Associative DNA methylation changes in children with prenatal alcohol exposure

Epigenomics

Volumn 7, Issue 8, 2015, Pages 1259-1274

  Laufer, Benjamin I ^a   Kapalanga, Joachim ^a   Castellani, Christina A ^a   Diehl, Eric J ^a   Yan, Liying ^b   Singh, Shiva M ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b EpigenDx   (United States)

Author keywords

Cohesin; CTCF; fetal alcohol spectrum disorders; glutamatergic synapse; hippo signaling; neurodevelopment; protocadherin; synapse

Indexed keywords

ALCOHOL; CADHERIN; DNA; UNTRANSLATED RNA; ALCOHOL DERIVATIVE;

ANXIETY; ARTICLE; CHILD; CLINICAL ARTICLE; CONDUCT DISORDER; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FETAL ALCOHOL SYNDROME; GLUTAMATERGIC SYNAPSE; HUMAN; HUMAN TISSUE; HYPERACTIVITY; LEARNING DISORDER; MACROCEPHALY; MALE; MOOD DISORDER; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OPPOSITIONAL DEFIANT DISORDER; ORAL BIOPSY; PRENATAL EXPOSURE; PRESCHOOL CHILD; PRIORITY JOURNAL; PYROSEQUENCING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; ADVERSE EFFECTS; ANIMAL; CASE CONTROL STUDY; CLUSTER ANALYSIS; CPG ISLAND; DISEASE MODEL; FEMALE; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MATERNAL EXPOSURE; METABOLISM; PREGNANCY;

ALCOHOLS; ANIMALS; CADHERINS; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; CPG ISLANDS; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; GENE EXPRESSION PROFILING; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MATERNAL EXPOSURE; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84950286817     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.15.60     Document Type: Article

References (64)

1. Guerri C, Bazinet A, Riley EP. Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol. 44(2), 108-114 (2009).
2. Lee S, Choi I, Kang S, Rivier C. Role of various neurotransmitters in mediating the long-term endocrine consequences of prenatal alcohol exposure. Ann. NY Acad. Sci. 1144, 176-188 (2008).
3. Bosco C, Diaz E. Placental hypoxia and foetal development versus alcohol exposure in pregnancy. Alcohol Alcohol. 47(2), 109-117 (2012).
4. Kleiber ML, Wright E, Singh SM. Maternal voluntary drinking in C57BL/6J mice: advancing a model for fetal alcohol spectrum disorders. Behav. Brain Res. 223(2), 376-387 (2011).
5. Kleiber ML, Laufer BI, Wright E, Diehl EJ, Singh SM. Long-term alterations to the brain transcriptome in a maternal voluntary consumption model of fetal alcohol spectrum disorders. Brain Res. 1458, 18-33 (2012).
6. Mantha K, Kleiber M, Singh S. Neurodevelopmental timing of ethanol exposure may contribute to observed heterogeneity of behavioral deficits in a mouse model of Fetal Alcohol Spectrum Disorder (FASD). J. Behav. Brain Sci. 3, 85-99 (2013).
7. Kleiber ML, Mantha K, Stringer RL, Singh SM. Neurodevelopmental alcohol exposure elicits long-term changes to gene expression that alter distinct molecular pathways dependent on timing of exposure. J. Neurodev. Disord. 5(1), 6 (2013).
8. Laufer BI, Mantha K, Kleiber ML, Diehl EJ, Addison SM, Singh SM. Long-lasting alterations to DNA methylation and ncRNAs could underlie the effects of fetal alcohol exposure in mice. Dis. Model. Mech. 6(4), 977-992 (2013).
9. Olney JW, Tenkova T, Dikranian K, Qin YQ, Labruyere J, Ikonomidou C. Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res. Dev. Brain Res. 133(2), 115-126 (2002).
10. Choi IY, Allan AM, Cunningham LA. Moderate fetal alcohol exposure impairs the neurogenic response to an enriched environment in adult mice. Alcohol. Clin. Exp. Res. 29(11), 2053-2062 (2005).
11. Young C, Olney JW. Neuroapoptosis in the infant mouse brain triggered by a transient small increase in blood alcohol concentration. Neurobiol. Dis. 22(3), 548-554 (2006).
12. Green ML, Singh AV, Zhang Y, Nemeth KA, Sulik KK, Knudsen TB. Reprogramming of genetic networks during initiation of the Fetal Alcohol Syndrome. Dev. Dyn. 236(2), 613-631 (2007).
13. Kajimoto K, Allan A, Cunningham LA. Fate analysis of adult hippocampal progenitors in a murine model of Fetal Alcohol Spectrum Disorder (FASD). PLoS ONE 8(9), e73788 (2013).
14. Subbanna S, Nagre NN, Shivakumar M, Umapathy NS, Psychoyos D, Basavarajappa BS. Ethanol induced acetylation of histone at G9a Exon1 and G9a-mediated histone H3 dimethylation leads to neurodegeneration in neonatal mice. Neuroscience 258, 422-432 (2013).
15. El Shawa H, Abbott CW, 3rd, Huffman KJ. Prenatal ethanol exposure disrupts intraneocortical circuitry, cortical gene expression, and behavior in a mouse model of FASD. J. Neurosci. 33(48), 18893-18905 (2013).
16. Kleiber ML, Diehl EJ, Laufer BI et al. Long-term genomic and epigenomic dysregulation as a consequence of prenatal alcohol exposure: a model for fetal alcohol spectrum disorders. Front. Genet. 5, 161 (2014).
17. Zhou FC. Dissecting FASD through the global transcriptome. Alcohol. Clin. Exp. Res. 39(3), 408-412 (2015).
18. Haycock PC. Fetal alcohol spectrum disorders: the epigenetic perspective. Biol. Reprod. 81(4), 607-617 (2009).
19. Hutson JR, Stade B, Lehotay DC, Collier CP, Kapur BM. Folic acid transport to the human fetus is decreased in pregnancies with chronic alcohol exposure. PLoS ONE 7(5), e38057 (2012).
20. Ungerer M, Knezovich J, Ramsay M. In utero alcohol exposure, epigenetic changes, and their consequences. Alcohol. Res. 35(1), 37-46 (2013).
21. Perkins A, Lehmann C, Lawrence RC, Kelly SJ. Alcohol exposure during development: impact on the epigenome. Int. J. Dev. Neurosci. 31(6), 391-397 (2013).
22. Veazey KJ, Carnahan MN, Muller D, Miranda RC, Golding MC. Alcohol-induced epigenetic alterations to developmentally crucial genes regulating neural stemness and differentiation. Alcohol. Clin. Exp. Res. 37(7), 1111-1122 (2013).
23. Stringer R, Laufer B, Kleiber M, Singh S. Reduced expression of brain cannabinoid receptor 1 (Cnr1) is coupled with an increased complementary micro-RNA (miR-26b) in a mouse model of fetal alcohol spectrum disorders. Clin. Epigenetics 5(1), 14 (2013).
24. Mantha K, Laufer BI, Singh SM. Molecular changes during Neurodevelopment following second-trimester binge ethanol exposure in a mouse model of Fetal Alcohol Spectrum Disorder: from immediate effects to long-term adaptation. Dev. Neurosci. 36(1), 29-43 (2014).
25. Kleiber ML, Laufer BI, Stringer RL, Singh SM. Third trimester-equivalent ethanol exposure is characterized by an acute cellular stress response and an ontogenetic disruption of genes critical for synaptic establishment and function in mice. Dev. Neurosci. 36(6), 499-519 (2014).
26. Laufer BI, Diehl EJ, Singh SM. Neurodevelopmental epigenetic etiologies: insights from studies on mouse models of fetal alcohol spectrum disorders. Epigenomics 5(5), 465-468 (2013).
27. Hard ML, Abdolell M, Robinson BH, Koren G. Gene-expression analysis after alcohol exposure in the developing mouse. J. Lab. Clin. Med. 145(1), 47-54 (2005).
28. Sur M, Leamey CA. Development and plasticity of cortical areas and networks. Nat. Rev. Neurosci. 2(4), 251-262 (2001).
29. Hirano S, Takeichi M. Cadherins in brain morphogenesis and wiring. Physiol. Rev. 92(2), 597-634 (2012).
30. Chen EY, Tan CM, Kou Y et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128-2105-14-128 (2013).
31. Maksimovic J, Gordon L, Oshlack A. SWAN: Subset-quantile within array normalization for illumina infinium HumanMethylation450 BeadChips. Genome Biol. 13(6), R44-2012-13-6-r44 (2012).
32. Pidsley R, Y Wong CC, Volta M, Lunnon K, Mill J, Schalkwyk LC. A data-driven approach to preprocessing Illumina 450K methylation array data. BMC Genomics 14, 293-2164-14-293 (2013).
33. EpigenDx. www.EpigenDx.com
34. Lim A, Candiloro I, Wong N et al. Quantitative methodology is critical for assessing DNA methylation and impacts on correlation with patient outcome. Clin. Epigenetics 6(1), 22 (2014).
35. The UCSC Genome Browser database (2015). www.genome.ucsc.edu
36. Oh H, Slattery M, Ma L, White KP, Mann RS, Irvine KD. Yorkie promotes transcription by recruiting a histone methyltransferase complex. Cell. Rep. 8(2), 449-459 (2014).
37. Sarikaya DP, Extavour CG. The hippo pathway regulates homeostatic growth of stem cell niche precursors in the drosophila ovary. PLoS Genet. 11(2), e1004962 (2015).
38. Aryee MJ, Jaffe AE, Corrada-Bravo H et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics 30(10), 1363-1369 (2014).
39. Rooryck C, Diaz-Font A, Osborn DP et al. Mutations in lectin complement pathway genes COLEC11 and MASP1 cause 3MC syndrome. Nat. Genet. 43(3), 197-203 (2011).
40. Halsted CH, Villanueva JA, Devlin AM, Chandler CJ. Metabolic interactions of alcohol and folate. J. Nutr. 132(8 Suppl.), S2367-S2372 (2002).
41. Sathyan P, Golden HB, Miranda RC. Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J. Neurosci. 27(32), 8546-8557 (2007).
42. Haycock PC, Ramsay M. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the H19 imprinting control region. Biol. Reprod. 81(4), 618-627 (2009).
43. Liu Y, Balaraman Y, Wang G, Nephew KP, Zhou FC. Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics 4(7), 500-511 (2009).
44. Kaminen-Ahola N, Ahola A, Maga M et al. Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLoS Genet. 6(1), e1000811 (2010).
45. Hirano S, Takeichi M. Cadherins in brain morphogenesis and wiring. Physiol. Rev. 92(2), 597-634 (2012).
46. Chen WV, Maniatis T. Clustered protocadherins. Development 140(16), 3297-3302 (2013).
47. Sano K, Tanihara H, Heimark RL et al. Protocadherins: a large family of cadherin-related molecules in central nervous system. EMBO J. 12(6), 2249-2256 (1993).
48. Kohmura N, Senzaki K, Hamada S et al. Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20(6), 1137-1151 (1998).
49. Wang X, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR. Gamma protocadherins are required for survival of spinal interneurons. Neuron 36(5), 843-854 (2002).
50. Kallenbach S, Khantane S, Carroll P et al. Changes in subcellular distribution of protocadherin gamma proteins accompany maturation of spinal neurons. J. Neurosci. Res. 72(5), 549-556 (2003).
51. Phillips GR, Tanaka H, Frank M et al. Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J. Neurosci. 23(12), 5096-5104 (2003).
52. Junghans D, Heidenreich M, Hack I, Taylor V, Frotscher M, Kemler R. Postsynaptic and differential localization to neuronal subtypes of protocadherin beta16 in the mammalian central nervous system. Eur. J. Neurosci. 27(3), 559-571 (2008).
53. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488(7412), 517-521 (2012).
54. Chen WV, Alvarez FJ, Lefebvre JL et al. Functional significance of isoform diversification in the protocadherin gamma gene cluster. Neuron 75(3), 402-409 (2012).
55. Golan-Mashiach M, Grunspan M, Emmanuel R, Gibbs-Bar L, Dikstein R, Shapiro E. Identification of CTCF as a master regulator of the clustered protocadherin genes. Nucleic Acids Res. 40(8), 3378-3391 (2012).
56. Toyoda S, Kawaguchi M, Kobayashi T et al. Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity. Neuron 82(1), 94-108 (2014).
57. Bonn S, Seeburg PH, Schwarz MK. Combinatorial expression of alpha-and gamma-protocadherins alters their presenilin-dependent processing. Mol. Cell. Biol. 27(11), 4121-4132 (2007).
58. Schreiner D, Weiner JA. Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc. Natl Acad. Sci. USA 107(33), 14893-14898 (2010).
59. Kalmady SV, Venkatasubramanian G. Evidence for positive selection on Protocadherin Y gene in Homo sapiens: implications for schizophrenia. Schizophr. Res. 108(1-3), 299-300 (2009).
60. Kim TH, Abdullaev ZK, Smith AD et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128(6), 1231-1245 (2007).
61. Nitzsche A, Paszkowski-Rogacz M, Matarese F et al. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS ONE 6(5), e19470 (2011).
62. Guo Y, Monahan K, Wu H et al. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl Acad. Sci. USA 109(51), 21081-21086 (2012).
63. Biswas S, Emond MR, Duy PQ, Hao le T, Beattie CE, Jontes JD. Protocadherin-18b interacts with Nap1 to control motor axon growth and arborization in zebrafish. Mol. Biol. Cell 25(5), 633-642 (2014).
64. Paley B, O'Connor MJ. Intervention for individuals with fetal alcohol spectrum disorders: treatment approaches and case management. Dev. Disabil. Res. Rev. 15(3), 258-267 (2009).