific sequence motifs: association with genetic instability in p53 in cancer, and other loci in degenerative disorders and aging. Arist. Univ. Med. J. 2007, 34:41-48.
13. Fragou D., Fragou A., Kouidou S., Njau S., Kovatsi L. Epigenetic mechanisms in metal toxicity. Toxicol. Mech. Methods 2011, 21:343-352.
14. Fragou D., Zanos P., Kouidou S., Njau S., Kitchen I., Bailey A., Kovatsi L. Effect of chronic heroin and cocaine administration on global DNA methylation in brain and liver. Toxicol. Lett. 2013, 218:260-265.
15. Fuke C., Shimabukuro M., Petronis A., Sugimoto J., Oda T., Miura K., Miyazaki T., Ogura C., Okazaki Y., Jinno Y. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann. Hum. Genet. 2004, 68:196-204.
16. Gorelick D.A., Kim Y.K., Bencherif B., Boyd S.J., Nelson R., Copersino M., Endres C.J., Dannals R.F., Frost J.J. Imaging brain mu-opioid receptors in abstinent cocaine users: time course and relation to cocaine craving. Biol. Psychiatry 2005, 57:1573-1582.
17. Handy D.E., Castro R., Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation 2011, 123:2145-2156.
18. Hope B.T., Skinner M.K., Kenny P.J., Akbarian S. Exploring the epigenetics of cocaine resistance. Nat. Med. 2013, 19:136-137.
19. Hu C.W., Lee H., Chen J.L., Li Y.J., Chao M.R. Optimization of global DNA methylation measurement by LC-MS/MS and its application in lung cancer patients. Anal. Bioanal. Chem. 2013, 405:8859-8869.
20. Hu, C.W., Chen, J.L., Hsu Y.W., Yen C.C., Chao, M.R., 2014. Trace analysis of methylated and hydroxymethylated cytosines in DNA by isotope-dilution LC-MS/MS: first evidence of DNA methylation in Caenorhabditis elegans (submitted for publication).
21. Ivanov M., Kals M., Kacevska M., Barragan I., Kasuga K., Rane A., Metspalu A., Milani L., Ingelman-Sundberg M. Ontogeny, distribution and potential roles of 5-hydroxymethylcytosine in human liver function. Genome Biol. 2013, 14:R83.
22. Jayanthi S., McCoy M.T., Chen B., Britt J.P., Kourrich S., Yau H.J., Ladenheim B., Krasnova I.N., Bonci A., Cadet J.L. Methamphetamine downregulates striatal glutamate receptors via diverse epigenetic mechanisms. Biol. Psychiatry 2013, 76:47-56.
23. Khare T., Pai S., Koncevicius K., Pal M., Kriukiene E., Liutkeviciute Z., Irimia M., Jia P., Ptak C., Xia M., Tice R., Tochigi M., Morera S., Nazarians A., Belsham D., Wong A.H., Blencowe B.J., Wang S.C., Kapranov P., Kustra R., Labrie V., Klimasauskas S., Petronis A. 5-hmC in the brain is abundant in synaptic genes and shows differences at the exon-intron boundary. Nat. Struct. Mol. Biol. 2012, 19:1037-1043.
24. Kouidou S., Kovatsi L., Ioannou A. Seeking the 5th base of DNA using chromatographic methods of analysis. Curr. Org. Chem. 2010, 14:2268-2281.
25. Kovatsi L., Fragou D., Samanidou V., Njau S., Kouidou S. Drugs of abuse: epigenetic mechanisms in toxicity and addiction. Curr. Med. Chem. 2011, 18:1765-1774.
26. Kreek M.J., LaForge K.S., Butelman E. Pharmacotherapy of addictions. Nat. Rev. Drug Discov. 2002, 1:710-726.
27. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
28. Laird A., Thomson J.P., Harrison D.J., Meehan R.R. 5-Hydroxymethylcytosine profiling as an indicator of cellular state. Epigenomics 2013, 5:655-669.
29. Liu C., Liu L., Chen X., Shen J., Shan J., Xu Y., Yang Z., Wu L., Xia F., Bie P., Cui Y., Bian X.W., Qian C. Decrease of 5-hydroxymethylcytosine is associated with progression of hepatocellular carcinoma through downregulation of TET1. PLoS One 2013, 8:e62828.
30. Maze I., Feng J., Wilkinson M.B., Sun H., Shen L., Nestler E.J. Cocaine dynamically regulates heterochromatin and repetitive element unsilencing in nucleus accumbens. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3035-3040.
31. Meyer K., Zhang H., Zhang L. Direct effect of cocaine on epigenetic regulation of PKCepsilon gene repression in the fetal rat heart. J. Mol. Cell. Cardiol. 2009, 47:504-511.
32. Muller D.L., Unterwald E.M. In vivo regulation of extracellular signal-regulated protein kinase (ERK) and protein kinase B (Akt) phosphorylation by acute and chronic morphine. J. Pharmacol. Exp. Ther. 2004, 310:774-782.
33. Nestler E.J. Epigenetic mechanisms of drug addiction. Neuropharmacology 2014, 76 Pt. B:259-268.
34. Nestor C.E., Ottaviano R., Reddington J., Sproul D., Reinhardt D., Dunican D., Katz E., Dixon J.M., Harrison D.J., Meehan R.R. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 2012, 22:467-477.
35. Nielsen D.A., Yuferov V., Hamon S., Jackson C., Ho A., Ott J., Kreek M.J. Increased OPRM1 DNA methylation in lymphocytes of methadone-maintained former heroin addicts. Neuropsychopharmacology 2009, 34:867-873.
36. Nielsen D.A., Hamon S., Yuferov V., Jackson C., Ho A., Ott J., Kreek M.J. Ethnic diversity of DNA methylation in the OPRM1 promoter region in lymphocytes of heroin addicts. Hum. Genet. 2010, 127:639-649.
37. Nielsen D.A., Huang W., Hamon S.C., Maili L., Witkin B.M., Fox R.G., Cunningham K.A., Moeller F.G. Forced abstinence from cocaine self-administration is associated with DNA methylation changes in myelin genes in the corpus callosum: a preliminary study. Front Psychiatry 2012, 3:60.
38. Nielsen D.A., Utrankar A., Reyes J.A., Simons D.D., Kosten T.R. Epigenetics of drug abuse: predisposition or response. Pharmacogenomics 2012, 13:1149-1160.
39. Novikova S.I., He F., Bai J., Cutrufello N.J., Lidow M.S., Undieh A.S. Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS One 2008, 3:e1919.
40. Oertel B.G., Doehring A., Roskam B., Kettner M., Hackmann N., Ferreiros N., Schmidt P.H., Lotsch J. Genetic-epigenetic interaction modulates mu-opioid receptor regulation. Hum. Mol. Genet. 2012, 21:4751-4760.
41. Pfeifer G.P., Kadam S., Jin S.G. 5-Hydroxymethylcytosine and its potential roles in development and cancer. Epigenetics Chromatin 2013, 6. 10.1186/1756-8935-6-10.
42. Pol Bodetto S., Carouge D., Fonteneau M., Dietrich J.B., Zwiller J., Anglard P. Cocaine represses protein phosphatase-1Cbeta through DNA methylation and methyl-CpG binding protein-2 recruitment in adult rat brain. Neuropharmacology 2013, 73:31-40.
43. Richardson B. DNA methylation and autoimmune disease. Clin. Immunol. 2003, 109:72-79.
44. Schlussman S.D., Zhou Y., Bailey A., Ho A., Kreek M.J. Steady-dose and escalating-dose binge administration of cocaine alter expression of behavioral stereotypy and striatal preprodynorphin mRNA levels in rats. Brain Res. Bull. 2005, 67:169-175.
45. Schmidt H.D., McGinty J.F., West A.E., Sadri-Vakili G. Epigenetics and psychostimulant addiction. Cold Spring Harb. Perspect. Med. 2013, 3:a012047.
46. Shimabukuro M., Jinno Y., Fuke C., Okazaki Y. Haloperidol treatment induces tissue- and sex-specific changes in DNA methylation: a control study using rats. Behav. Brain Funct. 2006, 2:37.
47. Shirazi J., Shah S., Sagar D., Nonnemacher M.R., Wigdahl B., Khan Z.K., Jain P. Epigenetics, drugs of abuse, and the retroviral promoter. J. Neuroimmune Pharmacol. 2013, 8:1181-1196.
48. Song C.X., Szulwach K.E., Fu Y., Dai Q., Yi C., Li X., Li Y., Chen C.H., Zhang W., Jian X., Wang J., Zhang L., Looney T.J., Zhang B., Godley L.A., Hicks L.M., Lahn B.T., Jin P., He C. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol. 2011, 29:68-72.
49. Spanagel R. Modulation of drug-induced sensitization processes by endogenous opioid systems. Behav. Brain Res. 1995, 70:37-49.
50. Spellicy C.J., Kosten T.R., Hamon S.C., Harding M.J., Nielsen D.A. The MTHFR C677T variant is associated with responsiveness to disulfiram treatment for cocaine dependency. Front Psychiatry 2013, 3:109.
51. Sun H., Maze I., Dietz D.M., Scobie K.N., Kennedy P.J., Damez-Werno D., Neve R.L., Zachariou V., Shen L., Nestler E.J. Morphine epigenomically regulates behavior through alterations in histone H3 lysine 9 dimethylation in the nucleus accumbens. J. Neurosci. 2012, 32:17454-17464.
52. Taylor S.E., Smeriglio P., Dhulipala L., Rath M., Bhutani N. A global increase in 5-hydroxymethylcytosine levels marks osteoarthritic chondrocytes. Arthritis Rheumatol. 2014, 66:90-100.
53. Tian W., Zhao M., Li M., Song T., Zhang M., Quan L., Li S., Sun Z.S. Reversal of cocaine-conditioned place preference through methyl supplementation in mice: altering global DNA methylation in the prefrontal cortex. PLoS One 2012, 7:e33435.
54. Tsukada H., Kreuter J., Maggos C.E., Unterwald E.M., Kakiuchi T., Nishiyama S., Futatsubashi M., Kreek M.J. Effects of binge pattern cocaine administration on dopamine D1 and D2 receptors in the rat brain: an in vivo study using positron emission tomography. J. Neurosci. 1996, 16:7670-7677.
55. Unterberger A., Szyf M., Nathanielsz P.W., Cox L.A. Organ and gestational age effects of maternal nutrient restriction on global methylation in fetal baboons. J. Med. Primatol. 2009, 38:219-227.
56. Yao B., Lin L., Street R.C., Zalewski Z.A., Galloway J.N., Wu H., Nelson D.L., Jin P. Genome-wide alteration of 5-hydroxymethylcytosine in a mouse model of fragile X-associated tremor/ataxia syndrome. Hum. Mol. Genet. 2014, 23:1095-1107.
57. Yoo J.H., Kitchen I., Bailey A. The endogenous opioid system in cocaine addiction: what lessons have opioid peptide and receptor knockout mice taught us?. Br. J. Pharmacol. 2012, 166:1993-2014.
58. Yuferov V., Levran O., Proudnikov D., Nielsen D.A., Kreek M.J. Search for genetic markers and functional variants involved in the development of opiate and cocaine addiction and treatment. Ann. N. Y. Acad. Sci. 2010, 1187:184-207.
59. Zhang H., Darwanto A., Linkhart T.A., Sowers L.C., Zhang L. Maternal cocaine administration causes an epigenetic modification of protein kinase Cepsilon gene expression in fetal rat heart. Mol. Pharmacol. 2007, 71:1319-1328.
60. Zhang H., Meyer K.D., Zhang L. Fetal exposure to cocaine causes programming of Prkce gene repression in the left ventricle of adult rat offspring. Biol. Reprod. 2009, 80:440-448.