{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T15:57:16Z","timestamp":1790524636768,"version":"4.1.0"},"reference-count":60,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2014,11,18]],"date-time":"2014-11-18T00:00:00Z","timestamp":1416268800000},"content-version":"unspecified","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.0113389","type":"journal-article","created":{"date-parts":[[2014,11,18]],"date-time":"2014-11-18T19:37:38Z","timestamp":1416339458000},"page":"e113389","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Maternal Exposure to Low Levels of Corticosterone during Lactation Protects against Experimental Inflammatory Colitis-Induced Damage in Adult Rat Offspring"],"prefix":"10.1371","volume":"9","author":[{"given":"Carla","family":"Petrella","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Giuli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simona","family":"Agostini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Val\u00e9rie","family":"Bacquie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manuela","family":"Zinni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vassilia","family":"Theodorou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Broccardo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paola","family":"Casolini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giovanna","family":"Improta","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2014,11,18]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1192\/bjp.159.1.115","article-title":"Early sexual abuse and clinical depression in adult life","volume":"159","author":"A Bifulco","year":"1991","journal-title":"Br J Psychiatry"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1176\/ajp.148.1.55","article-title":"Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse","volume":"148","author":"GR Brown","year":"1991","journal-title":"Am J Psychiatry"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/S0749-3797(98)00017-8","article-title":"Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study","volume":"14","author":"VJ Felitti","year":"1998","journal-title":"Am J Prev Med"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1001\/jama.1997.03540410040028","article-title":"Clinical characteristics of women with a history of childhood abuse: unhealed wounds","volume":"277","author":"J McCauley","year":"1997","journal-title":"Jama"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"2252","DOI":"10.1001\/jama.2009.754","article-title":"Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention","volume":"301","author":"JP Shonkoff","year":"2009","journal-title":"Jama"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/j.bbi.2005.07.003","article-title":"Neonatal maternal deprivation promotes Nippostrongylus brasiliensis infection in adult rats","volume":"20","author":"F Barreau","year":"2006","journal-title":"Brain Behav Immun"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1136\/gut.2003.024174","article-title":"Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats","volume":"53","author":"F Barreau","year":"2004","journal-title":"Gut"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1053\/gast.2002.36019","article-title":"Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine","volume":"123","author":"JD Soderholm","year":"2002","journal-title":"Gastroenterology"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1053\/j.gastro.2012.10.003","article-title":"Brain-gut interactions in inflammatory bowel disease","volume":"144","author":"BL Bonaz","year":"2013","journal-title":"Gastroenterology"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"Ringel Y, Drossman DA (2001) Psychosocial aspects of Crohn&apos;s disease. Surg Clin North Am 81: 231\u2013252, x.","DOI":"10.1016\/S0039-6109(05)70283-8"},{"key":"ref11","doi-asserted-by":"crossref","unstructured":"Ringel Y, Sperber AD, Drossman DA (2001) Irritable bowel syndrome. Annu Rev Med.","DOI":"10.1146\/annurev.med.52.1.319"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1172\/JCI30085","article-title":"Corticotropin-releasing factor receptors and stress-related alterations of gut motor function","volume":"117","author":"Y Tache","year":"2007","journal-title":"J Clin Invest"},{"key":"ref13","first-page":"319","article-title":"Role of peripheral CRF signalling pathways in stress-related alterations of gut motility and mucosal function. Neurogastroenterol Motil 16 Suppl 1: 137\u2013142","volume":"52","author":"Y Tache","year":"2004"},{"key":"ref14","first-page":"324","article-title":"Protective factors in children&apos;s responses to stress and disadvantage","volume":"8","author":"M Rutter","year":"1979","journal-title":"Ann Acad Med Singapore"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"283","DOI":"10.2307\/1129404","article-title":"Maternal deprivation, 1972-1978: new findings, new concepts, new approaches","volume":"50","author":"M Rutter","year":"1979","journal-title":"Child Dev"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1037\/0033-2909.128.2.330","article-title":"Risky families: family social environments and the mental and physical health of offspring","volume":"128","author":"RL Repetti","year":"2002","journal-title":"Psychol Bull"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1097\/00004583-199502000-00012","article-title":"Temperament and stress resilience in school-age children: a within-families study","volume":"34","author":"J Smith","year":"1995","journal-title":"J Am Acad Child Adolesc Psychiatry"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbr.2006.08.016","article-title":"Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress","volume":"175","author":"C Fox","year":"2006","journal-title":"Behav Brain Res"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1016\/j.nlm.2012.01.003","article-title":"Environmental enrichment protects against the effects of chronic stress on cognitive and morphological measures of hippocampal integrity","volume":"97","author":"KM Hutchinson","year":"2012","journal-title":"Neurobiol Learn Mem"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"7840","DOI":"10.1523\/JNEUROSCI.22-18-07840.2002","article-title":"Environmental enrichment reverses the effects of maternal separation on stress reactivity","volume":"22","author":"DD Francis","year":"2002","journal-title":"J Neurosci"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"103","DOI":"10.31887\/DCNS.2005.7.2\/mmeaney","article-title":"Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome","volume":"7","author":"MJ Meaney","year":"2005","journal-title":"Dialogues Clin Neurosci"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1038\/npp.2012.149","article-title":"Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans","volume":"38","author":"TY Zhang","year":"2013","journal-title":"Neuropsychopharmacology"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"7041","DOI":"10.1523\/JNEUROSCI.1074-07.2007","article-title":"Maternal exposure to low levels of corticosterone during lactation protects the adult offspring against ischemic brain damage","volume":"27","author":"P Casolini","year":"2007","journal-title":"J Neurosci"},{"key":"ref24","first-page":"191","article-title":"Perinatal mother-offspring pituitary-adrenal interrelationship in rats: corticosterone in milk may affect adult life","volume":"17","author":"L Angelucci","year":"1983","journal-title":"Endocrinol Exp"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"R1316","DOI":"10.1152\/ajpregu.00685.2003","article-title":"Impact of maternal stress on the transmammary transfer and protective capacity of herpes simplex virus-specific immunity","volume":"287","author":"JL Yorty","year":"2004","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1016\/S0306-4522(96)00668-9","article-title":"Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life","volume":"79","author":"P Casolini","year":"1997","journal-title":"Neuroscience"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S0306-4522(00)00277-3","article-title":"Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny","volume":"100","author":"A Catalani","year":"2000","journal-title":"Neuroscience"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1111\/j.1365-2982.2005.00648.x","article-title":"Corticotropin-releasing factor 1 receptor-mediated mechanisms inhibit colonic hypersensitivity in rats","volume":"17","author":"B Greenwood-Van Meerveld","year":"2005","journal-title":"Neurogastroenterol Motil"},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"Im E, Rhee SH, Park YS, Fiocchi C, Tache Y, et al.. (2010) Corticotropin-releasing hormone family of peptides regulates intestinal angiogenesis. Gastroenterology 138: 2457\u20132467, 2467 e2451\u20132455.","DOI":"10.1053\/j.gastro.2010.02.055"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1053\/gast.2000.20251","article-title":"Peripheral corticotropin-releasing factor and stress-stimulated colonic motor activity involve type 1 receptor in rats","volume":"119","author":"C Maillot","year":"2000","journal-title":"Gastroenterology"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/S0006-8993(03)03027-0","article-title":"A novel water-soluble selective CRF1 receptor antagonist, NBI 35965, blunts stress-induced visceral hyperalgesia and colonic motor function in rats","volume":"985","author":"M Million","year":"2003","journal-title":"Brain Res"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"G452","DOI":"10.1152\/ajpgi.90210.2008","article-title":"Chronic peripheral administration of corticotropin-releasing factor causes colonic barrier dysfunction similar to psychological stress","volume":"295","author":"AA Teitelbaum","year":"2008","journal-title":"Am J Physiol Gastrointest Liver Physiol"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1136\/gut.2006.117549","article-title":"Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro","volume":"57","author":"C Wallon","year":"2008","journal-title":"Gut"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1007\/BF02093789","article-title":"Experimental colitis alters visceromotor response to colorectal distension in awake rats","volume":"39","author":"O Morteau","year":"1994","journal-title":"Dig Dis Sci"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/0016-5085(92)91779-4","article-title":"Exacerbation of experimental colitis by nonsteroidal anti-inflammatory drugs is not related to elevated leukotriene B4 synthesis","volume":"102","author":"JL Wallace","year":"1992","journal-title":"Gastroenterology"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1159\/000200969","article-title":"Effects of phosphatidylcholine and phosphatidylinositol on acetic-acid-induced colitis in the rat","volume":"53","author":"R Fabia","year":"1992","journal-title":"Digestion"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1111\/1523-1747.ep12506462","article-title":"Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker","volume":"78","author":"PP Bradley","year":"1982","journal-title":"J Invest Dermatol"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1016\/j.neubiorev.2010.10.017","article-title":"Maternal corticosterone effects on hypothalamus-pituitary-adrenal axis regulation and behavior of the offspring in rodents","volume":"35","author":"A Catalani","year":"2011","journal-title":"Neurosci Biobehav Rev"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.bbi.2009.08.006","article-title":"Stress-related modulation of inflammation in experimental models of bowel disease and post-infectious irritable bowel syndrome: role of corticotropin-releasing factor receptors","volume":"24","author":"C Kiank","year":"2010","journal-title":"Brain Behav Immun"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1073\/pnas.96.3.1059","article-title":"Enhancing versus suppressive effects of stress hormones on skin immune function","volume":"96","author":"FS Dhabhar","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1111\/j.1365-2567.2007.02611.x","article-title":"Glucocorticoids exert opposing effects on macrophage function dependent on their concentration","volume":"122","author":"HY Lim","year":"2007","journal-title":"Immunology"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"2160","DOI":"10.1007\/s10620-007-0125-6","article-title":"Glucocorticoid availability in colonic inflammation of rat","volume":"53","author":"P Ergang","year":"2008","journal-title":"Dig Dis Sci"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1136\/gut.39.3.385","article-title":"Local production of corticotropin releasing hormone is increased in experimental intestinal inflammation in rats","volume":"39","author":"EA van Tol","year":"1996","journal-title":"Gut"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"e88382","DOI":"10.1371\/journal.pone.0088382","article-title":"Changes in intestinal glucocorticoid sensitivity in early life shape the risk of epithelial barrier defect in maternal-deprived rats","volume":"9","author":"N Moussaoui","year":"2014","journal-title":"PLoS One"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"2017","DOI":"10.1046\/j.1365-2036.2002.01359.x","article-title":"Review article: mechanisms of initiation and perpetuation of gut inflammation by stress","volume":"16","author":"A Hart","year":"2002","journal-title":"Aliment Pharmacol Ther"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1053\/gast.2000.18152","article-title":"Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat","volume":"119","author":"JB Meddings","year":"2000","journal-title":"Gastroenterology"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1038\/nri2653","article-title":"Intestinal mucosal barrier function in health and disease","volume":"9","author":"JR Turner","year":"2009","journal-title":"Nat Rev Immunol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0378-3782(03)00087-2","article-title":"The effect of antenatal corticosteroids on gut peptides of preterm infants\u2014a matched group comparison: corticosteroids and gut development","volume":"74","author":"C Costalos","year":"2003","journal-title":"Early Hum Dev"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"R162","DOI":"10.1152\/ajpregu.00721.2001","article-title":"Normal and glucocorticoid-induced development of the human small intestinal xenograft","volume":"285","author":"NN Nanthakumar","year":"2003","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"G85","DOI":"10.1152\/ajpgi.00169.2004","article-title":"Glucocorticoid responsiveness in developing human intestine: possible role in prevention of necrotizing enterocolitis","volume":"288","author":"NN Nanthakumar","year":"2005","journal-title":"Am J Physiol Gastrointest Liver Physiol"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"2933","DOI":"10.3748\/wjg.v17.i24.2933","article-title":"alpha-fetoprotein involvement during glucocorticoid-induced precocious maturation in rat colon","volume":"17","author":"M Chen","year":"2011","journal-title":"World J Gastroenterol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1203\/01.PDR.0000058923.08017.6F","article-title":"Carbenoxolone accelerates maturation of rat intestine","volume":"53","author":"J Pacha","year":"2003","journal-title":"Pediatr Res"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1016\/S0021-9258(19)41684-0","article-title":"A study of the cytoplasmic receptors for glucocorticoids in intestine of pre- and postweanling rats","volume":"250","author":"SJ Henning","year":"1975","journal-title":"J Biol Chem"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"e127","DOI":"10.1111\/nmo.12066","article-title":"Corticosterone mediates stress-related increased intestinal permeability in a region-specific manner","volume":"25","author":"G Zheng","year":"2013","journal-title":"Neurogastroenterol Motil"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"4517","DOI":"10.1210\/endo.136.10.7664672","article-title":"Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress","volume":"136","author":"S Makino","year":"1995","journal-title":"Endocrinology"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/j.peptides.2007.05.008","article-title":"Urocortin 2 expression in the rat gastrointestinal tract under basal conditions and in chemical colitis","volume":"28","author":"J Chang","year":"2007","journal-title":"Peptides"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.1210\/en.2006-0967","article-title":"Corticotropin-releasing factor (CRF) and the urocortins differentially regulate catecholamine secretion in human and rat adrenals, in a CRF receptor type-specific manner","volume":"148","author":"E Dermitzaki","year":"2007","journal-title":"Endocrinology"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"G1257","DOI":"10.1152\/ajpgi.00314.2002","article-title":"Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress","volume":"283","author":"JD Soderholm","year":"2002","journal-title":"Am J Physiol Gastrointest Liver Physiol"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/s00281-009-0165-4","article-title":"Physiological and pathophysiological functions of intestinal mast cells","volume":"31","author":"SC Bischoff","year":"2009","journal-title":"Semin Immunopathol"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.physbeh.2004.01.002","article-title":"The effects of postnatal maternal separation on stress responsivity and experimentally induced colitis in adult rats","volume":"81","author":"AM Milde","year":"2004","journal-title":"Physiol Behav"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0113389","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,22]],"date-time":"2022-04-22T20:28:30Z","timestamp":1650659310000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0113389"}},"subtitle":[],"editor":[{"given":"J\u00f6rn","family":"Karhausen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2014,11,18]]},"references-count":60,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2014,11,18]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0113389","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,11,18]]}}}