{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T05:14:25Z","timestamp":1790745265341,"version":"4.1.0"},"reference-count":34,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T00:00:00Z","timestamp":1583452800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0229904","type":"journal-article","created":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T18:29:37Z","timestamp":1583519377000},"page":"e0229904","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":34,"title":["Advanced paternal age directly impacts mouse embryonic placental imprinting"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7876-0462","authenticated-orcid":true,"given":"Michelle M.","family":"Denomme","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason C.","family":"Parks","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6142-032X","authenticated-orcid":true,"given":"Blair R.","family":"McCallie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan I.","family":"McCubbin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William B.","family":"Schoolcraft","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mandy G.","family":"Katz-Jaffe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2020,3,6]]},"reference":[{"key":"pone.0229904.ref001","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/978-981-10-5526-3_8","article-title":"Risk of Neurodevelopmental Disease by Paternal Aging: A Possible Influence of Epigenetic Alteration in Sperm","volume":"1012","author":"R Kimura","year":"2018","journal-title":"Adv Exp Med Biol"},{"issue":"5","key":"pone.0229904.ref002","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1177\/1557988312440718","article-title":"The effect of paternal age on fetal birth outcomes","volume":"6","author":"AP Alio","year":"2012","journal-title":"Am J Mens Health"},{"issue":"2","key":"pone.0229904.ref003","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1002\/pd.5402","article-title":"Advanced paternal age, infertility, and reproductive risks: A review of the literature","volume":"39","author":"JS Brandt","year":"2019","journal-title":"Prenat Diagn"},{"key":"pone.0229904.ref004","doi-asserted-by":"crossref","first-page":"k4372","DOI":"10.1136\/bmj.k4372","article-title":"Association of paternal age with perinatal outcomes between 2007 and 2016 in the United States: population based cohort study","volume":"363","author":"YS Khandwala","year":"2018","journal-title":"BMJ"},{"issue":"2","key":"pone.0229904.ref005","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1095\/biolreprod.108.073395","article-title":"Delayed fatherhood in mice decreases reproductive fitness and longevity of offspring","volume":"80","author":"S Garcia-Palomares","year":"2009","journal-title":"Biol Reprod"},{"issue":"2","key":"pone.0229904.ref006","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1095\/biolreprod.108.072066","article-title":"Long-term effects of delayed fatherhood in mice on postnatal development and behavioral traits of offspring","volume":"80","author":"S Garcia-Palomares","year":"2009","journal-title":"Biol Reprod"},{"issue":"1","key":"pone.0229904.ref007","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.fertnstert.2013.03.021","article-title":"Aging sperm negatively impacts in vivo and in vitro reproduction: a longitudinal murine study","volume":"100","author":"MG Katz-Jaffe","year":"2013","journal-title":"Fertil Steril"},{"issue":"22","key":"pone.0229904.ref008","first-page":"4996","article-title":"Paternal age effects on sperm FOXK1 and KCNA7 methylation and transmission into the next generation","volume":"25","author":"S Atsem","year":"2016","journal-title":"Hum Mol Genet"},{"issue":"7","key":"pone.0229904.ref009","doi-asserted-by":"crossref","first-page":"e1004458","DOI":"10.1371\/journal.pgen.1004458","article-title":"Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility","volume":"10","author":"TG Jenkins","year":"2014","journal-title":"PLoS Genet"},{"issue":"11","key":"pone.0229904.ref010","doi-asserted-by":"crossref","first-page":"e0167127","DOI":"10.1371\/journal.pone.0167127","article-title":"Genome-Scale Assessment of Age-Related DNA Methylation Changes in Mouse Spermatozoa","volume":"11","author":"N Kobayashi","year":"2016","journal-title":"PLoS One"},{"issue":"8","key":"pone.0229904.ref011","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1038\/mp.2014.84","article-title":"Age-related sperm DNA methylation changes are transmitted to offspring and associated with abnormal behavior and dysregulated gene expression","volume":"20","author":"MH Milekic","year":"2015","journal-title":"Mol Psychiatry"},{"issue":"3","key":"pone.0229904.ref012","doi-asserted-by":"crossref","first-page":"e0193271","DOI":"10.1371\/journal.pone.0193271","article-title":"Placental CpG methylation of infants born extremely preterm predicts cognitive impairment later in life","volume":"13","author":"SK Tilley","year":"2018","journal-title":"PLoS One"},{"issue":"21","key":"pone.0229904.ref013","first-page":"3542","article-title":"Epigenetic dysregulation of Insulin-like growth factor (IGF)-related genes and adverse pregnancy outcomes: a systematic review","volume":"29","author":"DM Toure","year":"2016","journal-title":"J Matern Fetal Neonatal Med"},{"issue":"7","key":"pone.0229904.ref014","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a002592","article-title":"Mammalian genomic imprinting","volume":"3","author":"MS Bartolomei","year":"2011","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"3","key":"pone.0229904.ref015","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1093\/hmg\/ddg024","article-title":"A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer","volume":"12","author":"D Mancini-DiNardo","year":"2003","journal-title":"Hum Mol Genet"},{"issue":"10","key":"pone.0229904.ref016","doi-asserted-by":"crossref","first-page":"2672","DOI":"10.1093\/humrep\/der238","article-title":"Analysis of global gene expression following mouse blastocyst cryopreservation","volume":"26","author":"MG Larman","year":"2011","journal-title":"Hum Reprod"},{"issue":"14","key":"pone.0229904.ref017","doi-asserted-by":"crossref","first-page":"5478","DOI":"10.1073\/pnas.0508035103","article-title":"Gene expression patterns in human placenta","volume":"103","author":"R Sood","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"pone.0229904.ref018","doi-asserted-by":"crossref","first-page":"e0156980","DOI":"10.1371\/journal.pone.0156980","article-title":"Epigenetic Dysregulation Observed in Monosomy Blastocysts Further Compromises Developmental Potential","volume":"11","author":"MM Denomme","year":"2016","journal-title":"PLoS One"},{"issue":"3","key":"pone.0229904.ref019","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1016\/j.fertnstert.2018.04.004","article-title":"Inheritance of epigenetic dysregulation from male factor infertility has a direct impact on reproductive potential","volume":"110","author":"MM Denomme","year":"2018","journal-title":"Fertil Steril"},{"issue":"9","key":"pone.0229904.ref020","doi-asserted-by":"crossref","first-page":"e36","DOI":"10.1093\/nar\/30.9.e36","article-title":"Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR","volume":"30","author":"MW Pfaffl","year":"2002","journal-title":"Nucleic Acids Res"},{"key":"pone.0229904.ref021","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1471-213X-10-50","article-title":"Rescue of placental phenotype in a mechanistic model of Beckwith-Wiedemann syndrome","volume":"10","author":"R Oh-McGinnis","year":"2010","journal-title":"BMC Dev Biol"},{"key":"pone.0229904.ref022","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1186\/s13148-016-0256-8","article-title":"DNA methylation: conducting the orchestra from exposure to phenotype?","volume":"8","author":"FA Leenen","year":"2016","journal-title":"Clin Epigenetics"},{"issue":"3","key":"pone.0229904.ref023","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.molcel.2011.08.032","article-title":"In embryonic stem cells, ZFP57\/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions","volume":"44","author":"S Quenneville","year":"2011","journal-title":"Mol Cell"},{"issue":"Suppl A","key":"pone.0229904.ref024","doi-asserted-by":"crossref","first-page":"S10","DOI":"10.1016\/j.placenta.2004.12.009","article-title":"Imprinted genes in the placenta\u2014a review","volume":"26","author":"PM Coan","year":"2005","journal-title":"Placenta"},{"issue":"3","key":"pone.0229904.ref025","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1101\/gr.175919.114","article-title":"A systems-level approach to parental genomic imprinting: the imprinted gene network includes extracellular matrix genes and regulates cell cycle exit and differentiation","volume":"25","author":"H Al Adhami","year":"2015","journal-title":"Genome Res"},{"issue":"5","key":"pone.0229904.ref026","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1016\/j.devcel.2006.09.003","article-title":"Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth","volume":"11","author":"A Varrault","year":"2006","journal-title":"Dev Cell"},{"issue":"20","key":"pone.0229904.ref027","doi-asserted-by":"crossref","first-page":"3413","DOI":"10.1242\/dev.036061","article-title":"H19 acts as a trans regulator of the imprinted gene network controlling growth in mice","volume":"136","author":"A Gabory","year":"2009","journal-title":"Development"},{"issue":"51","key":"pone.0229904.ref028","doi-asserted-by":"crossref","first-page":"20693","DOI":"10.1073\/pnas.1310201110","article-title":"H19 lncRNA controls gene expression of the Imprinted Gene Network by recruiting MBD1","volume":"110","author":"P Monnier","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"10","key":"pone.0229904.ref029","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1002\/humu.22623","article-title":"Complex tissue-specific epigenotypes in Russell-Silver Syndrome associated with 11p15 ICR1 hypomethylation","volume":"35","author":"S Azzi","year":"2014","journal-title":"Hum Mutat"},{"issue":"1","key":"pone.0229904.ref030","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1515\/bmc-2014-0037","article-title":"Multilocus methylation defects in imprinting disorders","volume":"6","author":"DJ Mackay","year":"2015","journal-title":"Biomol Concepts"},{"issue":"7","key":"pone.0229904.ref031","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1016\/j.tig.2016.05.001","article-title":"Causes and Consequences of Multi-Locus Imprinting Disturbances in Humans","volume":"32","author":"M Sanchez-Delgado","year":"2016","journal-title":"Trends Genet"},{"issue":"7","key":"pone.0229904.ref032","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1093\/molehr\/gax029","article-title":"Intergenerational impact of paternal lifetime exposures to both folic acid deficiency and supplementation on reproductive outcomes and imprinted gene methylation","volume":"23","author":"L Ly","year":"2017","journal-title":"Mol Hum Reprod"},{"issue":"4","key":"pone.0229904.ref033","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1002\/mrd.22784","article-title":"Gene expression and epigenetic aberrations in F1-placentas fathered by obese males","volume":"84","author":"M Mitchell","year":"2017","journal-title":"Mol Reprod Dev"},{"issue":"6","key":"pone.0229904.ref034","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1038\/mp.2012.88","article-title":"Advanced paternal age is associated with altered DNA methylation at brain-expressed imprinted loci in inbred mice: implications for neuropsychiatric disease","volume":"18","author":"RG Smith","year":"2013","journal-title":"Mol Psychiatry"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0229904","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T18:29:52Z","timestamp":1583519392000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0229904"}},"subtitle":[],"editor":[{"given":"Cheryl S.","family":"Rosenfeld","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2020,3,6]]},"references-count":34,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,3,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0229904","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,6]]}}}