Early-Life Origins of Type 2 Diabetes: Fetal Programming of the Beta-Cell Mass
Open accessAbstract
A substantial body of evidence suggests that an abnormal intrauterine milieu elicited by maternal metabolic disturbances as diverse as undernutrition, placental insufficiency, diabetes or obesity, may program susceptibility in the fetus to later develop chronic degenerative diseases, such as obesity, hypertension, cardiovascular diseases and diabetes. This paper examines the developmental programming of glucose intolerance/diabetes by disturbed intrauterine metabolic condition experimentally obtained in various rodent models of maternal protein restriction, caloric restriction, overnutrition or diabetes, with a focus on the alteration of the developing beta-cell mass. In most of the cases, whatever the type of initial maternal metabolic stress, the beta-cell adaptive growth which normally occurs during gestation, does not take place in the pregnant offspring and this results in the development of gestational diabetes. Therefore gestational diabetes turns to be the ultimate insult targeting the offspring beta-cell mass and propagates diabetes risk to the next generation again. The aetiology and the transmission of spontaneous diabetes as encountered in the GK/Par rat model of type 2 diabetes, are discussed in such a perspective. This review also discusses the non-genomic mechanisms involved in the installation of the programmed effect as well as in its intergenerational transmission.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Individuals who experienced overnutrition in the womb are more likely to have experienced hyperglycemia and β-cell fatigue before birth, predisposing them to hyperglycemia during later metabolic stress such as pregnancy.
“These individuals are more likely to have experienced hyperglycemia and β-cell fatigue even before birth, predisposing them to hyperglycemia during times of later metabolic stress, such as during pregnancy [55].”
From The Pathophysiology of Gestational Diabetes Mellitus (2018) · cites this paper as [55]
Section 4 (page unavailable) links early-life stressors, including maternal overnutrition, to later endocrine pancreatic deficiency and says pregnancy can expose a latent low insulin response in female offspring. It also describes hyperglycemia during fetal and/or early postnatal life. The copy does not establish that overnourished individuals experienced β-cell fatigue before birth; the discussion relies substantially on animal models and does not isolate prenatal exposure for every case. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Wild, S., Roglic, G., Green, A., Sicree, R., & King, H. (2004) · Diabetes Care · doi:10.2337/diacare.27.5.1047 · Cited by 15,297 · see citing works
(2000) · PubMed · Cited by 13,173 · see citing works
Obesity : Preventing and managing the global epidemic
Akram, D. S., Astrup, A. V., Atinmo, T., Boissin, J.-L., Bray, G. A., Carroll, K. N., Chitson, P., Chen, C., Dietz, W. H., Hill, J. O., et al. (2000) · Research at the University of Copenhagen (University of Copenhagen) · Cited by 12,945 · see citing works
β-Cell Deficit and Increased β-Cell Apoptosis in Humans With Type 2 Diabetes
Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., & Butler, P. C. (2003) · Diabetes · doi:10.2337/diabetes.52.1.102 · Cited by 4,011 · see citing works
Persistent epigenetic differences associated with prenatal exposure to famine in humans
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E., & Lumey, L. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806560105 · Cited by 3,082 · see citing works
DeFronzo, R. A. (2009) · Diabetes · doi:10.2337/db09-9028 · Cited by 3,016 · see citing works
Fetal and infant growth and impaired glucose tolerance at age 64
Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., & Winter, P. D. (1991) · BMJ · doi:10.1136/bmj.303.6809.1019 · Cited by 2,708 · see citing works
Barker, D. J. P., Hales, C. N., Fall, C. H. D., Osmond, C., Phipps, K., & Clark, P. M. S. (1993) · Diabetologia · doi:10.1007/bf00399095 · Cited by 2,468 · see citing works
The Developmental Origins of Adult Disease
Barker, D. J. P. (2004) · Journal of the American College of Nutrition · doi:10.1080/07315724.2004.10719428 · Cited by 1,854 · see citing works
Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring
Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., & Morris, M. J. (2010) · Nature · doi:10.1038/nature09491 · Cited by 1,327 · see citing works
Onset of NIDDM occurs at Least 4–7 yr Before Clinical Diagnosis
Harris, M. I., Klein, R., Welborn, T. A., & Knuiman, M. W. (1992) · Diabetes Care · doi:10.2337/diacare.15.7.815 · Cited by 1,306 · see citing works
Dabelea, D., Hanson, R. L., Lindsay, R. S., Pettitt, D. J., Imperatore, G., Gabir, M. M., Roumain, J., Bennett, P. H., & Knowler, W. C. (2000) · Diabetes · doi:10.2337/diabetes.49.12.2208 · Cited by 1,277 · cited 1× · see citing works
“Offspring born after their mother displayed diabetes had a fourfold higher risk of diabetes and a higher body mass index (BMI) than their full siblings born before their mother developed diabetes [8].”
BackgroundLillycrop, K. A., Phillips, E. S., Jackson, A. A., Hanson, M. A., & Burdge, G. C. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1382 · Cited by 1,139 · see citing works
Birth Weight and Risk of Type 2 Diabetes
Whincup, P. H., Kaye, S. J., Owen, C. G., Huxley, R., Cook, D. G., Anazawa, S., Barrett-Connor, E. L., Bhargava, S. K., Birgisdóttir, B. E., Carlsson, S., et al. (2008) · JAMA · doi:10.1001/jama.2008.886 · Cited by 939 · see citing works
Epigenetic Epidemiology of the Developmental Origins Hypothesis
Waterland, R. A., & Michels, K. B. (2007) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.27.061406.093705 · Cited by 883 · see citing works
Prenatal glucocorticoids and long-term programming
Seckl (2004) · European Journal of Endocrinology · doi:10.1530/eje.0.151u049 · Cited by 825 · see citing works
Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., & Fleming, T. P. (2000) · Development · doi:10.1242/dev.127.19.4195 · Cited by 798 · see citing works
Maternal Methyl Supplements in Mice Affect Epigenetic Variation and DNA Methylation of Offspring
Cooney, C. A., Dave, A. A., & Wolff, G. L. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2393s · Cited by 784 · see citing works
Differential Effects of Culture on Imprinted H19 Expression in the Preimplantation Mouse Embryo1
Doherty, A. S., Mann, M. R. W., Tremblay, K. D., Bartolomei, M. S., & Schultz, R. M. (2000) · Biology of Reproduction · doi:10.1095/biolreprod62.6.1526 · Cited by 723 · see citing works
Thinness at birth and insulin resistance in adult life
Phillips, D. I. W., Barker, D. J. P., Hales, C. N., Hirst, S. D., & Osmond, C. (1994) · Diabetologia · doi:10.1007/s001250050086 · Cited by 698 · see citing works
Effect of a Low Protein Diet during Pregnancy on the Fetal Rat Endocrine Pancreas
Snoeck, A., Remacle, C., Reusens, B., & Hoet, J. J. (2009) · Biology of the Neonate · doi:10.1159/000243170 · Cited by 652 · see citing works
Park, J. H., Stoffers, D. A., Nicholls, R. D., & Simmons, R. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33655 · Cited by 640 · see citing works
Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat
Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2279 · Cited by 638 · see citing works
Neonatal Leptin Treatment Reverses Developmental Programming
Vickers, M. H., Gluckman, P. D., Coveny, A. H., Hofman, P. L., Cutfield, W. S., Gertler, A., Breier, B. H., & Harris, M. A. (2005) · Endocrinology · doi:10.1210/en.2005-0581 · Cited by 616 · see citing works
Perinatal risk factors for childhood obesity and metabolic dysregulation
Catalano, P. M., Farrell, K., Thomas, A., Huston-Presley, L., Mencin, P., de Mouzon, S. H., & Amini, S. B. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.27416 · Cited by 553 · see citing works
Small for Gestational Age: Short Stature and Beyond
Saenger, P. H., Czernichow, P., Hughes, I. A., & Reiter, E. O. (2007) · Endocrine Reviews · doi:10.1210/er.2006-0039 · Cited by 531 · see citing works
DNA damage, cellular senescence and organismal ageing: causal or correlative?
Chen, J.-H., Hales, C. N., & Ozanne, S. E. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm681 · Cited by 481 · see citing works
Epigenetic Modification of the Renin-Angiotensin System in the Fetal Programming of Hypertension
Bogdarina, I. G., Welham, S. J. M., King, P., BURNS, S. P., & Clark, A. J. L. (2007) · Circulation Research · doi:10.1161/01.res.0000258855.60637.58 · Cited by 478 · see citing works
Lillycrop, K. A., Phillips, E. S., Torrens, C., Hanson, M. A., Jackson, A. A., & Burdge, G. C. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114507894438 · Cited by 461 · see citing works
Islet Function in Offspring of Mothers on Low-Protein Diet During Gestation
Dahri, S., Snoeck, A., Reusens-Billen, B., Remacle, C., & Hote, J. J. (1991) · Diabetes · doi:10.2337/diab.40.2.s115 · Cited by 445 · see citing works
Methyl donor supplementation prevents transgenerational amplification of obesity
Waterland, R. A., Travisano, M., Tahiliani, K. G., Rached, M.-T., & Mirza, S. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.100 · Cited by 414 · see citing works
Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats
Drake, A. J., Walker, B. R., & Seckl, J. R. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00106.2004 · Cited by 409 · see citing works
Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver
Stanger, B. Z., Tanaka, A., & Melton, D. A. (2007) · Nature · doi:10.1038/nature05537 · Cited by 385 · see citing works
Non‐genomic transgenerational inheritance of disease risk
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · BioEssays · doi:10.1002/bies.20522 · Cited by 381 · see citing works
Dean, W., Bowden, L., Aitchison, A., Klose, J., Moore, T., Meneses, J. J., Reik, W., & Feil, R. (1998) · Development · doi:10.1242/dev.125.12.2273 · Cited by 375 · see citing works
Organ-selective growth in the offspring of protein-restricted mothers
Desai, M., Crowther, N. J., Lucas, A., & Hales, C. N. (1996) · British Journal Of Nutrition · doi:10.1079/bjn19960065 · Cited by 367 · see citing works
Gender-linked hypertension in offspring of lard-fed pregnant rats
Khan, I. Y., Taylor, P. D., Dekou, V., Seed, P. T., Lakasing, L., Graham, D., Dominiczak, A. F., Hanson, M. A., & Poston, L. (2003) · Hypertension · doi:10.1161/01.hyp.0000047511.97879.fc · Cited by 365 · see citing works
Khan, I. Y., Dekou, V., Douglas, G., Jensen, R., Hanson, M. A., Poston, L., & Taylor, P. D. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00354.2004 · Cited by 357 · see citing works
Petrik, J., Reusens, B., Arany, E. J., Remacle, C., Coelho, C., Hoet, J., & Hill, D. J. (1999) · Endocrinology · doi:10.1210/endo.140.10.7042 · Cited by 337 · see citing works
Zambrano, E., Martínez‐Samayoa, P. M., Bautista, C. J., Deás, M., Guillén-Pineda, L. E., Rodríguez-González, G. L., Guzmán, C., Larrea, F., & Nathanielsz, P. W. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.086462 · Cited by 325 · see citing works
Obesity and Pregnancy—The Propagation of a Viscous Cycle?
Catalano, P. M. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031046 · Cited by 322 · see citing works
In utero undernutrition impairs rat beta-cell development
Garofano, A., Czernichow, P., & Bréant, B. (1997) · Diabetologia · doi:10.1007/s001250050812 · Cited by 320 · see citing works
Dunn, G. A., & Bale, T. L. (2009) · Endocrinology · doi:10.1210/en.2009-0500 · Cited by 317 · see citing works
Jennings, B. J., Ozanne, S. E., Dorling, M. W., & Hales, C. N. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00336-1 · Cited by 303 · see citing works
Chromosomal mapping of genetic loci associated with non-insulin dependent diabetes in the GK rat
Gauguier, D., Froguel, P., Parent, V., Bernard, C., Bihoreau, M., Portha, B., James, M. R., Pénicaud, L., Lathrop, M. G., & Ktorza, A. (1996) · Nature Genetics · doi:10.1038/ng0196-38 · Cited by 301 · see citing works
Self-citationTaylor, P. D., McConnell, J., Khan, I. Y., Holemans, K., Lawrence, K. M., Asare-Anane, H., Persaud, S. J., Jones, P. M., Petrie, L., Hanson, M. A., et al. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00355.2004 · Cited by 297 · see citing works
Florez, J. C. (2008) · Diabetologia · doi:10.1007/s00125-008-1025-9 · Cited by 290 · see citing works
Low birthweight is associated with specific changes in muscle insulin-signalling protein expression
Ozanne, S. E., Jensen, C. B., Tingey, K., Storgaard, H., Madsbad, S., & Vaag, A. A. (2005) · Diabetologia · doi:10.1007/s00125-005-1669-7 · Cited by 286 · see citing works
Tourrel‐Cuzin, C., Bailbé, D., Lacorne, M., Meile, M.-J., Kergoat, M., & Portha, B. (2002) · Diabetes · doi:10.2337/diabetes.51.5.1443 · Cited by 285 · see citing works
Self-citationEffect of a diabetic environment in utero on predisposition to type 2 diabetes
Sobngwi, E., Boudou, P., Mauvais‐Jarvis, F., Leblanc, H., Velho, G., Vexiau, P., Porcher, R., Hadjadj, S., Pratley, R. E., Tataranni, P. A., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13505-2 · Cited by 285 · see citing works
Spontaneous Diabetes Produced by Selective Breeding of Normal Wistar Rats
Gotō, Y., KAKIZAKI, M., & MASAKI, N. (1975) · Proceedings of the Japan Academy · doi:10.2183/pjab1945.51.80 · Cited by 270 · see citing works
Kulkarni, R., Jhala, U. S., Winnay, J. N., Krajewski, S., Montminy, M., & Kahn, C. R. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21845 · Cited by 263 · see citing works
Neonatal Exendin-4 Prevents the Development of Diabetes in the Intrauterine Growth Retarded Rat
Stoffers, D. A., Desai, B. M., León, D. D. D., & Simmons, R. A. (2003) · Diabetes · doi:10.2337/diabetes.52.3.734 · Cited by 261 · see citing works
Kanagalingam, M. G., Forouhi, N. G., Greer, I. A., & Sattar, N. A. (2005) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2005.00685.x · Cited by 256 · see citing works
Fernandez‐Twinn, D. S., Wayman, A., Ekizoglou, S., Martin, M. S., Hales, C. N., & Ozanne, S. E. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00206.2004 · Cited by 256 · see citing works
Srinivasan, M., Katewa, S. D., Palaniyappan, A., Pandya, J. D., & Patel, M. S. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00078.2006 · Cited by 254 · see citing works
Diabetes in old male offspring of rat dams fed a reduced protein diet
Petry, C. J., Dorling, M. W., Pawlak, D. B., Ozanne, S. E., & Hales, C. N. (2001) · Journal of Diabetes Research · doi:10.1155/edr.2001.139 · Cited by 254 · see citing works
High-fat feeding during pregnancy and lactation affects offspring metabolism in rats
Guo, F., & Jen, K. ‐. C. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00342-4 · Cited by 250 · see citing works
de Vries, A., Holmes, M. C., Heijnis, A., Seier, J. V., van Heerden, J., Louw, J., Wolfe‐Coote, S. A., Meaney, M. J., Levitt, N. S., & Seckl, J. R. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30982 · Cited by 238 · see citing works
Mechanisms of disease: the developmental origins of disease and the role of the epigenotype
Ozanne, S. E., & Constância, M. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0531 · Cited by 232 · see citing works
Raychaudhuri, N., Raychaudhuri, S., Thamotharan, M., & Devaskar, S. U. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800128200 · Cited by 227 · see citing works
Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat
Garofano, A., Czernichow, P., & Bréant, B. (1998) · Diabetologia · doi:10.1007/s001250051038 · Cited by 226 · see citing works
Nivoit, P., Morens, C., Assche, F. A. V., Jansen, E. H. J. M., Poston, L., Remacle, C., & Reusens, B. (2009) · Diabetologia · doi:10.1007/s00125-009-1316-9 · Cited by 221 · see citing works
Maternal diabetes during pregnancy: Consequences for the offspring
Aerts, L., Holemans, K., & Assche, F. A. V. (1990) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610060303 · Cited by 215 · see citing works
Benyshek, D. C., Johnston, C. S., & Martin, J. F. (2006) · Diabetologia · doi:10.1007/s00125-006-0196-5 · Cited by 210 · see citing works
Animal evidence for the transgenerational development of diabetes mellitus
Aerts, L., & Assche, F. A. V. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.07.006 · Cited by 210 · see citing works
Epigenetic mechanisms in the development of type 2 diabetes
Pinney, S. E., & Simmons, R. A. (2010) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.10.002 · Cited by 205 · see citing works
Tarry‐Adkins, J. L., Chen, J. H., Smith, N. S., Jones, R. H., Cherif, H., & Ozanne, S. E. (2009) · The FASEB Journal · doi:10.1096/fj.08-122796 · Cited by 198 · see citing works
Simmons, R. A., Suponitsky-Kroyter, I., & Selak, M. A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505695200 · Cited by 194 · see citing works
Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams
Ozanne, S. E., Smith, G. D., Tikerpae, J., & Hales, C. N. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.4.e559 · Cited by 191 · see citing works
Cell populations in the endocrine pancreas of human neonates and infants
Rahier, J., Wallon, J., & Henquin, J. (1981) · Diabetologia · doi:10.1007/bf00252762 · Cited by 186 · see citing works
Adult phenotype in the mouse can be affected by epigenetic events in the early embryo
Reik, W., Römer, I., Barton, S. C., Surani, M. A., Howlett, S., & Klose, J. (1993) · Development · doi:10.1242/dev.119.3.933 · Cited by 182 · see citing works
Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period
Garofano, A., Czernichow, P., & Bréant, B. (1999) · Diabetologia · doi:10.1007/s001250051219 · Cited by 178 · see citing works
THE ENDOCRINE PANCREAS IN SMALL‐FOR‐DATES INFANTS
Assche, F. A. V., Prins, F. D., Aerts, L., & Verjans, M. (1977) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1977.tb12486.x · Cited by 171 · see citing works
Gestational diabetes leads to the development of diabetes in adulthood in the rat
Boloker, J., Gertz, S. J., & Simmons, R. A. (2002) · Diabetes · doi:10.2337/diabetes.51.5.1499 · Cited by 170 · see citing works
Ogata, E. S., Bussey, M. E., & Finley, S. L. (1986) · Metabolism · doi:10.1016/0026-0495(86)90064-8 · Cited by 167 · see citing works
Modifiers of epigenetic reprogramming show paternal effects in the mouse
Chong, S., Vickaryous, N., Ashe, A., Zamudio, N., Youngson, N., Hemley, S., Stopka, T., Skoultchi, A., Matthews, J., Scott, H. S., et al. (2007) · Nature Genetics · doi:10.1038/ng2031 · Cited by 166 · see citing works
Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats
Peterside, I., Selak, M. A., & Simmons, R. A. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00437.2002 · Cited by 164 · see citing works
Altered adipocyte properties in the offspring of protein malnourished rats
Shepherd, P. R., Crowther, N. J., Desai, M., Hales, C. N., & Ozanne, S. E. (1997) · British Journal Of Nutrition · doi:10.1079/bjn19970124 · Cited by 164 · see citing works
Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats
Selak, M. A., Storey, B. T., Peterside, I., & Simmons, R. A. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00322.2002 · Cited by 162 · see citing works
Martin, A. O., Simpson, J. L., Ober, C., & Freinkel, N. (1985) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(85)90272-8 · Cited by 158 · see citing works
Palinski, W., D’Armiento, F. P., Witztum, J. L., de Nigris, F., Casanada, F., Condorelli, M., Silvestre, M., & Claudio Napoli, A. (2001) · Circulation Research · doi:10.1161/hh2301.099646 · Cited by 158 · see citing works
Plasma insulin in appropriate- and small-for-gestational-age fetuses
Economides, D. L., Proudler, A., & Nicolaides, K. H. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90167-1 · Cited by 149 · see citing works
The endocrine pancreas of the fetus from diabetic pregnant rat
Kervran, A., Guillaume, M., & JOST, A. (1978) · Diabetologia · doi:10.1007/bf01219648 · Cited by 148 · see citing works
Maternal Antioxidant Supplementation Prevents Adiposity in the Offspring of Western Diet–Fed Rats
Sen, S., & Simmons, R. A. (2010) · Diabetes · doi:10.2337/db10-0301 · Cited by 146 · see citing works
Metabolic Programming: Causes and Consequences
Patel, M. S., & Srinivasan, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.r100017200 · Cited by 143 · see citing works
Chakrabarti, S. K., Francis, J. W., Ziesmann, S. M., Garmey, J. C., & Mirmira, R. G. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303423200 · Cited by 142 · see citing works
The maternal endocrine environment in the low-protein model of intra-uterine growth restriction
Fernandez‐Twinn, D. S., Ozanne, S. E., Ekizoglou, S., Doherty, C., James, L. A., Gusterson, B. A., & Hales, C. N. (2003) · British Journal Of Nutrition · doi:10.1079/bjn2003967 · Cited by 140 · see citing works
Lifetime consequences of abnormal fetal pancreatic development
Holemans, K., Aerts, L., & Assche, F. A. V. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.036582 · Cited by 135 · see citing works
Low Acute Insulin Secretory Responses in Adult Offspring of People With Early Onset Type 2 Diabetes
Gautier, J., Wilson, C., Weyer, C., Mott, D., Knowler, W. C., Cavaghan, M. K., Polonsky, K. S., Bogardus, C., & Pratley, R. E. (2001) · Diabetes · doi:10.2337/diabetes.50.8.1828 · Cited by 133 · see citing works
Intrauterine Growth Retardation: Fetal Glucose Transport is Diminished in Lung but Spared in Brain
Simmons, R. A., Gounis, A. S., Bangalore, S., & Ogata, E. S. (1992) · Pediatric Research · doi:10.1203/00006450-199201000-00011 · Cited by 128 · see citing works
Dissecting the role of glucocorticoids on pancreas development.
Gésina, E., Tronche, F., Herrera, P., Duchêne, B., Tales, W., Czernichow, P., & Bréant, B. (2004) · Diabetes · doi:10.2337/diabetes.53.9.2322 · Cited by 124 · see citing works
Glucocorticoids impair fetal β-cell development in rats
Blondeau, B., Lésage, J., Czernichow, P., Dupouy, J., & Bréant, B. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.3.e592 · Cited by 124 · see citing works
Dumortier, O., Blondeau, B., Duvillié, B., Reusens, B., Bréant, B., & Remacle, C. (2007) · Diabetologia · doi:10.1007/s00125-007-0811-0 · Cited by 124 · see citing works
Pampfer, S., Vanderheyden, I., McCracken, J. E., Veselá, J., & Hertogh, R. D. (1997) · Development · doi:10.1242/dev.124.23.4827 · Cited by 123 · see citing works
Methyltransferase Set7/9 Maintains Transcription and Euchromatin Structure at Islet-Enriched Genes
Deering, T. G., Ogihara, T., Trace, A. P., Maier, B., & Mirmira, R. G. (2008) · Diabetes · doi:10.2337/db08-1150 · Cited by 117 · see citing works
Fu, Q., McKnight, R. A., Yu, X., Wang, L., Callaway, C. W., & Lane, R. H. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00175.2004 · Cited by 114 · see citing works
Islet cell response in the neonatal rat after exposure to a high-fat diet during pregnancy
Cerf, M. E., Williams, K. G., Nkomo, X. I., Muller, C. J. F., Toit, D. F. D., Louw, J., & Wolfe‐Coote, S. A. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00335.2004 · Cited by 107 · see citing works
Nutritional Programming of Blood Pressure and Renal Morphology
Langley‐Evans, S. C., Langley-Evans, A. J., & Marchand, M. C. (2003) · Archives of Physiology and Biochemistry · doi:10.1076/apab.111.1.8.15136 · Cited by 106 · see citing works
Glycemic memory associated epigenetic changes
Siebel, A. L., Fernández, A. Z., & El‐Osta, A. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.06.005 · Cited by 103 · see citing works
Intergenerational transmission of programmed effects: public health consequences
Drake, A. J., & Liu, L. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.11.006 · Cited by 101 · see citing works
Bhasin, K. K. S., van Nas, A., Martin, L. J., Davis, R. C., Devaskar, S. U., & Lusis, A. J. (2008) · Diabetes · doi:10.2337/db07-1530 · Cited by 100 · see citing works
Unterman, T. G., Lascon, R., Gotway, M. B., OEHLER, D. T., Gounis, A. S., Simmons, R. A., & Ogata, E. S. (1990) · Endocrinology · doi:10.1210/endo-127-4-2035 · Cited by 97 · see citing works
Theys, N., Bouckenooghe, T., Ahn, M., Remacle, C., & Reusens, B. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00280.2009 · Cited by 94 · see citing works
Francis, J. W., Chakrabarti, S. K., Garmey, J. C., & Mirmira, R. G. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505741200 · Cited by 93 · see citing works
Intrauterine programming of hypertension in the rat: Nutrient interactions
Langley‐Evans, S. C. (1996) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(96)00018-7 · Cited by 91 · see citing works
Maternal transmission of diabetes
Alcolado, J. C., Laji, K., & Gill-Randall, R. J. (2002) · Diabetic Medicine · doi:10.1046/j.1464-5491.2002.00675.x · Cited by 82 · see citing works
Caldérari, S., Gangnerau, M.-N., Thibault, M., Meile, M.-J., Kassis, N., Álvarez, C., Portha, B., & Serradas, P. (2007) · Diabetologia · doi:10.1007/s00125-007-0676-2 · Cited by 75 · see citing works
Self-citationOh, W., Gelardi, N. L., & Cha, C. (1988) · Metabolism · doi:10.1016/0026-0495(88)90192-8 · Cited by 74 · see citing works
Langley‐Evans, S. C., & Nwagwu, M. O. (1998) · Life Sciences · doi:10.1016/s0024-3205(98)00311-7 · Cited by 73 · see citing works
Early development of beta-cells is impaired in the GK rat model of type 2 diabetes.
Miralles, F., & Portha, B. (2001) · Diabetes · doi:10.2337/diabetes.50.2007.s84 · Cited by 72 · see citing works
Self-citationDisturbed Development of the Preimplantation Embryo in the Insulin-Dependent Diabetic BB/E Rat
Lea, R. G., McCracken, J. E., McIntyre, S. S., Smith, W. J. B., & BAIRD, J. D. (1996) · Diabetes · doi:10.2337/diab.45.11.1463 · Cited by 71 · see citing works
Impaired Glucose Homeostasis in Adult Rats From Hyperglycemic Mothers
Bihoreau, M.-T., Ktorza, A., Kinebanyan, M. F., & Picon, L. (1986) · Diabetes · doi:10.2337/diab.35.9.979 · Cited by 71 · see citing works
Han, J., Xu, J., Epstein, P. N., & Liu, Y. Q. (2005) · Diabetologia · doi:10.1007/s00125-005-1854-8 · Cited by 70 · see citing works
Bertin, É., Gangnerau, M.-N., Bellon, G., Bailbé, D., Vacqueur, A. A. D., & Portha, B. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00037.2002 · Cited by 69 · see citing works
Self-citationHanson, R. L., Elston, R. C., Pettitt, D. J., Bennett, P. H., & Knowler, W. C. (1995) · PubMed Central · Cited by 65 · see citing works
Blondeau, B., Avril, I., Duchêne, B., & Bréant, B. (2002) · Diabetologia · doi:10.1007/s00125-001-0767-4 · Cited by 63 · see citing works
Type�2 diabetes mellitus ? genes or intrauterine environment? An embryo transfer paradigm in rats
Gill-Randall, R. J., Adams, D. M., Ollerton, R. L., Lewis, M., & Alcolado, J. C. (2004) · Diabetologia · doi:10.1007/s00125-004-1464-x · Cited by 62 · see citing works
Nutrition, Glucocorticoids and Pancreas Development
Bréant, B., Gesina, E., & Blondeau, B. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091513 · Cited by 61 · see citing works
The endocrine pancreas in virgin and pregnant offspring of diabetic pregnant rats
Aerts, L., Vercruysse, L., & Van Assche, F. A. (1997) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(97)00080-6 · Cited by 55 · see citing works
Higher Maternal Than Paternal Inheritance of Diabetes in GK Rats
Gauguier, D., Nelson, I. P., Bernard, C., Parent, V., Marsac, C., Cohen, D., & Froguel, P. (1994) · Diabetes · doi:10.2337/diab.43.2.220 · Cited by 53 · see citing works
Contrasted Impact of Maternal Rat Food Restriction on the Fetal Endocrine Pancreas
Álvarez, C., Martín, M. Á., Goya, L., Bertin, É., Portha, B., & Pascual-Leone, A. M. (1997) · Endocrinology · doi:10.1210/endo.138.6.5202 · Cited by 52 · see citing works
Self-citationImpaired pancreatic beta cell function in the fetal GK rat. Impact of diabetic inheritance.
Serradas, P., Gangnerau, M.-N., Giroix, M.-H., Saulnier, C., & Portha, B. (1998) · Journal of Clinical Investigation · doi:10.1172/jci368 · Cited by 49 · see citing works
Self-citationFetal Insulin-Like Growth Factor-2 Production Is Impaired in the GK Rat Model of Type 2 Diabetes
Serradas, P., Goya, L., Lacorne, M., Gangnerau, M.-N., Ramos, S., Álvarez, C., Pascual-Leone, A.-M., & Portha, B. (2002) · Diabetes · doi:10.2337/diabetes.51.2.392 · Cited by 49 · see citing works
Self-citationGauguier, D., Bihoreau, M., Picon, L., & Ktorza, A. (1991) · Diabetes · doi:10.2337/diab.40.2.s109 · Cited by 46 · see citing works
Rat maternal diabetes impairs pancreatic β-cell function in the offspring
Han, J., Xu, J., Long, Y. S., Epstein, P. N., & Liu, Y. Q. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00479.2006 · Cited by 45 · see citing works
Reusens, B., & Remacle, C. (2001) · Twin Research · doi:10.1375/1369052012597 · Cited by 43 · see citing works
Grill, V., Johansson, B., Jalkanen, P., & Eriksson, U. J. (1991) · Diabetologia · doi:10.1007/bf00403173 · Cited by 41 · see citing works
Matveyenko, A. V., Singh, I., Shin, B., Georgia, S. K., & Devaskar, S. U. (2010) · Endocrinology · doi:10.1210/en.2010-0978 · Cited by 40 · see citing works
Depot-Specific Effects of Early Growth Retardation on Adipocyte Insulin Action
Ozanne, S. E., Dorling, M. W., Wang, C., & Petry, C. J. (2000) · Hormone and Metabolic Research · doi:10.1055/s-2007-978592 · Cited by 37 · see citing works
Brufani, C., Grossi, A., Fintini, D., Tozzi, A. E., Nocerino, V., Patera, P. I., Ubertini, G., Porzio, O., Barbetti, F., & Cappa, M. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1079 · Cited by 35 · see citing works
Kim, S., Nian, C., & McIntosh, C. H. S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809046200 · Cited by 35 · see citing works
Ketosis resistance in the male offspring of protein-malnourished rat dams
Ozanne, S. E., Wang, C. L., Petry, C. J., Smith, J. M., & Hales, C. N. (1998) · Metabolism · doi:10.1016/s0026-0495(98)90068-3 · Cited by 34 · see citing works
Martín, M. Á., Álvarez, C., Goya, L., Portha, B., & Pascual-Leone, A. M. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.272.4.e634 · Cited by 34 · see citing works
Self-citationReduced beta cell function in offspring of mothers with young-onset type 2 diabetes
Singh, R., Pearson, E. R., Avery, P. J., McCarthy, M. I., Lévy, J., Hitman, G. A., Sampson, M., Walker, M., & Hattersley, A. T. (2006) · Diabetologia · doi:10.1007/s00125-006-0285-5 · Cited by 33 · see citing works
Ryan, E. A., Liu, D., Bell, R. C., Finegood, D. T., & Crawford, J. (1995) · Endocrinology · doi:10.1210/endo.136.12.7588312 · Cited by 33 · see citing works
Reusens-Billen, B., Remacle, C., Daniline, J., & Hoet, J. J. (1984) · Hormone and Metabolic Research · doi:10.1055/s-2007-1014853 · Cited by 31 · see citing works
Triadou, N., Portha, B., Picon, L., & Rosselin, G. (1982) · Diabetes · doi:10.2337/diab.31.1.75 · Cited by 30 · see citing works
Self-citationPlasma Amino Acids in Diabetic Pregnant Rats and in Their Fetal and Adult Offspring
Aerts, L., van Bree, R., Feytons, V., Rombauts, W., & Assche, F. A. V. (2009) · Biology of the Neonate · doi:10.1159/000242984 · Cited by 28 · see citing works
Intra-uterine origins of type 2 diabetes
Jones, R. H., & Ozanne, S. E. (2007) · Archives of Physiology and Biochemistry · doi:10.1080/13813450701318484 · Cited by 26 · see citing works
Protein-Caloric Food Restriction Affects Insulin-Like Growth Factor System in Fetal Wistar Rat
Martín, M. Á., Serradas, P., Ramos, S., Fernández‐Millán, E., Goya, L., Gangnerau, M.-N., Lacorne, M., Pascual-Leone, A. M., Escrivá, F., Portha, B., et al. (2004) · Endocrinology · doi:10.1210/en.2004-0665 · Cited by 25 · see citing works
Self-citationMaternal and Fetal Endocrine Pancreas in the Spontaneously Diabetic BB Rat
Verhaeghe, J., Peeters, T., Vandeputte, M., Rombauts, W., Bouillon, R., & Assche, F. A. V. (2009) · Biology of the Neonate · doi:10.1159/000242932 · Cited by 24 · see citing works
Portha, B., Kergoat, M., Blondel, O., & Bailbé, D. (1995) · European Journal of Endocrinology · doi:10.1530/eje.0.1330475 · Cited by 23 · see citing works
Self-citationFernández‐Millán, E., Martín, M. Á., Fajardo, S., Escrivá, F., & Álvarez, C. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00283.2006 · Cited by 22 · see citing works
Karnik, H. B., Sonawane, B. R., Adkins, J. S., & Mohla, S. (2019) · Developmental Pharmacology and Therapeutics · doi:10.1159/000480930 · Cited by 18 · see citing works
Dyrskog, S., Gregersen, S., & Hermansen, K. (2005) · The Review of Diabetic Studies · doi:10.1900/rds.2005.2.136 · Cited by 16 · see citing works
Portha, B., Chavey, A., Maulny, L., Gangnerau, M.-N., Bailbé, D., Dolz, M., Jammes, H., Renard, J. P. J. P., & Movassat, J. (2009) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2008.12.002 · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The Pathophysiology of Gestational Diabetes Mellitus
Plows, J. F., Stanley, J. L., Baker, P. N., Reynolds, C. M., & Vickers, M. H. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113342 · Cited by 1,874 · see citing works
“These individuals are more likely to have experienced hyperglycemia and β-cell fatigue even before birth, predisposing them to hyperglycemia during times of later metabolic stress, such as during pregnancy [55].”
BackgroundDifferentiation of diabetes by pathophysiology, natural history, and prognosis
Skyler, J. S., Bakris, G. L., Bonifacio, E., Darsow, T., Eckel, R. H., Groop, L., Groop, P.-H., Handelsman, Y., Insel, R. A., Mathieu, C., et al. (2017) · Diabetes · doi:10.2337/db16-0806 · Cited by 823 · see citing works
Janssen, J. A. M. J. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157797 · Cited by 296 · see citing works
Gut microbiota, immune development and function
Bengmark, S. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.09.002 · Cited by 264 · see citing works
Pathogenesis of MASLD and MASH – role of insulin resistance and lipotoxicity
Bansal, S., & Bansal, M. B. (2024) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.17930 · Cited by 204 · see citing works
Streptozotocin-Induced Diabetes Models: Pathophysiological Mechanisms and Fetal Outcomes
Damasceno, D. C., NETTO, A. O., Iessi, I. L., Gallego, F. Q., Corvino, S. B., Dallaqua, B., Sinzato, Y. K., Bueno, A., Calderon, I. D. M. P., & Rudge, M. V. C. (2014) · BioMed Research International · doi:10.1155/2014/819065 · Cited by 165 · see citing works
The Elevated Susceptibility to Diabetes in India: An Evolutionary Perspective
Wells, J. C. K., Pomeroy, E., Walimbe, S. R., Popkin, B. M., & Yajnik, C. S. (2016) · Frontiers in Public Health · doi:10.3389/fpubh.2016.00145 · Cited by 155 · see citing works
Obesity as malnutrition: The role of capitalism in the obesity global epidemic
Wells, J. C. K. (2012) · American Journal of Human Biology · doi:10.1002/ajhb.22253 · Cited by 129 · see citing works
The GK Rat: A Prototype for the Study of Non-overweight Type 2 Diabetes
Portha, B., Giroix, M.-H., Tourrel‐Cuzin, C., Stunff, H. L., & Movassat, J. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-068-7_9 · Cited by 112 · see citing works
Self-citationPsychological Stress, Intestinal Barrier Dysfunctions, and Autoimmune Disorders: An Overview
Ilchmann-Diounou, H., & Ménard, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01823 · Cited by 117 · see citing works
Moreno‐Fernández, J., Ochoa, J. J., López‐Frías, M., & Díaz‐Castro, J. (2020) · Nutrients · doi:10.3390/nu12123900 · Cited by 112 · see citing works
Fetal programming and gestational diabetes mellitus
Monteiro, L. J., Norman, J. E., Rice, G. E., & Illanes, S. E. (2015) · Placenta · doi:10.1016/j.placenta.2015.11.015 · Cited by 100 · see citing works
Fosgerau, K., Jessen, L., Tolborg, J. L., Østerlund, T., Larsen, K. S., Rolsted, K., Brorson, M., Jelsing, J., & Neerup, T. S. R. (2012) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2012.01676.x · Cited by 93 · see citing works
A critical review: early life nutrition and prenatal programming for adult disease
Carolan, M. C., Duarte‐Gardea, M., & Lechuga, J. (2015) · Journal of Clinical Nursing · doi:10.1111/jocn.12951 · Cited by 87 · see citing works
Rodríguez-González, G. L., Vega-García, C. C., Boeck, L., Vázquez, M., Bautista, C. J., Reyes‐Castro, L. A., Saldaña, O., Lovera, D., Nathanielsz, P. W., & Zambrano, E. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.209 · Cited by 83 · see citing works
Fox, M. M., Entringer, S., Buß, C., DeHaene, J., & Wadhwa, P. D. (2015) · American Journal of Public Health · doi:10.2105/ajph.2015.302571 · Cited by 81 · see citing works
Archer, E. (2014) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2014.08.006 · Cited by 78 · see citing works
Wells, J. C. K. (2016) · Cambridge University Press eBooks · doi:10.1017/cbo9780511972959 · Cited by 81 · see citing works
García‐Arévalo, M., Alonso‐Magdalena, P., Servitja, J., Boronat‐Belda, T., Merino, B., Villar-Pazos, S., Medina‐Gómez, G., Novials, A., Quesada, I., & Nadal, Á. (2016) · Endocrinology · doi:10.1210/en.2016-1390 · Cited by 73 · see citing works
Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility
Portha, B., Fournier, A., Kioon, M. D. A., Mezger, V., & Movassat, J. (2013) · Biochimie · doi:10.1016/j.biochi.2013.10.003 · Cited by 73 · see citing works
Self-citationChanging perspectives in pre-existing diabetes and obesity in pregnancy
Barbour, L. A. (2014) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000079 · Cited by 73 · see citing works
ACE2 deficiency reduces β-cell mass and impairs β-cell proliferation in obese C57BL/6 mice
Shoemaker, R., Yiannikouris, F. B., Thatcher, S. E., & Cassis, L. A. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00054.2015 · Cited by 69 · see citing works
Early-Life Nutritional Programming of Type 2 Diabetes: Experimental and Quasi-Experimental Evidence
Vaiserman, A. M. (2017) · Nutrients · doi:10.3390/nu9030236 · Cited by 69 · see citing works
Maternal obesity accelerates rat offspring metabolic ageing in a sex‐dependent manner
Rodríguez-González, G. L., Reyes‐Castro, L. A., Bautista, C. J., Beltrán, A. A., Ibáñez, C. A., Vega-García, C. C., Lomas‐Soria, C., Castro-Rodríguez, D. C., Elías‐López, A. L., Nathanielsz, P. W., et al. (2019) · The Journal of Physiology · doi:10.1113/jp278232 · Cited by 64 · see citing works
Ansari, M. A., Chauhan, W., Shoaib, S., Alyahya, S. A., Ali, M., Ashraf, H., Alomary, M. N., & Al-Suhaimi, E. A. (2023) · International Journal of Obesity · doi:10.1038/s41366-023-01369-3 · Cited by 65 · see citing works
Maternal Inactivity: 45-Year Trends in Mothers’ Use of Time
Archer, E., Lavie, C. J., McDonald, S. M., Thomas, D. M., Hébert, J. R., Ross, S. E. T., McIver, K. L., Malina, R. M., & Blair, S. N. (2013) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2013.09.009 · Cited by 62 · see citing works
Obesity in prematurely born children and adolescents: follow up in pediatric clinic
Vasylyeva, T. L., Barche, A., Chennasamudram, S. P., Sheehan, C., Singh, R., & Okogbo, M. E. (2013) · Nutrition Journal · doi:10.1186/1475-2891-12-150 · Cited by 61 · see citing works
Role of nutrients and mTOR signaling in the regulation of pancreatic progenitors development
Elghazi, L., Blandino-Rosano, M., Alejandro, E. U., CRAS-MÉNEUR, C. M. H., & Bernal‐Mizrachi, E. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.03.010 · Cited by 55 · see citing works
Dysglycaemia, Inflammation and Psychosis: Findings From the UK ALSPAC Birth Cohort
Perry, B. I., Upthegrove, R., Thompson, A. D., Marwaha, S., Zammit, S., Singh, S. P., & Khandaker, G. M. (2018) · Schizophrenia Bulletin · doi:10.1093/schbul/sby040 · Cited by 55 · see citing works
Weller, M. M. D. C. A., Fortes, M. R. S., Marcondes, M. I., Rotta, P. P., Gionbeli, T. R. S., Filho, S. D. C. V., Campos, M. M., Silva, F. F. E., da Silva, W., Moore, S. S., et al. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-9673 · Cited by 50 · see citing works
Rodríguez-González, G. L., Reyes‐Castro, L. A., Vega-García, C. C., Boeck, L., Ibáñez, C. A., Nathanielsz, P. W., Larrea, F., & Zambrano, E. (2014) · AGE · doi:10.1007/s11357-014-9721-5 · Cited by 45 · see citing works
Cerf, M. E., Chapman, C. S., & Louw, J. (2012) · ISRN Endocrinology · doi:10.5402/2012/627270 · Cited by 45 · see citing works
Review: Effects of maternal micronutrient supplementation on placental function
Richard, K., Holland, O. J., Landers, K., Vanderlelie, J. J., Hofstee, P., Cuffe, J. S. M., & Perkins, A. V. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.022 · Cited by 43 · see citing works
Maternal high-fat diet is associated with altered pancreatic remodelling in mice offspring
Gregório, B. M., Souza‐Mello, V., Mandarim‐de‐Lacerda, C. A., & Águila, M. B. (2012) · European Journal of Nutrition · doi:10.1007/s00394-012-0382-9 · Cited by 40 · see citing works
Fetal Programming of the Neuroendocrine-Immune System and Metabolic Disease
Fisher, R. E., Steele, M. A., & Karrow, N. A. (2012) · Journal of Pregnancy · doi:10.1155/2012/792934 · Cited by 38 · see citing works
GPR119 agonists: Novel therapeutic agents for type 2 diabetes mellitus
Manaithiya, A., Alam, O., Sharma, V., Naim, M. J., Mittal, S., & Khan, I. A. (2021) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2021.104998 · Cited by 36 · see citing works
Wang, J., Zhu, Y., Cai, L., Jin, J., Chen, Y., Mai, J., Ma, L., Ma, Y., & Ma, J. (2015) · Public Health Nutrition · doi:10.1017/s1368980015002542 · Cited by 35 · see citing works
Agarwal, P., Brar, N., Morriseau, T. S., Kereliuk, S. M., Fonseca, M. A., Cole, L. K., Jha, A., Xiang, B., Hunt, K. L., Seshadri, N., et al. (2019) · Endocrinology · doi:10.1210/en.2019-00232 · Cited by 34 · see citing works
Dietert, R. R., & Dietert, J. M. (2012) · Entropy · doi:10.3390/e14112036 · Cited by 32 · see citing works
Contraceptive Use Among Women with Prediabetes and Diabetes in a US National Sample
Britton, L. E., Hussey, J. M., Berry, D. C., Crandell, J., Brooks, J. L., & Bryant, A. G. (2018) · Journal of Midwifery & Women s Health · doi:10.1111/jmwh.12936 · Cited by 32 · see citing works
Harris, S., Blasio, M. J. D., Davis, M. A., Kelly, A. C., Davenport, H. M., Wooding, F. B. P., Blache, D., Meredith, D., Anderson, M. J., Fowden, A. L., et al. (2017) · The Journal of Physiology · doi:10.1113/jp273555 · Cited by 30 · see citing works
Endocrine pancreatic development: impact of obesity and diet
O'Dowd, J., & Stocker, C. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00170 · Cited by 27 · see citing works
Maternal hypothyroidism in mice influences glucose metabolism in adult offspring
Kemkem, Y., Nasteska, D., de Bray, A., Bargi‐Souza, P., Garcia, R. A. P., Guillou, A., Mollard, P., Hodson, D. J., & Schaeffer, M. (2020) · Diabetologia · doi:10.1007/s00125-020-05172-x · Cited by 26 · see citing works
Pancreatic progenitor epigenome maps prioritize type 2 diabetes risk genes with roles in development
Geusz, R. J., Wang, A., Chiou, J., Lancman, J. J., Wetton, N., Kefalopoulou, S., Wang, J., Qiu, Y., Yan, J., Aylward, A., et al. (2021) · eLife · doi:10.7554/elife.59067 · Cited by 26 · see citing works
Jørgensen, S. W., Brøns, C., Bluck, L. J. C., Hjort, L., Færch, K., Thankamony, A., Gillberg, L., Friedrichsen, M. H., Dunger, D. B., & Vaag, A. A. (2014) · Diabetologia · doi:10.1007/s00125-014-3432-4 · Cited by 26 · see citing works
Hjort, R., Alfredsson, L. S., Carlsson, P., Groop, L., Martinell, M., Storm, P., Tuomilehto, J., & Carlsson, S. (2015) · Diabetologia · doi:10.1007/s00125-015-3711-8 · Cited by 25 · see citing works
Berry, D. C., Boggess, K., & Johnson, Q. B. (2016) · Current Diabetes Reports · doi:10.1007/s11892-016-0733-7 · Cited by 25 · see citing works
Jawerbaum, A., & White, V. (2017) · Placenta · doi:10.1016/j.placenta.2017.02.009 · Cited by 25 · see citing works
Calzada, L., Morales, A., Sosa-Larios, T. C., Reyes‐Castro, L. A., Rodríguez-González, G. L., Rodríguez‐Mata, V., Zambrano, E., & Morimoto, S. (2016) · Nutrition Research · doi:10.1016/j.nutres.2016.03.007 · Cited by 23 · see citing works
Maternal dietary free or bound fructose diversely influence developmental programming of lipogenesis
Yürük, A. A., & Nergiz‐Unal, R. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0618-z · Cited by 22 · see citing works
Malo, E., Saukko, M., Santaniemi, M., Hietaniemi, M., Lammentausta, E., Sequeiros, R. T. B., Ukkola, O. H., & Kesäniemi, Y. A. (2012) · Pediatric Research · doi:10.1038/pr.2012.173 · Cited by 23 · see citing works
Chen, Y.-C. D., Huang, Y.-H., Sheen, J., Tain, Y., Yu, H., Chen, C., Tiao, M., Kuo, H., & Huang, L. (2016) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2016.02.008 · Cited by 21 · see citing works
Archer, E., Pavela, G., McDonald, S. M., Lavie, C. J., & Hill, J. O. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01053 · Cited by 22 · see citing works
Głombik, K., Trojan, E., Kurek, A., Budziszewska, B., & Basta‐Kaim, A. (2019) · Neurotoxicity Research · doi:10.1007/s12640-019-00070-6 · Cited by 21 · see citing works
Nutrition Board (2014) · Cited by 20 · see citing works
Svingen, T., Ramhøj, L., Mandrup, K. R., Christiansen, S., Axelstad, M., Vinggaard, A. M., & Hass, U. (2018) · Scientific Reports · doi:10.1038/s41598-017-18626-x · Cited by 19 · see citing works
The Constitutive Lack of α7 Nicotinic Receptor Leads to Metabolic Disorders in Mouse
Gausserès, B., Liu, J., Foppen, E., Tourrel‐Cuzin, C., Sánchez-Archidona, A. R., Delangre, E., Cruciani‐Guglielmacci, C., Pons, S., Maskos, U., Thorens, B., et al. (2020) · Biomolecules · doi:10.3390/biom10071057 · Cited by 18 · see citing works
Self-citationMiranda, J. J., Wells, J. C. K., & Smeeth, L. L. (2012) · Revista Peruana de Medicina Experimental y Salud Pública · doi:10.1590/s1726-46342012000300012 · Cited by 18 · see citing works
de Almeida-Faria, J., de Araújo, T. M. F., Mancuso, R. I., Meulman, J., Ferreira, D. D. S., Batista, T. M., Vettorazzi, J. F., da Silva, P. M. R., Rodrigues, S. C., Kinote, A. P. B. D. M., et al. (2016) · Acta Physiologica · doi:10.1111/apha.12684 · Cited by 18 · see citing works
Lindsay, K. L., Entringer, S., Buß, C., & Wadhwa, P. D. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104659 · Cited by 17 · see citing works
Nascimento, E., Guzmán‐Quevedo, O., Delacourt, N., Aragão, R. D. S., Perez-Garcia, G., de Souza, S. L., Manhães‐de‐Castro, R., Bolaños, F. J., & Kaeffer, B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056231 · Cited by 17 · see citing works
Maternal obesity exacerbates insulitis and type 1 diabetes in non-obese diabetic mice
Wang, H., Xue, Y., Wang, B., Zhao, J., Yan, X., Huang, Y., Du, ., & Zhu, M.-J. (2014) · Reproduction · doi:10.1530/rep-13-0614 · Cited by 17 · see citing works
(-)-Epicatechin reduces adiposity in male offspring of obese rats
Santos, S. D. L., Reyes‐Castro, L. A., Coral‐Vázquez, R. M., Méndez, J. P., Leal-García, M., Zambrano, E., & Canto, P. (2019) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174419000345 · Cited by 17 · see citing works
Beta-Cell Adaptation to Pregnancy – Role of Calcium Dynamics
Pretorius, M., & Huang, C. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.853876 · Cited by 16 · see citing works
Islet Cell Response to High Fat Programming in Neonate, Weanling and Adolescent Wistar Rats
Cerf, M. E., & Louw, J. (2013) · PubMed · doi:10.6092/1590-8577/1534 · Cited by 15 · see citing works
Higa, R., Roberti, S. L., Capobianco, E., Fornes, D. D., White, V., & Jawerbaum, A. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2017.06.051 · Cited by 15 · see citing works
Relationship between Birth Weight and Metabolic Status in Obese Adolescents
Hill, D. J., Harry Prapavessis, A., Shoemaker, J. K., Jackman, M., Mahmud, F. H., & Clarson, C. L. (2013) · ISRN Obesity · doi:10.1155/2013/490923 · Cited by 14 · see citing works
Fu, J., Wang, T., Liu, J. Y., Wang, X., Li, M., & Xiao, X. (2019) · Endocrine · doi:10.1007/s12020-019-01929-6 · Cited by 14 · see citing works
Wium‐Andersen, M. K., Jørgensen, T. S. H., Jørgensen, M. B., Rungby, J., Hjorthøj, C. R., Sørensen, H. J., & Osler, M. (2022) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2022.108181 · Cited by 11 · see citing works
Nema, P., Asati, V., Kendya, P., Gupta, T., Agarwal, S., Kori, S. K., Kashaw, V., Iyer, A. K., & Kashaw, S. K. (2023) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557523666230302140658 · Cited by 11 · see citing works
Wicklow, B. A., & Sellers, E. A. C. (2014) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2014.04.017 · Cited by 11 · see citing works
Lu, Y., Jia, Y., Lü, J., Liu, J., Xu, Y., Liu, Y., & Chen, K. (2021) · Archives of Physiology and Biochemistry · doi:10.1080/13813455.2021.1991957 · Cited by 10 · see citing works
Maternal micronutrient disturbance as risks of offspring metabolic syndrome
Shi, Y., Zhong, H., & Pang, L. (2023) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2022.127097 · Cited by 10 · see citing works
Developmental effects of in utero metformin exposure.
Carroll, D. T., Sassin, A. M., Aagaard, K. M., & GANNON, M. A. (2021) · PubMed · Cited by 9 · see citing works
Maternal hypertension programs increased cerebral tissue damage following stroke in adult offspring
Ventura, N. M., Jin, A. Y., Tse, M. Y., Peterson, N. T., Andrew, R. D., Mewburn, J. D., & Pang, S. C.-N. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2498-8 · Cited by 9 · see citing works
Fisher-Heffernan, R. E., Or-Rashid, M. M., AlZahal, O., Quinton, M., Boermans, H. J., McBride, B. W., Regnault, T. R. H., & Karrow, N. A. (2015) · BMC Veterinary Research · doi:10.1186/s12917-015-0573-8 · Cited by 9 · see citing works
Effect of transgenerational diabetes via maternal lineage in female rats
Gallego, F. Q., Barco, V. S., Sinzato, Y. K., Paula, V. G., de Souza, M. R., da Cruz, L. L., Roy, S., Corrente, J. E., & Damasceno, D. C. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e31049 · Cited by 8 · see citing works
Dichotomy in the Impact of Elevated Maternal Glucose Levels on Neonatal Epigenome
Lim, I. Y., Lin, X., Teh, A. L., Wu, Y., Chen, L., He, M., Chan, S., MacIsaac, J. L., Chan, J. K. Y., Tan, K. H., et al. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab710 · Cited by 6 · see citing works
Samaan, M. C., Valencia, M., Cheung, C., Wilk, B., Lau, K. K., & Thabane, L. (2014) · Journal of Multidisciplinary Healthcare · doi:10.2147/jmdh.s63842 · Cited by 7 · see citing works
Food contaminants and programming of type 2 diabetes: recent findings from animal studies
Firmin, S., Bahi-Jaber, N., & Abdennebi‐Najar, L. (2016) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000210 · Cited by 7 · see citing works
Aydos, D., Aksoy, Z. B., Ünal, M. A., Akçalı, K. C., Bitirim, C. V., & Turan, B. (2025) · Cardiovascular Diabetology · doi:10.1186/s12933-025-02828-z · Cited by 7 · see citing works
Bailey, S. C., Pack, A. P., Wismer, G. A., Calderon, N., Velazquez, E., Batio, S., Ekong, A., Eggleston, A., Wallia, A., Wolf, M. S., et al. (2023) · BMJ Open · doi:10.1136/bmjopen-2023-078282 · Cited by 5 · see citing works
El-Gammal, H., Omar, F., & Hyder, A. (2025) · Food and Chemical Toxicology · doi:10.1016/j.fct.2025.115265 · Cited by 5 · see citing works
Ergaz, Z., Neeman-azulay, M., Weinstein‐Fudim, L., Weksler‐Zangen, S., Shoshani-Dror, D., Moshe Szyf, A., & Ornoy, A. (2016) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.21169 · Cited by 5 · see citing works
Kurian, J., & Mavathur, R. N. (2023) · Journal of Bodywork and Movement Therapies · doi:10.1016/j.jbmt.2023.08.003 · Cited by 6 · see citing works
Cai, W., Chen, L., Zhang, M., Ouyang, J., Wu, P., Tong, J., Gao, G., Yan, S., Tao, F., & Huang, K. (2025) · Thyroid · doi:10.1089/thy.2024.0334 · Cited by 4 · see citing works
Entringer, S., de Punder, K., Verner, G., & Wadhwa, P. D. (2017) · Springer eBooks · doi:10.1007/978-3-319-60289-9_41 · Cited by 4 · see citing works
de Maredsous, C. D., Carlin, G., Oosting, A., Delteil, C., Azzout‐Marniche, D., Chaumontet, C., Blachier, F., Barbillon, P., Mary‐Huard, T., Tomé, D., et al. (2020) · Nutrients · doi:10.3390/nu12020315 · Cited by 4 · see citing works
Programmed for sex: Nutrition–reproduction relationships from an inter-generational perspective
Sharpe, R. M. (2017) · Reproduction · doi:10.1530/rep-17-0537 · Cited by 4 · see citing works
Kong, C. M., Subramanian, A., Gan, S. U., Biswas, A., Bongso, A., & Fong, C. (2020) · Stem Cell Research · doi:10.1016/j.scr.2020.101880 · Cited by 4 · see citing works
Basic Experimental and Clinical Advances in the Mechanisms Underlying Abnormal Pregnancy Outcomes
Regnault, T. R. H., Nijland, M. J., Budge, H., & Morrison, J. L. (2013) · Journal of Pregnancy · doi:10.1155/2013/327638 · Cited by 3 · see citing works
Kamel, M. A. E.-N., Mahmoud, S. A., & Elfetooh, H. A. (2014) · American Journal of Biomedical Sciences · doi:10.5099/aj140300201 · Cited by 2 · see citing works
Le diabete de type 2: voyage au coeur d'une maladie complexe.
Scheen, A. J., & Paquot, N. (2012) · RMLG. Revue médicale de Liège · Cited by 2 · see citing works
Das, A. C., Foroutan, A., Qian, B., Naghavi, N. H., Shabani, K., & Shooshtari, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911456 · Cited by 2 · see citing works
Mojammamy, N., Alayed, N., Aljerian, K., Aldahmash, W., Harrath, A. H., & Alwasel, S. H. (2022) · Saudi Journal of Biological Sciences · doi:10.1016/j.sjbs.2022.103482 · Cited by 2 · see citing works
Mukonowenzou, N. C. (2016) · Cited by 2 · see citing works
Portha, B., Fournier, A., Kioon, M. D. A., Mezger, V., & Movassat, J. (2013) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2013.07.002 · Cited by 1 · see citing works
Self-citationBenyshek, D. C. (2015) · Springer eBooks · doi:10.1007/978-3-319-16853-1_13 · Cited by 1 · see citing works
Aryaie, M., Hosseini, S. M., Sabzi, Z., Rafeeinia, A., Teymoori, H., & Dadashi, N. (2017) · Journal of Clinical and Basic Research · doi:10.29252/jcbr.1.4.41 · Cited by 1 · see citing works
Miranda, J. J., Wells, J. C. K., & Smeeth, L. L. (2014) · Revista Peruana de Medicina Experimental y Salud Pública · doi:10.17843/rpmesp.2012.293.371 · Cited by 1 · see citing works
- Authors
- Portha, B., Chavey, A., & Movassat, J.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Portha, Bernard
- ORCID
- Movassat, Jamileh
- Venue
- Experimental Diabetes Research
- Publisher
- Wiley
- Published
- 2011
- Volume
- 2011
- Pages
- 1-16
- ISSN
- 1687-5214 (ISSN-L)
- 1687-5303
- PMC
- PMC3202114
- OpenAlex
- W2154337610
- Cited by
- 127
- References
- 147
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 3 · 2023: 4 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 7 · 2018: 6 · 2017: 10 · 2016: 15 · 2015: 11 · 2014: 13 · 2013: 11 · 2012: 14
- FWCI
- 1.82
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Experimental Diabetes Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- French National Research Agency (ANR-06-PHYSIO-028)
- Égide (ANR-06-PHYSIO-028)
- NEB Association (ANR-06-PHYSIO-028)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Keywords
- type 2 diabetes, fetal programming, beta-cell mass, maternal protein restriction, caloric restriction, maternal overnutrition, maternal diabetes, gestational diabetes mellitus, impaired glucose tolerance, intergenerational transmission, developmental programming
- MeSH terms
- Animals, Energy Intake, Diabetes Mellitus, Type 2, Disease Models, Animal, Female, Humans, Male, Pancreas, Pregnancy, Pregnancy in Diabetics, Prenatal Exposure Delayed Effects, Protein Deficiency, Risk Factors, Diabetes, Gestational, Overnutrition, Fetal Development, Insulin-Secreting Cells, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review