{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T06:52:28Z","timestamp":1791355948111,"version":"4.3.1"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"12","license":[{"start":{"date-parts":[[2007,9,19]],"date-time":"2007-09-19T00:00:00Z","timestamp":1190160000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diabetologia"],"published-print":{"date-parts":[[2007,11,5]]},"DOI":"10.1007\/s00125-007-0811-0","type":"journal-article","created":{"date-parts":[[2007,9,18]],"date-time":"2007-09-18T11:20:08Z","timestamp":1190114408000},"page":"2495-2503","source":"Crossref","is-referenced-by-count":103,"title":["Different mechanisms operating during different critical time-windows reduce rat fetal beta cell mass due to a maternal low-protein or low-energy diet"],"prefix":"10.1007","volume":"50","author":[{"given":"O.","family":"Dumortier","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B.","family":"Blondeau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B.","family":"Duvilli\u00e9","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B.","family":"Reusens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B.","family":"Br\u00e9ant","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Remacle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2007,9,19]]},"reference":[{"key":"811_CR1","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1136\/bmj.303.6809.1019","volume":"303","author":"CN Hales","year":"1991","unstructured":"Hales CN, Barker DJ, Clark PM et al (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303:1019\u20131022","journal-title":"BMJ"},{"key":"811_CR2","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1152\/physrev.00053.2003","volume":"85","author":"IC McMillen","year":"2005","unstructured":"McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol Rev 85:571\u2013633","journal-title":"Physiol Rev"},{"key":"811_CR3","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1046\/j.1464-5491.2003.00871.x","volume":"20","author":"CA Newsome","year":"2003","unstructured":"Newsome CA, Shiell AW, Fall CH, Phillips DI, Shier R, Law CM (2003) Is birth weight related to later glucose and insulin metabolism?\u2014A systematic review. Diabet Med 20:339\u2013348","journal-title":"Diabet Med"},{"key":"811_CR4","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/bmb\/60.1.5","volume":"60","author":"CN Hales","year":"2001","unstructured":"Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5\u201320","journal-title":"Br Med Bull"},{"key":"811_CR5","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1113\/jphysiol.2004.079756","volume":"565","author":"JA Armitage","year":"2005","unstructured":"Armitage JA, Taylor PD, Poston L (2005) Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol 565:3\u20138","journal-title":"J Physiol"},{"key":"811_CR6","doi-asserted-by":"crossref","first-page":"2820","DOI":"10.1093\/jn\/133.9.2820","volume":"133","author":"S Boujendar","year":"2003","unstructured":"Boujendar S, Arany E, Hill D, Remacle C, Reusens B (2003) Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr 133:2820\u20132825","journal-title":"J Nutr"},{"key":"811_CR7","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1007\/s00125-002-0833-6","volume":"45","author":"S Boujendar","year":"2002","unstructured":"Boujendar S, Reusens B, Merezak S et al (2002) Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia 45:856\u2013866","journal-title":"Diabetologia"},{"key":"811_CR8","doi-asserted-by":"crossref","first-page":"4861","DOI":"10.1210\/endo.140.10.7042","volume":"140","author":"J Petrik","year":"1999","unstructured":"Petrik J, Reusens B, Arany E et al (1999) A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 140:4861\u20134873","journal-title":"Endocrinology"},{"key":"811_CR9","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1159\/000243170","volume":"57","author":"A Snoeck","year":"1990","unstructured":"Snoeck A, Remacle C, Reusens B, Hoet JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57:107\u2013118","journal-title":"Biol Neonate"},{"key":"811_CR10","doi-asserted-by":"crossref","first-page":"4208","DOI":"10.1210\/endo.140.9.6960","volume":"140","author":"B Blondeau","year":"1999","unstructured":"Blondeau B, Garofano A, Czernichow P, Breant B (1999) Age-dependent inability of the endocrine pancreas to adapt to pregnancy: a long-term consequence of perinatal malnutrition in the rat. Endocrinology 140:4208\u20134213","journal-title":"Endocrinology"},{"key":"811_CR11","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1159\/000013964","volume":"73","author":"A Garofano","year":"1998","unstructured":"Garofano A, Czernichow P, Breant B (1998) Postnatal somatic growth and insulin contents in moderate or severe intrauterine growth retardation in the rat. Biol Neonate 73:89\u201398","journal-title":"Biol Neonate"},{"key":"811_CR12","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1017\/S0007114599000847","volume":"81","author":"MJ Holness","year":"1999","unstructured":"Holness MJ, Fryer LG, Sugden MC (1999) Protein restriction during early development enhances insulin responsiveness but selectively impairs sensitivity to insulin at low concentrations in white adipose tissue during a later pregnancy. Br J Nutr 81:481\u2013489","journal-title":"Br J Nutr"},{"key":"811_CR13","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1007\/s00125-004-1357-z","volume":"47","author":"S Merezak","year":"2004","unstructured":"Merezak S, Reusens B, Renard A et al (2004) Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia 47:669\u2013675","journal-title":"Diabetologia"},{"key":"811_CR14","first-page":"E1128","volume":"271","author":"SE Ozanne","year":"1996","unstructured":"Ozanne SE, Wang CL, Coleman N, Smith GD (1996) Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol 271:E1128\u20131134","journal-title":"Am J Physiol"},{"key":"811_CR15","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1079\/BJN19970124","volume":"78","author":"PR Shepherd","year":"1997","unstructured":"Shepherd PR, Crowther NJ, Desai M, Hales CN, Ozanne SE (1997) Altered adipocyte properties in the offspring of protein malnourished rats. Br J Nutr 78:121\u2013129","journal-title":"Br J Nutr"},{"issue":"2","key":"811_CR16","doi-asserted-by":"crossref","first-page":"115","DOI":"10.2337\/diab.40.2.S115","volume":"40","author":"S Dahri","year":"1991","unstructured":"Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ (1991) Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 40(2):115\u2013120","journal-title":"Diabetes"},{"key":"811_CR17","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1007\/s001250050812","volume":"40","author":"A Garofano","year":"1997","unstructured":"Garofano A, Czernichow P, Breant B (1997) In utero undernutrition impairs rat beta-cell development. Diabetologia 40:1231\u20131234","journal-title":"Diabetologia"},{"key":"811_CR18","doi-asserted-by":"crossref","first-page":"1493","DOI":"10.1093\/jn\/134.6.1493","volume":"134","author":"F Bieswal","year":"2004","unstructured":"Bieswal F, Hay SM, McKinnon C et al (2004) Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J Nutr 134:1493\u20131499","journal-title":"J Nutr"},{"key":"811_CR19","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/0167-0115(94)90053-1","volume":"52","author":"F Bernet","year":"1994","unstructured":"Bernet F, Maubert E, Bernard J, Montel V, Dupouy JP (1994) In vitro steroidogenic effects of neuropeptide Y (NPY1-36), Y1 and Y2 receptor agonists (Leu31-Pro34 NPY, NPY18-36) and peptide YY (PYY) on rat adrenal capsule\/zona glomerulosa. Regul Pept 52:187\u2013193","journal-title":"Regul Pept"},{"key":"811_CR20","doi-asserted-by":"crossref","first-page":"2035","DOI":"10.2337\/diabetes.52.8.2035","volume":"52","author":"B Duvillie","year":"2003","unstructured":"Duvillie B, Attali M, Aiello V, Quemeneur E, Scharfmann R (2003) Label-retaining cells in the rat pancreas: location and differentiation potential in vitro. Diabetes 52:2035\u20132042","journal-title":"Diabetes"},{"key":"811_CR21","doi-asserted-by":"crossref","first-page":"2322","DOI":"10.2337\/diabetes.53.9.2322","volume":"53","author":"E Gesina","year":"2004","unstructured":"Gesina E, Tronche F, Herrera P et al (2004) Dissecting the role of glucocorticoids on pancreas development. Diabetes 53:2322\u20132329","journal-title":"Diabetes"},{"key":"811_CR22","doi-asserted-by":"crossref","first-page":"E592","DOI":"10.1152\/ajpendo.2001.281.3.E592","volume":"281","author":"B Blondeau","year":"2001","unstructured":"Blondeau B, Lesage J, Czernichow P, Dupouy JP, Breant B (2001) Glucocorticoids impair fetal beta-cell development in rats. Am J Physiol Endocrinol Metab 281:E592\u2013E599","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"811_CR23","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.2337\/diabetes.48.12.2422","volume":"48","author":"A Bavdekar","year":"1999","unstructured":"Bavdekar A, Yajnik CS, Fall CH et al (1999) Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8\u00a0years, or both? Diabetes 48:2422\u20132429","journal-title":"Diabetes"},{"key":"811_CR24","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/S0140-6736(97)07244-9","volume":"351","author":"AC Ravelli","year":"1998","unstructured":"Ravelli AC, van der Meulen JH, Michels RP et al (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351:173\u2013177","journal-title":"Lancet"},{"key":"811_CR25","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1007\/s001250051219","volume":"42","author":"A Garofano","year":"1999","unstructured":"Garofano A, Czernichow P, Breant B (1999) Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia 42:711\u2013718","journal-title":"Diabetologia"},{"key":"811_CR26","doi-asserted-by":"crossref","first-page":"R623","DOI":"10.1152\/ajpregu.00037.2002","volume":"283","author":"E Bertin","year":"2002","unstructured":"Bertin E, Gangnerau MN, Bellon G, Bailbe D, Arbelot De Vacqueur A, Portha B (2002) Development of beta-cell mass in fetuses of rats deprived of protein and\/or energy in last trimester of pregnancy. Am J Physiol Regul Integr Comp Physiol 283:R623\u2013630","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"811_CR27","doi-asserted-by":"crossref","first-page":"2279","DOI":"10.2337\/diabetes.50.10.2279","volume":"50","author":"RA Simmons","year":"2001","unstructured":"Simmons RA, Templeton LJ, Gertz SJ (2001) Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50:2279\u20132286","journal-title":"Diabetes"},{"key":"811_CR28","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1002\/aja.1002000208","volume":"200","author":"HL Kaung","year":"1994","unstructured":"Kaung HL (1994) Growth dynamics of pancreatic islet cell populations during fetal and neonatal development of the rat. Dev Dyn 200:163\u2013175","journal-title":"Dev Dyn"},{"key":"811_CR29","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1038\/23716","volume":"400","author":"A Apelqvist","year":"1999","unstructured":"Apelqvist A, Li H, Sommer L et al (1999) Notch signalling controls pancreatic cell differentiation. Nature 400:877\u2013881","journal-title":"Nature"},{"key":"811_CR30","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1073\/pnas.97.4.1607","volume":"97","author":"G Gradwohl","year":"2000","unstructured":"Gradwohl G, Dierich A, LeMeur M, Guillemot F (2000) neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 97:1607\u20131611","journal-title":"Proc Natl Acad Sci U S A"},{"key":"811_CR31","doi-asserted-by":"crossref","first-page":"163","DOI":"10.2337\/diabetes.49.2.163","volume":"49","author":"J Jensen","year":"2000","unstructured":"Jensen J, Heller RS, Funder-Nielsen T et al (2000) Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: A role for the notch pathway in repression of premature differentiation. Diabetes 49:163\u2013176","journal-title":"Diabetes"},{"key":"811_CR32","doi-asserted-by":"crossref","first-page":"3533","DOI":"10.1242\/dev.127.16.3533","volume":"127","author":"VM Schwitzgebel","year":"2000","unstructured":"Schwitzgebel VM, Scheel DW, Conners JR et al (2000) Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127:3533\u20133542","journal-title":"Development"},{"key":"811_CR33","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/S0925-4773(02)00333-7","volume":"120","author":"ME Wilson","year":"2003","unstructured":"Wilson ME, Scheel D, German MS (2003) Gene expression cascades in pancreatic development. Mech Dev 120:65\u201380","journal-title":"Mech Dev"},{"key":"811_CR34","first-page":"1174","volume":"77","author":"RS Goland","year":"1993","unstructured":"Goland RS, Jozak S, Warren WB, Conwell IM, Stark RI, Tropper PJ (1993) Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth-retarded fetuses. J Clin Endocrinol Metab 77:1174\u20131179","journal-title":"J Clin Endocrinol Metab"},{"key":"811_CR35","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1126\/science.705336","volume":"202","author":"JM Reinisch","year":"1978","unstructured":"Reinisch JM, Simon NG, Karow WG, Gandelman R (1978) Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 202:436\u2013438","journal-title":"Science"},{"key":"811_CR36","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1210\/endo.142.5.8139","volume":"142","author":"J Lesage","year":"2001","unstructured":"Lesage J, Blondeau B, Grino M, Breant B, Dupouy JP (2001) Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 142:1692\u20131702","journal-title":"Endocrinology"},{"key":"811_CR37","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1042\/bj20030140","volume":"375","author":"CN Shen","year":"2003","unstructured":"Shen CN, Seckl JR, Slack JM, Tosh D (2003) Glucocorticoids suppress beta-cell development and induce hepatic metaplasia in embryonic pancreas. Biochem J 375:41\u201350","journal-title":"Biochem J"},{"key":"811_CR38","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1079\/BJN2003967","volume":"90","author":"DS Fernandez-Twinn","year":"2003","unstructured":"Fernandez-Twinn DS, Ozanne SE, Ekizoglou S et al (2003) The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br J Nutr 90:815\u2013822","journal-title":"Br J Nutr"},{"key":"811_CR39","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/S0024-3205(98)00311-7","volume":"63","author":"SC Langley-Evans","year":"1998","unstructured":"Langley-Evans SC, Nwagwu M (1998) Impaired growth and increased glucocorticoid-sensitive enzyme activities in tissues of rat fetuses exposed to maternal low protein diets. Life Sci 63:605\u2013615","journal-title":"Life Sci"},{"key":"811_CR40","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.ydbio.2005.11.023","volume":"290","author":"P Jacquemin","year":"2006","unstructured":"Jacquemin P, Yoshitomi H, Kashima Y, Rousseau GG, Lemaigre FP, Zaret KS (2006) An endothelial\u2013mesenchymal relay pathway regulates early phases of pancreas development. Dev Biol 290:189\u2013199","journal-title":"Dev Biol"},{"key":"811_CR41","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1126\/science.1064344","volume":"294","author":"E Lammert","year":"2001","unstructured":"Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294:564\u2013567","journal-title":"Science"},{"key":"811_CR42","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1016\/S0960-9822(03)00378-6","volume":"13","author":"E Lammert","year":"2003","unstructured":"Lammert E, Gu G, McLaughlin M et al (2003) Role of VEGF\u2014a in vascularization of pancreatic islets. Curr Biol 13:1070\u20131074","journal-title":"Curr Biol"},{"key":"811_CR43","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/j.devcel.2006.01.015","volume":"10","author":"G Nikolova","year":"2006","unstructured":"Nikolova G, Jabs N, Konstantinova I et al (2006) The vascular basement membrane: A niche for insulin gene expression and Beta cell proliferation. Dev Cell 10:397\u2013405","journal-title":"Dev Cell"},{"key":"811_CR44","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1016\/0012-1606(72)90083-8","volume":"29","author":"RL Pictet","year":"1972","unstructured":"Pictet RL, Clark WR, Williams RH, Rutter WJ (1972) An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 29:436\u2013467","journal-title":"Dev Biol"},{"key":"811_CR45","doi-asserted-by":"crossref","first-page":"2315","DOI":"10.1210\/en.2005-0997","volume":"147","author":"M Johansson","year":"2006","unstructured":"Johansson M, Mattsson G, Andersson A, Jansson L, Carlsson PO (2006) Islet endothelial cells and pancreatic beta-cell proliferation: studies in vitro and during pregnancy in adult rats. Endocrinology 147:2315\u20132324","journal-title":"Endocrinology"}],"container-title":["Diabetologia"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-007-0811-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00125-007-0811-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-007-0811-0","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,23]],"date-time":"2021-08-23T16:40:20Z","timestamp":1629736820000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00125-007-0811-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,9,19]]},"references-count":45,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2007,11,5]]}},"alternative-id":["811"],"URL":"https:\/\/doi.org\/10.1007\/s00125-007-0811-0","relation":{},"ISSN":["0012-186X","1432-0428"],"issn-type":[{"value":"0012-186X","type":"print"},{"value":"1432-0428","type":"electronic"}],"subject":[],"published":{"date-parts":[[2007,9,19]]}}}