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Genetic influences on the association between fetal growth and susceptibility to type 2 diabetes

Published online by Cambridge University Press:  10 March 2010

B. M. Shields*
Affiliation:
Peninsula NIHR Clinical Research Facility, Peninsula Medical School, University of Exeter, Exeter, UK
R. M. Freathy
Affiliation:
Genetics of Complex Traits, Peninsula Medical School, University of Exeter, Exeter, UK
A. T. Hattersley
Affiliation:
Peninsula NIHR Clinical Research Facility, Peninsula Medical School, University of Exeter, Exeter, UK
*
Address for correspondence: B. M. Shields, Peninsula NIHR Clinical Research Facility, Peninsula Medical School, Barrack Road, Exeter, EX2 5DW, UK. (Email Beverley.Shields@pms.ac.uk)

Abstract

The fetal insulin hypothesis proposes that low birth weight and susceptibility to type 2 diabetes (T2D) could both be two phenotypes of the same genotype. Insulin is a key growth factor in utero, and T2D is characterized by insulin resistance and/or beta-cell dysfunction. Therefore, genetic variants impacting on insulin secretion and action are likely to alter both fetal growth and susceptibility to T2D. There are three lines of evidence in support of this hypothesis. (1) Studies of rare monogenic diabetes have shown mutations in a single gene, such as GCK or KCNJ11, can cause diabetes by reducing insulin secretion, and these mutations are also associated with reduced birth weight. (2) Epidemiological studies have indicated that children born to fathers with diabetes are born smaller. As the father cannot influence the intrauterine environment, this association is likely to reflect genes inherited by the fetus from the father. (3) The most compelling evidence comes from recent genome-wide association studies. Variants in the CDKAL1 and HHEX-IDE genes that predispose to diabetes, if present in the fetus, are associated with reduced birth weight. These data provide evidence for a genetic contribution to the association between low birth weight and susceptibility to T2D. This genetic background is important to take into consideration when investigating the impact of environmental determinants and developing strategies for intervention and prevention.

Type
Review
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

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References

1.Godfrey, K. The developmental origins hypothesis: epidemiology. In Developmental Origins of Health and Disease (eds. Gluckman PD, Hanson MA), 2006; pp. 632. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
2.Barker, DJP. Mothers, Babies and Health in Later Life 1998. Harcourt Brace & Co Ltd, Edinburgh.Google Scholar
3.Yajnik, CS, Godbole, K, Otiv, SR, Lubree, HG. Fetal programming of type 2 diabetes: is sex important? Diabetes Care. 2007; 30, 27542755.CrossRefGoogle ScholarPubMed
4.Poulsen, P, Grunnet, LG, Pilgaard, K, et al. Increased risk of type 2 diabetes in elderly twins. Diabetes. 2009; 58, 13501355.CrossRefGoogle ScholarPubMed
5.Poulsen, P, Vaag, AA, Kyvik, KO, Moller Jensen, D, Beck-Nielsen, H. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia. 1997; 40, 439446.CrossRefGoogle ScholarPubMed
6.Hattersley, AT, Tooke, JE. The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet. 1999; 353, 17891792.CrossRefGoogle ScholarPubMed
7.Kramer, MS. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ. 1987; 65, 663737.Google ScholarPubMed
8.Cogswell, ME, Yip, R. The influence of fetal and maternal factors on the distribution of birthweight. Semin Perinatol. 1995; 19, 222240.CrossRefGoogle ScholarPubMed
9.Guihard-Costa, AM, Grange, G, Larroche, JC, Papiernik, E. Sexual differences in anthropometric measurements in French newborns. Biol Neonate. 1997; 72, 156164.CrossRefGoogle ScholarPubMed
10.Guihard-Costa, AM, Papiernik, E, Grange, G, Richard, A. Gender differences in neonatal subcutaneous fat store in late gestation in relation to maternal weight gain. Ann Hum Biol. 2002; 29, 2636.CrossRefGoogle ScholarPubMed
11.Copper, RL, Goldenberg, RL, Cliver, SP, et al. Anthropometric assessment of body size differences of full-term male and female infants. Obstet Gynecol. 1993; 81, 161164.Google ScholarPubMed
12.Yajnik, CS, Fall, CH, Coyaji, KJ, et al. Neonatal anthropometry: the thin-fat Indian baby. The Pune Maternal Nutrition Study. Int J Obes Relat Metab Disord. 2003; 27, 173180.CrossRefGoogle ScholarPubMed
13.Shields, BM, Knight, BA, Powell, RJ, Hattersley, AT, Wright, DE. Assessing newborn body composition using principal components analysis: differences in the determinants of fat and skeletal size. BMC Pediatr. 2006; 6, 24.CrossRefGoogle ScholarPubMed
14.Shiono, PH, Klebanoff, MA, Graubard, BI, Berendes, HW, Rhoads, GG. Birth weight among women of different ethnic groups. JAMA. 1986; 255, 4852.CrossRefGoogle ScholarPubMed
15.Yajnik, CS, Lubree, HG, Rege, SS, et al. Adiposity and hyperinsulinemia in Indians are present at birth. J Clin Endocrinol Metab. 2002; 87, 55755580.CrossRefGoogle ScholarPubMed
16.Denham, M, Schell, LM, Gallo, M, Stark, A. Neonatal size of low socio-economic status Black and White term births in Albany County, NYS. Ann Hum Biol. 2001; 28, 172183.Google ScholarPubMed
17.Tanner, JM, Lejarraga, H, Turner, G. Within-family standards for birth-weight. Lancet. 1972; 2, 193197.CrossRefGoogle ScholarPubMed
18.Morton, NE. The inheritance of human birth weight. Ann Hum Genet. 1955; 20, 125134.CrossRefGoogle ScholarPubMed
19.Langhoff-Roos, J, Lindmark, G, Gustavson, KH, Gebre-Medhin, M, Meirik, O. Relative effect of parental birth weight on infant birth weight at term. Clin Genet. 1987; 32, 240248.CrossRefGoogle ScholarPubMed
20.Hennessy, E, Alberman, E. Intergenerational influences affecting birth outcome. I. Birthweight for gestational age in the children of the 1958 British birth cohort. Paediatr Perinat Epidemiol. 1998; 12(Suppl 1), 4560.CrossRefGoogle ScholarPubMed
21.Catalano, PM, Drago, NM, Amini, SB. Factors affecting fetal growth and body composition. Am J Obstet Gynecol. 1995; 172, 14591463.CrossRefGoogle ScholarPubMed
22.Wilcox, MA, Newton, CS, Johnson, IR. Paternal influences on birthweight. Acta Obstet Gynecol Scand. 1995; 74, 1518.CrossRefGoogle ScholarPubMed
23.Knight, B, Shields, BM, Turner, M, et al. Evidence of genetic regulation of fetal longitudinal growth. Early Hum Dev. 2005; 81, 823831.CrossRefGoogle ScholarPubMed
24.Klebanoff, MA, Mednick, BR, Schulsinger, C, Secher, NJ, Shiono, PH. Father’s effect on infant birth weight. Am J Obstet Gynecol. 1998; 178, 10221026.CrossRefGoogle ScholarPubMed
25.Magnus, P. Causes of variation in birth weight: a study of offspring of twins. Clin Genet. 1984; 25, 1524.CrossRefGoogle ScholarPubMed
26.Magnus, P. Further evidence for a significant effect of fetal genes on variation in birth weight. Clin Genet. 1984; 26, 289296.CrossRefGoogle ScholarPubMed
27.Magnus, P, Berg, K, Bjerkedal, T, Nance, WE. Parental determinants of birth weight. Clin Genet. 1984; 26, 397405.CrossRefGoogle ScholarPubMed
28.Magnus, P, Gjessing, HK, Skrondal, A, Skjaerven, R. Paternal contribution to birth weight. J Epidemiol Community Health. 2001; 55, 873877.CrossRefGoogle ScholarPubMed
29.Gielen, M, Lindsey, PJ, Derom, C, et al. Modeling genetic and environmental factors to increase heritability and ease the identification of candidate genes for birth weight: a twin study. Behav Genet. 2008; 38, 4454.CrossRefGoogle ScholarPubMed
30.Lunde, A, Melve, KK, Gjessing, HK, Skjaerven, R, Irgens, LM. Genetic and environmental influences on birth weight, birth length, head circumference, and gestational age by use of population-based parent-offspring data. Am J Epidemiol. 2007; 165, 734741.CrossRefGoogle ScholarPubMed
31.Clausson, B, Lichtenstein, P, Cnattingius, S. Genetic influence on birthweight and gestational length determined by studies in offspring of twins. BJOG. 2000; 107, 375381.CrossRefGoogle ScholarPubMed
32.Vlietinck, R, Derom, R, Neale, MC, et al. Genetic and environmental variation in the birth weight of twins. Behav Genet. 1989; 19, 151161.CrossRefGoogle ScholarPubMed
33.Johnston, LB, Clark, AJ, Savage, MO. Genetic factors contributing to birth weight. Arch Dis Child Fetal Neonatal Ed. 2002; 86, F2F3.CrossRefGoogle ScholarPubMed
34.Li, M, Squire, JA, Weksberg, R. Molecular genetics of Wiedemann-Beckwith syndrome. Am J Med Genet. 1998; 79, 253259.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
35.Fisher, AM, Thomas, NS, Cockwell, A, et al. Duplications of chromosome 11p15 of maternal origin result in a phenotype that includes growth retardation. Hum Genet. 2002; 111, 290296.CrossRefGoogle Scholar
36.King, H, Rewers, M. Global estimates for prevalence of diabetes mellitus and impaired glucose tolerance in adults. WHO Ad Hoc Diabetes Reporting Group. Diabetes Care. 1993; 16, 157177.CrossRefGoogle ScholarPubMed
37.Barroso, I. Genetics of Type 2 diabetes. Diabet Med. 2005; 22, 517535.CrossRefGoogle ScholarPubMed
38.Gloyn, AL, McCarthy, MI. The genetics of type 2 diabetes. Best Pract Res Clin Endocrinol Metab. 2001; 15, 293308.CrossRefGoogle ScholarPubMed
39.Rich, SS. Mapping genes in diabetes. Genetic epidemiological perspective. Diabetes. 1990; 39, 13151319.CrossRefGoogle ScholarPubMed
40.Stumvoll, M, Goldstein, BJ, van Haeften, TW. Type 2 diabetes: principles of pathogenesis and therapy. Lancet. 2005; 365, 13331346.CrossRefGoogle ScholarPubMed
41.Altshuler, D, Hirschhorn, JN, Klannemark, M, et al. The common PPARgamma Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes. Nat Genet. 2000; 26, 7680.CrossRefGoogle ScholarPubMed
42.Gloyn, AL, Weedon, MN, Owen, KR, et al. Large-scale association studies of variants in genes encoding the pancreatic beta-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) confirm that the KCNJ11 E23K variant is associated with type 2 diabetes. Diabetes. 2003; 52, 568572.CrossRefGoogle ScholarPubMed
43.Grant, SF, Thorleifsson, G, Reynisdottir, I, et al. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet. 2006; 38, 320323.CrossRefGoogle ScholarPubMed
44.Sandhu, MS, Weedon, MN, Fawcett, KA, et al. Common variants in WFS1 confer risk of type 2 diabetes. Nat Genet. 2007; 39, 951953.CrossRefGoogle ScholarPubMed
45.Winckler, W, Weedon, MN, Graham, RR, et al. Evaluation of common variants in the six known maturity-onset diabetes of the young (MODY) genes for association with type 2 diabetes. Diabetes. 2007; 56, 685693.CrossRefGoogle ScholarPubMed
46.Gudmundsson, J, Sulem, P, Steinthorsdottir, V, et al. Two variants on chromosome 17 confer prostate cancer risk, and the one in TCF2 protects against type 2 diabetes. Nat Genet. 2007; 39, 977983.CrossRefGoogle ScholarPubMed
47.Prokopenko, I, Langenberg, C, Florez, JC, et al. Variants in MTNR1B influence fasting glucose levels. Nat Genet. 2009; 41, 7781.CrossRefGoogle ScholarPubMed
48.Sladek, R, Rocheleau, G, Rung, J, et al. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature. 2007; 445, 881885.CrossRefGoogle ScholarPubMed
49.Zeggini, E, Weedon, MN, Lindgren, CM, et al. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science. 2007; 316, 13361341.CrossRefGoogle ScholarPubMed
50.Saxena, R, Voight, BF, Lyssenko, V, et al. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science. 2007; 316, 13311336.CrossRefGoogle ScholarPubMed
51.Scott, LJ, Mohlke, KL, Bonnycastle, LL, et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science. 2007; 316, 13411345.CrossRefGoogle ScholarPubMed
52.Steinthorsdottir, V, Thorleifsson, G, Reynisdottir, I, et al. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat Genet. 2007; 39, 770775.CrossRefGoogle ScholarPubMed
53.Frayling, TM, Timpson, NJ, Weedon, MN, et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science. 2007; 316, 889894.CrossRefGoogle ScholarPubMed
54.Zeggini, E, Scott, LJ, Saxena, R, et al. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet. 2008; 40, 638645.CrossRefGoogle ScholarPubMed
55.Yasuda, K, Miyake, K, Horikawa, Y, et al. Variants in KCNQ1 are associated with susceptibility to type 2 diabetes mellitus. Nat Genet. 2008; 40, 10921097.CrossRefGoogle ScholarPubMed
56.Unoki, H, Takahashi, A, Kawaguchi, T, et al. SNPs in KCNQ1 are associated with susceptibility to type 2 diabetes in East Asian and European populations. Nat Genet. 2008; 40, 10981102.CrossRefGoogle ScholarPubMed
57.Lyssenko, V, Nagorny, CL, Erdos, MR, et al. Common variant in MTNR1B associated with increased risk of type 2 diabetes and impaired early insulin secretion. Nat Genet. 2009; 41, 8288.CrossRefGoogle ScholarPubMed
58.Bouatia-Naji, N, Bonnefond, A, Cavalcanti-Proenca, C, et al. A variant near MTNR1B is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat Genet. 2009; 41, 8994.CrossRefGoogle ScholarPubMed
59.Rung, J, Cauchi, S, Albrechtsen, A, et al. Genetic variant near IRS1 is associated with type 2 diabetes, insulin resistance and hyperinsulinemia. Nat Genet. 2009; 41, 11101115.CrossRefGoogle ScholarPubMed
60.Prokopenko, I, McCarthy, MI, Lindgren, CM. Type 2 diabetes: new genes, new understanding. Trends Genet. 2008; 24, 613621.CrossRefGoogle ScholarPubMed
61.Weedon, MN, McCarthy, MI, Hitman, G, et al. Combining information from common type 2 diabetes risk polymorphisms improves disease prediction. PLoS Med. 2006; 3, e374.CrossRefGoogle ScholarPubMed
62.Lango, H, Palmer, CN, Morris, AD, et al. Assessing the combined impact of 18 common genetic variants of modest effect sizes on type 2 diabetes risk. Diabetes. 2008; 57, 31293135.CrossRefGoogle ScholarPubMed
63.Lyssenko, V, Jonsson, A, Almgren, P, et al. Clinical risk factors, DNA variants, and the development of type 2 diabetes. N Engl J Med. 2008; 359, 22202232.CrossRefGoogle ScholarPubMed
64.van Hoek, M, Dehghan, A, Witteman, JC, et al. Predicting type 2 diabetes based on polymorphisms from genome-wide association studies: a population-based study. Diabetes. 2008; 57, 31223128.CrossRefGoogle ScholarPubMed
65.Meigs, JB, Shrader, P, Sullivan, LM, et al. Genotype score in addition to common risk factors for prediction of type 2 diabetes. N Engl J Med. 2008; 359, 22082219.CrossRefGoogle ScholarPubMed
66.Lin, X, Song, K, Lim, N, et al. Risk prediction of prevalent diabetes in a Swiss population using a weighted genetic score – the CoLaus Study. Diabetologia. 2009; 52, 600608.CrossRefGoogle Scholar
67.Frayling, TM, Hattersley, AT. The role of genetic susceptibility in the association of low birth weight with type 2 diabetes. Br Med Bull. 2001; 60, 89101.CrossRefGoogle ScholarPubMed
68.Froguel, P, Zouali, H, Vionnet, N, et al. Familial hyperglycemia due to mutations in glucokinase. Definition of a subtype of diabetes mellitus. N Engl J Med. 1993; 328, 697702.CrossRefGoogle ScholarPubMed
69.Hattersley, AT, Beards, F, Ballantyne, E, et al. Mutations in the glucokinase gene of the fetus result in reduced birth weight. Nat Genet. 1998; 19, 268270.CrossRefGoogle ScholarPubMed
70.Edghill, EL, Bingham, C, Slingerland, AS, et al. Hepatocyte nuclear factor-1 beta mutations cause neonatal diabetes and intrauterine growth retardation: support for a critical role of HNF-1beta in human pancreatic development. Diabet Med. 2006; 23, 13011306.CrossRefGoogle ScholarPubMed
71.Slingerland, AS, Hattersley, AT. Activating mutations in the gene encoding Kir6.2 alter fetal and postnatal growth and also cause neonatal diabetes. J Clin Endocrinol Metab. 2006; 91, 27822788.CrossRefGoogle ScholarPubMed
72.Stoy, J, Edghill, EL, Flanagan, SE, et al. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A. 2007; 104, 1504015044.CrossRefGoogle ScholarPubMed
73.Babenko, AP, Polak, M, Cave, H, et al. Activating mutations in the ABCC8 gene in neonatal diabetes mellitus. N Engl J Med. 2006; 355, 456466.CrossRefGoogle ScholarPubMed
74.Pearson, ER, Boj, SF, Steele, AM, et al. Macrosomia and hyperinsulinaemic hypoglycaemia in patients with heterozygous mutations in the HNF4A gene. PLoS Med. 2007; 4, e118.CrossRefGoogle ScholarPubMed
75.Aparicio, L, Carpenter, MW, Schwartz, R, Gruppuso, PA. Prenatal diagnosis of familial neonatal hyperinsulinemia. Acta Paediatr. 1993; 82, 683686.CrossRefGoogle ScholarPubMed
76.McCarthy, MI, Hattersley, AT. Learning from molecular genetics: novel insights arising from the definition of genes for monogenic and type 2 diabetes. Diabetes. 2008; 57, 28892898.CrossRefGoogle ScholarPubMed
77.Lindsay, RS, Dabelea, D, Roumain, J, et al. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes. 2000; 49, 445449.CrossRefGoogle ScholarPubMed
78.Davey Smith, G, Sterne, JA, Tynelius, P, Rasmussen, F. Birth characteristics of offspring and parental diabetes: evidence for the fetal insulin hypothesis. J Epidemiol Community Health. 2004; 58, 126128.CrossRefGoogle ScholarPubMed
79.Hypponen, E, Smith, GD, Power, C. Parental diabetes and birth weight of offspring: intergenerational cohort study. BMJ. 2003; 326, 1920.CrossRefGoogle ScholarPubMed
80.Wannamethee, SG, Lawlor, DA, Whincup, PH, et al. Birthweight of offspring and paternal insulin resistance and paternal diabetes in late adulthood: cross sectional survey. Diabetologia. 2004; 47, 1218.CrossRefGoogle ScholarPubMed
81.Knight, B, Shields, BM, Hill, A, et al. Offspring birthweight is not associated with paternal insulin resistance. Diabetologia. 2006; 49, 26752678.CrossRefGoogle Scholar
82.Yajnik, CS, Coyaji, KJ, Joglekar, CV, Kellingray, S, Fall, C. Paternal insulin resistance and fetal growth: problem for the ‘fetal insulin’ and the ‘fetal origins’ hypotheses. Diabetologia. 2001; 44, 11971198.Google ScholarPubMed
83.Shields, BM, Knight, B, Turner, M, et al. Paternal insulin resistance and its association with umbilical cord insulin concentrations. Diabetologia. 2006; 49, 26682674.CrossRefGoogle ScholarPubMed
84.Shields, BM, Knight, B, Hopper, H, et al. Measurement of cord insulin and insulin-related peptides suggests that girls are more insulin resistant than boys at birth. Diabetes Care. 2007; 30, 26612666.CrossRefGoogle ScholarPubMed
85.Weedon, MN, Frayling, TM, Shields, B, et al. Genetic regulation of birth weight and fasting glucose by a common polymorphism in the islet cell promoter of the glucokinase gene. Diabetes. 2005; 54, 576581.CrossRefGoogle ScholarPubMed
86.Weedon, MN, Clark, VJ, Qian, Y, et al. A common haplotype of the glucokinase gene alters fasting glucose and birth weight: association in six studies and population-genetics analyses. Am J Hum Genet. 2006; 79, 9911001.CrossRefGoogle ScholarPubMed
87.Groves, CJ, Zeggini, E, Minton, J, et al. Association analysis of 6,736 UK subjects provides replication and confirms TCF7L2 as a type 2 diabetes susceptibility gene with a substantial effect on individual risk. Diabetes. 2006; 55, 26402644.CrossRefGoogle ScholarPubMed
88.Damcott, CM, Pollin, TI, Reinhart, LJ, et al. Polymorphisms in the transcription factor 7-like 2 (TCF7L2) gene are associated with type 2 diabetes in the Amish: replication and evidence for a role in both insulin secretion and insulin resistance. Diabetes. 2006; 55, 26542659.CrossRefGoogle ScholarPubMed
89.Scott, LJ, Bonnycastle, LL, Willer, CJ, et al. Association of transcription factor 7-like 2 (TCF7L2) variants with type 2 diabetes in a Finnish sample. Diabetes. 2006; 55, 26492653.CrossRefGoogle Scholar
90.Cauchi, S, Meyre, D, Dina, C, et al. Transcription factor TCF7L2 genetic study in the French population: expression in human beta-cells and adipose tissue and strong association with type 2 diabetes. Diabetes. 2006; 55, 29032908.CrossRefGoogle ScholarPubMed
91.Florez, JC, Jablonski, KA, Bayley, N, et al. TCF7L2 polymorphisms and progression to diabetes in the Diabetes Prevention Program. N Engl J Med. 2006; 355, 241250.CrossRefGoogle ScholarPubMed
92.Zhang, C, Qi, L, Hunter, DJ, et al. Variant of transcription factor 7-like 2 (TCF7L2) gene and the risk of type 2 diabetes in large cohorts of US women and men. Diabetes. 2006; 55, 26452648.CrossRefGoogle ScholarPubMed
93.van Vliet-Ostaptchouk, JV, Shiri-Sverdlov, R, Zhernakova, A, et al. Association of variants of transcription factor 7-like 2 (TCF7L2) with susceptibility to type 2 diabetes in the Dutch Breda cohort. Diabetologia. 2007; 50, 5962.CrossRefGoogle ScholarPubMed
94.Chandak, GR, Janipalli, CS, Bhaskar, S, et al. Common variants in the TCF7L2 gene are strongly associated with type 2 diabetes mellitus in the Indian population. Diabetologia. 2007; 50, 6367.CrossRefGoogle ScholarPubMed
95.Saxena, R, Gianniny, L, Burtt, NP, et al. Common single nucleotide polymorphisms in TCF7L2 are reproducibly associated with type 2 diabetes and reduce the insulin response to glucose in nondiabetic individuals. Diabetes. 2006; 55, 28902895.CrossRefGoogle ScholarPubMed
96.Munoz, J, Lok, KH, Gower, BA, et al. Polymorphism in the transcription factor 7-like 2 (TCF7L2) gene is associated with reduced insulin secretion in nondiabetic women. Diabetes. 2006; 55, 36303634.CrossRefGoogle ScholarPubMed
97.Freathy, RM, Weedon, MN, Bennett, A, et al. Type 2 diabetes TCF7L2 risk genotypes alter birth weight: a study of 24,053 individuals. Am J Hum Genet. 2007; 80, 11501161.CrossRefGoogle Scholar
98.Freathy, RM, Bennett, AJ, Ring, SM, et al. Type 2 diabetes risk alleles are associated with reduced size at birth. Diabetes. 2009; 58, 14281433.CrossRefGoogle ScholarPubMed
99.Zhao, J, Li, M, Bradfield, JP, et al. Examination of type 2 diabetes loci implicates CDKAL1 as a birth weight gene. Diabetes. 2009; 58, 24142418.CrossRefGoogle ScholarPubMed
100.Pulizzi, N, Lysseako, V, Jonsson, A, et al. Interaction between prenatal growth and high-risk genotypes in the development of type 2 diabetes. Diabetologia. 2009; 52, 825829.CrossRefGoogle ScholarPubMed
101.Bernstein, IM, Mongeon, JA, Badger, GJ, et al. Maternal smoking and its association with birth weight. Obstet Gynecol. 2005; 106, 986991.CrossRefGoogle ScholarPubMed
102.Bennett, AJ, Sovio, U, Ruokonen, A, et al. No evidence that established type 2 diabetes susceptibility variants in the PPARG and KCNJ11 genes have pleiotropic effects on early growth. Diabetologia. 2008; 51, 8285.CrossRefGoogle ScholarPubMed
103.Byrne, MM, Sturis, J, Clement, K, et al. Insulin secretory abnormalities in subjects with hyperglycemia due to glucokinase mutations. J Clin Invest. 1994; 93, 11201130.CrossRefGoogle ScholarPubMed
104.Pascoe, L, Tura, A, Patel, SK, et al. Common variants of the novel type 2 diabetes genes CDKAL1 and HHEX/IDE are associated with decreased pancreatic beta-cell function. Diabetes. 2007; 56, 31013104.CrossRefGoogle ScholarPubMed
105.Grarup, N, Rose, CS, Andersson, EA, et al. Studies of association of variants near the HHEX, CDKN2A/B, and IGF2BP2 genes with type 2 diabetes and impaired insulin release in 10,705 Danish subjects: validation and extension of genome-wide association studies. Diabetes. 2007; 56, 31053111.CrossRefGoogle Scholar
106.Palmer, ND, Goodarzi, MO, Langefeld, CD, et al. Quantitative trait analysis of type 2 diabetes susceptibility loci identified from whole genome association studies in the Insulin Resistance Atherosclerosis Family Study. Diabetes. 2008; 57, 10931100.CrossRefGoogle ScholarPubMed
107.Stoffers, DA, Zinkin, NT, Stanojevic, V, Clarke, WL, Habener, JF. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet. 1997; 15, 106110.CrossRefGoogle ScholarPubMed
108.Wright, NM, Metzger, DL, Borowitz, SM, Clarke, WL. Permanent neonatal diabetes mellitus and pancreatic exocrine insufficiency resulting from congenital pancreatic agenesis. Am J Dis Child. 1993; 147, 607609.Google ScholarPubMed
109.Temple, IK, Gardner, RJ, Robinson, DO, et al. Further evidence for an imprinted gene for neonatal diabetes localised to chromosome 6q22-q23. Hum Mol Genet. 1996; 5, 11171121.CrossRefGoogle ScholarPubMed
110.Temple, IK, James, RS, Crolla, JA, et al. An imprinted gene(s) for diabetes? Nat Genet. 1995; 9, 110112.CrossRefGoogle ScholarPubMed
111.Flanagan, SE, Patch, AM, Mackay, DJ, et al. Mutations in ATP-sensitive K+ channel genes cause transient neonatal diabetes and permanent diabetes in childhood or adulthood. Diabetes. 2007; 56, 19301937.CrossRefGoogle ScholarPubMed
112.Gloyn, AL, Pearson, ER, Antcliff, JF, et al. Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J Med. 2004; 350, 18381849.CrossRefGoogle ScholarPubMed
113.Horikawa, Y, Iwasaki, N, Hara, M, et al. Mutation in hepatocyte nuclear factor-1 beta gene (TCF2) associated with MODY. Nat Genet. 1997; 17, 384385.CrossRefGoogle ScholarPubMed
114.Yamagata, K, Furuta, H, Oda, N, et al. Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature. 1996; 384, 458460.CrossRefGoogle ScholarPubMed
115.Thomas, P, Ye, Y, Lightner, E. Mutation of the pancreatic islet inward rectifier Kir6.2 also leads to familial persistent hyperinsulinemic hypoglycemia of infancy. Hum Mol Genet. 1996; 5, 18091812.CrossRefGoogle ScholarPubMed
116.Thomas, PM, Cote, GJ, Wohllk, N, et al. Mutations in the sulfonylurea receptor gene in familial persistent hyperinsulinemic hypoglycemia of infancy. Science. 1995; 268, 426429.CrossRefGoogle ScholarPubMed
117.Elsas, LJ, Endo, F, Strumlauf, E, Elders, J, Priest, JH. Leprechaunism: an inherited defect in a high-affinity insulin receptor. Am J Hum Genet. 1985; 37, 7388.Google Scholar
118.Donohue, WL, Uchida, I. Leprechaunism: a euphemism for a rare familial disorder. J Pediatr. 1954; 45, 505519.CrossRefGoogle ScholarPubMed