{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,22]],"date-time":"2026-02-22T09:44:25Z","timestamp":1771753465863,"version":"3.50.1"},"reference-count":54,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2015,3,1]],"date-time":"2015-03-01T00:00:00Z","timestamp":1425168000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2015,3,1]],"date-time":"2015-03-01T00:00:00Z","timestamp":1425168000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Physiology &amp; Behavior"],"published-print":{"date-parts":[[2015,3]]},"DOI":"10.1016\/j.physbeh.2014.12.017","type":"journal-article","created":{"date-parts":[[2014,12,10]],"date-time":"2014-12-10T02:04:03Z","timestamp":1418177043000},"page":"89-95","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":9,"special_numbering":"C","title":["Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet"],"prefix":"10.1016","volume":"140","author":[{"given":"L.A.","family":"Reyes-Castro","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"G.L.","family":"Rodr\u00edguez-Gonz\u00e1lez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"R.","family":"Chavira","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C.","family":"Ib\u00e1\u00f1ez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C.","family":"Lomas-Soria","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.S.","family":"Rodriguez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P.W.","family":"Nathanielsz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"E.","family":"Zambrano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.physbeh.2014.12.017_bb0005","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1159\/000273066","article-title":"Developmental origins of adult disease","volume":"19","author":"Langley-Evans","year":"2010","journal-title":"Med. Princ. Pract."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0010","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1097\/GCO.0b013e3282f76753","article-title":"Prenatal origins of adult disease","volume":"20","author":"Nijland","year":"2008","journal-title":"Curr. Opin. Obstet. Gynecol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0015","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1016\/j.beem.2010.05.007","article-title":"Developmental programming and diabetes \u2014 the human experience and insight from animal models","volume":"24","author":"Poston","year":"2010","journal-title":"Best Pract. Res. Clin. Endocrinol. Metab."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0020","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1055\/s-0029-1237424","article-title":"Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms","volume":"27","author":"Wadhwa","year":"2009","journal-title":"Semin. Reprod. Med."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0025","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.yhbeh.2010.07.001","article-title":"Epigenetic modifications of brain and behavior: theory and practice","volume":"59","author":"Crews","year":"2011","journal-title":"Horm. Behav."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0030","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1002\/bdrc.20199","article-title":"Role of epigenetics in developmental biology and transgenerational inheritance","volume":"93","author":"Skinner","year":"2011","journal-title":"Birth Defects Res. C Embryo Today"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0035","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1038\/embor.2011.125","article-title":"Environmental epigenomics and disease susceptibility","volume":"12","author":"Skinner","year":"2011","journal-title":"EMBO Rep."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0040","doi-asserted-by":"crossref","first-page":"9143","DOI":"10.1073\/pnas.1118514109","article-title":"Epigenetic transgenerational inheritance of altered stress responses","volume":"109","author":"Crews","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0045","doi-asserted-by":"crossref","first-page":"E1270","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. Physiol. Endocrinol. Metab."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0050","doi-asserted-by":"crossref","first-page":"381","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":"10.1016\/j.physbeh.2014.12.017_bb0055","doi-asserted-by":"crossref","first-page":"1117","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":"10.1016\/j.physbeh.2014.12.017_bb0060","doi-asserted-by":"crossref","first-page":"460","DOI":"10.2337\/db08-0490","article-title":"Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice","volume":"58","author":"Jimenez-Chillaron","year":"2009","journal-title":"Diabetes"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0065","doi-asserted-by":"crossref","first-page":"e3745","DOI":"10.1371\/journal.pone.0003745","article-title":"Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior","volume":"3","author":"Skinner","year":"2008","journal-title":"PLoS One"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0070","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1113\/jphysiol.2005.086462","article-title":"Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation","volume":"566","author":"Zambrano","year":"2005","journal-title":"J. Physiol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0075","doi-asserted-by":"crossref","first-page":"4999","DOI":"10.1210\/en.2009-0500","article-title":"Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice","volume":"150","author":"Dunn","year":"2009","journal-title":"Endocrinology"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0080","doi-asserted-by":"crossref","first-page":"2228","DOI":"10.1210\/en.2010-1461","article-title":"Maternal high-fat diet effects on third-generation female body size via the paternal lineage","volume":"152","author":"Dunn","year":"2011","journal-title":"Endocrinology"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0085","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1113\/jphysiol.2004.078543","article-title":"A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development","volume":"563","author":"Zambrano","year":"2005","journal-title":"J. Physiol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0090","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.bbr.2011.06.008","article-title":"Pre- and\/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats","volume":"227","author":"Reyes-Castro","year":"2012","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0095","doi-asserted-by":"crossref","first-page":"48R","DOI":"10.1203\/pdr.0b013e3180457671","article-title":"Endocrine disruptors and epigenetic transgenerational disease etiology","volume":"61","author":"Skinner","year":"2007","journal-title":"Pediatr. Res."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0100","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.reprotox.2007.09.001","article-title":"What is an epigenetic transgenerational phenotype? F3 or F2","volume":"25","author":"Skinner","year":"2008","journal-title":"Reprod. Toxicol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0105","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.expneurol.2011.01.009","article-title":"Transgenerational inheritance of stress pathology","volume":"233","author":"Matthews","year":"2012","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0110","doi-asserted-by":"crossref","first-page":"12815","DOI":"10.1523\/JNEUROSCI.3331-09.2009","article-title":"The epigenetics of sex differences in the brain","volume":"29","author":"McCarthy","year":"2009","journal-title":"J. Neurosci."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0115","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1677\/joe.0.1800001","article-title":"The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk","volume":"180","author":"Drake","year":"2004","journal-title":"J. Endocrinol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0120","doi-asserted-by":"crossref","first-page":"E270","DOI":"10.1152\/ajpendo.00437.2009","article-title":"Protein restriction during pregnancy affects maternal liver lipid metabolism and fetal brain lipid composition in the rat","volume":"298","author":"Torres","year":"2009","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0125","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.ijdevneu.2011.10.002","article-title":"Maternal protein restriction in the rat during pregnancy and\/or lactation alters cognitive and anxiety behaviors of female offspring","volume":"30","author":"Reyes-Castro","year":"2012","journal-title":"Int. J. Dev. Neurosci."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0130","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.tips.2008.07.005","article-title":"Animal models of anxiety: do I need multiple tests?","volume":"29","author":"Ramos","year":"2008","journal-title":"Trends Pharmacol. Sci."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0135","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/S0149-7634(97)00001-8","article-title":"Stress and emotionality: a multidimensional and genetic approach","volume":"22","author":"Ramos","year":"1998","journal-title":"Neurosci. Biobehav. Rev."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0140","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/BF02244948","article-title":"Differences in fear motivated behaviors among inbred mouse strains","volume":"111","author":"Trullas","year":"1993","journal-title":"Psychopharmacology (Berl)"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0145","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1007\/s00213-003-1545-4","article-title":"Evaluation of the anxiolytic-like effect of NKP608, a NK1-receptor antagonist, in two rat strains that differ in anxiety-related behaviors","volume":"170","author":"Vendruscolo","year":"2003","journal-title":"Psychopharmacology (Berl)"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0150","doi-asserted-by":"crossref","first-page":"2393S","DOI":"10.1093\/jn\/132.8.2393S","article-title":"Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring","volume":"132","author":"Cooney","year":"2002","journal-title":"J. Nutr."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0155","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1038\/nrg2045","article-title":"Environmental epigenomics and disease susceptibility","volume":"8","author":"Jirtle","year":"2007","journal-title":"Nat. Rev. Genet."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0160","doi-asserted-by":"crossref","first-page":"5293","DOI":"10.1128\/MCB.23.15.5293-5300.2003","article-title":"Transposable elements: targets for early nutritional effects on epigenetic gene regulation","volume":"23","author":"Waterland","year":"2003","journal-title":"Mol. Cell. Biol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0165","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1096\/fasebj.12.11.949","article-title":"Maternal epigenetics and methyl supplements affect agouti gene expression in Avy\/a mice","volume":"12","author":"Wolff","year":"1998","journal-title":"FASEB J."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0170","doi-asserted-by":"crossref","first-page":"17308","DOI":"10.1073\/pnas.0607090103","article-title":"Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation","volume":"103","author":"Cropley","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0175","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1016\/j.yhbeh.2012.03.006","article-title":"Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the precocial chicken","volume":"61","author":"Goerlich","year":"2012","journal-title":"Horm. Behav."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0180","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1080\/10253890601056192","article-title":"Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis","volume":"9","author":"Lesage","year":"2006","journal-title":"Stress"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0185","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1203\/PDR.0b013e318191fb44","article-title":"Blunted stress response in small for gestational age neonates","volume":"65","author":"Schaffer","year":"2009","journal-title":"Pediatr. Res."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0190","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1017\/S1461145708008997","article-title":"Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus","volume":"12","author":"Fuchikami","year":"2009","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0195","doi-asserted-by":"crossref","first-page":"20912","DOI":"10.1073\/pnas.0911143106","article-title":"Regulation of hippocampal H3 histone methylation by acute and chronic stress","volume":"106","author":"Hunter","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0200","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1038\/227622a0","article-title":"Pre-mating and pregnancy stress in rats affects behaviour of grandpups","volume":"227","author":"Wehmer","year":"1970","journal-title":"Nature"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0205","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.expneurol.2011.01.009","article-title":"Transgenerational inheritance of stress pathology","volume":"233","author":"Matthews","year":"2011","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0210","doi-asserted-by":"crossref","first-page":"2217","DOI":"10.1113\/jphysiol.2007.147967","article-title":"Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic\u2013pituitary\u2013adrenal function","volume":"586","author":"Bertram","year":"2008","journal-title":"J. Physiol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0215","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.nbd.2009.11.012","article-title":"Epigenetic inheritance in mammals: evidence for the impact of adverse environmental effects","volume":"39","author":"Franklin","year":"2010","journal-title":"Neurobiol. Dis."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0220","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.1126\/science.1108190","article-title":"Epigenetic transgenerational actions of endocrine disruptors and male fertility","volume":"308","author":"Anway","year":"2005","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0225","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.biopsych.2010.05.036","article-title":"Epigenetic transmission of the impact of early stress across generations","volume":"68","author":"Franklin","year":"2010","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0230","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1086\/598822","article-title":"Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution","volume":"84","author":"Jablonka","year":"2009","journal-title":"Q. Rev. Biol."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0235","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1038\/nn.3695","article-title":"Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice","volume":"17","author":"Gapp","year":"2014","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0240","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1002\/jemt.20715","article-title":"The dynamic epigenetic program in male germ cells: its role in spermatogenesis, testis cancer, and its response to the environment","volume":"72","author":"Godmann","year":"2009","journal-title":"Microsc. Res. Tech."},{"key":"10.1016\/j.physbeh.2014.12.017_bb9000","doi-asserted-by":"crossref","first-page":"9721","DOI":"10.1007\/s11357-014-9721-5","article-title":"Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress","volume":"36","author":"Rodr\u00edguez-Gonz\u00e1lez","year":"2014","journal-title":"Age (Dordr)"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0245","doi-asserted-by":"crossref","first-page":"e100832","DOI":"10.1371\/journal.pone.0100832","article-title":"Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring","volume":"9","author":"Lane","year":"2014","journal-title":"PLoS One"},{"key":"10.1016\/j.physbeh.2014.12.017_bb0250","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.brainresbull.2010.11.003","article-title":"Long-lasting and transgenerational effects of an environmental enrichment on memory formation","volume":"85","author":"Arai","year":"2011","journal-title":"Brain Res. Bull."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0255","doi-asserted-by":"crossref","first-page":"1496","DOI":"10.1523\/JNEUROSCI.5057-08.2009","article-title":"Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment","volume":"29","author":"Arai","year":"2009","journal-title":"J. Neurosci."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0260","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/0031-9384(85)90207-0","article-title":"Facilitative effects of maternal environmental enrichment on maze learning in rat offspring","volume":"34","author":"Kiyono","year":"1985","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2014.12.017_bb0265","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/0031-9384(87)90008-4","article-title":"Transfer of effects from environmentally enriched and impoverished female rats to future offspring","volume":"39","author":"Dell","year":"1987","journal-title":"Physiol. Behav."}],"container-title":["Physiology &amp; Behavior"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938414006209?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938414006209?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,21]],"date-time":"2025-09-21T18:00:52Z","timestamp":1758477652000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0031938414006209"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,3]]},"references-count":54,"alternative-id":["S0031938414006209"],"URL":"https:\/\/doi.org\/10.1016\/j.physbeh.2014.12.017","relation":{},"ISSN":["0031-9384"],"issn-type":[{"value":"0031-9384","type":"print"}],"subject":[],"published":{"date-parts":[[2015,3]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet","name":"articletitle","label":"Article Title"},{"value":"Physiology & Behavior","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.physbeh.2014.12.017","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2015 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}