{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,25]],"date-time":"2026-07-25T04:22:05Z","timestamp":1784953325561,"version":"3.55.0"},"reference-count":95,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,3,31]],"date-time":"2022-03-31T00:00:00Z","timestamp":1648684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Endocrinol."],"abstract":"<jats:p>A poorly functioning placenta results in impaired exchanges of oxygen, nutrition, wastes and hormones between the mother and her fetus. This can lead to restriction of fetal growth. These growth restricted babies are at increased risk of developing chronic diseases, such as type-2 diabetes, hypertension, and kidney disease, later in life. Animal studies have shown that growth restricted phenotypes are sex-dependent and can be transmitted to subsequent generations through both the paternal and maternal lineages. Altered epigenetic mechanisms, specifically changes in DNA methylation, histone modifications, and non-coding RNAs that regulate expression of genes that are important for fetal development have been shown to be associated with the transmission pattern of growth restricted phenotypes. This review will discuss the subsequent health outcomes in the offspring after growth restriction and the transmission patterns of these diseases. Evidence of altered epigenetic mechanisms in association with fetal growth restriction will also be reviewed.<\/jats:p>","DOI":"10.3389\/fendo.2022.838737","type":"journal-article","created":{"date-parts":[[2022,3,31]],"date-time":"2022-03-31T06:56:05Z","timestamp":1648709765000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":23,"title":["Epigenetic Mechanisms Responsible for the Transgenerational Inheritance of Intrauterine Growth Restriction Phenotypes"],"prefix":"10.3389","volume":"13","author":[{"given":"Thu Ngoc Anh","family":"Doan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa K.","family":"Akison","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tina","family":"Bianco-Miotto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,3,31]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1523-1755.2005.09712.x","article-title":"Low Birth Weight, Nephron Number, and Kidney Disease","volume":"68","author":"Luyckx","year":"2005","journal-title":"Kidney Int"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.2009.170407","article-title":"Uteroplacental Insufficiency Causes a Nephron Deficit, Modest Renal Insufficiency But No Hypertension With Ageing in Female Rats","volume":"587","author":"Moritz","year":"2009","journal-title":"J Physiol"},{"key":"B3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1159\/000365790","article-title":"Global Prevalence of Small for Gestational Age Births","volume":"81","author":"Black","year":"2015","journal-title":"Nestle Nutr Inst Workshop Ser"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(13)60311-6","article-title":"Effect of Fetal and Child Health on Kidney Development and Long-Term Risk of Hypertension and Kidney Disease","volume":"382","author":"Luyckx","year":"2013","journal-title":"Lancet"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1016\/j.puhe.2012.03.010","article-title":"Intra-Uterine Growth Restriction and Increased Risk of Hypertension in Adult Life: A Follow-Up Study of 50-Year-Olds","volume":"126","author":"Spence","year":"2012","journal-title":"Public Health"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1001\/archpedi.160.9.977","article-title":"Fetal Origin of Childhood Disease: Intrauterine Growth Restriction in Term Infants and Risk for Hypertension at 6 Years of Age","volume":"160","author":"Shankaran","year":"2006","journal-title":"Arch Pediatr Adolesc Med"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa020549","article-title":"Nephron Number in Patients With Primary Hypertension","volume":"348","author":"Keller","year":"2003","journal-title":"N Engl J Med"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1038\/sj.ki.5000041","article-title":"Hypertension, Glomerular Number, and Birth Weight in African Americans and White Subjects in the Southeastern United States","volume":"69","author":"Hughson","year":"2006","journal-title":"Kidney Int"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1177\/1470320314543808","article-title":"Effects of a Restricted Fetal Growth Environment on Human Kidney Morphology, Cell Apoptosis and Gene Expression","volume":"16","author":"Wang","year":"2014","journal-title":"J Renin Angiotensin Aldosterone Syst"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/ki.2008.153","article-title":"Growth Restriction Before or After Birth Reduces Nephron Number and Increases Blood Pressure in Male Rats","volume":"74","author":"Wlodek","year":"2008","journal-title":"Kidney Int"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1111\/apha.12982","article-title":"Uteroplacental Insufficiency in Rats Induces Renal Apoptosis and Delays Nephrogenesis Completion","volume":"222","author":"Cuffe","year":"2018","journal-title":"Acta Physiol"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1530\/JOE-12-0560","article-title":"Transgenerational Metabolic Outcomes Associated With Uteroplacental Insufficiency","volume":"217","author":"Melanie","year":"2013","journal-title":"J Endocrinol"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1071\/RD13133","article-title":"Transgenerational Programming of Fetal Nephron Deficits and Sex-Specific Adult Hypertension in Rats","volume":"26","author":"Gallo","year":"2014","journal-title":"Reprod Fertil Dev"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1111\/1440-1681.12303","article-title":"Transgenerational Left Ventricular Hypertrophy and Hypertension in Offspring After Uteroplacental Insufficiency in Male Rats","volume":"41","author":"Master","year":"2014","journal-title":"Clin Exp Pharmacol Physiol"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1016\/j.earlhumdev.2008.12.015","article-title":"Uteroplacental Insufficiency Affects Kidney VEGF Expression in a Model of IUGR With Compensatory Glomerular Hypertrophy and Hypertension","volume":"85","author":"Baserga","year":"2009","journal-title":"Early Hum Dev"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1210\/en.2016-1335","article-title":"Sex-Specific Metabolic Outcomes in Offspring of Female Rats Born Small or Exposed to Stress During Pregnancy","volume":"157","author":"Jefferies","year":"2016","journal-title":"Endocrinology"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1016\/j.semcdb.2018.05.025","article-title":"Transgenerational Programming of Nephron Deficits and Hypertension","author":"Briffa","year":"2018","journal-title":"Semin Cell Dev Biol"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1159\/000086136","article-title":"Experimental Intrauterine Growth Retardation in the Rat Causes a Reduction of Pancreatic B-Cell Mass, Which Persists Into Adulthood","volume":"88","author":"Styrud","year":"2005","journal-title":"Neonatology"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1007\/BF00399095","article-title":"Type 2 (non-Insulin-Dependent) Diabetes Mellitus, Hypertension and Hyperlipidaemia (Syndrome X): Relation to Reduced Fetal Growth","volume":"36","author":"Barker","year":"1993","journal-title":"Diabetologia"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1006\/pmed.1999.0577","article-title":"Relationship Between Birth Weight and Blood Pressure in Adolescence","volume":"29","author":"Rabbia","year":"1999","journal-title":"Prev Med"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-130-4_part_1-199902160-00005","article-title":"Birthweight and the Risk for Type 2 Diabetes Mellitus in Adult Women","volume":"130","author":"Rich-Edwards","year":"1999","journal-title":"Ann Intern Med"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1210\/jcem.85.4.6544","article-title":"Insulin Resistance Early in Adulthood in Subjects Born With Intrauterine Growth Retardation","volume":"85","author":"Gaboriau","year":"2000","journal-title":"J Clin Endocrinol Metab"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1007\/s00431-002-0985-x","article-title":"The Influence of Age and Gender on the Relationship Between Birth Weight and Blood Pressure in Childhood: A Study Using 24-Hour and Casual Blood Pressure","volume":"161","author":"O\u2019Sullivan","year":"2002","journal-title":"Eur J Pediatr"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1542\/peds.2010-2213","article-title":"Birth Weight, Postnatal Weight Change, and Risk for High Blood Pressure Among Chinese Children","volume":"127","author":"Bowers","year":"2011","journal-title":"Pediatrics"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2005.07.004","article-title":"Unbalanced Placental Expression of Imprinted Genes in Human Intrauterine Growth Restriction","volume":"27","author":"McMinn","year":"2006","journal-title":"Placenta"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1093\/ije\/dym126","article-title":"Cohort Profile: The Dutch Hunger Winter Families Study","volume":"36","author":"Lumey","year":"2007","journal-title":"Int J Epidemiol"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0008887","article-title":"Cytosine Methylation Dysregulation in Neonates Following Intrauterine Growth Restriction","volume":"5","author":"Einstein","year":"2010","journal-title":"PLoS One"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1007\/s10815-014-0278-0","article-title":"Relevance of Genomic Imprinting in Intrauterine Human Growth Expression of CDKN1C, H19, IGF2, KCNQ1 and PHLDA2 Imprinted Genes","volume":"31","author":"Cordeiro","year":"2014","journal-title":"J Assist Reprod Genet"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2013.11.003","article-title":"The Long non-Coding RNA NEAT1 is Increased in IUGR Placentas, Leading to Potential New Hypotheses of IUGR Origin\/Development","volume":"35","author":"Gremlich","year":"2014","journal-title":"Placenta"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0138383","article-title":"Cardiovascular and Cerebrovascular Disease Associated microRNAs are Dysregulated in Placental Tissues Affected With Gestational Hypertension, Preeclampsia and Intrauterine Growth Restriction","volume":"10","author":"Hromadnikova","year":"2015","journal-title":"PLoS One"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.9534","article-title":"H19 Long Noncoding RNA Alters Trophoblast Cell Migration and Invasion by Regulating T\u03b2r3 in Placentae With Fetal Growth Restriction","volume":"7","author":"Zuckerwise","year":"2016","journal-title":"Oncotarget"},{"key":"B32","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.placenta.2017.05.008","article-title":"Mitochondrial DNA Content and Methylation in Fetal Cord Blood of Pregnancies With Placental Insufficiency","volume":"55","author":"Novielli","year":"2017","journal-title":"Placenta"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1186\/s12920-019-0548-x","article-title":"Placental microRNAs in Pregnancies With Early Onset Intrauterine Growth Restriction and Preeclampsia: Potential Impact on Gene Expression and Pathophysiology","volume":"12","author":"Awamleh","year":"2019","journal-title":"BMC Med Genomics"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1016\/j.pedneo.2019.01.001","article-title":"DNA Methylation of the Rtl1 Promoter in the Placentas With Fetal Growth Restriction","volume":"60","author":"Fujioka","year":"2019","journal-title":"Pediatr Neonatol"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1210\/jc.2018-02346","article-title":"Umbilical Cord miRNAs in Small-for-Gestational-Age Children and Association With Catch-Up Growth: A Pilot Study","volume":"104","author":"Mas-Par\u00e9s","year":"2019","journal-title":"J Clin Endocrinol Metab"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1007\/s11033-020-05705-y","article-title":"Potential Pathophysiological Role of microRNA 193b-5p in Human Placentae From Pregnancies Complicated by Preeclampsia and Intrauterine Growth Restriction","volume":"47","author":"Awamleh","year":"2020","journal-title":"Mol Biol Rep"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1016\/j.preghy.2020.01.002","article-title":"Identification of miR-210-5p in Human Placentae From Pregnancies Complicated by Preeclampsia and Intrauterine Growth Restriction, and its Potential Role in the Pregnancy Complications","volume":"19","author":"Awamleh","year":"2020","journal-title":"Pregnancy Hypertens"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21103597","article-title":"Placental Microarray Profiling Reveals Common mRNA and lncRNA Expression Patterns in Preeclampsia and Intrauterine Growth Restriction","volume":"21","author":"Medina-Bastidas","year":"2020","journal-title":"Int J Mol Sci"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1186\/s13148-019-0630-4","article-title":"Differences in Expression Rather Than Methylation at Placenta-Specific Imprinted Loci is Associated With Intrauterine Growth Restriction","volume":"11","author":"Monteagudo-S\u00e1nchez","year":"2019","journal-title":"Clin Epigenet"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.3390\/ijms20061510","article-title":"Placenta Transcriptome Profiling in Intrauterine Growth Restriction (IUGR)","volume":"20","author":"Majewska","year":"2019","journal-title":"Int J Mol Sci"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1177\/1470320316654810","article-title":"Increased Renal Apoptosis and Reduced Renin\u2013Angiotensin System in Fetal Growth Restriction","volume":"17","author":"Wang","year":"2016","journal-title":"J Renin Angiotensin Aldosterone Syst"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.2337\/diabetes.50.10.2279","article-title":"Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat","volume":"50","author":"Simmons","year":"2001","journal-title":"Diabetes"},{"key":"B43","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1161\/01.HYP.0000053448.95913.3D","article-title":"Placental Insufficiency Leads to Development of Hypertension in Growth-Restricted Offspring","volume":"41","author":"Alexander","year":"2003","journal-title":"Hypertension"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00201.2003","article-title":"Uteroplacental Insufficiency Increases Apoptosis and Alters P53 Gene Methylation in the Full-Term IUGR Rat Kidney","volume":"285","author":"Pham","year":"2003","journal-title":"Am J Physiology-Regulat Integr Comp Physiol"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.2337\/diabetes.53.10.2617","article-title":"Hepatic Insulin Resistance Precedes the Development of Diabetes in a Model of Intrauterine Growth Retardation","volume":"53","author":"Vuguin","year":"2004","journal-title":"Diabetes"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1007\/s00125-006-0196-5","article-title":"Glucose Metabolism is Altered in the Adequately-Nourished Grand-Offspring (F3 Generation) of Rats Malnourished During Gestation and Perinatal Life","volume":"49","author":"Benyshek","year":"2006","journal-title":"Diabetologia"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1210\/en.2008-0128","article-title":"Improved Lactational Nutrition and Postnatal Growth Ameliorates Impairment of Glucose Tolerance by Uteroplacental Insufficiency in Male Rat Offspring","volume":"149","author":"Mibus","year":"2008","journal-title":"Endocrinology"},{"key":"B48","doi-asserted-by":"publisher","first-page":"1997","DOI":"10.1113\/jphysiol.2010.187849","article-title":"Uteroplacental Insufficiency Programs Regional Vascular Dysfunction and Alters Arterial Stiffness in Female Offspring","volume":"588","author":"Mazzuca","year":"2010","journal-title":"J Physiol"},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.1016\/j.cmet.2014.03.026","article-title":"In Utero Undernutrition in Male Mice Programs Liver Lipid Metabolism in the Second-Generation Offspring Involving Altered Lxra DNA Methylation","volume":"19","author":"Mart\u00ednez","year":"2014","journal-title":"Cell Metab"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1111\/nep.12340","article-title":"Apoptosis in the Kidneys of Rats That Experienced Intrauterine Growth Restriction","volume":"20","author":"He","year":"2015","journal-title":"Nephrology"},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0121587","article-title":"Long non-Coding RNA Expression Profile in the Kidneys of Male, Low Birth Weight Rats Exposed to Maternal Protein Restriction at Postnatal Day 1 and Day 10","volume":"10","author":"Li","year":"2015","journal-title":"PLoS One"},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1016\/j.jksus.2016.03.004","article-title":"Glomerular Filtration Barrier in Rat Offspring Exposed to Maternal Undernutrition","volume":"29","author":"Alwasel","year":"2017","journal-title":"J King Saud Univ - Sci"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1017\/S2040174420001257","article-title":"Epigenetic Mechanisms Involved in Intrauterine Growth Restriction and Aberrant Kidney Development and Function","volume":"12","author":"Doan","year":"2020","journal-title":"J Dev Orig Health Dis"},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1002\/cbf.3575","article-title":"The Mechanisms of lncRNA Tug1 in Islet Dysfunction in a Mouse Model of Intrauterine Growth Retardation","volume":"38","author":"Li","year":"2020","journal-title":"Cell Biochem Funct"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.1186\/s12916-014-0121-6","article-title":"Ancestral Exposure to Stress Epigenetically Programs Preterm Birth Risk and Adverse Maternal and Newborn Outcomes","volume":"12","author":"Yao","year":"2014","journal-title":"BMC Med"},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1161\/HYPERTENSIONAHA.119.13634","article-title":"Intrauterine Growth\u00a0Restriction Programs Intergenerational Transmission of Pulmonary\u00a0Arterial\u00a0Hypertension and Endothelial Dysfunction via Sperm Epigenetic Modifications","volume":"74","author":"Zhang","year":"2019","journal-title":"Hypertension"},{"key":"B57","doi-asserted-by":"publisher","DOI":"10.1152\/ajpendo.00462.2006","article-title":"Transgenerational Inheritance of the Insulin-Resistant Phenotype in Embryo-Transferred Intrauterine Growth-Restricted Adult Female Rat Offspring","volume":"292","author":"Thamotharan","year":"2007","journal-title":"Am J\u00a0Physiology-Endocrinol Metab"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00106.2004","article-title":"Intergenerational Consequences of Fetal Programming by In Utero Exposure to Glucocorticoids in Rats","volume":"288","author":"Drake","year":"2005","journal-title":"Am J Physiology-Regulat Integr Comp Physiol"},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.1042\/cs20070302","article-title":"Protein Restriction During Gestation and\/or Lactation Causes Adverse Transgenerational Effects on Biometry and Glucose Metabolism in F1 and F2 Progenies of Rats","volume":"114","author":"Pinheiro","year":"2008","journal-title":"Clin Sci (Lond)"},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2017.04.020","article-title":"Integrated Analysis of Genome-Wide DNA Methylation and Gene Expression Data Provide a Regulatory Network in Intrauterine Growth Restriction","volume":"179","author":"Ding","year":"2017","journal-title":"Life Sci"},{"key":"B61","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1152\/physiolgenomics.00042.2004","article-title":"Uteroplacental Insufficiency Alters DNA Methylation, One-Carbon Metabolism, and Histone Acetylation in IUGR Rats","volume":"18","author":"MacLennan","year":"2004","journal-title":"Physiol Genomics"},{"key":"B62","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1152\/physiolgenomics.00093.2005","article-title":"Uteroplacental Insufficiency Affects Epigenetic Determinants of Chromatin Structure in Brains of Neonatal and Juvenile IUGR Rats","volume":"25","author":"Ke","year":"2006","journal-title":"Physiol Genomics"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1172\/JCI33655","article-title":"Development of Type 2 Diabetes Following Intrauterine Growth Retardation in Rats Is Associated With Progressive Epigenetic Silencing of Pdx1","volume":"118","author":"Park","year":"2008","journal-title":"J Clin Invest"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-10-478","article-title":"Maternal High Fat Diet During Pregnancy and Lactation Alters Hepatic Expression of Insulin Like Growth Factor-2 and Key microRNAs in the Adult Offspring","volume":"10","author":"Zhang","year":"2009","journal-title":"BMC Genomics"},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M109.095133","article-title":"Experimental Intrauterine Growth Restriction Induces Alterations in DNA Methylation and Gene Expression in Pancreatic Islets of Rats","volume":"285","author":"Thompson","year":"2010","journal-title":"J Biol Chem"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajog.2016.01.194","article-title":"Alterations in Expression of Imprinted Genes From the H19\/Igf2 Loci in a Multigenerational Model of Intrauterine Growth Restriction (IUGR)","volume":"214","author":"Gonzalez-Rodriguez","year":"2016","journal-title":"Am J Obstet Gynecol"},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0190445","article-title":"Lung microRNA Deregulation Associated With Impaired Alveolarization in Rats After Intrauterine Growth Restriction","volume":"12","author":"Dravet-Gounot","year":"2017","journal-title":"PLoS One"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00155.2018","article-title":"Role of miR-29 in Mediating Offspring Lung Phenotype in a Rodent Model of Intrauterine Growth Restriction","volume":"315","author":"Chuang","year":"2018","journal-title":"Am J Physiology-Regulat Integr Comp Physiol"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1152\/ajpgi.00052.2010","article-title":"Epigenetics of Programmed Obesity: Alteration in IUGR Rat Hepatic IGF1 mRNA Expression and Histone Structure in Rapid vs. Delayed Postnatal Catch-Up Growth","volume":"299","author":"Tosh","year":"2010","journal-title":"Am J Physiol Gastrointest Liver Physiol"},{"key":"B70","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/j.cell.2013.09.002","article-title":"Mutation in Folate Metabolism Causes Epigenetic Instability and Transgenerational Effects on Development","volume":"155","author":"Padmanabhan","year":"2013","journal-title":"Cell"},{"key":"B71","doi-asserted-by":"publisher","DOI":"10.1007\/s004670000457","article-title":"Experimental Intrauterine Growth Retardation Alters Renal Development","volume":"15","author":"Bassan","year":"2000","journal-title":"Pediatr Nephrol"},{"key":"B72","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajog.2004.01.050","article-title":"Cardiovascular and Renal Disease in the Adolescent Guinea Pig After Chronic Placental Insufficiency","volume":"191","author":"Briscoe","year":"2004","journal-title":"Am J Obstet Gynecol"},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.1038\/nrneph.2012.38","article-title":"The Long-Term Renal and Cardiovascular Consequences of Prematurity","volume":"8","author":"Abitbol","year":"2012","journal-title":"Nat Rev Nephrol"},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.1093\/abbs\/gmw088","article-title":"Decreased Expression of GLUT4 in Male CG-IUGR Rats may Play a Vital Role in Their Increased Susceptibility to Diabetes Mellitus in Adulthood","volume":"48","author":"Duan","year":"2016","journal-title":"Acta Biochim Biophys Sin"},{"key":"B75","doi-asserted-by":"publisher","first-page":"65","DOI":"10.2337\/db11-1727","article-title":"Increased Hepatic Glucose Production in Fetal Sheep With Intrauterine Growth Restriction is Not Suppressed by Insulin","volume":"62","author":"Thorn","year":"2013","journal-title":"Diabetes"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2796.2007.01809.x","article-title":"The Developmental Origins of Adult Disease","volume":"23","author":"Barker","year":"2004","journal-title":"J Am Coll Nutr"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.2991\/jegh.k.191028.001","article-title":"Epidemiology of Type 2 Diabetes - Global Burden of Disease and Forecasted Trends","volume":"10","author":"Khan","year":"2020","journal-title":"J Epidemiol Glob Health"},{"key":"B78","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(19)32977-0","article-title":"The Global Burden of Chronic Kidney Disease","volume":"395","author":"Cockwell","year":"2020","journal-title":"Lancet"},{"key":"B79","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(21)01330-1","article-title":"Worldwide Trends in Hypertension Prevalence and Progress in Treatment and Control From 1990 to 2019: A Pooled Analysis of 1201 Population-Representative Studies With 104 Million Participants","volume":"398","author":"Zhou","year":"2021","journal-title":"Lancet"},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1159\/000358666","article-title":"Analysis of Genomic DNA Methylation Levels in Human Placenta Using Liquid Chromatography-Electrospray Ionization Tandem Mass Spectrometry","volume":"33","author":"Dwi Putra","year":"2014","journal-title":"Cell Physiol Biochem"},{"key":"B81","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1093\/humupd\/dmq052","article-title":"Epigenetics and the Placenta","volume":"17","author":"Nelissen","year":"2010","journal-title":"Hum Reprod Update"},{"key":"B82","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.22.9.3157-3173.2002","article-title":"Molecular Mechanisms of Gene Silencing Mediated by DNA Methylation","volume":"22","author":"Curradi","year":"2002","journal-title":"Mol Cell Biol"},{"key":"B83","doi-asserted-by":"publisher","DOI":"10.1161\/circulationaha.110.956839","article-title":"Epigenetic Modifications: Basic Mechanisms and Role in Cardiovascular Disease","volume":"123","author":"Handy","year":"2011","journal-title":"Circulation"},{"key":"B84","doi-asserted-by":"publisher","DOI":"10.1007\/pl00000895","article-title":"Emerging Connections Between DNA Methylation and Histone Acetylation","volume":"58","author":"Dobosy","year":"2001","journal-title":"Cell Mol Life Sci CMLS"},{"key":"B85","doi-asserted-by":"publisher","DOI":"10.1002\/bies.201100084","article-title":"Long non-Coding RNA Modifies Chromatin","volume":"33","author":"Saxena","year":"2011","journal-title":"Bioessays"},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.3390\/cancers10110440","article-title":"Epigenetic Regulation by lncRNAs: An Overview Focused on UCA1 in Colorectal Cancer","volume":"10","author":"Neve","year":"2018","journal-title":"Cancers (Basel)"},{"key":"B87","doi-asserted-by":"publisher","first-page":"3","DOI":"10.3892\/or.2016.5236","article-title":"Non-Coding RNAs as Regulators in Epigenetics (Review)","volume":"37","author":"Wei","year":"2017","journal-title":"Oncol Rep"},{"key":"B88","doi-asserted-by":"crossref","DOI":"10.1007\/978-981-15-1671-9_7","article-title":"Non-Coding RNAs as Epigenetic Gene Regulators in Cardiovascular Diseases","volume-title":"Non-Coding RNAs in Cardiovascular Diseases","author":"Jiang","year":"2020"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.3390\/ijms22063014","article-title":"Non-Coding RNAs in Hereditary Kidney Disorders","volume":"22","author":"Zhou","year":"2021","journal-title":"Int J Mol Sci"},{"key":"B90","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0806560105","article-title":"Persistent Epigenetic Differences Associated With Prenatal Exposure to Famine in Humans","volume":"105","author":"Heijmans","year":"2008","journal-title":"Proc Natl Acad Sci"},{"key":"B91","doi-asserted-by":"publisher","first-page":"1","DOI":"10.4161\/15592294.2014.989741","article-title":"Novel DNA Methylation Profiles Associated With Key Gene Regulation and Transcription Pathways in Blood and Placenta of Growth-Restricted Neonates","volume":"10","author":"Hillman","year":"2015","journal-title":"Epigenetics"},{"key":"B92","doi-asserted-by":"publisher","DOI":"10.1096\/fj.08-124768","article-title":"Epigenetics: Intrauterine Growth Retardation (IUGR) Modifies the Histone Code Along the Rat Hepatic IGF-1 Gene","volume":"23","author":"Fu","year":"2009","journal-title":"FASEB J"},{"key":"B93","doi-asserted-by":"publisher","DOI":"10.1016\/j.molmet.2020.101083","article-title":"Changes in Circulating Mirna19a-3p Precede Insulin Resistance Programmed by Intra-Uterine Growth Retardation in Mice","volume":"42","author":"Saget","year":"2020","journal-title":"Mol Metab"},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.1186\/s13148-016-0238-x","article-title":"Genome-Wide Placental DNA Methylation Analysis of Severely Growth-Discordant Monochorionic Twins Reveals Novel Epigenetic Targets for Intrauterine Growth Restriction","volume":"8","author":"Roifman","year":"2016","journal-title":"Clin Epigenet"},{"key":"B95","first-page":"25","article-title":"Expression of Long Non-Coding RNAs in Placentas of Intrauterine Growth Restriction (IUGR) Pregnancies","volume":"8","author":"Azari","year":"2019","journal-title":"Rep Biochem Mol Biol"}],"container-title":["Frontiers in Endocrinology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fendo.2022.838737\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,31]],"date-time":"2022-03-31T06:56:10Z","timestamp":1648709770000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fendo.2022.838737\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,31]]},"references-count":95,"alternative-id":["10.3389\/fendo.2022.838737"],"URL":"https:\/\/doi.org\/10.3389\/fendo.2022.838737","relation":{},"ISSN":["1664-2392"],"issn-type":[{"value":"1664-2392","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,31]]},"article-number":"838737"}}