Antipsychotic drugs attenuate aberrant DNA methylation of DTNBP1 (dysbindin) promoter in saliva and post-mortem brain of patients with schizophrenia and Psychotic bipolar disorder

American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics

Volumn 168, Issue 8, 2015, Pages 687-696

  Abdolmaleky, Hamid M ^a,b   Pajouhanfar, Sara ^b   Faghankhani, Masoomeh ^c   Joghataei, Mohammad Taghi ^d   Mostafavi, Ashraf ^e   Thiagalingam, Sam ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e Arian Salamat Counseling and Nursing Cervices Center   (Iran)

Author keywords

DNA methylation; DTNBP1; Post mortem brain; Saliva; Schizophrenia

Indexed keywords

DYSBINDIN; GENOMIC DNA; LITHIUM; NEUROLEPTIC AGENT; REELIN; SEROTONIN 2A RECEPTOR; TRANSCRIPTION FACTOR SP1; VALPROIC ACID; DNA; DTNBP1 PROTEIN, HUMAN; DYSTROPHIN ASSOCIATED PROTEIN;

ARTICLE; AUTOPSY; BINDING AFFINITY; BINDING SITE; BIPOLAR DISORDER; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CPG ISLAND; DEPRESSIVE PSYCHOSIS; DNA METHYLATION; DNA SEQUENCE; DTNBP1 GENE; EPIGENETICS; FIRST DEGREE RELATIVE; GENE EXPRESSION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC RISK; HTR2A GENE; HUMAN; HUMAN TISSUE; NEUROPATHOLOGY; ONSET AGE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE METHYLATION SPECIFIC POLYMERASE CHAIN REACTION; RELN GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVA ANALYSIS; SCHIZOPHRENIA; TREND STUDY; BRAIN CHEMISTRY; CASE CONTROL STUDY; CHEMISTRY; DRUG EFFECTS; FEMALE; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; ISOLATION AND PURIFICATION; MALE; MIDDLE AGED; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SALIVA;

ANTIPSYCHOTIC AGENTS; BASE SEQUENCE; BIPOLAR DISORDER; BRAIN CHEMISTRY; CASE-CONTROL STUDIES; CPG ISLANDS; DNA; DNA METHYLATION; DYSTROPHIN-ASSOCIATED PROTEINS; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SALIVA; SCHIZOPHRENIA;

EID: 84947019946     PISSN: 15524841     EISSN: 1552485X     Source Type: Journal    
DOI: 10.1002/ajmg.b.32361     Document Type: Article

References (52)

1. Abdolmaleky HM, Cheng KH, Russo A, Smith CL, Faraone SV, Wilcox M, Shafa R, Glatt SJ, Nguyen G, Ponte JF, Thiagalingam S, Tsuang MT. 2005. Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: A preliminary report. Am J Med Genetics Part B Neuropsychiatr Genet 134B:60-66.
2. Abdolmaleky HM, Cheng KH, Faraone SV, Wilcox M, Glatt SJ, Gao F, Smith CL, Shafa R, Aeali B, Carnevale J, Pan H, Papageorgis P, Ponte JF, Sivaraman V, Tsuang MT, Thiagalingam S. 2006. Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Hum Mol Genet 15:3132-3145.
3. Abdolmaleky HM, Smith CL, Zhou RJ, Thiagalingam S. 2008. Epigenetic alterations of dopaminergic system in major psychiatric disorders. In: Yan Q, editor. Pharmacogenomics in drug discovery and development. Totowa, NJ: Humana Press. pp 187-212.
4. Abdolmaleky HM, Yaqubi S, Papageorgis P, Lambert AW, Ozturk S, Sivaraman V, Thiagalingam S. 2011. Epigenetic dysregulation of HTR2A in the brain of patients with schizophrenia and bipolar disorder. Schizophr Res 129:183-190.
5. Abdolmaleky HM, Nohesara S, Ghadirivasfi M, Lambert AW, Ahmadkhaniha H, Ozturk S, Wong CK, Shafa R, Mostafavi A, Thiagalingam S. 2014. Hypermethylation of serotonin transporter gene in drug naïve patients with schizophrenia. Schizophr Res 152:373-380.
6. Aberg KA, McClay JL, Nerella S, Clark S, Kumar G, Chen W, Khachane AN, Xie L, Hudson A, Gao G, Harada A, Hultman CM, Sullivan PF, Magnusson PK, van den Oord EJ. 2014. Methylome-wide association study of schizophrenia: Identifying blood biomarker signatures of environmental insults. JAMA Psychiatry 71:255-264.
7. Allen NC, Bagade S, McQueen MB, Ioannidis JP, Kavvoura FK, Khoury MJ, Tanzi RE, Bertram L. 2008. Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: The SzGene database. Nat Genet 40:827-834.
8. Ben-Shachar D, Karry R. 2007. Sp1 expression is disrupted in schizophrenia; a possible mechanism for the abnormal expression of mitochondrial complex I genes, NDUFV1 and NDU FV2. PLoS One 2:e817.
9. Benson MA, Newey SE, Martin-Rendon E, Hawkes R, Blake DJ. 2001. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. J Biol Chem 276:24232-24241.
10. Bhojraj TS, Francis AN, Rajarethinam R, Eack S, Kulkarni S, Prasad KM, Montrose DM, Dworakowski D, Diwadkar V, Keshavan MS. 2009. Verbal fluency deficits and altered lateralization of language brain areas in individuals genetically predisposed to schizophrenia. Schizophr Res 115:202-208.
11. Burdick KE, Lencz T, Funke B, Finn CT, Szeszko PR, Kane JM, Kucherlapati R, Malhotra AK. 2006. Genetic variation in DTNBP1 influences general cognitive ability. Hum Mol Genet 15:1563-1568.
12. Burdick KE, Goldberg TE, Funke B, Bates JA, Lencz T, Kucherlapati R, Malhotra AK. 2007. DTNBP1 genotype influences cognitive decline in schizophrenia. Schizophr Res 89:169-172.
13. Cannon TD, Huttunen MO, Lonnqvist J, Tuulio-Henriksson A, Pirkola T, Glahn D, Finkelstein J, Hietanen M, Kaprio J, Koskenvuo M. 2000. The inheritance of neuropsychological dysfunction in twins discordant schizophrenia. Am J Hum Genet 67:369-382.
14. Carrard A, Salzmann A, Malafosse A, Karege F. 2011. Increased DNA methylation status of the serotonin receptor 5HTR1A gene promoter in schizophrenia and bipolar disorder. J Affect Disord 132:450-453.
15. Chagnon YC, Roy MA, Bureau A, Merette C, Maziade M. 2008. Differential RNA expression between schizophrenic patients and controls of the dystrobrevin binding protein 1 and neuregulin 1 genes in immortalized lymphocytes. Schizophr Res 100:281-290.
16. Folsom TD, Fatemi SH. 2013. The involvement of reelin in neurodevelopmental disorders. Neuropharmacology 68:122-135.
17. Ghadirivasfi M, Nohesara S, Ahmadkhaniha HR, Eskandari MR, Mostafavi S, Thiagalingam S, Abdolmaleky HM. 2011. Hypomethylation of the serotonin receptor type-2A Gene (HTR2A) at T102C polymorphic site in DNA derived from the saliva of patients with schizophrenia and bipolar disorder. Am J Med Genet Part B Neuropsychiatr Genet 156B:536-545.
18. Ghiani CA, Starcevic M, Rodriguez-Fernandez IA, Nazarian R, Cheli VT, Chan LN, Malvar JS, de Vellis J, Sabatti C, Dell'Angelica EC. 2010. The dysbindin-containing complex (BLOC-1) in brain: Developmental regulation, interaction with SNARE proteins and role in neurite outgrowth. Mol Psychiatry 15:204-215.
19. Gokhale A, Mullin AP, Zlatic SA, Easley CA 4th, Merritt ME, Raj N, Larimore J, Gordon DE, Peden AA, Sanyal S, Faundez V. 2015. The N-ethylmaleimide-sensitive factor and dysbindin interact to modulate synaptic plasticity. J Neurosci 35:7643-7653.
20. Gower AC, Steiling K, Brothers JF 2nd, Lenburg ME, Spira A. 2011. Transcriptomic studies of the airway field of injury associated with smoking-related lung disease. Proc Am Thorac Soc 8:173-179.
21. Grayson DR, Jia X, Chen Y, Sharma RP, Mitchell CP, Guidotti A, Costa E. 2005. Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci USA 102:9341-9346.
22. Greenwood TA, Light GA, Swerdlow NR, Radant AD, Braff DL. 2012. Association analysis of 94 candidate genes and schizophrenia-related endophenotypes. PLoS One 7:e29630.
23. Guo AY, Sun J, Riley BP, Thiselton DL, Kendler KS, Zhao Z. 2009. The dystrobrevin-binding protein 1 gene: Features and networks. Mol Psychiatry 14:18-29.
24. Hamshere ML, Walters JT, Smith R, Richards AL, Green E, Grozeva D, Jones I, Forty L, Jones L, Gordon-Smith K, Riley B, O'Neill FA, Kendler KS, Sklar P, Purcell S, Kranz J, Schizophrenia Psychiatric Genome-wide Association Study Consortium, Wellcome Trust Case Control Consortium, Wellcome Trust Case Control Consortium 2, Morris D, Gill M, Holmans P, Craddock N, Corvin A, Owen MJ, O'Donovan MC. 2013. Genome-wide significant associations in schizophrenia to ITIH3/4, CACNA1C and SDCCAG8, and extensive replication of associations reported by the schizophrenia PGC. Mol Psychiatry 18:708-712.
25. Huang HS, Matevossian A, Whittle C, Kim SY, Schumacher A, Baker SP, Akbarian S. 2007. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. J Neurosci 27:11254-11262.
26. Ikegame T, Bundo M, Sunaga F, Asai T, Nishimura F, Yoshikawa A, Kawamura Y, Hibino H, Tochigi M, Kakiuchi C, Sasaki T, Kato T, Kasai K, Iwamoto K. 2013. DNA methylation analysis of BDNF gene promoters in peripheral blood cells of schizophrenia patients. Neurosci Res 77:208-214.
27. Iwamoto K, Bundo M, Yamada K, Takao H, Iwayama-Shigeno Y, Yoshikawa T, Kato T. 2005. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J Neurosci 25:5376-5381.
28. Kordi-Tamandani DM, Sahranavard R, Torkamanzehi A. 2012. DNA methylation and expression profiles of the brain-derived neurotrophic factor (BDNF) and dopamine transporter (DAT1) genes in patients with schizophrenia. Mol Biol Rep 39:10889-10893.
29. Kordi-Tamandani DM, Dahmardeh N, Torkamanzehi A. 2013. Evaluation of hypermethylation and expression pattern of GMR2, GMR5, GMR8, and GRIA3 in patients with schizophrenia. Gene 515:163-166.
30. Lee SA, Kim SM, Suh BK, Sun HY, Park YU, Hong JH, Park C, Nguyen MD, Nagata K, Yoo JY, Park SK. 2015. Disrupted-in-schizophrenia 1 (DISC1) regulates dysbindin function by enhancing its stability. J Biol Chem 290:7087-7096.
31. Li W, Zhang Q, Oiso N, Novak EK, Gautam R, O'Brien EP, Tinsley CL, Blake DJ, Spritz RA, Copeland NG, Jenkins NA, Amato D, Roe BA, Starcevic M, Dell'Angelica EC, Elliott RW, Mishra V, Kingsmore SF, Paylor RE, Swank RT. 2003. Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat Genet 35:84-89.
32. Luciano M, Miyajima F, Lind PA, Bates TC, Horan M, Harris SE, Wright MJ, Ollier WE, Hayward C, Pendleton N, Gow AJ, Visscher PM, Starr JM, Deary IJ, Martin NG, Payton A. 2009. Variation in the dysbindin gene and normal cognitive function in three independent population samples. Genes Brain Behav 8:218-227.
33. Markov V, Krug A, Krach S, Whitney C, Eggermann T, Zerres K, Stöcker T, Shah NJ, Nöthen MM, Treutlein J, Rietschel M, Kircher T. 2009. Genetic variation in schizophrenia-risk-gene dysbindin 1 modulates brain activation in anterior cingulate cortex and right temporal gyrus during language production in healthy individuals. NeuroImage 47:2016-2022.
34. Meltzer HY. 1999. Outcome in schizophrenia: Beyond symptom reduction. J Clinical Psychiatry 60:3-7.
35. Mill J, Tang T, Kaminsky Z, Khare T, Yazdanpanah S, Bouchard L, Jia P, Assadzadeh A, Flanagan J, Schumacher A, Wang SC, Petronis A. 2008. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am J Hum Genet 82:696-711.
36. Mittal VA, Ellman LM, Cannon TD. 2008. Gene-environment interaction and covariation in schizophrenia: The role of obstetric complications. Schizophr Bull 34:1083-1094.
37. Modinos G, Iyegbe C, Prata D, Rivera M, Kempton MJ, Valmaggia LR, Sham PC, van Os J, McGuire P. 2013. Molecular genetic gene-environment studies using candidate genes in schizophrenia: A systematic review. Schizophr Res 150:356-365.
38. Nicodemus KK, Marenco S, Batten AJ, Vakkalanka R, Egan MF, Straub RE, Weinberger DR. 2008. Serious obstetric complications interact with hypoxia-regulated/vascular-expression genes to influence schizophrenia risk. Mol Psychiatry 13:873-877.
39. Nohesara S, Ghadirivasfi M, Mostafavi S, Eskandari MR, Ahmadkhaniha H, Thiagalingam S, Abdolmaleky HM. 2011. DNA hypomethylation of MB-COMT promoter in the DNA derived from saliva in schizophrenia and bipolar disorder. J Psychiatr Res 45:1432-1438.
40. Nuechterlein KH, Dawson ME. 1984. Information processing and attentional functioning in the developmental course of schizophrenic disorders. Schizophr Bull 10:160-203.
41. Papaleo F, Burdick MC, Callicott JH, Weinberger DR. 2014. Epistatic interaction between COMT and DTNBP1 modulates prefrontal function in mice and in humans. Mol Psychiatry 19:311-316.
42. Pun FW, Zhao C, Lo WS, Ng SK, Tsang SY, Nimgaonkar V, Chung WS, Ungvari GS, Xue H. 2011. Imprinting in the schizophrenia candidate gene GABRB2 encoding GABA(A) receptor beta(2) subunit. Mol Psychiatry 16:557-568.
43. Stefanis NC, Trikalinos TA, Avramopoulos D, Smyrnis N, Evdokimidis I, Ntzani EE, Ioannidis JP, Stefanis CN. 2007. Impact of schizophrenia candidate genes on schizotypy and cognitive endophenotypes at the population level. Biol Psychiatry 62:784-792.
44. Straub RE, Jiang Y, MacLean CJ, Ma Y, Webb BT, Myakishev MV, Harris-Kerr C, Wormley B, Sadek H, Kadambi B, Cesare AJ, Gibberman A, Wang X, O'Neill FA, Walsh D, Kendler KS. 2002. Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. Am J Hum Genet 71:337-348.
45. Talbot K, Cho DS, Ong WY, Benson MA, Han LY, Kazi HA, Kamins J, Hahn CG, Blake DJ, Arnold SE. 2006. Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum Mol Genet 15:3041-3054.
46. Talbot K, Blake OW, Tang DJ, Louneva J, Carlson N, Arnold GC, . 2009. Dysbindin-1 and its protein family. In: Javitt D, Kantrowitz J, editors. Schizophrenia. New York, USA: Springer Science+Business Media, LLC. pp 110-241.
47. Tolosa A, Sanjuan J, Dagnall AM, Molto MD, Herrero N, de Frutos R. 2010. FOXP2 gene and language impairment in schizophrenia: Association and epigenetic studies. BMC Med Genet 11:114.
48. Wall PM, Messier C. 2001. The hippocampal formation-orbitomedial prefrontal cortex circuit in the attentional control of active memory. Behav Brain Res 127:99-117.
49. Weickert CS, Straub RE, McClintock BW, Matsumoto M, Hashimoto R, Hyde TM, Herman MM, Weinberger DR, Kleinman JE. 2004. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch Gen Psychiatry 61:544-555.
50. Wockner LF, Noble EP, Lawford BR, Young RM, Morris CP, Whitehall VL, Voisey J. 2014. Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients. Transl Psychiatry 4:e339.
51. Xiao Y, Camarillo C, Ping Y, Arana TB, Zhao H, Thompson PM, Xu C, Su BB, Fan H, Ordonez J, Wang L, Mao C, Zhang Y, Cruz D, Escamilla MA, Li X, Xu C. 2014. The DNA methylome and transcriptome of different brain regions in schizophrenia and bipolar disorder. PLoS One 9:e95875.
52. Zhang JP, Burdick KE, Lencz T, Malhotra AK. 2010. Meta-analysis of genetic variation in DTNBP1 and general cognitive ability. Biol Psychiatry 68:1126-1133.