{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T17:13:39Z","timestamp":1790183619900,"version":"4.1.0"},"reference-count":57,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2019,8,1]],"date-time":"2019-08-01T00:00:00Z","timestamp":1564617600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01HD054751"],"award-info":[{"award-number":["R01HD054751"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01DK081756"],"award-info":[{"award-number":["R01DK081756"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Neuroscience"],"published-print":{"date-parts":[[2019,8]]},"DOI":"10.1016\/j.neuroscience.2019.05.044","type":"journal-article","created":{"date-parts":[[2019,5,31]],"date-time":"2019-05-31T02:40:39Z","timestamp":1559270439000},"page":"60-71","source":"Crossref","is-referenced-by-count":14,"special_numbering":"C","title":["Programmed Epigenetic DNA Methylation-Mediated Reduced Neuroprogenitor Cell Proliferation and Differentiation in Small-for-Gestational-Age Offspring"],"prefix":"10.1016","volume":"412","author":[{"given":"Mina","family":"Desai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guang","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tie","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael G.","family":"Ross","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.neuroscience.2019.05.044_bb0005","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1002\/uog.11112","article-title":"Neurodevelopmental delay in small babies at term: a systematic review","volume":"40","author":"Arcangeli","year":"2012","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0010","doi-asserted-by":"crossref","first-page":"R813","DOI":"10.1152\/ajpregu.00201.2009","article-title":"The timing of \"catch-up growth\" affects metabolism and appetite regulation in male rats born with intrauterine growth restriction","volume":"297","author":"Coupe","year":"2009","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0015","doi-asserted-by":"crossref","first-page":"R2306","DOI":"10.1152\/ajpregu.00783.2006","article-title":"Programmed metabolic syndrome: prenatal undernutrition and postweaning overnutrition","volume":"293","author":"Desai","year":"2007","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0020","doi-asserted-by":"crossref","first-page":"R91","DOI":"10.1152\/ajpregu.00340.2004","article-title":"Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition","volume":"288","author":"Desai","year":"2005","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0025","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1177\/1933719107303983","article-title":"Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring","volume":"14","author":"Desai","year":"2007","journal-title":"Reprod Sci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0030","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.appet.2016.01.023","article-title":"Programmed hyperphagia in offspring of obese dams: altered expression of hypothalamic nutrient sensors, neurogenic factors and epigenetic modulators","volume":"99","author":"Desai","year":"2016","journal-title":"Appetite"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0035","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1038\/ijo.2015.13","article-title":"Epigenomics, gestational programming and risk of metabolic syndrome","volume":"39","author":"Desai","year":"2015","journal-title":"Int J Obes (Lond)"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0040","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.brainres.2014.09.031","article-title":"Programmed hyperphagia secondary to increased hypothalamic SIRT1","volume":"1589","author":"Desai","year":"2014","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0045","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.brainres.2010.12.080","article-title":"Hypothalamic neurosphere progenitor cells in low birth-weight rat newborns: neurotrophic effects of leptin and insulin","volume":"1378","author":"Desai","year":"2011","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0050","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1093\/toxsci\/kfi178","article-title":"Comparisons of brain, uterus, and liver mRNA expression for cytochrome p450s, DNA methyltransferase-1, and catechol-o-methyltransferase in prepubertal female Sprague-Dawley rats exposed to a mixture of aryl hydrocarbon receptor agonists","volume":"86","author":"Desaulniers","year":"2005","journal-title":"Toxicol Sci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb5005","doi-asserted-by":"crossref","first-page":"1884","DOI":"10.1002\/jnr.21631","article-title":"Roles of insulin and transferrin in neural progenitor survival and proliferation","volume":"86","author":"Erickson","year":"2008","journal-title":"J Neurosci Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0055","doi-asserted-by":"crossref","first-page":"3345","DOI":"10.1242\/dev.01912","article-title":"DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling","volume":"132","author":"Fan","year":"2005","journal-title":"Development"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0060","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1002\/jnr.20404","article-title":"Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system","volume":"79","author":"Feng","year":"2005","journal-title":"J Neurosci Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0065","doi-asserted-by":"crossref","first-page":"4941","DOI":"10.1091\/mbc.e09-03-0200","article-title":"RhoG promotes neural progenitor cell proliferation in mouse cerebral cortex","volume":"20","author":"Fujimoto","year":"2009","journal-title":"Mol Biol Cell"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0070","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1177\/1933719111424448","article-title":"Mechanism of programmed obesity in intrauterine fetal growth restricted offspring: paradoxically enhanced appetite stimulation in fed and fasting states","volume":"19","author":"Fukami","year":"2012","journal-title":"Reprod Sci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0075","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1017\/S2040174413000019","article-title":"Mechanism of programmed obesity: altered central insulin sensitivity in growth-restricted juvenile female rats","volume":"4","author":"Fukami","year":"2013","journal-title":"J Dev Orig Health Dis"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0080","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1096\/fj.14-259614","article-title":"Essential nutrient supplementation prevents heritable metabolic disease in multigenerational intrauterine growth-restricted rats","volume":"29","author":"Goodspeed","year":"2015","journal-title":"FASEB J"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0085","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/s002580050019","article-title":"Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice","volume":"56","author":"Goto","year":"1994","journal-title":"Differentiation"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0090","doi-asserted-by":"crossref","first-page":"E7398","DOI":"10.1073\/pnas.1721876115","article-title":"Mouse maternal protein restriction during preimplantation alone permanently alters brain neuron proportion and adult short-term memory","volume":"115","author":"Gould","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0095","doi-asserted-by":"crossref","first-page":"2186","DOI":"10.1126\/science.1065518","article-title":"Negative regulation of neural stem\/progenitor cell proliferation by the Pten tumor suppressor gene in vivo","volume":"294","author":"Groszer","year":"2001","journal-title":"Science"},{"issue":"Suppl 1","key":"10.1016\/j.neuroscience.2019.05.044_bb0100","doi-asserted-by":"crossref","first-page":"i132","DOI":"10.1093\/cercor\/bhj166","article-title":"Notch1 expression is spatiotemporally correlated with neurogenesis and negatively regulated by Notch1-independent Hes genes in the developing nervous system","volume":"16","author":"Hatakeyama","year":"2006","journal-title":"Cereb.Cortex"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0105","doi-asserted-by":"crossref","first-page":"15599","DOI":"10.1073\/pnas.0800612105","article-title":"Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation","volume":"105","author":"Hisahara","year":"2008","journal-title":"Proc NatlAcadSci USA"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0110","first-page":"103","article-title":"The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function","volume":"7","author":"Hoeijmakers","year":"2014","journal-title":"Front Mol Neurosci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0115","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1017\/S0007114515001579","article-title":"Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction","volume":"114","author":"Hu","year":"2015","journal-title":"Br J Nutr"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0120","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1007\/s13238-012-2916-6","article-title":"Epigenetic control on cell fate choice in neural stem cells","volume":"3","author":"Hu","year":"2012","journal-title":"Protein Cell"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0125","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1007\/s00125-005-1724-4","article-title":"Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth","volume":"48","author":"Jaquet","year":"2005","journal-title":"Diabetologia"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0130","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1242\/dev.000786","article-title":"The Hes gene family: repressors and oscillators that orchestrate embryogenesis","volume":"134","author":"Kageyama","year":"2007","journal-title":"Development"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0135","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.bbr.2015.08.038","article-title":"Physical exercise affects the epigenetic programming of rat brain and modulates the adaptive response evoked by repeated restraint stress","volume":"296","author":"Kashimoto","year":"2016","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0140","first-page":"249","volume":"37","author":"Katai","year":"1997","journal-title":"Rinsho Shinkeigaku"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb5010","doi-asserted-by":"crossref","first-page":"e4213","DOI":"10.1371\/journal.pone.0004213","article-title":"Cell lineage and regional identity of cultured spinal cord neural stem cells and comparison to brain-derived neural stem cells","volume":"4","author":"Kelly","year":"2009","journal-title":"PLoS. ONE"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0145","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1097\/01.mco.0000232898.74415.42","article-title":"The Dutch famine of 1944-1945: a pathophysiological model of long-term consequences of wasting disease","volume":"9","author":"Kyle","year":"2006","journal-title":"Curr Opin Clin Nutr Metab Care"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0150","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.1016\/j.jnutbio.2012.11.001","article-title":"DNA methyltransferase mediates dose-dependent stimulation of neural stem cell proliferation by folate","volume":"24","author":"Li","year":"2013","journal-title":"J Nutr Biochem"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0155","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1017\/S0029665110004027","article-title":"Effect of maternal diet on the epigenome: implications for human metabolic disease","volume":"70","author":"Lillycrop","year":"2011","journal-title":"Proc Nutr Soc"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0160","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1071\/RD15130","article-title":"Effect of intra-uterine growth restriction on long-term fertility in boars","volume":"29","author":"Lin","year":"2017","journal-title":"Reprod Fertil Dev"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0165","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1080\/1745039X.2011.594352","article-title":"Effects of maternal folic acid supplementation on morphology and apoptosis-related gene expression in jejunum of newborn intrauterine growth retarded piglets","volume":"65","author":"Liu","year":"2011","journal-title":"Arch Anim Nutr"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0170","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1007\/s12013-012-9503-6","article-title":"Folic acid acts through DNA methyltransferases to induce the differentiation of neural stem cells into neurons","volume":"66","author":"Luo","year":"2013","journal-title":"Cell Biochem Biophys"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0175","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1007\/s00125-009-1650-y","article-title":"Independent effects of weight gain and fetal programming on metabolic complications in adults born small for gestational age","volume":"53","author":"Meas","year":"2010","journal-title":"Diabetologia"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb5000","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/0022-1759(83)90303-4","article-title":"Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays","volume":"65","author":"Mosmann","year":"1983","journal-title":"J. Immunol. Methods"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0180","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.devcel.2008.12.014","article-title":"Committed neuronal precursors confer astrocytic potential on residual neural precursor cells","volume":"16","author":"Namihira","year":"2009","journal-title":"Dev Cell"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0185","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neures.2015.01.014","article-title":"Expression of DNMT1 in neural stem\/precursor cells is critical for survival of newly generated neurons in the adult hippocampus","volume":"95","author":"Noguchi","year":"2015","journal-title":"Neurosci Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0190","doi-asserted-by":"crossref","first-page":"F197","DOI":"10.1136\/archdischild-2016-310791","article-title":"Thin-for-gestational age infants are at increased risk of neurodevelopmental delay at 2 years","volume":"102","author":"O'Neill","year":"2017","journal-title":"Arch Dis Child Fetal Neonatal Ed"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0195","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.reprotox.2005.04.005","article-title":"Prenatal exposure to the Dutch famine and disease in later life: an overview","volume":"20","author":"Painter","year":"2005","journal-title":"Reprod Toxicol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0200","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.maturitas.2011.06.017","article-title":"Hungry in the womb: what are the consequences? Lessons from the Dutch famine","volume":"70","author":"Roseboom","year":"2011","journal-title":"Maturitas"},{"issue":"Suppl 1","key":"10.1016\/j.neuroscience.2019.05.044_bb0205","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1159\/000360508","article-title":"Developmental programming of appetite\/satiety","volume":"64","author":"Ross","year":"2014","journal-title":"Ann Nutr Metab"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0210","doi-asserted-by":"crossref","first-page":"213","DOI":"10.2174\/156720507780362056","article-title":"Gestational programming of offspring obesity: a potential contributor to Alzheimer's disease","volume":"4","author":"Ross","year":"2007","journal-title":"Curr Alzheimer Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0215","doi-asserted-by":"crossref","first-page":"5332","DOI":"10.1093\/nar\/gks207","article-title":"Neural stem cells exposed to BrdU lose their global DNA methylation and undergo astrocytic differentiation","volume":"40","author":"Schneider","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0220","doi-asserted-by":"crossref","first-page":"1953S","DOI":"10.3945\/ajcn.110.001040","article-title":"The early programming of metabolic health: is epigenetic setting the missing link?","volume":"94","author":"Sebert","year":"2011","journal-title":"Am J Clin Nutr"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0225","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/fnins.2018.00005","article-title":"DNA-methylation: master or slave of neural fate decisions?","volume":"12","author":"Stricker","year":"2018","journal-title":"Front Neurosci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0230","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1016\/S1534-5807(01)00101-0","article-title":"DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain","volume":"1","author":"Takizawa","year":"2001","journal-title":"Dev Cell"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0235","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.alcohol.2014.06.001","article-title":"Prenatal alcohol exposure alters expression of neurogenesis-related genes in an ex vivo cell culture model","volume":"48","author":"Tyler","year":"2014","journal-title":"Alcohol"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0240","doi-asserted-by":"crossref","first-page":"E83","DOI":"10.1152\/ajpendo.2000.279.1.E83","article-title":"Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition","volume":"279","author":"Vickers","year":"2000","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0245","doi-asserted-by":"crossref","first-page":"401","DOI":"10.2217\/epi.15.119","article-title":"DNA methylation dynamics in neurogenesis","volume":"8","author":"Wang","year":"2016","journal-title":"Epigenomics"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0250","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/B978-0-12-800222-3.00011-5","article-title":"Integrating early life experience, gene expression, brain development, and emergent phenotypes: unraveling the thread of nature via nurture","volume":"86","author":"Weaver","year":"2014","journal-title":"Adv Genet"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0255","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1101\/gad.241547.114","article-title":"Unlocking epigenetic codes in neurogenesis","volume":"28","author":"Yao","year":"2014","journal-title":"Genes Dev"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0260","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1177\/1933719108316982","article-title":"Programmed alterations in hypothalamic neuronal orexigenic responses to ghrelin following gestational nutrient restriction","volume":"15","author":"Yousheng","year":"2008","journal-title":"Reprod Sci"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0265","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.jnutbio.2013.12.010","article-title":"Folic acid stimulation of neural stem cell proliferation is associated with altered methylation profile of PI3K\/Akt\/CREB","volume":"25","author":"Yu","year":"2014","journal-title":"J Nutr Biochem"},{"key":"10.1016\/j.neuroscience.2019.05.044_bb0270","doi-asserted-by":"crossref","first-page":"353","DOI":"10.3177\/jnsv.54.353","article-title":"Effects of folate on notch signaling and cell proliferation in neural stem cells of neonatal rats in vitro","volume":"54","author":"Zhang","year":"2008","journal-title":"J Nutr Sci Vitaminol (Tokyo)"}],"container-title":["Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452219303744?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452219303744?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,9,23]],"date-time":"2019-09-23T23:39:20Z","timestamp":1569281960000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0306452219303744"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8]]},"references-count":57,"alternative-id":["S0306452219303744"],"URL":"https:\/\/doi.org\/10.1016\/j.neuroscience.2019.05.044","relation":{},"ISSN":["0306-4522"],"issn-type":[{"value":"0306-4522","type":"print"}],"subject":[],"published":{"date-parts":[[2019,8]]}}}