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Research Paper

Periconceptional folate consumption is associated with neonatal DNA methylation modifications in neural crest regulatory and cancer development genes

, MD, , MA, , ScD, , PhD, , MD, , MD, PhD, , PhD, , PhD, , PhD, , MD, PhD & , PhD show all
Pages 1166-1176 | Received 26 Aug 2015, Accepted 03 Nov 2015, Published online: 01 Feb 2016

References

  • Blom HJ, Shaw GM, den Heijer M, Finnell RH. Neural tube defects and folate: case far from closed. Nat Rev Neurosci 2006; 7:724-31; PMID:16924261; http://dx.doi.org/10.1038/nrn1986
  • Mossey PA, Little J, Munger RG, Dixon MJ, Shaw WC. Cleft lip and palate. Lancet 2009; 374:1773-85; PMID:19747722; http://dx.doi.org/10.1016/S0140-6736(09)60695-4
  • Hernández-Díaz S, Werler MM, Walker AM, Mitchell AA. Folic Acid Antagonists during Pregnancy and the Risk of Birth Defects. N Engl J Med 2000; 343:1608-14; http://dx.doi.org/10.1056/NEJM200011303432204
  • Metayer C, Milne E, Dockerty JD, Clavel J, Pombo-de-Oliveira MS, Wesseling C, Spector LG, Schüz J, Petridou E, Ezzat S, et al. Maternal Supplementation with Folic Acid and Other Vitamins and Risk of Leukemia in Offspring: A Childhood Leukemia International Consortium Study. Epidemiol Camb Mass 2014; 25:811-22; http://dx.doi.org/10.1097/EDE.0000000000000141
  • Beaudin AE, Stover PJ. Folate-mediated one-carbon metabolism and neural tube defects: Balancing genome synthesis and gene expression. Birth Defects Res. Part C Embryo Today Rev 2007; 81:183-203; http://dx.doi.org/10.1002/bdrc.20100
  • Alonso-Aperte E, Ubeda N, Achon M, Perez-Miguelsanz J, Varela-Moreiras G. Impaired methionine synthesis and hypomethylation in rats exposed to valproate during gestation. Neurol March 10 1999 1999; 52:750-6
  • Finnell RH, Spiegelstein O, Wlodarczyk B, Triplett A, Pogribny IP, Melnyk S, James JS. DNA Methylation in Folbp1 Knockout Mice Supplemented with Folic Acid during Gestation. J Nutr 2002; 132:2457S-61S; PMID:12163711
  • Waterland RA, Jirtle RL. Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation. Mol Cell Biol 2003; 23:5293-300; http://dx.doi.org/10.1128/MCB.23.15.5293-5300.2003
  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary Protein Restriction of Pregnant Rats Induces and Folic Acid Supplementation Prevents Epigenetic Modification of Hepatic Gene Expression in the Offspring. J Nutr 2005; 135:1382-6; PMID:15930441
  • Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. Maternalmethyl supplements increase offspring DNA methylation at Axin fused. Genesis 2006; 44:401-6; PMID:16868943; http://dx.doi.org/10.1002/dvg.20230
  • Maloney CA, Hay SM, Rees WD. Folate deficiency during pregnancy impacts on methyl metabolism without affecting global DNA methylation in the rat fetus. Br J Nutr 2007; 97:1090-8; PMID:17433124; http://dx.doi.org/10.1017/S0007114507670834
  • Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 2007; 104:13056-61; PMID:17670942; http://dx.doi.org/10.1073/pnas.0703739104
  • Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 2007; 104:19351-6; PMID:18042717; http://dx.doi.org/10.1073/pnas.0707258104
  • Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR? promoter of the offspring. Br J Nutr 2008; 100:278-82; PMID:18186951; http://dx.doi.org/10.1017/S0007114507894438
  • Kim JM, Hong K, Lee JH, Lee S, Chang N. Effect of folate deficiency on placental DNA methylation in hyperhomocysteinemic rats. J Nutr Biochem 2009; 20:172-6; PMID:18547797; http://dx.doi.org/10.1016/j.jnutbio.2008.01.010
  • Lawrance AK, Deng L, Rozen R. Methylenetetrahydrofolate reductase deficiency and low dietary folate reduce tumorigenesis in Apcmin/+ mice. Gut 2009; 58:805-11; PMID:19174418; http://dx.doi.org/10.1136/gut.2007.143107
  • Gong L, Pan YX, Chen H. Gestational low protein diet in the rat mediates Igf2 gene expression in male offspring via altered hepatic DNA methylation. Epigenetics Off J DNA Methylation Soc 2010; 5:619-26; http://dx.doi.org/10.4161/epi.5.7.12882
  • Downing C, Johnson TE, Larson C, Leakey TI, Siegfried RN, Rafferty TM, Cooney CA. Subtle Decreases in DNA Methylation and Gene Expression at the Mouse Igf2 Locus Following Prenatal Alcohol Exposure: Effects of a Methyl-Supplemented Diet. Alcohol Fayettev N 2011; 45:65-71; http://dx.doi.org/10.1016/j.alcohol.2010.07.006
  • Schaible TD, Harris RA, Dowd SE, Smith CW, Kellermayer R. Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 2011; 20:1687-96; PMID:21296867; http://dx.doi.org/10.1093/hmg/ddr044
  • Kulkarni A, Dangat K, Kale A, Sable P, Chavan-Gautam P, Joshi S. Effects of Altered Maternal Folic Acid, Vitamin B12 and Docosahexaenoic Acid on Placental Global DNA Methylation Patterns in Wistar Rats. PLoS One 2011; 6:e17706; PMID:21423696; http://dx.doi.org/10.1371/journal.pone.0017706
  • Chmurzynska A, Stachowiak M, Pruszynska-Oszmalek E. Maternal protein and folic acid intake during gestation does not program leptin transcription or serum concentration in rat progeny. Genes Nutr 2012; 7:217-22; PMID:21735287; http://dx.doi.org/10.1007/s12263-011-0239-5
  • Cooper WN, Khulan B, Owens S, Elks CE, Seidel V, Prentice AM, Belteki G, Ong KK, Affara NA, Constância M, et al. DNA methylation profiling at imprinted loci after periconceptional micronutrient supplementation in humans: results of a pilot randomized controlled trial. FASEB J 2012; 26:1782-90; PMID:22267336; http://dx.doi.org/10.1096/fj.11-192708
  • Dominguez-Salas P, Moore SE, Baker MS, Bergen AW, Cox SE, Dyer RA, Fulford AJ, Guan Y, Laritsky E, Silver MJ, et al. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Commun 2014; 5:3746; PMID:24781383; http://dx.doi.org/10.1038/ncomms4746
  • Fryer AA, Nafee TM, Ismail K.M.K., Carroll, WD, Emes RD, Farrell WE. LINE-1 DNA methylation is inversely correlated with cord plasma homocysteine in man: a preliminary study. Epigenetics 2009; 4:394-8; PMID:19755846; http://dx.doi.org/10.4161/epi.4.6.9766
  • Fryer AA, Emes RD, Ismail KM, Haworth KE, Mein C, Carroll WD, Farrell WE. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics 2011; 6:86-94; PMID:20864804; http://dx.doi.org/10.4161/epi.6.1.13392
  • Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT. Periconceptional Maternal Folic Acid Use of 400 µg per Day Is Related to Increased Methylation of the IGF2 Gene in the Very Young Child. PLoS One 2009; 4:e7845; PMID:19924280; http://dx.doi.org/10.1371/journal.pone.0007845
  • Ba Y, Yu H, Liu F, Geng X, Zhu, C., Zhu, Q., Zheng, T., Ma, S., Wang, G., Li, Z., et al. Relationship of folate, vitamin B12 and methylation of insulin-like growth factor-II in maternal and cord blood. Eur J Clin Nutr 2011; 65:480-5; PMID:21245875; http://dx.doi.org/10.1038/ejcn.2010.294
  • Chang H, Zhang T, Zhang Z, Bao R, Fu C, Wang Z, Bao Y, Li Y, Wu L, Zheng X. Tissue-specific distribution of aberrant DNA methylation associated with maternal low-folate status in human neural tube defects. J Nutr Biochem 2011; 22:1172-7; PMID:21333513; http://dx.doi.org/10.1016/j.jnutbio.2010.10.003
  • Hoyo C, Murtha AP, Schildkraut JM, Jirtle R, Demark-Wahnefried W, Forman MR, Iversen ES, Kurtzberg J, Overcash F, Huang Z, et al. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics 2011; 6:928-36; PMID:21636975; http://dx.doi.org/10.4161/epi.6.7.16263
  • McKay JA, Groom A, Potter C, Coneyworth LJ, Ford D, Mathers JC, Relton CL. Genetic and Non-Genetic Influences during Pregnancy on Infant Global and Site Specific DNA Methylation: Role for Folate Gene Variants and Vitamin B12. Plos One 2012; 7:e33290; PMID:22479380; http://dx.doi.org/10.1371/journal.pone.0033290
  • Haggarty P, Hoad G, Campbell DM, Horgan GW, Piyathilake C, McNeill G. Folate in pregnancy and imprinted gene and repeat element methylation in the offspring. Am J Clin Nutr 2013; 97:94-9; PMID:23151531; http://dx.doi.org/10.3945/ajcn.112.042572
  • Loke YJ, Galati JC, Morley R, Joo EJH, Novakovic B, Li X, Weinrich B, Carson N, Ollikainen M, Ng HK, et al Association of maternal and nutrient supply line factors with DNA methylation at the imprinted IGF2/H19 locus in multiple tissues of newborn twins. Epigenetics 2013; 8:1069-79; PMID:23917818; http://dx.doi.org/10.4161/epi.25908
  • Crider KS, Yang TP, Berry RJ, Bailey LB, Folate and DNA methylation: a review of molecular mechanisms and the evidence for folate's role. Adv Nutr Int Rev J 2012; 3:21-38; http://dx.doi.org/10.3945/an.111.000992
  • Amarasekera M, Martino D, Ashley S, Harb H, Kesper D, Strickland D, Saffery R, Prescott SL. Genome-wide DNA methylation profiling identifies a folate-sensitive region of differential methylation upstream of ZFP57-imprinting regulator in humans. FASEB J 2014; 28(9):4068-76; PMID:24891518; http://dx.doi.org/10.1096/fj.13-249029
  • Kelsey G. Epigenome Changes During Development. In Epigenetic Epidemiology. Springer US, pp. 2012; 77-103
  • Rakyan VK, Blewitt ME, Druker R, Preis JI, Whitelaw E. Metastable epialleles in mammals. Trends Genet 2002; 18:348-51; PMID:12127774; http://dx.doi.org/10.1016/S0168-9525(02)02709-9
  • Price ME, Cotton AM, Lam LL, Farré P, Emberly E, Brown CJ, Robinson WP, Kobor MS. Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array. Epigenetics Chromatin 2013; 6:4-4; PMID:23452981; http://dx.doi.org/10.1186/1756-8935-6-4
  • Chen Y, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, Gallinger S, Hudson TJ, Weksberg R. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics 2013; 8:203-9; PMID:23314698; http://dx.doi.org/10.4161/epi.23470
  • Karin B. Michels Epigenetic Epidemiology
  • Westfall PH. Resampling-based multiple testing: Examples and methods for p-value adjustment John Wiley & Sons 1993
  • Hernandez-Vargas H, Castelino J, Silver MJ, Dominguez-Salas P, Cros MP, Durand G, Calvez-Kelm FL, Prentice AM, Wild CP, Moore SE, et al. Exposure to aflatoxin B1 in utero is associated with DNA methylation in white blood cells of infants in The Gambia. Int J Epidemiol 2015; 44(4):1238-48; PMID:25855716; http://dx.doi.org/10.1093/ije/dyv027
  • Silver MJ, Kessler NJ, Hennig BJ, Dominguez-Salas P, Laritsky E, Baker MS, Coarfa C, Hernandez-Vargas H, Castelino JM, Routledge MN, et al. Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment. Genome Biol 2015; 16:118; PMID:26062908; http://dx.doi.org/10.1186/s13059-015-0660-y
  • Dominguez-Salas P, Moore SE, Cole D, da Costa KA, Cox SE, Dyer RA, Fulford AJ, Innis SM, Waterland RA, Zeisel SH, et al. DNA methylation potential: dietary intake and blood concentrations of one-carbon metabolites and cofactors in rural African women. Am J Clin Nutr 2013; 97:1217-27; PMID:23576045; http://dx.doi.org/10.3945/ajcn.112.048462
  • Barrallo-Gimeno A, Holzschuh J, Driever W, Knapik EW. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 2004; 131:1463-77; PMID:14985255; http://dx.doi.org/10.1242/dev.01033
  • Meshcheryakova TI, Zinchenko RA, Vasilyeva TA, Marakhonov AV, Zhylina SS, Petrova NV, Kozhanova TV, Belenikin MS, Petrin AN, Mutovin GR. A Clinical and Molecular Analysis of Branchio-Oculo-Facial Syndrome Patients in Russia Revealed New Mutations in TFAP2A. Ann Hum Genet 2015; 79(2):148-52; PMID:25590586; http://dx.doi.org/10.1111/ahg.12098
  • Gerth-Kahlert C, Williamson K, Ansari M, Rainger JK, Hingst V, Zimmermann T, Tech S, Guthoff RF, van Heyningen V, FitzPatrick DR. Clinical and mutation analysis of 51 probands with anophthalmia and/or severe microphthalmia from a single center. Mol Genet Genomic Med 2013; 1:15-31; PMID:24498598; http://dx.doi.org/10.1002/mgg3.2
  • Di C, Liao S, Adamson DC, Parrett TJ, Broderick DK, Shi Q, Lengauer C, Cummins JM, Velculescu VE, Fults DW, et al. Identification of OTX2 as a Medulloblastoma Oncogene Whose Product can be Targeted by All-Trans Retinoic Acid. Cancer Res 2005; 65:919-24; PMID:15705891
  • Moritake H, Kamimura S, Nunoi H, Nakayama H, Suminoe A, Inada H, Inagaki J, Yanai F, Okamoto Y, Shinkoda Y, et al. Clinical characteristics and genetic analysis of childhood acute lymphoblastic leukemia with hemophagocytic lymphohistiocytosis: a Japanese retrospective study by the Kyushu–Yamaguchi Children's Cancer Study Group. Int J Hematol 2014; 100:70-8; PMID:24827398; http://dx.doi.org/10.1007/s12185-014-1591-1
  • Hou X, Mrug M, Yoder BK, Lefkowitz EJ, Kremmidiotis G, D'Eustachio P, Beier DR, Guay-Woodford LM. Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model of polycystic kidney disease. J Clin Invest 2002; 109:533-40; PMID:11854326; http://dx.doi.org/10.1172/JCI0214099
  • Wang X, Southard RC, Allred CD, Talbert DR, Wilson ME, Kilgore MW. MAZ drives tumor-specific expression of PPAR gamma 1 in breast cancer cells. Breast Cancer Res Treat 2008; 111:103-11; PMID:17902047; http://dx.doi.org/10.1007/s10549-007-9765-7
  • Jiao L, Li Y, Shen D, Xu C, Wang L, Huang G, Chen L, Yang Y, Yang C, Yu Y, et al. The prostate cancer-up-regulated Myc-associated zinc-finger protein (MAZ) modulates proliferation and metastasis through reciprocal regulation of androgen receptor. Med Oncol Northwood Lond Engl 2013; 30:570; http://dx.doi.org/10.1007/s12032-013-0570-3
  • Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on Folate, O.B.V. 1998 Folate
  • Boeke CE, Baccarelli A, Kleinman KP, Burris HH, Litonjua AA, Rifas-Shiman SL, Tarantini L, Gillman MW. Gestational intake of methyl donors and global LINE-1 DNA methylation in maternal and cord blood. Epigenetics 2012; 7:253-60; PMID:22430801; http://dx.doi.org/10.4161/epi.7.3.19082
  • Aarabi M, Gabriel MCS, Chan D, Behan NA, Caron M, Pastinen T, Bourque G, MacFarlane AJ, Zini A, Trasler J. High-dose folic acid supplementation alters the human sperm methylome and is influenced by the MTHFR C677T polymorphism. Hum Mol Genet 2015; 24(22):6301-13; PMID:26307085; http://dx.doi.org/10.1093/hmg/ddv338
  • Branum AM, Bailey R, Singer BJ. Dietary Supplement Use and Folate Status during Pregnancy in the United States. J Nutr 2013; 143:486-92; PMID:23365107; http://dx.doi.org/10.3945/jn.112.169987
  • Sobell J, Block G, Koslowe P, Tobin J, Andres R. Validation of a retrospective questionnaire assessing diet 10-15 years ago. Am J Epidemiol 1989; 130:173-87; PMID:2741904
  • Teschendorff AE, Zhuang J, Widschwendter M. Independent surrogate variable analysis to deconvolve confounding factors in large-scale microarray profiling studies. Bioinformatics 2011; 27:1496-505; PMID:21471010; http://dx.doi.org/10.1093/bioinformatics/btr171
  • Leek JT, Storey JD. Capturing heterogeneity in gene expression studies by surrogate variable analysis. PLoS Genet 2007; 3:1724-35; PMID:17907809; http://dx.doi.org/10.1371/journal.pgen.0030161
  • Knight RD, Nair S, Nelson SS, Afshar A, Javidan Y, Geisler R, Rauch GJ, Schilling TF. lockjaw encodes a zebrafish tfap2a required for early neural crest. Development 2003; 130:5755-68; PMID:14534133; http://dx.doi.org/10.1242/dev.00575
  • Milne E, Greenop KR, Bower C, Miller M, Bockxmeer FM, van Scott RJ, Klerk NH, de Ashton LJ, Gottardo NG, Armstrong BK. Maternal Use of Folic Acid and Other Supplements and Risk of Childhood Brain Tumors. Cancer Epidemiol Biomarkers Prev 2012; 21:1933-41; PMID:22941336; http://dx.doi.org/10.1158/1055-9965.EPI-12-0803
  • Zhang X, Inukai T, Hirose K, Akahane K, Kuroda I, Honna-Oshiro H, Kagami K, Goi K, Nakamura K, Kobayashi M, et al. Oncogenic fusion E2A-HLF sensitizes t(17;19)-positive acute lymphoblastic leukemia to TRAIL-mediated apoptosis by upregulating the expression of death receptors. Leukemia 2012; 26:2483-93; PMID:22743623; http://dx.doi.org/10.1038/leu.2012.139
  • SP1 Sp1 transcription factor [Homo sapiens (human)] - Gene - NCBI
  • LEF1 lymphoid enhancer-binding factor 1 [Homo sapiens (human)] - Gene - NCBI
  • Jensen CD, Block G, Buffler P, Ma X, Selvin S, Month S. Maternal dietary risk factors in childhood acute lymphoblastic leukemia (United States). Cancer Causes Control CCC 2004; 15:559-70; PMID:15280635; http://dx.doi.org/10.1023/B:CACO.0000036161.98734.17
  • Fortin JP, Labbe A, Lemire M, Zanke BW, Hudson TJ, Fertig EJ, Greenwood CM, Hansen KD. Functional normalization of 450k methylation array data improves replication in large cancer studies. Genome Biol 2014; 15(12):503; PMID:25599564; http://dx.doi.org/10.1186/s13059-014-0503-2
  • Joo JE, Wong EM, Baglietto L, Jung CH, Tsimiklis H, Park DJ, Wong NC, English DR, Hopper JL, Severi G, et al. The use of DNA from archival dried blood spots with the Infinium HumanMethylation450 array. BMC Biotechnol 2013; 13:23; PMID:23497093; http://dx.doi.org/10.1186/1472-6750-13-23
  • Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012; 13:86; PMID:22568884; http://dx.doi.org/10.1186/1471-2105-13-86
  • Devlin B, Roeder K. Genomic Control for Association Studies. Biometrics 1999; 55:997-1004; PMID:11315092; http://dx.doi.org/10.1111/j.0006-341X.1999.00997.x
  • R Core Team, R: A Language and Environment for Statistical Computing 2013
  • Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 2015; 43(7):e47; PMID:25605792; http://dx.doi.org/10.1093/nar/gkv007
  • Hahne F, Durinck S, Ivanek R, Mueller A, Lianoglou S, Tan G, Gviz LP. Plotting data and annotation information along genomic coordinates
  • Gjessing HK. Haplin: Analyzing Case-Parent Triad and/or Case-Control Data with SNP Haplotypes 2015
  • Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes and its Panel on Folate, Other B Vitamins, and Choline. Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline National Academies Press (US), Washington (DC) 1998
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102:15545-50; PMID:16199517; http://dx.doi.org/10.1073/pnas.0506580102
  • Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34:267-73; PMID:12808457; http://dx.doi.org/10.1038/ng1180

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