Impact on offspring methylation patterns of maternal gestational diabetes mellitus and intrauterine growth restraint suggest common genes and pathways linked to subsequent type 2 diabetes risk

FASEB Journal

Volumn 28, Issue 11, 2014, Pages 4868-4879

  Quilter, Claire R ^a   Cooper, Wendy N ^a,b,c   Cliffe, Kerry M ^a   Skinner, Benjamin M ^a   Prentice, Philippa M ^b,c   Nelson, Latasha ^d   Bauer, Julien ^a   Ong, Ken K ^b,c   Constância, Miguel ^a,b,c   Lowe, William L ^d   Affara, Nabeel A ^a   Dunger, David B ^b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Epigenetics; Fetal programming; Maternal environment

Indexed keywords

ADULT; ARTICLE; CATCH UP GROWTH; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DIET SUPPLEMENTATION; DNA METHYLATION; DNA MODIFICATION; ENVIRONMENTAL EXPOSURE; FEMALE; GAMBIAN; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HIGH BIRTH WEIGHT; HUMAN; INFANT; LONG TERM CARE; MALE; MATERNAL DEPRIVATION; MATERNAL DIABETES MELLITUS; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; POSTNATAL GROWTH; PREGNANCY OUTCOME; PRENATAL EXPOSURE; PRENATAL GROWTH; PROGENY; REPLICATION STUDY; RISK FACTOR; SIGNAL TRANSDUCTION; UMBILICAL CORD BLOOD; BIRTH WEIGHT; DIABETES MELLITUS, TYPE 2; DIABETES, GESTATIONAL; FETUS DEVELOPMENT; GENETICS; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; METABOLISM; PHYSIOLOGY; PREGNANCY; RISK; WEIGHT GAIN; YOUNG ADULT;

GLUCOSE BLOOD LEVEL;

ADULT; BIRTH WEIGHT; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DIABETES, GESTATIONAL; DNA METHYLATION; FEMALE; FETAL DEVELOPMENT; HUMANS; HYPERGLYCEMIA; MALE; PREGNANCY; RISK; WEIGHT GAIN; YOUNG ADULT;

EID: 84912060350     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-255240     Document Type: Article

References (53)

1. Sobngwi, E., Boudou, P., Mauvais-Jarvis, F., Leblanc, H., Velho, G., Vexiau, P., Porcher, R., Hadjadj, S., Pratley, R., Tataranni, P. A., Calvo, F., and Gautier, J. F. (2003) Effect of a diabetic environment in utero on predisposition to type 2 diabetes. Lancet 361, 1861-1865
2. Seghieri, G., Anichini, R., De Bellis, A., Alviggi, L., Franconi, F., and Breschi, M. C. (2002) Relationship between gestational diabetes mellitus and low maternal birth weight. Diabetes Care 25, 1761-1765
3. McLean, M., Chipps, D., and Cheung, N. W. (2006) Mother to child transmission of diabetes mellitus: does gestational diabetes program type 2 diabetes in the next generation? Diabet. Med. 23, 1213-1215
4. Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., and Winter, P. D. (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303, 1019-1022
5. Ong, K. K., Ahmed, M. L., Emmett, P. M., Preece, M. A., and Dunger, D. B. (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 320, 967-971
6. Ibanez, L., Ong, K., Dunger, D. B., and de Zegher, F. (2006) Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J. Clin. Endocrinol. Metab. 91, 2153-2158
7. Ong, K. K., Petry, C. J., Emmett, P. M., Sandhu, M. S., Kiess, W., Hales, C. N., Ness, A. R., and Dunger, D. B. (2004) Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth, and plasma insulin-like growth factor- I levels. Diabetologia 47, 1064-1070
8. Gluckman, P. D., Hanson, M. A., and Low, F. M. (2011) The role of developmental plasticity and epigenetics in human health. Birth Defects Res. C Embryo Today 93, 12-18
9. Lillycrop, K. A., and Burdge, G. C. (2012) Epigenetic mechanisms linking early nutrition to long term health. Best Pract. Res. Clin. Endocrinol. Metab. 26, 667-676
10. Kanaka-Gantenbein, C. (2010) Fetal origins of adult diabetes. Ann. N.Y. Acad. Sci. 1205, 99-105
11. Gluckman, P. D., Hanson, M. A., Spencer, H. G., and Bateson, P. (2005b) Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc. Biol. Sci. 272, 671-677
12. Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E., and Lumey, L. H. (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. U. S. A. 105, 17046-17049
13. Van Abeelen, A. F., Elias, S. G., Bossuyt, P. M., Grobbee, D. E., van der Schouw, Y. T., Roseboom, T. J., and Uiterwaal, C. S. (2012) Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes 61, 2255-2260
14. Khulan, B., Cooper, W. N., Skinner, B. M., Bauer, J., Owens, S., Prentice, A. M., Belteki, G., Constancia, M., Dunger, D., and Affara, N. A. (2012) Periconceptional maternal micronutrient supplementation is associated with widespread gender related changes in the epigenome: a study of a unique resource in the Gambia. Hum. Mol. Genet. 21, 2086-2101
15. Cooper, W. N., Khulan, B., Owens, S., Elks, C. E., Seidel, V., Prentice, A. M., Belteki, G., Ong, K. K., Affara, N. A., Constância, M., and Dunger, D. B. (2012) DNA methylation profiling at imprinted loci after periconceptional micronutrient supplementation in humans: results of a pilot randomized controlled trial. FASEB J. 26, 1782-1790
16. HAPO Study Cooperative Research Group. (2002) The Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study. Int. J. Gynaecol. Obstet. 78, 69-77
17. Metzger, B. E., Lowe, L. P., Dyer, A. R., Trimble, E. R., Chaovarindr, U., Coustan, D. R., Hadden, D. R., McCance, D. R., Hod, M., McIntyre, H. D., Oats, J. J., Persson, B., Rogers, M. S., and Sacks, D. A. (2008) HAPO Study Cooperative Research Group, Hyperglycemia and adverse pregnancy outcomes. N. Engl. J. Med. 358, 1991-2002
18. Ong, K. K., Langkamp, M., Ranke, M. B., Whitehead, K., Hughes, I. A., Acerini, C. L., and Dunger, D. B. (2009) Insulinlike growth factor I concentrations in infancy predict differential gains in body length and adiposity: the Cambridge Baby Growth Study. Am. J. Clin. Nutr. 90, 156-161
19. Ong, K. K., Diderholm, B., Salzano, G., Wingate, D., Hughes, I. A., MacDougall, J., Acerini, C. L., and Dunger, D. B. (2008) Pregnancy insulin, glucose, and BMI contribute to birth outcomes in nondiabetic mothers. Diabetes Care 31, 2193-2197
20. Freeman, J. V., Cole, T. J., Chinn, S., Jones, P. R., White, E. M., and Preece, M. A. (1995) Cross sectional stature and weight reference curves for the UK, 1990. Arch. Dis. Child. 73, 17-24
21. Pan, H., and Cole, T. (2012) LMSgrowth, a Microsoft Excel add-in to access growth references based on the LMS method. Version 2.77. http://www.healthforallchildren.co.uk/
22. Chen, Y. A., Choufani, S., Ferreira, J. C., Grafodatskaya, D., Butcher, D. T., and Weksberg, R. (2011) Sequence overlap between autosomal and sex-linked probes on the Illumina HumanMethylation27 microarray. Genomics 97, 214-222
23. Heneghan, C., Thompson, M., Billingsley, M., and Cohen, D. (2011) Medical-device recalls in the UK and the device-regulation process: retrospective review of safety notices and alerts. BMJ Open 1, e000155. Excerpted data posted at Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.585t4
24. Aouizerat, B. E., Vittinghoff, E., Musone, S. L., Pawlikowska, L., Kwok, P. Y., Olgin, J. E., and Tseng, Z. H. (2011) GWAS for discovery and replication of genetic loci associated with sudden cardiac arrest in patients with coronary artery disease. BMC Cardiovasc. Disord. 11, 29
25. National Heart, Lung, and Blood Institute (2011, June 21) NHLBI Family Heart Study (FamHS-Visit1 and FamHS-Visit2). dbGaP Study Accession: phs000221. http://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/study.cgi?study-idphs000221.v1.p1/
26. Newton-Cheh, C., Guo, C. Y., Wang, T. J., O'Donnell, C. J., Levy, D., and Larson, M. G. (2007) Genome-wide association study of electrocardiographic and heart rate variability traits: the Framingham Heart Study. BMC Med. Genet. 8(Suppl. 11) S7
27. Lango Allen, H., Estrada, K., Lettre, G., Berndt, S. I., Weedon, M. N., Rivadeneira, F., Willer, C. J., Jackson, A. U., Vedantam, S., Raychaudhuri, S., Ferreira, T., Wood, A. R., Weyant, R. J., Segrè, A. V., Speliotes, E. K., Wheeler, E., Soranzo, N., Park, J. H., Yang, J., Gudbjartsson, D., Heard-Costa, N. L., Randall, J. C., Qi, L., Vernon Smith, A., Mägi, R., Pastinen, T., Liang, L., Heid, I. M., Luan, J., Thorleifsson, G., Winkler, T. W., Goddard, M. E., Sin Lo, K., Palmer, C., Workalemahu, T., Aulchenko, Y. S., Johansson, A., Zillikens, M. C., Feitosa, M. F., Esko, T., Johnson, T., Ketkar, S., Kraft, P., Mangino, M., Prokopenko, I., Absher, D., Albrecht, E., Ernst, F., Glazer, N. L., Hayward, C., Hottenga, J. J., Jacobs, K. B., Knowles, J. W., Kutalik, Z., Monda, K. L., Polasek, O., Preuss, M., Rayner, N. W., Robertson, N. R., Steinthorsdottir, V., Tyrer, J. P., Voight, B. F., Wiklund, F., Xu, J., Zhao, J. H., Nyholt, D. R., Pellikka, N., Perola, M., Perry, J. R., Surakka, I., Tammesoo, M. L., Altmaier, E. L., Amin, N., Aspelund, T., Bhangale, T., Boucher, G., Chasman, D. I., Chen, C., Coin, L., Cooper, M. N., Dixon, A. L., Gibson, Q., Grundberg, E., Hao, K., Juhani Junttila, M., Kaplan, L. M., Kettunen, J., König, I. R., Kwan, T., Lawrence, R. W., Levinson, D. F., Lorentzon, M., McKnight, B., Morris, A. P., Müller, M., Suh Ngwa, J., Purcell, S., Rafelt, S., Salem, R. M., Salvi, E., Sann, S., Shi, J., Sovio, U., Thompson, J. R., Turchin, M. C., Vandenput, L., Verlaan, D. J., Vitart, V., White, C. C., Ziegler, A., Almgren, P., Balmforth, A. J., Campbell, H., Citterio, L., De Grandi, A., Dominiczak, A., Duan, J., Elliott, P., Elosua, R., Eriksson, JG., Freimer, N. B., Geus, E. J., Glorioso, N., Haiqing, S., Hartikainen, A. L., Havulinna, A. S., Hicks, A. A., Hui, J., Igl, W., Illig, T., Jula, A., Kajantie, E., Kilpeläinen, T. O., Koiranen, M., Kolcic, I., Koskinen, S., Kovacs, P., Laitinen, J., Liu, J., Lokki, M. L., Marusic, A., Maschio, A., Meitinger, T., Mulas, A., Paré, G., Parker, A. N., Peden, J. F., Petersmann, A., Pichler, I., Pietiläinen, K. H., Pouta, A., Ridderstrale, M., Rotter, J. I., Sambrook, J. G., Sanders, A. R., Schmidt, C. O., Sinisalo, J., Smit, J. H., Stringham, H. M., Bragi Walters, G., Widen, E., Wild, S. H., Willemsen, G., Zagato, L., Zgaga, L., Zitting, P., Alavere, H., Farrall, M., McArdle, W. L., Nelis, M., Peters, M. J., Ripatti, S., van Meurs, J. B., Aben, K. K., Ardlie, K. G., Beckmann, J. S., Beilby, J. P., Bergman, R. N., Bergmann, S., Collins, F. S., Cusi, D., den Heijer, M., Eiriksdottir, G., Gejman, P. V., Hall, A. S., Hamsten, A., Huikuri, H. V., Iribarren, C., Kähönen, M., Kaprio, J., Kathiresan, S., Kiemeney, L., Kocher, T., Launer, L. J., Lehtimäki, T., Melander, O., Mosley, T. H., Jr., Musk, A. W., Nieminen, M. S., O'Donnell, C. J., Ohlsson, C., Oostra, B., Palmer, L. J., Raitakari, O., Ridker, P. M., Rioux, J. D., Rissanen, A., Rivolta, C., Schunkert, H., Shuldiner, A. R., Siscovick, D. S., Stumvoll, M., Tönjes, A., Tuomilehto, J., van Ommen, G. J., Viikari, J., Heath, A. C., Martin, N. G., Montgomery, G. W., Province, M. A., Kayser, M., Arnold, A. M., Atwood, L. D., Boerwinkle, E., Chanock, S. J., Deloukas, P., Gieger, C., Grönberg, H., Hall, P., Hattersley, A. T., Hengstenberg, C., Hoffman W., Lathrop, G. M., Salomaa, V., Schreiber, S., Uda, M., Waterworth, D., Wright, A. F., Assimes, T. L., Barroso, I., Hofman, A., Mohlke, K. L., Boomsma, D. I., Caulfield, M. J., Cupples, L. A., Erdmann, J., Fox, C. S., Gudnason, V., Gyllensten, U., Harris, T. B., Hayes, R. B., Jarvelin, M. R., Mooser, V., Munroe, P. B., Ouwehand, W. H., Penninx, B. W., Pramstaller, P. P., Quertermous, T., Rudan, I., Samani, N. J., Spector, T. D., Völzke, H., Watkins, H., Wilson, J. F., Groop, L. C., Haritunians, T., Hu, F. B., Kaplan, R. C., Metspalu, A., North, K. E., Schlessinger, D., Wareham, N. J., Hunter, D. J., O'Connell, J. R., Strachan, D. P., Wichmann, H. E., Borecki, I. B., van Duijn, C. M., Schadt, E. E., Thorsteinsdottir, U., Peltonen, L., Uitterlinden, A. G., Visscher, P. M., Chatterjee, N., Loos, R. J., Boehnke, M., McCarthy, M. I., Ingelsson, E., Lindgren, C. M., Abecasis, G. R., Stefansson, K., Frayling, T. M., and Hirschhorn, J. N. (2010) Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467, 832-838
28. Ng, M. C., Lam, V. K., Tam, C. H., Chan, A. W., So, W. Y., Ma, R. C., Zee, B. C., Waye, M. M., Mak, W. W., Hu, C., Wang, C. R., Tong, P. C., Jia, W. P., and Chan, J. C. International Type 2 Diabetes 1q Consortium. Association of the POU class 2 homeobox 1 gene (POU2F1) with susceptibility to type 2 diabetes in Chinese populations. Diabet. Med. 27, 1443-1449
29. Amine, K., Atouk, A., Moussamih, S., Saile, R., Mikou, A., and Kettani, A. (2011) Paraoxonase-1 (PON1) activity in patients with coronary artery diseases and in diabetic patients (in French). Ann. Biol. Clin. (Paris) 69, 671-677
30. Ergun, M. A., Yurtcu, E., Demirci, H., Ilhan, M. N., Barkar, V., Yetkin, I., and Menevse, A. (2011) PON1 55 and 192 gene polymorphisms in type 2 diabetes mellitus patients in a Turkish population. Biochem. Genet. 49, 1-8
31. Xie, J., Zhu, H., Larade, K., Ladoux, A., Seguritan, A., Chu, M., Ito, S., Bronson, R. T., Leiter, E. H., Zhang, C. Y., Rosen, E. D., and Bunn, H. F. (2004) Absence of a reductase, NCB5OR, causes insulin-deficient diabetes. Proc. Natl. Acad. Sci. U. S. A. 101, 10750-10755
32. Finkenstedt, A., Wolf, E., Höfner, E., Gasser, B. I., Bösch, S., Bakry, R., Creus, M., Kremser, C., Schocke, M., Theurl, M., Moser, P., Schranz, M., Bonn, G., Poewe, W., Vogel, W., Janecke, A. R., and Zoller, H. (2010) Hepatic but not brain iron is rapidly chelated by deferasirox in aceruloplasminemia due to a novel gene mutation. J. Hepatol. 53, 1101-1107
33. Proshchina, A. E., Savelyev, S. V., Barabanov, V. M., and Krivova, Y. S. (2010) Immunoreactivity of neuron-specific enolase (NSE) in human pancreas in health and type 1 diabetes mellitus. Bull. Exp. Biol. Med. 149, 763-767
34. Ichimura, A., Hirasawa, A., Hara, T., and Tsujimoto, G. (2009) Free fatty acid receptors act as nutrient sensors to regulate energy homeostasis. Prostaglandins Other Lipid Mediat. 89, 82-88
35. Heard-Costa, N. L., Zillikens, M. C., Monda, K. L., Johansson, A., Harris, T. B., Fu, M., Haritunians, T., Feitosa, M. F., Aspelund, T., Eiriksdottir, G., Garcia, M., Launer, L. J., Smith, A. V., Mitchell, B. D., McArdle, P. F., Shuldiner, A. R., Bielinski, S. J., Boerwinkle, E., Brancati, F., Demerath, E. W., Pankow, J. S., Arnold, A. M., Chen, Y. D., Glazer, N. L., McKnight, B., Psaty, B. M., Rotter, J. I., Amin, N., Campbell, H., Gyllensten, U., Pattaro, C., Pramstaller, P. P., Rudan, I., Struchalin, M., Vitart, V., Gao, X., Kraja, A., Province, M. A., Zhang, Q., Atwood, L. D., Dupuis, J., Hirschhorn, J. N., Jaquish, C. E., O'Donnell, C. J., Vasan, R. S., White, C. C., Aulchenko, Y. S., Estrada, K., Hofman, A., Rivadeneira, F., Uitterlinden, A. G., Witteman, J. C., Oostra, B. A., Kaplan, R. C., Gudnason, V., O'Connell, J. R., Borecki, I. B., van Duijn, C. M., Cupples, LA., Fox, C. S., and North, K. E. (2009) NRXN3 is a novel locus for waist circumference: a genome-wide association study from the CHARGE Consortium. PLoS Genet. 5, e1000539
36. Coyle, C. A., Jing, E., Hosmer, T., Powers, J. B., Wade, G., and Good, D. J. (2002) Reduced voluntary activity preceded adultonset obesity in Nhlh2 knockout mice. Physiol. Behav. 77, 387-402
37. Good, D. J., Coyle, C. A., and Fox, D. L. (2008) Nhlh2: a basic helix-loop-helix transcription factor controlling physical activity (review). Exerc. Sport Sci. Rev. 36, 187-192
38. Hamada, T., Kotani, K., Nagai, N., Tsuzaki, K., Sano, Y., Matsuoka, Y., Fujibayashi, M., Kiyohara, N., Tanaka, S., Yoshimura, M., Egawa, K., Kitagawa, Y., Kiso, Y., Moritani, T., and Sakane, N. (2011) Genetic polymorphisms of the renin-angiotensin system and obesity-related metabolic changes in response to low energy diets in obese women. Nutrition 27, 34-39
39. Murea, M., Lu, L., Ma, L., Hicks, P. J., Divers, J., McDonough, C. W., Langefeld, C. D., Bowden, D. W., and Freedman, B. I. (2011) Genome-wide association scan for survival on dialysis in African-Americans with type 2 diabetes. Am. J. Nephrol. 33, 502-509
40. Yang, H. C., Liang, Y. J., Wu, Y. L., Chung, C. M., Chiang, K. M., Ho, H. Y., Ting, C. T., Lin, T. H., Sheu, S. H., Tsai, W. C., Chen, J. H., Leu, H. B., Yin, W. H., Chiu, T. Y., Chen, C. I., Fann, C. S., Wu, J. Y., Lin, T. N., Lin, S. J., Chen, Y. T., Chen, J. W., and Pan, W. H. (2009) Genome-wide association study of young-onset hypertension in the Han Chinese population of Taiwan. PLoS One 4, e5459
41. Astorri, E., Guglielmi, C., Bombardieri, M., Alessandri, C., Buzzetti, R., Maggi, D., Valesini, G., Pitzalis, C., and Pozzilli, P. (2010) Circulating Reg1α proteins and autoantibodies to Reg1α proteins as biomarkers of β-cell regeneration and damage in type 1 diabetes. Horm. Metab. Res. 2, 955-960
42. Fatima, W., Shahid, A., Imran, M., Manzoor, J., Hasnain, S., Rana, S., and Mahmood, S. (2011) Leptin deficiency and leptin gene mutations in obese children from Pakistan. Int. J. Pediatr. Obes. 6, 419-427
43. Amitani, M., Asakawa, A., Amitani, H., and Inui, A. (2013) The role of leptin in the control of insulin-glucose axis. Front. Neurosci. 7, 51
44. Speliotes, E. K., Willer, C. J., Berndt, S. I., Monda, K. L., Thorleifsson, G., Jackson, A. U., Lango Allen, H., Lindgren, C. M., Luan, J., Mägi, R., Randall, J. C., Vedantam, S., Winkler, T. W., Qi, L., Workalemahu, T., Heid, IM., Steinthorsdottir, V., Stringham, H. M., Weedon, M. N., Wheeler, E., Wood, A. R., Ferreira, T., Weyant, R. J., Segrè, A. V., Estrada, K., Liang, L., Nemesh, J., Park, J. H., Gustafsson, S., Kilpeläinen, T. O., Yang, J., Bouatia-Naji, N., Esko, T., Feitosa, MF., Kutalik, Z., Mangino, M., Raychaudhuri, S., Scherag, A., Smith, AV., Welch, R., Zhao, J. H., Aben, K. K., Absher, D. M., Amin, N., Dixon, A. L., Fisher, E., Glazer, N. L., Goddard, M. E., Heard-Costa, N. L., Hoesel, V., Hottenga, J. J., Johansson, A., Johnson, T., Ketkar, S., Lamina, C., Li, S., Moffatt, M. F., Myers, R. H., Narisu, N., Perry, J. R., Peters, M. J., Preuss, M., Ripatti, S., Rivadeneira, F., Sandholt, C., Scott, L. J., Timpson, N. J., Tyrer, J. P., van Wingerden, S., Watanabe, R. M., White, C. C., Wiklund, F., Barlassina, C., Chasman, D. I., Cooper, M. N., Jansson, J. O., Lawrence, R. W., Pellikka, N., Prokopenko, I., Shi, J., Thiering, E., Alavere, H., Alibrandi, M. T., Almgren, P., Arnold, A. M., Aspelund, T., Atwood, L. D., Balkau, B., Balmforth, A. J., Bennett, A. J., Ben-Shlomo, Y., Bergman, R. N., Bergmann, S., Biebermann, H., Blakemore, A. I., Boes, T., Bonnycastle, L. L., Bornstein, S. R., Brown, M. J., Buchanan, T. A., Busonero, F., Campbell, H., Cappuccio, F. P., Cavalcanti-Proença, C., Chen, Y. D., Chen, C. M., Chines, P. S., Clarke, R., Coin, L., Connell, J., Day, I. N., den Heijer, M., Duan, J., Ebrahim, S., Elliott, P., Elosua, R., et al.(2010) Association analyses of 249, 796 individuals reveal 18 new loci associated with body mass index. Nat. Genet. 42, 937-948
45. Hall, E., Dayeh, T., Kirkpatrick, C. L., Wollheim, C. B., Dekker Nitert, M., and Ling, C. (2013) DNA methylation of the glucagon- like peptide 1 receptor (GLP1R) in human pancreatic islets. BMC Med. Genet. 23, 14:76
46. Bouqbis, L., Akhayat, O., Garchon, H. J., Calafell, F., and Izaabel, H. (2003) TNFA-TNFB haplotypes modify susceptibility to type I diabetes mellitus independently of HLA class II in a Moroccan population. Tissue Antigens 61, 72-79
47. Meloni G., Bottini N., Borgiani P., Lucarelli P., Meloni, T., and Bottini, E. (2003) Association of the ACP1 genotype with metabolic parameters upon initial diagnosis of type 1 diabetes. Med. Sci. Monit. 9, CR105-CR108
48. Mallone, R., and Perin, P. C. (2006) Anti-CD38 autoantibodies in type diabetes (review). Diabetes Metab. Res. Rev. 22, 284-294
49. Murthi, P., Doherty, V. L., Said, J. M., Donath, S., Brennecke, S. P., and Kalionis, B. (2006) Homeobox gene ESX1L expression is decreased in human pre-term idiopathic fetal growth restriction. Mol. Hum. Reprod. 12, 335-340
50. Maiti, A., Noon, M. S., MacKerell, A.D. Jr., Pozharski, E., and Drohat, A. C. (2012) Lesion processing by a repair enzyme is severely curtailed by residues needed to prevent aberrant activity on undamaged DNA. Proc. Natl. Acad. Sci. U. S. A. 109, 8091-8096
51. McMinn, J., Wei, M., Schupf, N., Cusmai, J., Johnson, E. B., Smith, A. C., Weksberg, R., Thaker, H. M., and Tycko, B. (2006) Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 27, 540-549
52. Geneviève, D., Sanlaville, D., Faivre, L., Kottler, M. L., Jambou, M., Gosset, P., Boustani-Samara, D., Pinto, G., Ozilou, C., Abeguilé, G., Munnich, A., Romana, S., Raoul, O., Cormier- Daire, V., and Vekemans, M. (2005) Paternal deletion of the GNAS imprinted locus(including Gnasxl) in 2 girls presenting with severe pre- and post-natal growth retardation and intractable feeding difficulties. Eur. J. Hum. Genet. 13, 1033-1039
53. Metzger, B. E., Gabbe, S. G., Persson, B., Buchanan, T. A., Catalano, P. A., Damm, P., Dyer, A. R., de Leiva, A., Hod, M., Kitzmiler, J. L., Lowe, L. P., McIntyre, H. D., Oats, J. J., Omori, Y., and Schmidt, M. I.; International Association of Diabetes and Pregnancy Study Groups Consensus Panel (2010) International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33, 676-682 (review)