{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T10:34:49Z","timestamp":1791974089932,"version":"4.4.0"},"reference-count":49,"publisher":"Elsevier BV","issue":"4","license":[{"start":{"date-parts":[[2017,4,1]],"date-time":"2017-04-01T00:00:00Z","timestamp":1491004800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2017,2,17]],"date-time":"2017-02-17T00:00:00Z","timestamp":1487289600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["clinicalkey.jp","journals.elsevierhealth.com","clinicalkey.com","clinicalkey.es","clinicalkey.com.au","clinicalkey.fr","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["The American Journal of Pathology"],"published-print":{"date-parts":[[2017,4]]},"DOI":"10.1016\/j.ajpath.2016.12.002","type":"journal-article","created":{"date-parts":[[2017,2,1]],"date-time":"2017-02-01T20:45:34Z","timestamp":1485981934000},"page":"908-920","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":56,"title":["Placental Stem Villus Arterial Remodeling Associated with Reduced Hydrogen Sulfide Synthesis Contributes to Human Fetal Growth Restriction"],"prefix":"10.1016","volume":"187","author":[{"given":"Liangjian","family":"Lu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John","family":"Kingdom","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Graham J.","family":"Burton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tereza","family":"Cindrova-Davies","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.ajpath.2016.12.002_bib1","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/0140-6736(93)91224-A","article-title":"Fetal nutrition and cardiovascular disease in adult life","volume":"341","author":"Barker","year":"1993","journal-title":"Lancet"},{"key":"10.1016\/j.ajpath.2016.12.002_bib2","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1053\/j.ackd.2008.01.001","article-title":"Intrauterine growth restriction: fetal programming of hypertension and kidney disease","volume":"15","author":"Ojeda","year":"2008","journal-title":"Adv Chronic Kidney Dis"},{"key":"10.1016\/j.ajpath.2016.12.002_bib3","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1079\/PNS2005417","article-title":"Fetal origins of insulin resistance and obesity","volume":"64","author":"Stocker","year":"2005","journal-title":"Proc Nutr Soc"},{"key":"10.1016\/j.ajpath.2016.12.002_bib4","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1177\/1933719107302324","article-title":"Fetal programming of cardiac function and disease","volume":"14","author":"Meyer","year":"2007","journal-title":"Reprod Sci"},{"key":"10.1016\/j.ajpath.2016.12.002_bib5","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1056\/NEJMra0708473","article-title":"Effect of in utero and early-life conditions on adult health and disease","volume":"359","author":"Gluckman","year":"2008","journal-title":"N Engl J Med"},{"key":"10.1016\/j.ajpath.2016.12.002_bib6","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/S0301-2115(97)00202-9","article-title":"Fetal arterial Doppler-IUGR and hypoxia","volume":"75","author":"Arbeille","year":"1997","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib7","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1080\/jmf.11.3.199.203","article-title":"Prognostic role of umbilical artery Doppler velocimetry in growth-restricted fetuses","volume":"11","author":"Soregaroli","year":"2002","journal-title":"J Matern Fetal Neonatal Med"},{"key":"10.1016\/j.ajpath.2016.12.002_bib8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0378-3782(94)01596-H","article-title":"Growth deficient fetuses with absent or reversed umbilical artery end-diastolic flow are metabolically compromised","volume":"41","author":"Steiner","year":"1995","journal-title":"Early Hum Dev"},{"key":"10.1016\/j.ajpath.2016.12.002_bib9","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0301-2115(00)00423-1","article-title":"Development of the placental villous tree and its consequences for fetal growth","volume":"92","author":"Kingdom","year":"2000","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib10","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1002\/uog.9008","article-title":"Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction","volume":"37","author":"Baschat","year":"2011","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib11","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1126\/science.1111726","article-title":"Latest advances in understanding preeclampsia","volume":"308","author":"Redman","year":"2005","journal-title":"Science"},{"key":"10.1016\/j.ajpath.2016.12.002_bib12","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.jsgi.2004.03.003","article-title":"Placental oxidative stress: from miscarriage to preeclampsia","volume":"11","author":"Burton","year":"2004","journal-title":"J Soc Gynecol Investig"},{"key":"10.1016\/j.ajpath.2016.12.002_bib13","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/0143-4004(91)90023-9","article-title":"Autacoids and the control of vascular tone in the human umbilical-placental circulation","volume":"12","author":"Boura","year":"1991","journal-title":"Placenta"},{"key":"10.1016\/j.ajpath.2016.12.002_bib14","doi-asserted-by":"crossref","first-page":"6008","DOI":"10.1093\/emboj\/20.21.6008","article-title":"The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener","volume":"20","author":"Zhao","year":"2001","journal-title":"EMBO J"},{"key":"10.1016\/j.ajpath.2016.12.002_bib15","doi-asserted-by":"crossref","first-page":"9161","DOI":"10.1073\/pnas.1202916109","article-title":"Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation","volume":"109","author":"Coletta","year":"2012","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2016.12.002_bib16","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1126\/science.1162667","article-title":"H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase","volume":"322","author":"Yang","year":"2008","journal-title":"Science"},{"key":"10.1016\/j.ajpath.2016.12.002_bib17","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1016\/j.ajpath.2013.01.001","article-title":"Reduced cystathionine gamma-lyase and increased miR-21 expression are associated with increased vascular resistance in growth-restricted pregnancies: hydrogen sulfide as a placental vasodilator","volume":"182","author":"Cindrova-Davies","year":"2013","journal-title":"Am J Pathol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib18","doi-asserted-by":"crossref","first-page":"2514","DOI":"10.1161\/CIRCULATIONAHA.113.001631","article-title":"Dysregulation of hydrogen sulfide producing enzyme cystathionine gamma-lyase contributes to maternal hypertension and placental abnormalities in preeclampsia","volume":"127","author":"Wang","year":"2013","journal-title":"Circulation"},{"key":"10.1016\/j.ajpath.2016.12.002_bib19","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.placenta.2016.01.019","article-title":"MiR 20a,-20b and -200c are involved in hydrogen sulfide stimulation of VEGF production in human placental trophoblasts","volume":"39","author":"Hu","year":"2016","journal-title":"Placenta"},{"key":"10.1016\/j.ajpath.2016.12.002_bib20","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/j.placenta.2012.02.014","article-title":"Hydrogen sulfide producing enzymes in pregnancy and preeclampsia","volume":"33","author":"Holwerda","year":"2012","journal-title":"Placenta"},{"key":"10.1016\/j.ajpath.2016.12.002_bib21","first-page":"578","article-title":"The correlation of arterial lesions with umbilical artery Doppler velocimetry in the placentas of small-for-dates pregnancies","volume":"75","author":"Fok","year":"1990","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib22","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1016\/S0029-7844(97)00473-0","article-title":"Placental pathology of absent and reversed end-diastolic flow in growth-restricted fetuses","volume":"90","author":"Salafia","year":"1997","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib23","first-page":"282","article-title":"Placental vessel morphometry in growth retardation and increased resistance of the umbilical artery Doppler flow","volume":"9","author":"Mitra","year":"2000","journal-title":"J Matern Fetal Med"},{"issue":"Suppl A","key":"10.1016\/j.ajpath.2016.12.002_bib24","doi-asserted-by":"crossref","first-page":"A25","DOI":"10.1016\/j.jvs.2007.03.001","article-title":"Regulation of vascular smooth muscle cell differentiation","volume":"45","author":"Rzucidlo","year":"2007","journal-title":"J Vasc Surg"},{"key":"10.1016\/j.ajpath.2016.12.002_bib25","doi-asserted-by":"crossref","first-page":"26450","DOI":"10.1074\/jbc.M111.266643","article-title":"Specificity protein-1 as a critical regulator of human cystathionine gamma-lyase in smooth muscle cells","volume":"286","author":"Yang","year":"2011","journal-title":"J Biol Chem"},{"key":"10.1016\/j.ajpath.2016.12.002_bib26","doi-asserted-by":"crossref","first-page":"3192","DOI":"10.1002\/jcp.24006","article-title":"MicroRNA-21 represses human cystathionine gamma-lyase expression by targeting at specificity protein-1 in smooth muscle cells","volume":"227","author":"Yang","year":"2012","journal-title":"J Cell Physiol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib27","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/cr.2008.24","article-title":"MicroRNA-21 targets tumor suppressor genes in invasion and metastasis","volume":"18","author":"Zhu","year":"2008","journal-title":"Cell Res"},{"key":"10.1016\/j.ajpath.2016.12.002_bib28","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.bbrc.2009.08.044","article-title":"MicroRNA-21 promotes cell proliferation and down-regulates the expression of programmed cell death 4 (PDCD4) in HeLa cervical carcinoma cells","volume":"388","author":"Yao","year":"2009","journal-title":"Biochem Biophys Res Commun"},{"key":"10.1016\/j.ajpath.2016.12.002_bib29","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.2353\/ajpath.2007.061170","article-title":"MicroRNAs are aberrantly expressed in hypertrophic heart: do they play a role in cardiac hypertrophy?","volume":"170","author":"Cheng","year":"2007","journal-title":"Am J Pathol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib30","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1291\/hypres.28.819","article-title":"Assessment of the microRNA system in salt-sensitive hypertension","volume":"28","author":"Naraba","year":"2005","journal-title":"Hypertens Res"},{"key":"10.1016\/j.ajpath.2016.12.002_bib31","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1161\/01.RES.75.1.41","article-title":"Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation","volume":"75","author":"Pauly","year":"1994","journal-title":"Circ Res"},{"key":"10.1016\/j.ajpath.2016.12.002_bib32","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1152\/physrev.00041.2003","article-title":"Molecular regulation of vascular smooth muscle cell differentiation in development and disease","volume":"84","author":"Owens","year":"2004","journal-title":"Physiol Rev"},{"key":"10.1016\/j.ajpath.2016.12.002_bib33","doi-asserted-by":"crossref","first-page":"2579","DOI":"10.1161\/01.ATV.0000249623.79871.bc","article-title":"Origin of neointimal smooth muscle: we've come full circle","volume":"26","author":"Hoofnagle","year":"2006","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib34","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/S1701-2163(16)35129-5","article-title":"Screening, diagnosis, and management of intrauterine growth restriction","volume":"34","author":"Lausman","year":"2012","journal-title":"J Obstet Gynaecol Can"},{"key":"10.1016\/j.ajpath.2016.12.002_bib35","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.2353\/ajpath.2007.070528","article-title":"Oxidative stress, gene expression, and protein changes induced in the human placenta during labor","volume":"171","author":"Cindrova-Davies","year":"2007","journal-title":"Am J Pathol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib36","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/0002-9378(95)90566-9","article-title":"Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms","volume":"172","author":"Jackson","year":"1995","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib37","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1080\/01445349908833025","article-title":"The diameter distribution of the stem villi arteries does not discriminate between normal and intra uterine growth restricted placentas","volume":"1","author":"Guiot","year":"1999","journal-title":"J Theor Med"},{"key":"10.1016\/j.ajpath.2016.12.002_bib38","first-page":"301","article-title":"Morphology of fetal placental stem arteries in hypertensive disorders (\u201ctoxemia\u201d) of pregnancy","volume":"1","author":"Las Heras","year":"1983","journal-title":"Appl Pathol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib39","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1161\/01.RES.87.3.179","article-title":"Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling","volume":"87","author":"Irani","year":"2000","journal-title":"Circ Res"},{"key":"10.1016\/j.ajpath.2016.12.002_bib40","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1007\/s10439-005-7545-2","article-title":"Oxidative stress produced with cell migration increases synthetic phenotype of vascular smooth muscle cells","volume":"33","author":"Sung","year":"2005","journal-title":"Ann Biomed Eng"},{"key":"10.1016\/j.ajpath.2016.12.002_bib41","doi-asserted-by":"crossref","first-page":"2523","DOI":"10.1161\/CIRCULATIONAHA.113.002208","article-title":"Decreased endogenous production of hydrogen sulfide accelerates atherosclerosis","volume":"127","author":"Mani","year":"2013","journal-title":"Circulation"},{"key":"10.1016\/j.ajpath.2016.12.002_bib42","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1046\/j.0960-7692.2001.00591.x","article-title":"The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens","volume":"18","author":"Baschat","year":"2001","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajpath.2016.12.002_bib43","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/1475-2891-1-4","article-title":"Effect of garlic on cardiovascular disorders: a review","volume":"1","author":"Banerjee","year":"2002","journal-title":"Nutr J"},{"key":"10.1016\/j.ajpath.2016.12.002_bib44","doi-asserted-by":"crossref","first-page":"17977","DOI":"10.1073\/pnas.0705710104","article-title":"Hydrogen sulfide mediates the vasoactivity of garlic","volume":"104","author":"Benavides","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2016.12.002_bib45","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1016\/j.lfs.2005.07.009","article-title":"Effects of hydrogen sulfide on hypoxic pulmonary vascular structural remodeling","volume":"78","author":"Hongfang","year":"2006","journal-title":"Life Sci"},{"key":"10.1016\/j.ajpath.2016.12.002_bib46","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1161\/CIRCRESAHA.109.199919","article-title":"Hydrogen sulfide mediates cardioprotection through Nrf2 signaling","volume":"105","author":"Calvert","year":"2009","journal-title":"Circ Res"},{"key":"10.1016\/j.ajpath.2016.12.002_bib47","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1161\/CIRCHEARTFAILURE.113.000299","article-title":"Hydrogen sulfide attenuates cardiac dysfunction following heart failure via induction of angiogenesis","volume":"6","author":"Polhemus","year":"2013","journal-title":"Circ Heart Fail"},{"key":"10.1016\/j.ajpath.2016.12.002_bib48","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1161\/CIRCULATIONAHA.112.000855","article-title":"H(2)S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase","volume":"127","author":"Kondo","year":"2013","journal-title":"Circulation"},{"key":"10.1016\/j.ajpath.2016.12.002_bib49","first-page":"CD006065","article-title":"Garlic for preventing pre-eclampsia and its complications","author":"Meher","year":"2006","journal-title":"Cochrane Database Syst Rev"}],"container-title":["The American Journal of Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002944017300238?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002944017300238?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2018,9,4]],"date-time":"2018-09-04T18:27:50Z","timestamp":1536085670000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0002944017300238"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,4]]},"references-count":49,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2017,4]]}},"alternative-id":["S0002944017300238"],"URL":"https:\/\/doi.org\/10.1016\/j.ajpath.2016.12.002","relation":{},"ISSN":["0002-9440"],"issn-type":[{"value":"0002-9440","type":"print"}],"subject":[],"published":{"date-parts":[[2017,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Placental Stem Villus Arterial Remodeling Associated with Reduced Hydrogen Sulfide Synthesis Contributes to Human Fetal Growth Restriction","name":"articletitle","label":"Article Title"},{"value":"The American Journal of Pathology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ajpath.2016.12.002","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2017 American Society for Investigative Pathology. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}