Differential gene body methylation and reduced expression of cell adhesion and neurotransmitter receptor genes in adverse maternal environment

Translational Psychiatry - Tập 3 Số 1 - Trang e218-e218
Ji-Eun Oh1, Nyasha Chambwe2, Shifra Klein1, J. Gál3, Sarah F. Andrews2, Georgia Gleason1, Rita Shaknovich4, Ari Melnick4, Fabien Campagne2, Miklós Tóth1
1Department of Pharmacology, Weill Cornell Medical College, New York, USA
2Department of Physiology and Biophysics and HRH Prince Alwaleed Bin Talal Bin Abdulaziz Alsaud Institute for Computational Biomedicine, Weill Cornell Medical College, New York, USA
3Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, New York, USA
4Department of Medicine, Weill Cornell Medical College, New York, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Gilbert R, Widom CS, Browne K, Fergusson D, Webb E, Janson S . Burden and consequences of child maltreatment in high-income countries. Lancet 2009; 373: 68–81.

Green JG, McLaughlin KA, Berglund PA, Gruber MJ, Sampson NA, Zaslavsky AM et al. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch Gen Psychiatry 2010; 67: 113–123.

Chen GH, Wang H, Yang QG, Tao F, Wang C, Xu DX . Acceleration of age-related learning and memory decline in middle-aged CD-1 mice due to maternal exposure to lipopolysaccharide during late pregnancy. Behav Brain Res 2011; 218: 267–279.

Veenema AH, Reber SO, Selch S, Obermeier F, Neumann ID . Early life stress enhances the vulnerability to chronic psychosocial stress and experimental colitis in adult mice. Endocrinology 2008; 149: 2727–2736.

Millstein RA, Holmes A . Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 2007; 31: 3–17.

Priebe K, Romeo RD, Francis DD, Sisti HM, Mueller A, McEwen BS et al. Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study. Dev Psychobiol 2005; 47: 398–407.

Gleason G, Liu B, Bruening S, Zupan B, Auerbach A, Mark W et al. The serotonin1A receptor gene as a genetic and prenatal maternal environmental factor in anxiety. Proc Natl Acad Sci USA 2010; 107: 7592–7597.

van Velzen A, Toth M . Role of maternal 5-HT(1A) receptor in programming offspring emotional and physical development. Genes Brain Behav 2010; 9: 877–885.

Gleason G, Zupan B, Toth M . Maternal genetic mutations as gestational and early life influences in producing psychiatric disease-like phenotypes in mice. Front Psychiatry/Front Res Foundation 2011; 2: 25.

Zoghbi HY, Warren ST . Neurogenetics: advancing the ‘next-generation’ of brain research. Neuron 2010; 68: 165–173.

Meaney MJ . Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001; 24: 1161–1192.

Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T et al. Regional dissociations within the hippocampus--memory and anxiety. Neurosci Biobehav Rev 2004; 28: 273–283.

Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB . Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 2002; 99: 10825–10830.

Adhikari A, Topiwala MA, Gordon JA . Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010; 65: 257–269.

Ishikawa A, Nakamura S . Ventral hippocampal neurons project axons simultaneously to the medial prefrontal cortex and amygdala in the rat. J Neurophysiol 2006; 96: 2134–2138.

Elliott E, Ezra-Nevo G, Regev L, Neufeld-Cohen A, Chen A . Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 2010; 13: 1351–1353.

Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM . Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008; 3: 97–106.

Zhang TY, Hellstrom IC, Bagot RC, Wen X, Diorio J, Meaney MJ . Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. J Neurosci 2010; 30: 13130–13137.

McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonte B, Szyf M et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009; 12: 342–348.

Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 2011; 14: 1345–1351.

Rollins RA, Haghighi F, Edwards JR, Das R, Zhang MQ, Ju J et al. Large-scale structure of genomic methylation patterns. Genome Res 2006; 16: 157–163.

Khulan B, Thompson RF, Ye K, Fazzari MJ, Suzuki M, Stasiek E et al. Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res 2006; 16: 1046–1055.

Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 2008; 30: 755–766.

Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008; 454: 766–770.

Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009; 12: 1559–1566.

Figueroa ME, Melnick A, Greally JM . Genome-wide determination of DNA methylation by Hpa II tiny fragment enrichment by ligation-mediated PCR (HELP) for the study of acute leukemias. Methods Mol Biol 2009; 538: 395–407.

Figueroa ME, Reimers M, Thompson RF, Ye K, Li Y, Selzer RR et al. An integrative genomic and epigenomic approach for the study of transcriptional regulation. PLoS ONE 2008; 3: e1882.

Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G et al. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Nat Acad Sci USA 2005; 102: 15785–15790.

Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A . Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat Protoc 2011; 6: 468–481.

Kielbasa SM, Wan R, Sato K, Horton P, Frith MC . Adaptive seeds tame genomic sequence comparison. Genome Res 2011; 21: 487–493.

Qi Y, Ranish JA, Zhu X, Krones A, Zhang J, Aebersold R et al. Atbf1 is required for the Pit1 gene early activation. Proc Nat Acad Sci USA 2008; 105: 2481–2486.

Jung CG, Kim HJ, Kawaguchi M, Khanna KK, Hida H, Asai K et al. Homeotic factor ATBF1 induces the cell cycle arrest associated with neuronal differentiation. Development (Cambridge, England) 2005; 132: 5137–5145.

Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG et al. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 2003; 39: 937–950.

Sanchez-Camacho C, Bovolenta P . Emerging mechanisms in morphogen-mediated axon guidance. Bioessays 2009; 31: 1013–1025.

Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009; 41: 178–186.

Giannopoulou EG, Elemento O . An integrated ChIP-seq analysis platform with customizable workflows. BMC Bioinformatics 2011; 12: 277.

Muramatsu R, Ikegaya Y, Matsuki N, Koyama R . Neonatally born granule cells numerically dominate adult mice dentate gyrus. Neuroscience 2007; 148: 593–598.

Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 2012; 484: 339–344.

Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H et al. Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 2010; 42: 1093–1100.

Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462: 315–322.

Wood SJ, Toth M . Molecular pathways of anxiety revealed by knockout mice. Mol Neurobiol 2001; 23: 101–119.

Charil A, Laplante DP, Vaillancourt C, King S . Prenatal stress and brain development. Brain Res Rev 2010; 65: 56–79.

Phillips NK, Hammen CL, Brennan PA, Najman JM, Bor W . Early adversity and the prospective prediction of depressive and anxiety disorders in adolescents. J Abnorm Child Psychol 2005; 33: 13–24.

Nemeroff CB . Early-life adversity, CRF dysregulation, and vulnerability to mood and anxiety disorders. Psychopharmacol Bull 2004; 38 (Suppl 1): 14–20.

McEwen BS . Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22: 105–122.

Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 2011; 44: 17–28.

Niehrs C, Schafer A . Active DNA demethylation by Gadd45 and DNA repair. Tr Cell Biol 2012; 22: 220–227.

Sutton RE, Koob GF, Le Moal M, Rivier J, Vale W . Corticotropin releasing factor produces behavioural activation in rats. Nature 1982; 297: 331–333.

Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH et al. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 1998; 20: 1093–1102.

Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK et al. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 1998; 19: 162–166.

Accili D, Fishburn CS, Drago J, Steiner H, Lachowicz JE, Park BH et al. A targeted mutation of the D3 dopamine receptor gene is associated with hyperactivity in mice. Proc Nat Acad Sci USA 1996; 93: 1945–1949.

Ledent C, Vaugeois JM, Schiffmann SN, Pedrazzini T, El Yacoubi M, Vanderhaeghen JJ et al. Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor. Nature 1997; 388: 674–678.

Ross SA, Wong JY, Clifford JJ, Kinsella A, Massalas JS, Horne MK et al. Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J Neurosci 2000; 20: 6431–6441.

Schlegel S, Steinert H, Bockisch A, Hahn K, Schloesser R, Benkert O . Decreased benzodiazepine receptor binding in panic disorder measured by IOMAZENIL-SPECT. A preliminary report. Eur Arch Psychiatry Clin Neurosci 1994; 244: 49–51.

Kaschka W, Feistel H, Ebert D . Reduced benzodiazepine receptor binding in panic disorders measured by iomazenil SPECT. J Psychiatr Res 1995; 29: 427–434.

Tiihonen J, Kuikka J, Rasanen P, Lepola U, Koponen H, Liuska A et al. Cerebral benzodiazepine receptor binding and distribution in generalized anxiety disorder: a fractal analysis. Mol Psychiatry 1997; 2: 463–471.

Mombereau C, Kaupmann K, Gassmann M, Bettler B, van der Putten H, Cryan JF . Altered anxiety and depression-related behaviour in mice lacking GABAB(2) receptor subunits. Neuroreport 2005; 16: 307–310.

Barkus C, McHugh SB, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM . Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur J Pharmacol 2010; 626: 49–56.

Lee AS, Ra S, Rajadhyaksha AM, Britt JK, De Jesus-Cortes H, Gonzales KL et al. Forebrain elimination of cacna1c mediates anxiety-like behavior in mice. Mol Psychiatry 2012; 17: 1054–5.

Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ et al. CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 2006; 9: 475–477.

Catches JS, Xu J, Contractor A . Genetic ablation of the GluK4 kainate receptor subunit causes anxiolytic and antidepressant-like behavior in mice. Behav Brain Res 2012; 228: 406–414.

Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J, Liu XQ et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 2007; 39: 319–328.

Kim HG, Kishikawa S, Higgins AW, Seong IS, Donovan DJ, Shen Y et al. Disruption of neurexin 1 associated with autism spectrum disorder. Am J Hum Genet 2008; 82: 199–207.

Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS et al. Identifying autism loci and genes by tracing recent shared ancestry. Science 2008; 321: 218–223.

Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS et al. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 2009; 459: 528–533.

Wisniowiecka-Kowalnik B, Nesteruk M, Peters SU, Xia Z, Cooper ML, Savage S et al. Intragenic rearrangements in NRXN1 in three families with autism spectrum disorder, developmental delay, and speech delay. Am J Med Genet B Neuropsychiatr Genet 2010; 153B: 983–993.

Attwood BK, Bourgognon JM, Patel S, Mucha M, Schiavon E, Skrzypiec AE et al. Neuropsin cleaves EphB2 in the amygdala to control anxiety. Nature 2011; 473: 372–375.