{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T15:04:10Z","timestamp":1787497450459,"version":"build-2736575974"},"reference-count":83,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2021,2,11]],"date-time":"2021-02-11T00:00:00Z","timestamp":1613001600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,2,11]],"date-time":"2021-02-11T00:00:00Z","timestamp":1613001600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Wellcome Trust and Royal Society Sir Henry Dale Fellowship","award":["105636\/Z\/14\/Z"],"award-info":[{"award-number":["105636\/Z\/14\/Z"]}]},{"DOI":"10.13039\/501100000272","name":"National Institute for Health Research","doi-asserted-by":"publisher","award":["Senior Investigator"],"award-info":[{"award-number":["Senior Investigator"]}],"id":[{"id":"10.13039\/501100000272","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004440","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["WT098395\/Z\/12\/Z"],"award-info":[{"award-number":["WT098395\/Z\/12\/Z"]}],"id":[{"id":"10.13039\/100004440","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Diabetologia"],"published-print":{"date-parts":[[2021,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>In 1998 the fetal insulin hypothesis proposed that lower birthweight and adult-onset type 2 diabetes are two phenotypes of the same genotype. Since then, advances in research investigating the role of genetics affecting insulin secretion and action have furthered knowledge of fetal insulin-mediated growth and the biology of type 2 diabetes. In this review, we discuss the historical research context from which the fetal insulin hypothesis originated and consider the position of the hypothesis in light of recent evidence. In summary, there is now ample evidence to support the idea that variants of certain genes which result in impaired pancreatic beta cell function and reduced insulin secretion contribute to both lower birthweight and higher type 2 diabetes risk in later life when inherited by the fetus. There is also evidence to support genetic links between type 2 diabetes secondary to reduced insulin action and lower birthweight but this applies only to loci implicated in body fat distribution and not those influencing insulin resistance via obesity or lipid metabolism by the liver. Finally, we also consider how advances in genetics are being used to explore alternative hypotheses, namely the role of the maternal intrauterine environment, in the relationship between lower birthweight and adult cardiometabolic disease.<\/jats:p>\n                  <jats:p>\n                    <jats:bold>Graphical abstract<\/jats:bold>\n                  <\/jats:p>","DOI":"10.1007\/s00125-021-05386-7","type":"journal-article","created":{"date-parts":[[2021,2,11]],"date-time":"2021-02-11T09:51:08Z","timestamp":1613037068000},"page":"717-726","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":47,"title":["Two decades since the fetal insulin hypothesis: what have we learned from genetics?"],"prefix":"10.1007","volume":"64","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1352-4447","authenticated-orcid":false,"given":"Alice E.","family":"Hughes","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5620-473X","authenticated-orcid":false,"given":"Andrew T.","family":"Hattersley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8670-6340","authenticated-orcid":false,"given":"Sarah E.","family":"Flanagan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4152-2238","authenticated-orcid":false,"given":"Rachel M.","family":"Freathy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,2,11]]},"reference":[{"issue":"1","key":"5386_CR1","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1007\/BF00399095","volume":"36","author":"DJP Barker","year":"1993","unstructured":"Barker DJP, Hales CN, Fall CHD, Osmond C, Phipps K, Clark PMS (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36(1):62\u201367. https:\/\/doi.org\/10.1007\/BF00399095","journal-title":"Diabetologia"},{"issue":"6809","key":"5386_CR2","doi-asserted-by":"publisher","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(6809):1019\u20131022","journal-title":"BMJ"},{"issue":"8","key":"5386_CR3","doi-asserted-by":"publisher","first-page":"849","DOI":"10.1093\/aje\/kwk071","volume":"165","author":"T Harder","year":"2007","unstructured":"Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A (2007) Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol 165(8):849\u2013857. https:\/\/doi.org\/10.1093\/aje\/kwk071","journal-title":"Am J Epidemiol"},{"issue":"1","key":"5386_CR4","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1093\/bmb\/60.1.5","volume":"60","author":"CN Hales","year":"2001","unstructured":"Hales CN, Barker DJP (2001) The thrifty phenotype hypothesis. Br Med Bull 60(1):5\u201320. https:\/\/doi.org\/10.1093\/bmb\/60.1.5","journal-title":"Br Med Bull"},{"issue":"5691","key":"5386_CR5","doi-asserted-by":"publisher","first-page":"1733","DOI":"10.1126\/science.1095292","volume":"305","author":"PD Gluckman","year":"2004","unstructured":"Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305(5691):1733\u20131736. https:\/\/doi.org\/10.1126\/science.1095292","journal-title":"Science"},{"issue":"3","key":"5386_CR6","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1038\/953","volume":"19","author":"AT Hattersley","year":"1998","unstructured":"Hattersley AT, Beards F, Ballantyne E, Appleton M, Harvey R, Ellard S (1998) Mutations in the glucokinase gene of the fetus result in reduced birth weight. Nat Genet 19(3):268\u2013270. https:\/\/doi.org\/10.1038\/953","journal-title":"Nat Genet"},{"issue":"9166","key":"5386_CR7","doi-asserted-by":"publisher","first-page":"1789","DOI":"10.1016\/S0140-6736(98)07546-1","volume":"353","author":"AT Hattersley","year":"1999","unstructured":"Hattersley AT, Tooke JE (1999) The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 353(9166):1789\u20131792. https:\/\/doi.org\/10.1016\/S0140-6736(98)07546-1","journal-title":"Lancet"},{"key":"5386_CR8","unstructured":"Pedersen J (1952) Diabetes and pregnancy: blood sugar of newborn infants during fasting and glucose administration. Danish Science Press, Copenhagen, pp 230 (Ph. D. thesis)"},{"issue":"10","key":"5386_CR9","doi-asserted-by":"publisher","first-page":"1789","DOI":"10.1007\/s00125-019-4951-9","volume":"62","author":"DS Fernandez-Twinn","year":"2019","unstructured":"Fernandez-Twinn DS, Hjort L, Novakovic B, Ozanne SE, Saffery R (2019) Intrauterine programming of obesity and type 2 diabetes. Diabetologia 62(10):1789\u20131801. https:\/\/doi.org\/10.1007\/s00125-019-4951-9","journal-title":"Diabetologia"},{"issue":"3","key":"5386_CR10","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1007\/s00125-001-0770-9","volume":"45","author":"A Stride","year":"2002","unstructured":"Stride A, Vaxillaire M, Tuomi T et al (2002) The genetic abnormality in the beta cell determines the response to an oral glucose load. Diabetologia 45(3):427\u2013435. https:\/\/doi.org\/10.1007\/s00125-001-0770-9","journal-title":"Diabetologia"},{"key":"5386_CR11","doi-asserted-by":"publisher","unstructured":"Steele AM, Wensley KJ, Ellard S et al (2013) Use of HbA1c in the Identification of Patients with Hyperglycaemia Caused by a Glucokinase Mutation: Observational Case Control Studies. PLoS One 8(6). https:\/\/doi.org\/10.1371\/journal.pone.0065326","DOI":"10.1371\/journal.pone.0065326"},{"issue":"7","key":"5386_CR12","doi-asserted-by":"publisher","first-page":"958","DOI":"10.1093\/clinchem\/hvaa104","volume":"66","author":"RC Caswell","year":"2020","unstructured":"Caswell RC, Snowsill T, Houghton JAL et al (2020) Noninvasive Fetal Genotyping by Droplet Digital PCR to Identify Maternally Inherited Monogenic Diabetes Variants. Clin Chem 66(7):958\u2013965. https:\/\/doi.org\/10.1093\/clinchem\/hvaa104","journal-title":"Clin Chem"},{"issue":"18","key":"5386_CR13","doi-asserted-by":"publisher","first-page":"1838","DOI":"10.1056\/NEJMoa032922","volume":"350","author":"AL Gloyn","year":"2004","unstructured":"Gloyn AL, Pearson ER, Antcliff JF et al (2004) Activating Mutations in the Gene Encoding the ATP-Sensitive Potassium-Channel Subunit Kir6.2 and Permanent Neonatal Diabetes. N Engl J Med 350(18):1838\u20131849. https:\/\/doi.org\/10.1056\/NEJMoa032922","journal-title":"N Engl J Med"},{"issue":"11","key":"5386_CR14","doi-asserted-by":"publisher","first-page":"1793","DOI":"10.1093\/hmg\/ddl101","volume":"15","author":"P Proks","year":"2006","unstructured":"Proks P, Arnold AL, Bruining J et al (2006) A heterozygous activating mutation in the sulphonylurea receptor SUR1 (ABCC8) causes neonatal diabetes. Hum Mol Genet 15(11):1793\u20131800. https:\/\/doi.org\/10.1093\/hmg\/ddl101","journal-title":"Hum Mol Genet"},{"issue":"7","key":"5386_CR15","doi-asserted-by":"publisher","first-page":"1930","DOI":"10.2337\/db07-0043","volume":"56","author":"SE Flanagan","year":"2007","unstructured":"Flanagan SE, Patch A-M, Mackay DJG et al (2007) Mutations in ATP-Sensitive K+ Channel Genes Cause Transient Neonatal Diabetes and Permanent Diabetes in Childhood or Adulthood. Diabetes 56(7):1930\u20131937. https:\/\/doi.org\/10.2337\/db07-0043","journal-title":"Diabetes"},{"issue":"7","key":"5386_CR16","doi-asserted-by":"publisher","first-page":"2782","DOI":"10.1210\/jc.2006-0201","volume":"91","author":"AS Slingerland","year":"2006","unstructured":"Slingerland AS, Hattersley AT (2006) Activating mutations in the gene encoding Kir6.2 alter fetal and postnatal growth and also cause neonatal diabetes. J Clin Endocrinol Metab 91(7):2782\u20132788. https:\/\/doi.org\/10.1210\/jc.2006-0201","journal-title":"J Clin Endocrinol Metab"},{"issue":"7","key":"5386_CR17","doi-asserted-by":"publisher","first-page":"3105","DOI":"10.1073\/pnas.0910533107","volume":"107","author":"I Garin","year":"2010","unstructured":"Garin I, Edghill EL, Akerman I et al (2010) Recessive mutations in the INS gene result in neonatal diabetes through reduced insulin biosynthesis. Proc Natl Acad Sci USA 107(7):3105\u20133110. https:\/\/doi.org\/10.1073\/pnas.0910533107","journal-title":"Proc Natl Acad Sci USA"},{"issue":"5","key":"5386_CR18","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1016\/j.ajhg.2019.03.018","volume":"104","author":"E De Franco","year":"2019","unstructured":"De Franco E, Watson RA, Weninger WJ et al (2019) A Specific CNOT1 Mutation Results in a Novel Syndrome of Pancreatic Agenesis and Holoprosencephaly through Impaired Pancreatic and Neurological Development. Am J Hum Genet 104(5):985\u2013989. https:\/\/doi.org\/10.1016\/j.ajhg.2019.03.018","journal-title":"Am J Hum Genet"},{"issue":"8","key":"5386_CR19","doi-asserted-by":"publisher","first-page":"2888","DOI":"10.2337\/db14-0061","volume":"63","author":"C Shaw-Smith","year":"2014","unstructured":"Shaw-Smith C, De Franco E, Allen HL et al (2014) GATA4 Mutations Are a Cause of Neonatal and Childhood-Onset Diabetes. Diabetes 63(8):2888\u20132894. https:\/\/doi.org\/10.2337\/db14-0061","journal-title":"Diabetes"},{"issue":"1","key":"5386_CR20","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1038\/ng.1035","volume":"44","author":"HL Allen","year":"2012","unstructured":"Allen HL, Flanagan SE, Shaw-Smith C et al (2012) GATA6 haploinsufficiency causes pancreatic agenesis in humans. Nat Genet 44(1):20\u201322. https:\/\/doi.org\/10.1038\/ng.1035","journal-title":"Nat Genet"},{"issue":"1","key":"5386_CR21","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1038\/ng0197-106","volume":"15","author":"DA Stoffers","year":"1997","unstructured":"Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF (1997) Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 15(1):106\u2013110. https:\/\/doi.org\/10.1038\/ng0197-106","journal-title":"Nat Genet"},{"issue":"1","key":"5386_CR22","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1038\/ng.2826","volume":"46","author":"MN Weedon","year":"2014","unstructured":"Weedon MN, Cebola I, Patch A-M et al (2014) Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis. Nat Genet 46(1):61\u201364. https:\/\/doi.org\/10.1038\/ng.2826","journal-title":"Nat Genet"},{"issue":"9","key":"5386_CR23","doi-asserted-by":"publisher","first-page":"2810","DOI":"10.2337\/db15-1666","volume":"65","author":"JAL Houghton","year":"2016","unstructured":"Houghton JAL, Swift GH, Shaw-Smith C et al (2016) Isolated Pancreatic Aplasia Due to a Hypomorphic PTF1A Mutation. Diabetes 65(9):2810\u20132815. https:\/\/doi.org\/10.2337\/db15-1666","journal-title":"Diabetes"},{"key":"5386_CR24","doi-asserted-by":"publisher","unstructured":"De Franco E, Flanagan SE, Houghton JA et al (2015) The effect of early, comprehensive genomic testing on clinical care in neonatal diabetes: an international cohort study. Lancet 386(9997):957\u2013963. https:\/\/doi.org\/10.1016\/S0140-6736(15)60098-8","DOI":"10.1016\/S0140-6736(15)60098-8"},{"issue":"5","key":"5386_CR25","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1159\/000245927","volume":"72","author":"AL Fowden","year":"2009","unstructured":"Fowden AL, Forhead AJ (2009) Endocrine Regulation of Feto-Placental Growth. Horm Res Paediatr 72(5):257\u2013265. https:\/\/doi.org\/10.1159\/000245927","journal-title":"Horm Res Paediatr"},{"issue":"6","key":"5386_CR26","doi-asserted-by":"publisher","first-page":"699","DOI":"10.2337\/diab.44.6.699","volume":"44","author":"MM Byrne","year":"1995","unstructured":"Byrne MM, Sturis J, Fajans SS et al (1995) Altered insulin secretory responses to glucose in subjects with a mutation in the MODY1 gene on chromosome 20. Diabetes 44(6):699\u2013704. https:\/\/doi.org\/10.2337\/diab.44.6.699","journal-title":"Diabetes"},{"issue":"11","key":"5386_CR27","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.2337\/diab.45.11.1503","volume":"45","author":"MM Byrne","year":"1996","unstructured":"Byrne MM, Sturis J, Menzel S et al (1996) Altered Insulin Secretory Responses to Glucose in Diabetic and Nondiabetic Subjects With Mutations in the Diabetes Susceptibility Gene MODY3 on Chromosome 12. Diabetes 45(11):1503\u20131510. https:\/\/doi.org\/10.2337\/diab.45.11.1503","journal-title":"Diabetes"},{"issue":"5","key":"5386_CR28","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1007\/s00125-005-1738-y","volume":"48","author":"ER Pearson","year":"2005","unstructured":"Pearson ER, Pruhova S, Tack CJ et al (2005) Molecular genetics and phenotypic characteristics of MODY caused by hepatocyte nuclear factor 4\u03b1 mutations in a large European collection. Diabetologia 48(5):878\u2013885. https:\/\/doi.org\/10.1007\/s00125-005-1738-y","journal-title":"Diabetologia"},{"issue":"4","key":"5386_CR29","doi-asserted-by":"publisher","first-page":"e118","DOI":"10.1371\/journal.pmed.0040118","volume":"4","author":"ER Pearson","year":"2007","unstructured":"Pearson ER, Boj SF, Steele AM et al (2007) Macrosomia and Hyperinsulinaemic Hypoglycaemia in Patients with Heterozygous Mutations in the HNF4A Gene. PLoS Med 4(4):e118. https:\/\/doi.org\/10.1371\/journal.pmed.0040118","journal-title":"PLoS Med"},{"issue":"4","key":"5386_CR30","doi-asserted-by":"publisher","first-page":"e148","DOI":"10.1371\/journal.pmed.0040148","volume":"4","author":"B Glaser","year":"2007","unstructured":"Glaser B (2007) Type 2 Diabetes: Hypoinsulinism, Hyperinsulinism, or Both? PLoS Med 4(4):e148. https:\/\/doi.org\/10.1371\/journal.pmed.0040148","journal-title":"PLoS Med"},{"issue":"6","key":"5386_CR31","doi-asserted-by":"publisher","first-page":"1745","DOI":"10.2337\/db07-1742","volume":"57","author":"LW Harries","year":"2008","unstructured":"Harries LW, Locke JM, Shields B et al (2008) The Diabetic Phenotype in HNF4A Mutation Carriers Is Moderated By the Expression of HNF4A Isoforms From the P1 Promoter During Fetal Development. Diabetes 57(6):1745\u20131752. https:\/\/doi.org\/10.2337\/db07-1742","journal-title":"Diabetes"},{"issue":"5","key":"5386_CR32","doi-asserted-by":"publisher","first-page":"808","DOI":"10.1074\/mcp.RA119.001909","volume":"19","author":"\u00c9 Lambert","year":"2020","unstructured":"Lambert \u00c9, Babeu J-P, Simoneau J et al (2020) Human Hepatocyte Nuclear factor 4-\u03b1 Encodes Isoforms with Distinct Transcriptional Functions. Mol Cell Proteomics 19(5):808\u2013827. https:\/\/doi.org\/10.1074\/mcp.RA119.001909","journal-title":"Mol Cell Proteomics"},{"issue":"5","key":"5386_CR33","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1016\/s0022-3476(54)80113-2","volume":"45","author":"WL Donohue","year":"1954","unstructured":"Donohue WL, Uchida I (1954) Leprechaunism: a euphemism for a rare familial disorder. J Pediatr 45(5):505\u2013519. https:\/\/doi.org\/10.1016\/s0022-3476(54)80113-2","journal-title":"J Pediatr"},{"issue":"1","key":"5386_CR34","first-page":"73","volume":"37","author":"LJ Elsas","year":"1985","unstructured":"Elsas LJ, Endo F, Strumlauf E, Elders J, Priest JH (1985) Leprechaunism: an inherited defect in a high-affinity insulin receptor. Am J Hum Genet 37(1):73\u201388","journal-title":"Am J Hum Genet"},{"issue":"8866","key":"5386_CR35","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/0140-6736(93)91820-C","volume":"342","author":"A Krook","year":"1993","unstructured":"Krook A, O\u2019Rahilly S, Brueton L (1993) Homozygous nonsense mutation in the insulin receptor gene in infant with leprechaunism. Lancet 342(8866):277\u2013278. https:\/\/doi.org\/10.1016\/0140-6736(93)91820-C","journal-title":"Lancet"},{"issue":"6","key":"5386_CR36","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1016\/j.bbalip.2008.12.014","volume":"1791","author":"A Garg","year":"2009","unstructured":"Garg A, Agarwal AK (2009) Lipodystrophies: Disorders of adipose tissue biology. Biochimica Biophysica Acta Mol Cell Biol Lipids 1791(6):507\u2013513. https:\/\/doi.org\/10.1016\/j.bbalip.2008.12.014","journal-title":"Biochimica Biophysica Acta Mol Cell Biol Lipids"},{"issue":"s413","key":"5386_CR37","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1111\/j.1651-2227.1996.tb14262.x","volume":"85","author":"M Seip","year":"1996","unstructured":"Seip M, Trygstad O (1996) Generalized lipodystrophy, congenital and acquired (lipoatrophy). Acta Paediatrica 85(s413):2\u201328. https:\/\/doi.org\/10.1111\/j.1651-2227.1996.tb14262.x","journal-title":"Acta Paediatrica"},{"issue":"23","key":"5386_CR38","doi-asserted-by":"publisher","first-page":"2810","DOI":"10.1002\/ajmg.a.32046","volume":"143A","author":"P Muschke","year":"2007","unstructured":"Muschke P, K\u00f6lsch U, Jakubiczka S, Wieland I, Brune T, Wieacker P (2007) The heterozygous LMNA mutation p.R471G causes a variable phenotype with features of two types of familial partial lipodystrophy. Am J Med Genet A 143A(23):2810\u20132814. https:\/\/doi.org\/10.1002\/ajmg.a.32046","journal-title":"Am J Med Genet A"},{"issue":"1","key":"5386_CR39","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s12887-016-0581-2","volume":"16","author":"P Krawiec","year":"2016","unstructured":"Krawiec P, Me\u0142ges B, Pac-Ko\u017cuchowska E, Mroczkowska-Juchkiewicz A, Czerska K (2016) Fitting the pieces of the puzzle together: a case report of the Dunnigan-type of familial partial lipodystrophy in the adolescent girl. BMC Pediatr 16(1):38. https:\/\/doi.org\/10.1186\/s12887-016-0581-2","journal-title":"BMC Pediatr"},{"issue":"2","key":"5386_CR40","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1038\/72807","volume":"24","author":"S Shackleton","year":"2000","unstructured":"Shackleton S, Lloyd DJ, Jackson SN et al (2000) LMNA, encoding lamin A\/C, is mutated in partial lipodystrophy. Nat Genet 24(2):153\u2013156. https:\/\/doi.org\/10.1038\/72807","journal-title":"Nat Genet"},{"issue":"6764","key":"5386_CR41","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1038\/47254","volume":"402","author":"I Barroso","year":"1999","unstructured":"Barroso I, Gurnell M, Crowley VE et al (1999) Dominant negative mutations in human PPARgamma associated with severe insulin resistance, diabetes mellitus and hypertension. Nature 402(6764):880\u2013883. https:\/\/doi.org\/10.1038\/47254","journal-title":"Nature"},{"issue":"8","key":"5386_CR42","doi-asserted-by":"publisher","first-page":"740","DOI":"10.1056\/NEJMoa1007487","volume":"354","author":"S Gandotra","year":"2011","unstructured":"Gandotra S, Le Dour C, Bottomley W et al (2011) Perilipin Deficiency and Autosomal Dominant Partial Lipodystrophy. N Engl J Med 354(8):740\u2013748. https:\/\/doi.org\/10.1056\/NEJMoa1007487","journal-title":"N Engl J Med"},{"issue":"6","key":"5386_CR43","doi-asserted-by":"publisher","first-page":"1714","DOI":"10.1093\/ije\/dyt220","volume":"42","author":"JS Tyrrell","year":"2013","unstructured":"Tyrrell JS, Yaghootkar H, Freathy RM, Hattersley AT, Frayling TM (2013) Parental diabetes and birthweight in 236 030 individuals in the UK Biobank Study. Int J Epidemiol 42(6):1714\u20131723. https:\/\/doi.org\/10.1093\/ije\/dyt220","journal-title":"Int J Epidemiol"},{"issue":"3","key":"5386_CR44","doi-asserted-by":"publisher","first-page":"445","DOI":"10.2337\/diabetes.49.3.445","volume":"49","author":"RS Lindsay","year":"2000","unstructured":"Lindsay RS, Dabelea D, Roumain J, Hanson RL, Bennett PH, Knowler WC (2000) Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes 49(3):445\u2013449. https:\/\/doi.org\/10.2337\/diabetes.49.3.445","journal-title":"Diabetes"},{"issue":"19","key":"5386_CR45","doi-asserted-by":"publisher","first-page":"1991","DOI":"10.1056\/NEJMoa0707943","volume":"358","author":"HAPO Study Cooperative Research Group","year":"2008","unstructured":"HAPO Study Cooperative Research Group (2008) Hyperglycemia and adverse pregnancy outcomes. N Engl J Med 358(19):1991\u20132002. https:\/\/doi.org\/10.1056\/NEJMoa0707943","journal-title":"N Engl J Med"},{"issue":"6","key":"5386_CR46","doi-asserted-by":"publisher","first-page":"1675","DOI":"10.2337\/dc12-1280","volume":"36","author":"S Hillman","year":"2013","unstructured":"Hillman S, Peebles DM, Williams DJ (2013) Paternal metabolic and cardiovascular risk factors for fetal growth restriction: a case-control study. Diabetes Care 36(6):1675\u20131680. https:\/\/doi.org\/10.2337\/dc12-1280","journal-title":"Diabetes Care"},{"issue":"1","key":"5386_CR47","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1007\/s00125-003-1270-x","volume":"47","author":"SG Wannamethee","year":"2004","unstructured":"Wannamethee SG, Lawlor DA, Whincup PH, Walker M, Ebrahim S, Davey-Smith G (2004) Birthweight of offspring and paternal insulin resistance and paternal diabetes in late adulthood: cross sectional survey. Diabetologia 47(1):12\u201318. https:\/\/doi.org\/10.1007\/s00125-003-1270-x","journal-title":"Diabetologia"},{"issue":"11","key":"5386_CR48","doi-asserted-by":"publisher","first-page":"2675","DOI":"10.1007\/s00125-006-0417-y","volume":"49","author":"B Knight","year":"2006","unstructured":"Knight B, Shields BM, Hill A et al (2006) Offspring birthweight is not associated with paternal insulin resistance. Diabetologia 49(11):2675\u20132678. https:\/\/doi.org\/10.1007\/s00125-006-0417-y","journal-title":"Diabetologia"},{"issue":"11","key":"5386_CR49","doi-asserted-by":"publisher","first-page":"2668","DOI":"10.1007\/s00125-006-0282-8","volume":"49","author":"BM Shields","year":"2006","unstructured":"Shields BM, Knight B, Turner M et al (2006) Paternal insulin resistance and its association with umbilical cord insulin concentrations. Diabetologia 49(11):2668\u20132674. https:\/\/doi.org\/10.1007\/s00125-006-0282-8","journal-title":"Diabetologia"},{"issue":"7130","key":"5386_CR50","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1038\/nature05616","volume":"445","author":"R Sladek","year":"2007","unstructured":"Sladek R, Rocheleau G, Rung J et al (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445(7130):881\u2013885. https:\/\/doi.org\/10.1038\/nature05616","journal-title":"Nature"},{"issue":"5829","key":"5386_CR51","doi-asserted-by":"publisher","first-page":"1336","DOI":"10.1126\/science.1142364","volume":"316","author":"E Zeggini","year":"2007","unstructured":"Zeggini E, Weedon MN, Lindgren CM et al (2007) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316(5829):1336\u20131341. https:\/\/doi.org\/10.1126\/science.1142364","journal-title":"Science"},{"issue":"5","key":"5386_CR52","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1038\/ng.120","volume":"40","author":"E Zeggini","year":"2008","unstructured":"Zeggini E, Scott LJ, Saxena R et al (2008) Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40(5):638\u2013645. https:\/\/doi.org\/10.1038\/ng.120","journal-title":"Nat Genet"},{"issue":"6","key":"5386_CR53","doi-asserted-by":"publisher","first-page":"1428","DOI":"10.2337\/db08-1739","volume":"58","author":"RM Freathy","year":"2009","unstructured":"Freathy RM, Bennett AJ, Ring SM et al (2009) Type 2 diabetes risk alleles are associated with reduced size at birth. Diabetes 58(6):1428\u20131433. https:\/\/doi.org\/10.2337\/db08-1739","journal-title":"Diabetes"},{"issue":"10","key":"5386_CR54","doi-asserted-by":"publisher","first-page":"2414","DOI":"10.2337\/db09-0506","volume":"58","author":"J Zhao","year":"2009","unstructured":"Zhao J, Li M, Bradfield JP et al (2009) Examination of type 2 diabetes loci implicates CDKAL1 as a birth weight gene. Diabetes 58(10):2414\u20132418. https:\/\/doi.org\/10.2337\/db09-0506","journal-title":"Diabetes"},{"issue":"5","key":"5386_CR55","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/ng.567","volume":"42","author":"RM Freathy","year":"2010","unstructured":"Freathy RM, Mook-Kanamori DO, Sovio U et al (2010) Variants in ADCY5 and near CCNL1 are associated with fetal growth and birth weight. Nat Genet 42(5):430\u2013435. https:\/\/doi.org\/10.1038\/ng.567","journal-title":"Nat Genet"},{"issue":"9","key":"5386_CR56","doi-asserted-by":"publisher","first-page":"3009","DOI":"10.2337\/db13-1607","volume":"63","author":"DJ Hodson","year":"2014","unstructured":"Hodson DJ, Mitchell RK, Marselli L et al (2014) ADCY5 Couples Glucose to Insulin Secretion in Human Islets. Diabetes 63(9):3009\u20133021. https:\/\/doi.org\/10.2337\/db13-1607","journal-title":"Diabetes"},{"issue":"7624","key":"5386_CR57","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1038\/nature19806","volume":"538","author":"M Horikoshi","year":"2016","unstructured":"Horikoshi M, Beaumont RN, Day FR et al (2016) Genome-wide associations for birth weight and correlations with adult disease. Nature 538(7624):248\u2013252. https:\/\/doi.org\/10.1038\/nature19806","journal-title":"Nature"},{"issue":"4","key":"5386_CR58","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1093\/hmg\/ddx429","volume":"27","author":"RN Beaumont","year":"2018","unstructured":"Beaumont RN, Warrington NM, Cavadino A et al (2018) Genome-wide association study of offspring birth weight in 86\u2009577 women identifies five novel loci and highlights maternal genetic effects that are independent of fetal genetics. Hum Mol Genet 27(4):742\u2013756. https:\/\/doi.org\/10.1093\/hmg\/ddx429","journal-title":"Hum Mol Genet"},{"issue":"5","key":"5386_CR59","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1038\/s41588-019-0403-1","volume":"51","author":"NM Warrington","year":"2019","unstructured":"Warrington NM, Beaumont RN, Horikoshi M et al (2019) Maternal and fetal genetic effects on birth weight and their relevance to cardio-metabolic risk factors. Nat Genet 51(5):804\u2013814. https:\/\/doi.org\/10.1038\/s41588-019-0403-1","journal-title":"Nat Genet"},{"issue":"4","key":"5386_CR60","doi-asserted-by":"publisher","first-page":"1229","DOI":"10.1093\/ije\/dyy015","volume":"47","author":"NM Warrington","year":"2018","unstructured":"Warrington NM, Freathy RM, Neale MC, Evans DM (2018) Using structural equation modelling to jointly estimate maternal and fetal effects on birthweight in the UK Biobank. Int J Epidemiol 47(4):1229\u20131241. https:\/\/doi.org\/10.1093\/ije\/dyy015","journal-title":"Int J Epidemiol"},{"issue":"11","key":"5386_CR61","doi-asserted-by":"publisher","first-page":"1505","DOI":"10.1038\/s41588-018-0241-6","volume":"50","author":"A Mahajan","year":"2018","unstructured":"Mahajan A, Taliun D, Thurner M et al (2018) Fine-mapping type 2 diabetes loci to single-variant resolution using high-density imputation and islet-specific epigenome maps. Nat Genet 50(11):1505\u20131513. https:\/\/doi.org\/10.1038\/s41588-018-0241-6","journal-title":"Nat Genet"},{"key":"5386_CR62","doi-asserted-by":"publisher","first-page":"331","DOI":"10.3389\/fgene.2015.00331","volume":"6","author":"M Lizio","year":"2015","unstructured":"Lizio M, Ishizu Y, Itoh M et al (2015) Mapping Mammalian Cell-type-specific Transcriptional Regulatory Networks Using KD-CAGE and ChIP-seq Data in the TC-YIK Cell Line. Front Genet 6:331. https:\/\/doi.org\/10.3389\/fgene.2015.00331","journal-title":"Front Genet"},{"issue":"8","key":"5386_CR63","doi-asserted-by":"publisher","first-page":"2448","DOI":"10.2337\/db15-1671","volume":"65","author":"H Yaghootkar","year":"2016","unstructured":"Yaghootkar H, Lotta LA, Tyrrell J et al (2016) Genetic Evidence for a Link Between Favorable Adiposity and Lower Risk of Type 2 Diabetes, Hypertension, and Heart Disease. Diabetes 65(8):2448\u20132460. https:\/\/doi.org\/10.2337\/db15-1671","journal-title":"Diabetes"},{"key":"5386_CR64","doi-asserted-by":"publisher","unstructured":"Thompson WD, Beaumont RN, Kuang A et al (2020) Fetal alleles predisposing to metabolically favourable adiposity are associated with higher birth weight. bioRxiv 302208 (Preprint). 17 Sep 2020. Available from: https:\/\/doi.org\/10.1101\/2020.09.17.302208","DOI":"10.1101\/2020.09.17.302208"},{"issue":"5","key":"5386_CR65","doi-asserted-by":"publisher","first-page":"1024","DOI":"10.2337\/db17-1188","volume":"67","author":"AE Hughes","year":"2018","unstructured":"Hughes AE, Nodzenski M, Beaumont RN et al (2018) Fetal Genotype and Maternal Glucose Have Independent and Additive Effects on Birth Weight. Diabetes 67(5):1024\u20131029. https:\/\/doi.org\/10.2337\/db17-1188","journal-title":"Diabetes"},{"issue":"1","key":"5386_CR66","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1093\/bmb\/60.1.103","volume":"60","author":"CE Bertram","year":"2001","unstructured":"Bertram CE, Hanson MA (2001) Animal models and programming of the metabolic syndrome: Type 2 diabetes. Br Med Bull 60(1):103\u2013121. https:\/\/doi.org\/10.1093\/bmb\/60.1.103","journal-title":"Br Med Bull"},{"issue":"10","key":"5386_CR67","doi-asserted-by":"publisher","first-page":"1773","DOI":"10.1007\/s00125-019-4930-1","volume":"62","author":"AD Stein","year":"2019","unstructured":"Stein AD, Obrutu OE, Behere RV, Yajnik CS (2019) Developmental undernutrition, offspring obesity and type 2 diabetes. Diabetologia 62(10):1773\u20131778. https:\/\/doi.org\/10.1007\/s00125-019-4930-1","journal-title":"Diabetologia"},{"issue":"4","key":"5386_CR68","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1007\/s001250050698","volume":"40","author":"P Poulsen","year":"1997","unstructured":"Poulsen P, Vaag AA, Kyvik KO, M\u00f8ller Jensen D, Beck-Nielsen H (1997) Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia 40(4):439\u2013446. https:\/\/doi.org\/10.1007\/s001250050698","journal-title":"Diabetologia"},{"issue":"8","key":"5386_CR69","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1002\/sim.3034","volume":"27","author":"DA Lawlor","year":"2008","unstructured":"Lawlor DA, Harbord RM, Sterne JAC, Timpson N, Smith GD (2008) Mendelian randomization: Using genes as instruments for making causal inferences in epidemiology. Stat Med 27(8):1133\u20131163. https:\/\/doi.org\/10.1002\/sim.3034","journal-title":"Stat Med"},{"issue":"9","key":"5386_CR70","doi-asserted-by":"publisher","first-page":"1920","DOI":"10.1007\/s00125-016-4019-z","volume":"59","author":"T Wang","year":"2016","unstructured":"Wang T, Huang T, Li Y et al (2016) Low birthweight and risk of type 2 diabetes: a Mendelian randomisation study. Diabetologia 59(9):1920\u20131927. https:\/\/doi.org\/10.1007\/s00125-016-4019-z","journal-title":"Diabetologia"},{"issue":"6","key":"5386_CR71","doi-asserted-by":"publisher","first-page":"e002054","DOI":"10.1161\/CIRCGEN.117.002054","volume":"11","author":"D Zanetti","year":"2018","unstructured":"Zanetti D, Tikkanen E, Gustafsson S, Priest JR, Burgess S, Ingelsson E (2018) Birthweight, Type 2 Diabetes Mellitus, and Cardiovascular Disease. Circ Genom Precisi Med 11(6):e002054. https:\/\/doi.org\/10.1161\/CIRCGEN.117.002054","journal-title":"Circ Genom Precisi Med"},{"issue":"9","key":"5386_CR72","doi-asserted-by":"publisher","first-page":"e1910915","DOI":"10.1001\/jamanetworkopen.2019.10915","volume":"2","author":"T Huang","year":"2019","unstructured":"Huang T, Wang T, Zheng Y et al (2019) Association of Birth Weight With Type 2 Diabetes and Glycemic Traits: A Mendelian Randomization Study. JAMA Netw Open 2(9):e1910915\u2013e1910915. https:\/\/doi.org\/10.1001\/jamanetworkopen.2019.10915","journal-title":"JAMA Netw Open"},{"issue":"9","key":"5386_CR73","doi-asserted-by":"publisher","first-page":"1850","DOI":"10.1007\/s00125-016-4057-6","volume":"59","author":"RM Freathy","year":"2016","unstructured":"Freathy RM (2016) Can genetic evidence help us to understand the fetal origins of type 2 diabetes? Diabetologia 59(9):1850\u20131854. https:\/\/doi.org\/10.1007\/s00125-016-4057-6","journal-title":"Diabetologia"},{"key":"5386_CR74","doi-asserted-by":"publisher","unstructured":"Cousminer DL, Freathy RM Genetics of early growth traits. Hum Mol Genet 29(R1):R66\u2013R72. https:\/\/doi.org\/10.1093\/hmg\/ddaa149","DOI":"10.1093\/hmg\/ddaa149"},{"key":"5386_CR75","doi-asserted-by":"publisher","first-page":"11","DOI":"10.12688\/wellcomeopenres.10567.1","volume":"2","author":"D Lawlor","year":"2017","unstructured":"Lawlor D, Richmond R, Warrington N et al (2017) Using Mendelian randomization to determine causal effects of maternal pregnancy (intrauterine) exposures on offspring outcomes: Sources of bias and methods for assessing them. Wellcome Open Res 2:11. https:\/\/doi.org\/10.12688\/wellcomeopenres.10567.1","journal-title":"Wellcome Open Res"},{"issue":"1","key":"5386_CR76","doi-asserted-by":"publisher","first-page":"5404","DOI":"10.1038\/s41467-020-19257-z","volume":"11","author":"G-H Moen","year":"2020","unstructured":"Moen G-H, Brumpton B, Willer C et al (2020) Mendelian randomization study of maternal influences on birthweight and future cardiometabolic risk in the HUNT cohort. Nat Commun 11(1):5404. https:\/\/doi.org\/10.1038\/s41467-020-19257-z","journal-title":"Nat Commun"},{"issue":"12","key":"5386_CR77","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.1111\/j.1464-5491.2006.01999.x","volume":"23","author":"EL Edghill","year":"2006","unstructured":"Edghill EL, Bingham C, Slingerland AS et al (2006) Hepatocyte nuclear factor-1 beta mutations cause neonatal diabetes and intrauterine growth retardation: support for a critical role of HNF-1\u03b2 in human pancreatic development. Diabet Med 23(12):1301\u20131306. https:\/\/doi.org\/10.1111\/j.1464-5491.2006.01999.x","journal-title":"Diabet Med"},{"issue":"1","key":"5386_CR78","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1038\/ng880","volume":"31","author":"AK Agarwal","year":"2002","unstructured":"Agarwal AK, Arioglu E, de Almeida S et al (2002) AGPAT2 is mutated in congenital generalized lipodystrophy linked to chromosome 9q34. Nat Genet 31(1):21\u201323. https:\/\/doi.org\/10.1038\/ng880","journal-title":"Nat Genet"},{"issue":"4","key":"5386_CR79","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1038\/ng585","volume":"28","author":"J Magr\u00e9","year":"2001","unstructured":"Magr\u00e9 J, Del\u00e9pine M, Khallouf E et al (2001) Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat Genet 28(4):365\u2013370. https:\/\/doi.org\/10.1038\/ng585","journal-title":"Nat Genet"},{"issue":"4","key":"5386_CR80","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.1210\/jc.2007-1328","volume":"93","author":"CA Kim","year":"2008","unstructured":"Kim CA, Del\u00e9pine M, Boutet E et al (2008) Association of a Homozygous Nonsense Caveolin-1 Mutation with Berardinelli-Seip Congenital Lipodystrophy. J Clin Endocrinol Metab 93(4):1129\u20131134. https:\/\/doi.org\/10.1210\/jc.2007-1328","journal-title":"J Clin Endocrinol Metab"},{"issue":"9","key":"5386_CR81","doi-asserted-by":"publisher","first-page":"e1002654","DOI":"10.1371\/journal.pmed.1002654","volume":"15","author":"MS Udler","year":"2018","unstructured":"Udler MS, Kim J, von Grotthuss M et al (2018) Type 2 diabetes genetic loci informed by multi-trait associations point to disease mechanisms and subtypes: A soft clustering analysis. PLoS Medicine 15(9):e1002654. https:\/\/doi.org\/10.1371\/journal.pmed.1002654","journal-title":"PLoS Medicine"},{"issue":"4","key":"5386_CR82","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1038\/s41588-018-0084-1","volume":"50","author":"A Mahajan","year":"2018","unstructured":"Mahajan A, Wessel J, Willems SM et al (2018) Refining the accuracy of validated target identification through coding variant fine-mapping in type 2 diabetes. Nat Genet 50(4):559\u2013571. https:\/\/doi.org\/10.1038\/s41588-018-0084-1","journal-title":"Nat Genet"},{"issue":"12","key":"5386_CR83","doi-asserted-by":"publisher","first-page":"3805","DOI":"10.2337\/db16-0361","volume":"65","author":"SK Thomsen","year":"2016","unstructured":"Thomsen SK, Ceroni A, van de Bunt M et al (2016) Systematic Functional Characterization of Candidate Causal Genes for Type 2 Diabetes Risk Variants. Diabetes 65(12):3805\u20133811. https:\/\/doi.org\/10.2337\/db16-0361","journal-title":"Diabetes"}],"container-title":["Diabetologia"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-021-05386-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00125-021-05386-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-021-05386-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T06:10:21Z","timestamp":1615183821000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00125-021-05386-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,11]]},"references-count":83,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2021,4]]}},"alternative-id":["5386"],"URL":"https:\/\/doi.org\/10.1007\/s00125-021-05386-7","relation":{},"ISSN":["0012-186X","1432-0428"],"issn-type":[{"value":"0012-186X","type":"print"},{"value":"1432-0428","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,11]]},"assertion":[{"value":"29 September 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 November 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 February 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}]}}