Lower LINE-1 methylation in first-episode schizophrenia patients with the history of childhood trauma

Epigenomics

Volumn 7, Issue 8, 2015, Pages 1275-1285

  Misiak, Błazej ^a   Szmida, Elzbieta ^a   Karpiński, Paweł ^a   Loska, Olga ^a   Sąsiadek, Maria M ^a   Frydecka, Dorota ^a  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

Author keywords

BAGE; childhood trauma; DNA methylation; first episode schizophrenia; LINE 1; repetitive DNA sequences; stress

Indexed keywords

B MELANOMA ANTIGEN; LINE 1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; BAGE PROTEIN, HUMAN; BIOLOGICAL MARKER; TUMOR ANTIGEN;

ADULT; ARTICLE; CHILDHOOD ADVERSITY; CHILDHOOD INJURY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; EARLY LIFE STRESS; EMOTIONAL ABUSE; FEMALE; FIRST EPISODE SCHIZOPHRENIA; HUMAN; LEUKOCYTE; LIFE EVENT; MALE; MEDICAL HISTORY; NEGATIVE SYNDROME; PHYSICAL PUNISHMENT; POSITIVE AND NEGATIVE SYNDROME SCALE; POSITIVE SYNDROME; PRIORITY JOURNAL; PUNISHMENT; SCHIZOPHRENIA; SEXUAL ABUSE; CASE CONTROL STUDY; COMPLICATION; GENETIC EPIGENESIS; GENETICS; INJURY; LONG INTERSPERSED REPEAT; RISK FACTOR; YOUNG ADULT;

ADULT; ANTIGENS, NEOPLASM; BIOMARKERS; CASE-CONTROL STUDIES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; RISK FACTORS; SCHIZOPHRENIA; WOUNDS AND INJURIES; YOUNG ADULT;

EID: 84950262568     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.15.68     Document Type: Article

References (74)

1. Gil A, Gama CS, De Jesus DR, Lobato MI, Zimmer M, Belmonte-De-Abreu P. The association of child abuse and neglect with adult disability in schizophrenia and the prominent role of physical neglect. Child Abuse Negl. 33(9), 618-624 (2009).
2. Boyette LL, Van Dam D, Meijer C et al. Personality compensates for impaired quality of life and social functioning in patients with psychotic disorders who experienced traumatic events. Schizophr. Bull. 40(6), 1356-1365 (2014).
3. Aas M, Dazzan P, Mondelli V, Melle I, Murray RM, Pariante CM. A systematic review of cognitive function in first-episode psychosis, including a discussion on childhood trauma, stress, and inflammation. Front. Psychiatry 4, 182 (2014).
4. Muenzenmaier KH, Seixas AA, Schneeberger AR, Castille DM, Battaglia J, Link BG. Cumulative effects of stressful childhood experiences on delusions and hallucinations. J. Trauma Dissociation 16(4), 442-462 (2015).
5. Bonoldi I, Simeone E, Rocchetti M et al. Prevalence of self-reported childhood abuse in psychosis: a meta-analysis of retrospective studies. Psychiatry Res. 210(1), 8-15 (2013).
6. Varese F, Smeets F, Drukker M et al. Childhood adversities increase the risk of psychosis: a meta-analysis of patient-control, prospective-and cross-sectional cohort studies. Schizophr. Bull. 38(4), 661-671 (2012).
7. Theleritis C, Fisher HL, Shafer I et al. Brain derived Neurotropic Factor (BDNF) is associated with childhood abuse but not cognitive domains in first episode psychosis. Schizophr. Res. 159(1), 56-61 (2014).
8. Dennison U, Mckernan D, Cryan J, Dinan T. Schizophrenia patients with a history of childhood trauma have a pro-inflammatory phenotype. Psychol. Med. 42(9), 1865-1871 (2012).
9. Mondelli V, Dazzan P, Hepgul N et al. Abnormal cortisol levels during the day and cortisol awakening response in first-episode psychosis: the role of stress and of antipsychotic treatment. Schizophr. Res. 116(2-3), 234-242 (2010).
10. Aas M, Dazzan P, Mondelli V et al. Abnormal cortisol awakening response predicts worse cognitive function in patients with first-episode psychosis. Psychol. Med. 41(3), 463-476 (2011).
11. Misiak B, Kiejna A, Frydecka D. The history of childhood trauma is associated with lipid disturbances and blood pressure in adult first-episode schizophrenia patients. Gen. Hosp. Psychiatry 37(4), 365-367 (2015).
12. Romero LM, Dickens MJ, Cyr NE. The Reactive Scope Model-a new model integrating homeostasis, allostasis, and stress. Horm. Behav. 55(3), 375-389 (2009).
13. Walker EF, Diforio D. Schizophrenia: a neural diathesis-stress model. Psychol. Rev. 104(4), 667-685 (1997).
14. Misiak B, Frydecka D, Zawadzki M, Krefft M, Kiejna A. Refining and integrating schizophrenia pathophysiology-relevance of the allostatic load concept. Neurosci. Biobehav. Rev. 45, 183-201 (2014).
15. Mcgowan PO. Epigenomic mechanisms of early adversity and HPA dysfunction: considerations for PTSD research. Front. Psychiatry 4, 110 (2013).
16. Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ. The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J. Neuroendocrinol. 26(10), 707-723 (2014).
17. Vukojevic V, Kolassa IT, Fastenrath M et al. Epigenetic modification of the glucocorticoid receptor gene is linked to traumatic memory and post-traumatic stress disorder risk in genocide survivors. J. Neurosci. 34(31), 10274-10284 (2014).
18. Yehuda R, Daskalakis NP, Lehrner A et al. Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am. J. Psychiatry 171(8), 872-880 (2014).
19. Labonte B, Azoulay N, Yerko V, Turecki G, Brunet A. Epigenetic modulation of glucocorticoid receptors in posttraumatic stress disorder. Transl. Psychiatry 4, e368 (2014).
20. Klengel T, Mehta D, Anacker C et al. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 16(1), 33-41 (2013).
21. Smith AK, Conneely KN, Kilaru V et al. Differential immune system DNA methylation and cytokine regulation in post-traumatic stress disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 156B(6), 700-708 (2011).
22. Uddin M, Aiello AE, Wildman DE et al. Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc. Natl Acad. Sci. USA 107(20), 9470-9475 (2010).
23. Koenen KC, Uddin M, Chang SC et al. SLC6A4 methylation modifies the effect of the number of traumatic events on risk for posttraumatic stress disorder. Depress. Anxiety 28(8), 639-647 (2011).
24. Labonte B, Suderman M, Maussion G et al. Genome-wide epigenetic regulation by early-life trauma. Arch. Gen. Psychiatry 69(7), 722-731 (2012).
25. Mehta D, Klengel T, Conneely KN et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc. Natl Acad. Sci. USA 110(20), 8302-8307 (2013).
26. Dempster E, Viana J, Pidsley R, Mill J. Epigenetic studies of schizophrenia: progress, predicaments, and promises for the future. Schizophr. Bull. 39(1), 11-16 (2013).
27. Nishioka M, Bundo M, Koike S et al. Comprehensive DNA methylation analysis of peripheral blood cells derived from patients with first-episode schizophrenia. J. Hum. Genet. 58(2), 91-97 (2013).
28. Ota VK, Noto C, Gadelha A et al. Changes in gene expression and methylation in the blood of patients with first-episode psychosis. Schizophr. Res. 159(2-3), 358-364 (2014).
29. Tang H, Dalton CF, Srisawat U, Zhang ZJ, Reynolds GP. Methylation at a transcription factor-binding site on the 5-HT1A receptor gene correlates with negative symptom treatment response in first episode schizophrenia. Int. J. Neuropsychopharmacol. 17(4), 645-649 (2014).
30. Abdolmaleky HM, Nohesara S, Ghadirivasfi M et al. DNA hypermethylation of serotonin transporter gene promoter in drug naive patients with schizophrenia. Schizophr. Res. 152(2-3), 373-380 (2014).
31. Wockner LF, Noble EP, Lawford BR et al. Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients. Transl. Psychiatry 4, e339 (2014).
32. Auta J, Smith RC, Dong E et al. DNA-methylation gene network dysregulation in peripheral blood lymphocytes of schizophrenia patients. Schizophr. Res. 150(1), 312-318 (2013).
33. Murphy BC, O'Reilly RL, Singh SM. Site-specific cytosine methylation in S-COMT promoter in 31 brain regions with implications for studies involving schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 133B(1), 37-42 (2005).
34. Nohesara S, Ghadirivasfi M, Mostafavi S et al. DNA hypomethylation of MB-COMT promoter in the DNA derived from saliva in schizophrenia and bipolar disorder. J. Psychiatr. Res. 45(11), 1432-1438 (2011).
35. Melas PA, Rogdaki M, Osby U, Schalling M, Lavebratt C, Ekstrom TJ. Epigenetic aberrations in leukocytes of patients with schizophrenia: association of global DNA methylation with antipsychotic drug treatment and disease onset. FASEB J. 26(6), 2712-2718 (2012).
36. Shimabukuro M, Sasaki T, Imamura A et al. Global hypomethylation of peripheral leukocyte DNA in male patients with schizophrenia: a potential link between epigenetics and schizophrenia. J. Psychiatr. Res. 41(12), 1042-1046 (2007).
37. Rusiecki JA, Chen L, Srikantan V et al. DNA methylation in repetitive elements and post-traumatic stress disorder: a case-control study of US military service members. Epigenomics 4(1), 29-40 (2012).
38. Capomaccio S, Verini-Supplizi A, Galla G et al. Transcription of LINE-derived sequences in exercise-induced stress in horses. Anim. Genet. 41(2 Suppl.), 23-27 (2010).
39. Li TH, Schmid CW. Differential stress induction of individual Alu loci: implications for transcription and retrotransposition. Gene 276(1-2), 135-141 (2001).
40. Darby MM, Sabunciyan S. Repetitive elements and epigenetic marks in behavior and psychiatric disease. Adv. Genet. 86, 185-252 (2014).
41. Muotri AR, Marchetto MC, Coufal NG et al. L1 retrotransposition in neurons is modulated by MeCP2. Nature 468(7322), 443-446 (2010).
42. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435(7044), 903-910 (2005).
43. Coufal NG, Garcia-Perez JL, Peng GE et al. L1 retrotransposition in human neural progenitor cells. Nature 460(7259), 1127-1131 (2009).
44. Muotri AR, Zhao C, Marchetto MC, Gage FH. Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus 19(10), 1002-1007 (2009).
45. Bundo M, Toyoshima M, Okada Y et al. Increased l1 retrotransposition in the neuronal genome in schizophrenia. Neuron 81(2), 306-313 (2014).
46. Coufal NG, Garcia-Perez JL, Peng GE et al. Ataxia telangiectasia mutated (ATM) modulates long interspersed element-1 (L1) retrotransposition in human neural stem cells. Proc. Natl Acad. Sci. USA 108(51), 20382-20387 (2011).
47. Grunau C, Sanchez C, Ehrlich M et al. Frequent DNA hypomethylation of human juxtacentromeric BAGE loci in cancer. Genes Chromosomes Cancer 43(1), 11-24 (2005).
48. Ruault M, Van Der Bruggen P, Brun ME, Boyle S, Roizes G, De Sario A. New BAGE (B melanoma antigen) genes mapping to the juxtacentromeric regions of human chromosomes 13 and 21 have a cancer/testis expression profile. Eur. J. Hum. Genet. 10(12), 833-840 (2002).
49. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 21(35), 5400-5413 (2002).
50. Boks MP, Derks EM, Weisenberger DJ et al. The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS ONE 4(8), e6767 (2009).
51. Liu J, Morgan M, Hutchison K, Calhoun VD. A study of the influence of sex on genome wide methylation. PLoS ONE 5(4), e10028 (2010).
52. Dick KJ, Nelson CP, Tsaprouni L et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet 383(9933), 1990-1998 (2014).
53. Moustafa AA, Hewedi DH, Eissa AM, Frydecka D, Misiak B. Homocysteine levels in schizophrenia and affective disorders-focus on cognition. Front. Behav. Neurosci. 8, 343 (2014).
54. Mcguffin P, Farmer A, Harvey I. A polydiagnostic application of operational criteria in studies of psychotic illness. Development and reliability of the OPCRIT system. Arch. Gen. Psychiatry 48(8), 764-770 (1991).
55. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13(2), 261-276 (1987).
56. Bremner JD, Vermetten E, Mazure CM. Development and preliminary psychometric properties of an instrument for the measurement of childhood trauma: the Early Trauma Inventory. Depress. Anxiety 12(1), 1-12 (2000).
57. Jeon JR, Lee EH, Lee SW et al. The early trauma inventory self report-short form: psychometric properties of the korean version. Psychiatry Investig. 9(3), 229-235 (2012).
58. Plaza A, Torres A, Martin-Santos R et al. Validation and test-retest reliability of Early Trauma Inventory in Spanish postpartum women. J. Nerv. Ment. Dis. 199(4), 280-285 (2011).
59. Osorio FL, Salum GA, Donadon MF, Forni-Dos-Santos L, Loureiro SR, Crippa JA. Psychometrics properties of early trauma inventory self report-short form (ETISR-SR) for the Brazilian context. PLoS ONE 8(10), e76337 (2013).
60. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucl. Acids Res. 25(12), 2532-2534 (1997).
61. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucl. Acids Res. 32(3), e38 (2004).
62. Sipahi L, Wildman DE, Aiello AE et al. Longitudinal epigenetic variation of DNA methyltransferase genes is associated with vulnerability to post-traumatic stress disorder. Psychol. Med. 44(15), 3165-3179 (2014).
63. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300(5618), 455 (2003).
64. Shalev I, Entringer S, Wadhwa PD et al. Stress and telomere biology: a lifespan perspective. Psychoneuroendocrinology 38(9), 1835-1842 (2013).
65. Smith CL, Bolton A, Nguyen G. Genomic and epigenomic instability, fragile sites, schizophrenia and autism. Curr. Genomics 11(6), 447-469 (2010).
66. Bromberg A, Levine J, Nemetz B, Belmaker RH, Agam G. No association between global leukocyte DNA methylation and homocysteine levels in schizophrenia patients. Schizophr. Res. 101(1-3), 50-57 (2008).
67. Bromberg A, Levine J, Belmaker R, Agam G. Hyperhomocysteinemia does not affect global DNA methylation and nicotinamide N-methyltransferase expression in mice. J. Psychopharmacol. 25(7), 976-981 (2011).
68. Kinoshita M, Numata S, Tajima A, Shimodera S, Imoto I, Ohmori T. Plasma total homocysteine is associated with DNA methylation in patients with schizophrenia. Epigenetics 8(6), 584-590 (2013).
69. Bonsch D, Wunschel M, Lenz B, Janssen G, Weisbrod M, Sauer H. Methylation matters Decreased methylation status of genomic DNA in the blood of schizophrenic twins. Psychiatry Res. 198(3), 533-537 (2012).
70. Melka MG, Laufer BI, Mcdonald P et al. The effects of olanzapine on genome-wide DNA methylation in the hippocampus and cerebellum. Clin. Epigenetics 6(1), 1 (2014).
71. Misiak B, Frydecka D, Piotrowski P, Kiejna A. The multidimensional nature of metabolic syndrome in schizophrenia: lessons from studies of one-carbon metabolism and DNA methylation. Epigenomics 5(3), 317-329 (2013).
72. Fisher HL, Craig TK, Fearon P et al. Reliability and comparability of psychosis patients' retrospective reports of childhood abuse. Schizophr. Bull. 37(3), 546-553 (2011).
73. Karimi M, Johansson S, Stach D et al. LUMA (LUminometric Methylation Assay)-a high throughput method to the analysis of genomic DNA methylation. Exp. Cell Res. 312(11), 1989-1995 (2006).
74. Karimi M, Johansson S, Ekstrom TJ. Using LUMA: a luminometric-based assay for global DNA-methylation. Epigenetics 1(1), 45-48 (2006).