{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T10:12:38Z","timestamp":1791108758073,"version":"4.1.0"},"reference-count":101,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2010,7,29]],"date-time":"2010-07-29T00:00:00Z","timestamp":1280361600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Birth Defects Research"],"published-print":{"date-parts":[[2010,8]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Neural tube defects (NTDs) represent some of the most common congenital malformations in humans. The causes of NTDs are complex with both genetic and environmental contributing factors. Periconception nutrition is an important environmental factor influencing the penetrance of NTDs. NTDs arise from failure to close the neural tube completely during development, an event that occurs before establishment of the chorioallantoic placenta. During neurulation, nutrients are absorbed by histotrophic mechanisms and absorbed by endocytosis in the endoderm\u2010derived cell layer of the visceral yolk sac (VYS). Here we review the histotrophic mechanisms by which nutrients are delivered to the human embryo during this critical time period. Because more detailed studies on the molecular mechanisms regulating uptake of nutrients have been performed using rodent models, most importantly mouse and rat models, we will also review nutrient uptake in these model organisms to set the stage for presentation of experimental data that have provided valuable information about how nutrients are delivered to the neurulating embryo. Birth Defects Research (Part A), 2010. \u00a9 2010 Wiley\u2010Liss, Inc.<\/jats:p>","DOI":"10.1002\/bdra.20705","type":"journal-article","created":{"date-parts":[[2010,7,29]],"date-time":"2010-07-29T14:46:16Z","timestamp":1280414776000},"page":"593-600","source":"Crossref","is-referenced-by-count":101,"title":["The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation"],"prefix":"10.1002","volume":"88","author":[{"given":"Irene E.","family":"Zohn","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anjali A.","family":"Sarkar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2010,8,13]]},"reference":[{"key":"e_1_2_3_2_1","doi-asserted-by":"publisher","DOI":"10.1038\/6831"},{"key":"e_1_2_3_3_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.physiol.69.031905.164337"},{"key":"e_1_2_3_4_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.104.036913"},{"key":"e_1_2_3_5_1","doi-asserted-by":"publisher","DOI":"10.1006\/mgme.1998.2772"},{"key":"e_1_2_3_6_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.157.3793.1180"},{"key":"e_1_2_3_7_1","first-page":"183","article-title":"Distinct roles for visceral endoderm during embryonic mouse development","volume":"43","author":"Bielinska M","year":"1999","journal-title":"Int J Dev Biol"},{"key":"e_1_2_3_8_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1742-4658.2005.04857.x"},{"key":"e_1_2_3_9_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20581"},{"key":"e_1_2_3_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-3476(98)70522-0"},{"key":"e_1_2_3_11_1","doi-asserted-by":"publisher","DOI":"10.1053\/plac.2001.0639"},{"key":"e_1_2_3_12_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-0528.1993.tb14271.x"},{"key":"e_1_2_3_13_1","doi-asserted-by":"publisher","DOI":"10.1136\/fn.71.1.F49"},{"key":"e_1_2_3_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2004.09.077"},{"key":"e_1_2_3_15_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.02568"},{"key":"e_1_2_3_16_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdrc.20027"},{"key":"e_1_2_3_17_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M002328200"},{"key":"e_1_2_3_18_1","doi-asserted-by":"publisher","DOI":"10.1101\/gad.8.20.2466"},{"key":"e_1_2_3_19_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrm778"},{"key":"e_1_2_3_20_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.10088"},{"key":"e_1_2_3_21_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.80.8.2258"},{"key":"e_1_2_3_22_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20183"},{"key":"e_1_2_3_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ntt.2004.12.007"},{"key":"e_1_2_3_24_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.humrep.a019346"},{"key":"e_1_2_3_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cmet.2005.01.003"},{"key":"e_1_2_3_26_1","doi-asserted-by":"publisher","DOI":"10.1002\/ar.a.10123"},{"key":"e_1_2_3_27_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.91.16.7598"},{"key":"e_1_2_3_28_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.124.2.279"},{"key":"e_1_2_3_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/0028-2243(95)02146-J"},{"key":"e_1_2_3_30_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.92.5.1774"},{"key":"e_1_2_3_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-2275(20)37621-5"},{"key":"e_1_2_3_32_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10995-005-0017-3"},{"key":"e_1_2_3_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2006.06.007"},{"key":"e_1_2_3_34_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20556"},{"key":"e_1_2_3_35_1","first-page":"63","article-title":"The effect of teratogenic antiserum on yolk\u2010sac function in rat embryos cultured in vitro","volume":"71","author":"Freeman SJ","year":"1982","journal-title":"J Embryol Exp Morphol"},{"key":"e_1_2_3_36_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20148"},{"key":"e_1_2_3_37_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20453"},{"key":"e_1_2_3_38_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-9-156"},{"key":"e_1_2_3_39_1","first-page":"47","article-title":"A preliminary report on hydrocephalus, spina bifida and other congenital anomalies in the rat produced by trypan blue; the significance of these results in the interpretation of congenital malformations following maternal rubella","volume":"13","author":"Gillman J","year":"1948","journal-title":"S Afr J Med Sci"},{"key":"e_1_2_3_40_1","doi-asserted-by":"publisher","DOI":"10.1093\/jn\/134.6.1516"},{"key":"e_1_2_3_41_1","doi-asserted-by":"crossref","first-page":"3289","DOI":"10.1242\/dev.120.11.3289","article-title":"Gp330 is specifically expressed in outer cells during epithelial differentiation in the preimplantation mouse embryo","volume":"120","author":"Gueth\u2010Hallonet C","year":"1994","journal-title":"Development"},{"key":"e_1_2_3_42_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.18.10158"},{"key":"e_1_2_3_43_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.275.16.12003"},{"issue":"2","key":"e_1_2_3_44_1","doi-asserted-by":"crossref","first-page":"473S","DOI":"10.1093\/jn\/129.2.473S","article-title":"The LDL receptor gene family, apolipoprotein B and cholesterol in embryonic development","volume":"129","author":"Herz J","year":"1999","journal-title":"J Nutr"},{"key":"e_1_2_3_45_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001260306"},{"key":"e_1_2_3_46_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00801907"},{"key":"e_1_2_3_47_1","doi-asserted-by":"publisher","DOI":"10.1002\/tera.1420510102"},{"key":"e_1_2_3_48_1","doi-asserted-by":"publisher","DOI":"10.1172\/JCI118269"},{"key":"e_1_2_3_49_1","doi-asserted-by":"publisher","DOI":"10.1053\/plac.2002.0932"},{"key":"e_1_2_3_50_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajog.2007.02.009"},{"key":"e_1_2_3_51_1","doi-asserted-by":"publisher","DOI":"10.1038\/86912"},{"key":"e_1_2_3_52_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1136244"},{"key":"e_1_2_3_53_1","doi-asserted-by":"publisher","DOI":"10.1038\/9504"},{"key":"e_1_2_3_54_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.211291398"},{"key":"e_1_2_3_55_1","doi-asserted-by":"publisher","DOI":"10.2174\/138161207782110507"},{"key":"e_1_2_3_56_1","first-page":"1526","article-title":"Antibodies to the 280\u2010kd coated pit protein, target of teratogenic antibodies, produce alterations in the traffic of internalized proteins","volume":"145","author":"Le Panse S","year":"1994","journal-title":"Am J Pathol"},{"key":"e_1_2_3_57_1","first-page":"257","article-title":"Internalization and recycling of glycoprotein 280 in epithelial cells of yolk sac","volume":"72","author":"Le Panse S","year":"1997","journal-title":"Eur J Cell Biol"},{"key":"e_1_2_3_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0890-6238(97)89178-2"},{"key":"e_1_2_3_59_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0890-6238(97)00148-2"},{"key":"e_1_2_3_60_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-3-6"},{"key":"e_1_2_3_61_1","unstructured":"MaoJ McKeanDM CorbinJG et al.The iron exporter ferroportin1 is essential for development of the mouse embryo forebrain patterning and neural tube closure. (submitted)."},{"key":"e_1_2_3_62_1","doi-asserted-by":"publisher","DOI":"10.1093\/jn\/134.4.711"},{"key":"e_1_2_3_63_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.pharmtox.46.120604.141156"},{"key":"e_1_2_3_64_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.02650"},{"key":"e_1_2_3_65_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.00313"},{"key":"e_1_2_3_66_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.93.16.8612"},{"key":"e_1_2_3_67_1","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/21.7.1555"},{"key":"e_1_2_3_68_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(09)60695-4"},{"key":"e_1_2_3_69_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0272-6386(01)80022-6"},{"key":"e_1_2_3_70_1","first-page":"543","article-title":"Effect of yolk\u2010sac antibody on rat embryos grown in culture","volume":"27","author":"New DA","year":"1972","journal-title":"J Embryol Exp Morphol"},{"key":"e_1_2_3_71_1","doi-asserted-by":"publisher","DOI":"10.1679\/aohc.57.107"},{"key":"e_1_2_3_72_1","doi-asserted-by":"publisher","DOI":"10.1007\/s007950050011"},{"key":"e_1_2_3_73_1","doi-asserted-by":"publisher","DOI":"10.1038\/13861"},{"key":"e_1_2_3_74_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.274.5285.255"},{"key":"e_1_2_3_75_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.15.8686"},{"key":"e_1_2_3_76_1","doi-asserted-by":"publisher","DOI":"10.1093\/qjmed\/hcg043"},{"key":"e_1_2_3_77_1","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa031145"},{"key":"e_1_2_3_78_1","doi-asserted-by":"publisher","DOI":"10.1002\/tera.10089"},{"key":"e_1_2_3_79_1","doi-asserted-by":"publisher","DOI":"10.1084\/jem.167.1.213"},{"key":"e_1_2_3_80_1","first-page":"33","article-title":"Coexpression in humans by kidney and fetal envelopes of a 280 kDa\u2010coated pit\u2010restricted protein. Similarity with the murine target of teratogenic antibodies","volume":"140","author":"Sahali D","year":"1992","journal-title":"Am J Pathol"},{"key":"e_1_2_3_81_1","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.10203"},{"key":"e_1_2_3_82_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20537"},{"key":"e_1_2_3_83_1","doi-asserted-by":"publisher","DOI":"10.1002\/bdra.20544"},{"key":"e_1_2_3_84_1","doi-asserted-by":"publisher","DOI":"10.1091\/mbc.e02-03-0145"},{"key":"e_1_2_3_85_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.aje.a115924"},{"key":"e_1_2_3_86_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-6-30"},{"key":"e_1_2_3_87_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M002886200"},{"key":"e_1_2_3_88_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.01580"},{"key":"e_1_2_3_89_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.272.29.18020"},{"issue":"6","key":"e_1_2_3_90_1","doi-asserted-by":"crossref","first-page":"S3","DOI":"10.1301\/nr.2004.jun.S3-S12","article-title":"Physiology of folate and vitamin B12 in health and disease","volume":"62","author":"Stover PJ","year":"2004","journal-title":"Nutr Rev"},{"key":"e_1_2_3_91_1","doi-asserted-by":"publisher","DOI":"10.1038\/ng1098"},{"key":"e_1_2_3_92_1","doi-asserted-by":"publisher","DOI":"10.1515\/CCLM.2007.345"},{"key":"e_1_2_3_93_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1998.9034"},{"key":"e_1_2_3_94_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod57.4.751"},{"key":"e_1_2_3_95_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.93.16.8460"},{"key":"e_1_2_3_96_1","doi-asserted-by":"publisher","DOI":"10.1093\/ajcn\/82.6.1155"},{"key":"e_1_2_3_97_1","doi-asserted-by":"publisher","DOI":"10.1177\/026010609300900106"},{"key":"e_1_2_3_98_1","doi-asserted-by":"publisher","DOI":"10.1016\/0143-4004(77)90010-8"},{"key":"e_1_2_3_99_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1064757"},{"key":"e_1_2_3_100_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0607974103"},{"key":"e_1_2_3_101_1","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2007-01-066068"},{"key":"e_1_2_3_102_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0070-2153(08)00601-7"}],"container-title":["Birth Defects Research Part A: Clinical and Molecular Teratology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fbdra.20705","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/bdra.20705","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,13]],"date-time":"2023-09-13T15:23:31Z","timestamp":1694618611000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/bdra.20705"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,8]]},"references-count":101,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2010,8]]}},"alternative-id":["10.1002\/bdra.20705"],"URL":"https:\/\/doi.org\/10.1002\/bdra.20705","archive":["Portico"],"relation":{},"ISSN":["1542-0752","1542-0760"],"issn-type":[{"value":"1542-0752","type":"print"},{"value":"1542-0760","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,8]]}}}