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Environmental Studies as a Tool for Detecting Epigenetic Mechanisms in Schizophrenia

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Brain, Behavior and Epigenetics

Part of the book series: Epigenetics and Human Health ((EHH))

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Abstract

Epigenetic mechanisms may play an important role in the etiological pathways of schizophrenia. Since the epigenetic status of the genome partly depends on environmental factors in pre- and postnatal environments, exposure to such factors should be taken into account in epigenetic studies of schizophrenia. Prenatal famine and childhood ethnic minority status have been identified as environmental risk factors for schizophrenia. These exposures can be used to investigate epigenetic effects on schizophrenia, since environmental exposure can be measured with sufficient precision, homogeneously exposed populations are available for study, and plausible biological pathways have been suggested (albeit less specific for migration). This chapter shows that epidemiological studies of famine and migration can help to detect epigenetic mechanisms in schizophrenia, by comparing the epigenome of exposed and unexposed schizophrenia cases and controls. The results of the comparisons will be different depending on the mechanism involved in the interplay between environment and epigenome. If these epidemiological designs are not applied, the overall result of epigenetic schizophrenia studies may well continue to be inconclusive.

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References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Allen NC, Bagade S, McQueen MB, Ioannidis JP, Kawoura FK, Khoury MJ, Tanzi RE, Bertram L (2008) Systematic meta-analyses and field synopsis of the genetic association studies in schizophrenia: the SzGene database. Nat Genet 40:827–834

    Article  PubMed  CAS  Google Scholar 

  • Berton O, McClung CA, DiLeone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ (2006) Essential role of BDNF in the mesolimbic pathway in social defeat stress. Science 311:864–868

    Article  PubMed  CAS  Google Scholar 

  • Brown AS, Susser ES (2008) Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull 34:1054–1063

    Article  PubMed  Google Scholar 

  • Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meany MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci 28:5335–5340

    Article  Google Scholar 

  • Cantor-Graae E, Selten JP (2005) Schizophrenia and migration: a meta-analysis and review. Am J Psychiatry 162:12–24

    Article  PubMed  Google Scholar 

  • Cantor-Graae E, Pedersen CB, McNeil TF, Mortensen PB (2003) Migration as a risk factor for schizophrenia: a Danish population-based cohort study. Br J Psychiatry 182:117–122

    Article  PubMed  Google Scholar 

  • Coid JW, Kirkbride JB, Barker D, Cowden F, Stamps R, Yang M, Jones PB (2008) Raised incidence rates of all psychoses among migrant groups. Arch Gen Psychiatry 65:1250–1258

    Article  PubMed  Google Scholar 

  • Czeizel AE, Dudás I (1992) Prevention of the first occurrence of neural-tube defects by periconceptual vitamin suppletion. New Eng J Med 327:1832–1835

    Article  PubMed  CAS  Google Scholar 

  • DeBaun MR, Niemitz EL, McNeil DE, Brandenburg SA, Lee MP, Feinberg AP (2002) Epigenetic alterations of H19 and LIT1 distinguish patients with Beckwith-Wiedemann syndrome with cancer and birth defects. Am J Hum Genet 70:604–611

    Article  PubMed  CAS  Google Scholar 

  • Dempster EL, Mill J, Craig IW, Collier DA (2006) The quantification of COMT mRNA in post mortem cerebellum tissue: diagnosis, genotype, methylation and expression. BMC Med Genet 7:10

    Article  PubMed  Google Scholar 

  • Drexhage RC, Knijff EM, Padmos RC, Heul-Nieuwenhuijzen L, Beumer W, Versnel MA, Drexhage HA (2010) The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder. Expert Rev Neurother 10:59–76

    Article  PubMed  CAS  Google Scholar 

  • Duthie SJ, Narayanan S, Blum S, Pirie L, Brand GM (2000) Folate deficiency in vitro induces uracil misincorporation and DNA hypomethylation and inhibits DNA excision repair in immortalized normal human colon epithelial cells. Nutr Cancer 37:245–251

    Article  PubMed  CAS  Google Scholar 

  • Fearon P, Kirkbride JB, Morgan C, Dazzan P, Morgan K, Lloyd T, Hutchinson G, Tarrant J, Fung WLA, Holloway J, Mallett R, Harrison G, Leff J, Jones PB, Murray RM (2006) Incidence of schizophrenia and other psychoses in ethnic minority groups: results from the MRC AESOP study. Psychol Med 36:1541–1550

    Article  PubMed  Google Scholar 

  • Feinberg AP (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447:433–440

    Article  PubMed  CAS  Google Scholar 

  • Foley DL, Craig JM, Morley R, Olsson CA, Dwyer T, Smith K, Saffery R (2009) Prospects for epigenetic epidemiology. Am J Epidemiol 169:389–400

    Article  PubMed  Google Scholar 

  • Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci 102:10604–10609

    Article  PubMed  CAS  Google Scholar 

  • Francis D, Diorio J, Liu D, Meany MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158

    Article  PubMed  CAS  Google Scholar 

  • Grayson DR, Jia X, Chen Y, Sharma RP, Mitchell CP, Guidotti A, Costa E (2005) Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci 102:9341–9346

    Article  PubMed  CAS  Google Scholar 

  • Group MVSR (1991) Prevention of neural tube defects: results of the Medical Research Council Vitamin Study. Lancet 338:131–137

    Article  Google Scholar 

  • Haberg S, London SJ, Stigum H, Nafstad P, Nystad W (2009) Folic acid supplements in pregnancy and early childhood respiratory health. Arch Dis Child 94:180–184

    Article  PubMed  CAS  Google Scholar 

  • Harrison G, Glazebrook C, Brewin J, Cantwell R, Dalkin T, Fox R, Jones P, Medley I (1997) Increased incidence of psychotic disorders in migrants from the Caribbean to the United Kingdom. Psychol Med 27:799–806

    Article  PubMed  CAS  Google Scholar 

  • Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci 105:17046–17049

    Article  PubMed  CAS  Google Scholar 

  • Heijmans BT, Tobi EW, Lumey LH, Slagboom PE (2009) The epigenome; archive of the prenatal environment. Epigenetics 4:526–531

    Article  PubMed  CAS  Google Scholar 

  • Hemsi LK (1967) Psychotic morbidity of West Indian immigrants. Soc Psychiatry 2:95–100

    Article  Google Scholar 

  • Isovich E, Engelmann M, Landgraf R, Fuchs E (2001) Social isolation after a single defeat reduces striatal dopamine transporter binding in rats. Eur J Neurosci 13:1254–1256

    Article  PubMed  CAS  Google Scholar 

  • Kehoe PG, Russ C, McIlory S, Williams H, Holmans P, Holmes C, Liolitsa D, Vahidassr D, Powell J, McGleenon B, Liddell M, Plomin R, Dynan K, Williams N, Neal J, Cairns NJ, Wilcock G, Passmore P, Lovestone S, Williams J, Owen MJ (1999) Variation in DCP1, encoding ACE, is associated with susceptibility to Alzheimer disease. Nat Genet 21:71–72

    Article  PubMed  CAS  Google Scholar 

  • King M, Coker E, Leavy G, Hoare A, Johnson-Sabine E (1994) Incidence of psychotic illness in London: comparison of ethnic groups. Br Med J 309:1115–1119

    CAS  Google Scholar 

  • Laruelle M (2003) Dopamine transmission in the schizophrenic brain. In: Hirsch SR, Weinberger D (eds) Schizophrenia. Blackwell, Oxford, pp 365–387

    Chapter  Google Scholar 

  • Levenson JM, O’Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279:40545–40549

    Article  PubMed  CAS  Google Scholar 

  • Lucock M (2000) Folic acid: nutritional biochemistry, molecular biology, and role in disease processes. Mol Genet Metab 71:121–138

    Article  PubMed  CAS  Google Scholar 

  • Magnus P, Irgens LM, Haug K, Nystad W, Skjaerven R, Stoltenberg C, Group TMS (2006) Cohort profile: the Norwegian mother and child cohort study. Int J Epidemiol 35:1146–1150

    Article  Google Scholar 

  • Malzberg B (1955) Mental disease among the native and foreign-born white populations of New York State, 1939–41. Ment Hyg 39:545–563

    PubMed  CAS  Google Scholar 

  • Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, McCarroll SA, Visscher PM (2009) Finding the missing heritability of complex disorders. Nature 461:747–753

    Article  PubMed  CAS  Google Scholar 

  • McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meany MJ (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342–348

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Miller CA, Campbell SL, Sweatt JD (2008) DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem 89:599–603

    Article  PubMed  CAS  Google Scholar 

  • Miltenberger RJ, Mynatt RL, Wilkinson JE, Woychik RP (1997) The role of the agouti gene in the yellow obese syndrome. J Nutr 127:1902S–1907S

    PubMed  CAS  Google Scholar 

  • Myin-Germeys I, van Os J, Schwartz JE, Stone AA, Delespaul PA (2001) Emotional reactivity to daily life stress in psychosis. Arch Gen Psychiatry 58:1137–1144

    Article  PubMed  CAS  Google Scholar 

  • Myin-Germeys I, Delespaul P, Van Os J (2005) Behavioural sensitization to daily life stress in psychosis. Psychol Med 35:733–741

    Article  PubMed  CAS  Google Scholar 

  • Ødegaard O (1932) Emigration and insanity: a study of mental disease among Norwegian-born population in Minnesota. Acta Psychiatrica et Neurologica Scandinavica 7:1–206

    Article  Google Scholar 

  • Oh G, Petronis A (2008) Environmental studies of schizophrenia through the prism of epigenetics. Schizophr Bull 34:1122–1129

    Article  PubMed  Google Scholar 

  • Padmos RC, Hillegers MH, Knijff EM, Vonk R, Bouvy A, Staal FJ, de Ridder D, Kupka RW, Nolen WA, Drexhage HA (2008) A discriminating messenger RNA signature for bipolar disorder formed by an aberrant expression of inflammatory genes in monocytes. Arch Gen Psychiatr 65:395–407

    Article  PubMed  CAS  Google Scholar 

  • Padmos RC, Van Baal GC, Vonk R, Wijkhuijs AJ, Kahn RS, Nolen WA, Drexhage HA (2009) Genetic and environmental influences on pro-inflammatory monocytes in bipolar disorder: a twin study. Arch Gen Psychiatr 66:957–965

    Article  PubMed  CAS  Google Scholar 

  • Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H, Whittaker P, McCann OT, Finer S, Valdes AM, Leslie RD, Deloukas P, Spector TD (2010) Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 20:434–439

    Article  PubMed  CAS  Google Scholar 

  • Read J, Van Os J, Morrison AP, Ross CA (2005) Childhood trauma, psychosis and schizophrenia: a literature review with theoretical and clinical implications. Acta Psychiatrica Scandinavica 112:330–350

    Article  PubMed  CAS  Google Scholar 

  • Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1092

    Article  PubMed  CAS  Google Scholar 

  • Renthal W, Maze I, Krishnan V, HEr C, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517–529

    Article  PubMed  CAS  Google Scholar 

  • Rose G (1985) Sick individuals and sick populations. Int J Epidemiol 14:32–38

    Article  PubMed  CAS  Google Scholar 

  • Schlotz W, Jones A, Phillips DI, Gale CR, Robinson SM, Godfrey KM (2009) Lower maternal folate status in early pregnancy is associated with childhood hyperactivity and peer problems in offspring. J Child Psychol Psychiatry Published online, 28 October 2009

    Google Scholar 

  • Selten JP, Cantor-Graae E (2007) Hypothesis: social defeat is a risk factor for schizophrenia? Br J Psychiatry 191:s9–s12

    Article  Google Scholar 

  • Selten JP, Sijben N (1994) First admission rates for schizophrenia in immigrants to The Netherlands. The Dutch National Register. Soc Psychiatry Psychiatr Epidemiol 29:71–77

    PubMed  CAS  Google Scholar 

  • Selten JP, Slaets JPJ, Kahn RS (1997) Schizophrenia in Surinamese and Dutch Antillean immigrants to The Netherlands: evidence of an increased incidence. Psychol Med 27:807–811

    Article  PubMed  CAS  Google Scholar 

  • Selten JP, Veen N, Feller W, Blom JD, Schols D, Camoenie W, Oolders J, van der Velden M, Hoek HW, Rivero VM, van der Graaf Y, Kahn R (2001) Incidence of psychotic disorders in immigrant groups to The Netherlands. Br J Psychiatry 178:367–372

    Article  PubMed  CAS  Google Scholar 

  • Smith RS (1992) A comprehensive macrophage-T-lymphocyte theory of schizophrenia. Med Hypotheses 39:248–257

    Article  PubMed  CAS  Google Scholar 

  • Smithells RW, Sheppard S, Schorah CJ, Seller MJ, Nevin NC, Harris R, Read AP, Fielding DW (1980) Possible prevention of neural-tube defects by periconceptional vitamin supplementation. Lancet 315:339–340

    Article  Google Scholar 

  • St Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, Zheng X, Gu N, Feng G, Sham P, He L (2005) Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. J Am Med Assoc 294:557–562

    Article  CAS  Google Scholar 

  • Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT (2009) Periconceptual maternal folic acid use of 400 ug per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 4:e7845. doi:10.1371/journal.pone.0007845

    Article  PubMed  Google Scholar 

  • Stefansson H, Rujescu D, Cichon S, Pietilainen OP, Ingason A, Steinberg S, Fossdal R, Sigurdsson E, Sigmundsson T, Buizer-Voskamp JE, Hansen T, Jakobsen KD, Muglia P, Francks C, Matthews PM, Gylfason A, Halldorsson BV, Gudbjartsson D, Thorgeirsson TE, Sigurdsson A, Jonasdottir A, Bjornsson A, Mattiasdottir S, Blondal T, Haraldsson M, Magnusdottir BB, Giegling I, Moller HJ, Hartmann A, Shianna KV, Ge D, Need AC, Crombie C, Fraser G, Walker N, Lonnqvist J, Suvisaari J, Tuulio-Henriksson A, Paunio T, Toulopoulou T, Bramon E, Di Forti M, Murray R, Ruggeri M, Vassos E, Tosato S, Walshe M, Li T, Vasilescu C, Muhleisen TW, Wang AG, Ullum H, Djurovic S, Melle I, Olesen J, Kiemeney LA, Franke B, Sabatti C, Freimer NB, Gulcher JR, Thorsteinsdottir U, Kong A, Andreassen OA, Ophoff RA, Georgi A, Rietschel M, Werge T, Petursson H, Goldstein DB, Nothen MM, Peltonen L, Collier DA, St Clair D, Stefansson K (2008) Large recurrent microdeletions associated with schizophrenia. Nature 455:232–236

    Article  PubMed  CAS  Google Scholar 

  • Sullivan PF, Kendler KS, Neale MC (2003) Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 60:1187–1192

    Article  PubMed  Google Scholar 

  • Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, Gorman JM (1996) Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry 53:25–31

    PubMed  CAS  Google Scholar 

  • Sweatt JD (2009) Experience-dependent epigenetic modifications in the central nervous system. Biol Psychiatry 65:191–197

    Article  PubMed  Google Scholar 

  • Szyf M, McGowan PO, Meany MJ (2008) The social environment and the epigenome. Environ Mol Mutagen 49:46–60

    Article  PubMed  CAS  Google Scholar 

  • Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, Putter H, Slagboom PE, Heijmans BT (2010) Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J: doi:10.1096/fj.09-150490

  • Tamura T, Goldenberg RL, Chapman VR, Johnston KE, Ramey SL, Nelson KG (2005) Folate status of mothers during pregnancy and mental and psychomotor development of their children at five years of age. Pediatrics 116:703–708

    Article  PubMed  Google Scholar 

  • Tidey JW, Miczek KA (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 721:140–149

    Article  PubMed  CAS  Google Scholar 

  • Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT (2009) DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 18:4046–4053

    Article  PubMed  CAS  Google Scholar 

  • Tochigi M, Iwamoto K, Bundo M, Komori A, Sasaki T, Kato N, Kato T (2008) Methylation status of the reelin promoter region in the brain of schizophrenic patients. Biol Psychiatry 63:530–533

    Article  PubMed  CAS  Google Scholar 

  • Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519–525

    Article  PubMed  CAS  Google Scholar 

  • Van Engeland M, Weijenberg MP, Roemen GMJM, Brink M, De Bruine AP, Goldbohm RA, Van den Brandt PA, Baylin SB, De Goeij AFPM, Herman JG (2003) Effects of dietary folate and alcohol intake on promoter methylation in sporadic colorectal cancer: The Netherlands cohort study on diet and cancer. Cancer Res 63:3133–3137

    PubMed  Google Scholar 

  • Van Os J, Kapur S (2009) Schizophrenia. Lancet 374:635–645

    Article  PubMed  CAS  Google Scholar 

  • Veling W (2008) Schizophrenia among ethnic minorities. Erasmus University, Rotterdam

    Google Scholar 

  • Veling W, Selten JP, Veen N, Laan W, Blom JD, Hoek HW (2006) Incidence of schizophrenia among ethnic minorities in the Netherlands: a four-year first-contact study. Schizophr Res 86:189–193

    Article  PubMed  Google Scholar 

  • Veling W, Susser E, Van Os J, Mackenbach JP, Selten JP, Hoek HW (2008) Ethnic density of neighborhoods and incidence of psychotic disorders among immigrants. Am J Psychiatry 165:66–73

    Article  PubMed  Google Scholar 

  • Walker EF, Diforio D (1997) Schizophrenia: a neural diathesis-stress model. Psychol Rev 104:667–685

    Article  PubMed  CAS  Google Scholar 

  • Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293–5300

    Article  PubMed  CAS  Google Scholar 

  • Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meany MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    Article  PubMed  CAS  Google Scholar 

  • Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meany MJ, Szyf M (2005) Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25:11045–11054

    Article  PubMed  CAS  Google Scholar 

  • Whitrow MJ, Moore VM, Rumbold AR, Davies MJ (2009) Effect of supplemental folic acid in pregnancy on childhood asthma: a prospective birth cohort study. Am J Epidemiol 170:1486–1493

    Article  PubMed  Google Scholar 

  • Wolff GL, Kodell RL, Moore SR, Cooney CA (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12:949–957

    PubMed  CAS  Google Scholar 

  • Xu MQ, Sun WS, Liu BQ, Feng BY, Yu L, Yang L, He G, Sham P, Susser E, St Clair D, He L (2009) Prenatal malnutrition and adult schizophrenia: further evidence from the 1959–1961 Chinese famine. Schizophr Bull 35:568–576

    Article  PubMed  Google Scholar 

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Veling, W., Lumey, L.H., Heijmans, B., Susser, E. (2011). Environmental Studies as a Tool for Detecting Epigenetic Mechanisms in Schizophrenia. In: Petronis, A., Mill, J. (eds) Brain, Behavior and Epigenetics. Epigenetics and Human Health. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-17426-1_6

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