CoChat
Sign Up
Cited by 208

The DOI matches its Crossref record; 26 of the 26 references it cites were found in a registry or an index.

Developmental Programming, a Pathway to Disease

Padmanabhan, Vasantha, Cardoso, Rodolfo C., Puttabyatappa, Muraly·2016·Endocrinology
DOI 10.1210/en.2016-1003
Open this paper in CoChat — free account

Abstract

Accumulating evidence suggests that insults occurring during the perinatal period alter the developmental trajectory of the fetus/offspring leading to long-term detrimental outcomes that often culminate in adult pathologies. These perinatal insults include maternal/fetal disease states, nutritional deficits/excess, stress, lifestyle choices, exposure to environmental chemicals, and medical interventions. In addition to reviewing the various insults that contribute to developmental programming and the benefits of animal models in addressing underlying mechanisms, this review focuses on the commonalities in disease outcomes stemming from various insults, the convergence of mechanistic pathways via which various insults can lead to common outcomes, and identifies the knowledge gaps in the field and future directions.

Overview

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1210/en.2016-1003

Cites

26 of 26 references verified0 citation errors · 0 not checkable

Statistics

Verification

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.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 174

  1. Gray, 1963, The descriptive study of imprinting in birds from 1873 to 1953, J Gen Psychol, 68, 333, 10.1080/00221309.1963.9920539 · DOI
  2. Forest, 1983, Role of androgens in fetal and pubertal development, Horm Res, 18, 69, 10.1159/000179780 · DOI
  3. Gorski, 1985, Sexual dimorphisms of the brain, J Anim Sci, 61, 38, 10.1093/ansci/61.Supplement_3.38 · DOI
  4. Jost, 1983, Genetic and hormonal factors in sex differentiation of the brain, Psychoneuroendocrinology, 8, 183, 10.1016/0306-4530(83)90055-0 · DOI
  5. Wood, 1998, Sexual differentiation of reproductive neuroendocrine function in sheep, Rev Reprod, 3, 130, 10.1530/ror.0.0030130 · DOI
  6. Lucas, 1991, Programming by early nutrition in man, Ciba Found Symp, 156, 38
  7. Gluckman, 2004, Maternal constraint of fetal growth and its consequences, Semin Fetal Neonatal Med, 9, 419, 10.1016/j.siny.2004.03.001 · DOI
  8. Nijland, 2008, Prenatal origins of adult disease, Curr Opin Obstet Gynecol, 20, 132, 10.1097/GCO.0b013e3282f76753 · DOI
  9. Treviño, 2015, Phosphorylation of epigenetic “readers, writers and erasers”: implications for developmental reprogramming and the epigenetic basis for health and disease, Prog Biophys Mol Biol, 118, 8, 10.1016/j.pbiomolbio.2015.02.013 · DOI
  10. Ganu, 2012, Maternal diet: a modulator for epigenomic regulation during development in nonhuman primates and humans, Int J Obes Suppl, 2, S14, 10.1038/ijosup.2012.16 · DOI
  11. West-Eberhard, 2005, Developmental plasticity and the origin of species differences, Proc Natl Acad Sci USA, 102, 6543, 10.1073/pnas.0501844102 · DOI
  12. Hales, 2001, The thrifty phenotype hypothesis, Br Med Bull, 60, 5, 10.1093/bmb/60.1.5 · DOI
  13. Tang, 2007, Epigenetic reprogramming and imprinting in origins of disease, Rev Endocr Metab Disord, 8, 173, 10.1007/s11154-007-9042-4 · DOI
  14. Puttabyatappa, Effect of maternal PCOS and PCOS-like phenotype on the offspring's health [published online ahead of print November 27, 2015], Mol Cell Endocrinol
  15. Finnell, 2002, Molecular basis of environmentally induced birth defects, Annu Rev Pharmacol Toxicol, 42, 181, 10.1146/annurev.pharmtox.42.083001.110955 · DOI
  16. Roseboom, 2001, Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview, Mol Cell Endocrinol, 185, 93, 10.1016/S0303-7207(01)00721-3 · DOI
  17. Sir-Petermann, 2005, Birth weight in offspring of mothers with polycystic ovarian syndrome, Hum Reprod, 20, 2122, 10.1093/humrep/dei009 · DOI
  18. Ibáñez, 1998, Precocious pubarche, hyperinsulinism, and ovarian hyperandrogenism in girls: relation to reduced fetal growth, J Clin Endocrinol Metab, 83, 3558, 10.1210/jcem.83.10.5205 · DOI
  19. Lakshmy, 2013, Metabolic syndrome: role of maternal undernutrition and fetal programming, Rev Endocr Metab Disord, 14, 229, 10.1007/s11154-013-9266-4 · DOI
  20. Symonds, 2009, Nutritional programming of the metabolic syndrome, Nat Rev Endocrinol, 5, 604, 10.1038/nrendo.2009.195 · DOI
  21. Lal, 2003, Chronic lung disease of prematurity and intrauterine growth retardation: a population-based study, Pediatrics, 111, 483, 10.1542/peds.111.3.483 · DOI
  22. Melo, 2010, High prevalence of polycystic ovary syndrome in women born small for gestational age, Hum Reprod, 25, 2124, 10.1093/humrep/deq162 · DOI
  23. Ravelli, 1999, Obesity at the age of 50 y in men and women exposed to famine prenatally, Am J Clin Nutr, 70, 811, 10.1093/ajcn/70.5.811 · DOI
  24. Ravelli, 1998, Glucose tolerance in adults after prenatal exposure to famine, Lancet, 351, 173, 10.1016/S0140-6736(97)07244-9 · DOI · Paper page
  25. Gluckman, 2004, Developmental origins of disease paradigm: a mechanistic and evolutionary perspective, Pediatr Res, 56, 311, 10.1203/01.PDR.0000135998.08025.FB · DOI · Paper page
  26. Armitage, 2005, Experimental models of developmental programming: consequences of exposure to an energy rich diet during development, J Physiol, 565, 3, 10.1113/jphysiol.2004.079756 · DOI
  27. J P Barker, 2011, How boys grow determines how long they live, Am J Hum Biol, 23, 412, 10.1002/ajhb.21165 · DOI
  28. Barker, 2002, Fetal origins of adult disease: strength of effects and biological basis, Int J Epidemiol, 31, 1235, 10.1093/ije/31.6.1235 · DOI · Paper page
  29. Kwong, 2000, Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension, Development, 127, 4195, 10.1242/dev.127.19.4195 · DOI
  30. Lecoutre, 2015, Maternal nutritional manipulations program adipose tissue dysfunction in offspring, Front Physiol, 6158
  31. Symonds, 2003, Endocrine and nutritional regulation of fetal adipose tissue development, J Endocrinol, 179, 293, 10.1677/joe.0.1790293 · DOI
  32. Gardner, 2005, Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition, Am J Physiol Regul Integr Comp Physiol, 289, R947, 10.1152/ajpregu.00120.2005 · DOI
  33. Todd, 2009, Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring, Pediatr Res, 65, 409, 10.1203/PDR.0b013e3181975efa · DOI
  34. Long, 2013, Maternal nutrient restriction in the ewe from early to midgestation programs reduced steroidogenic enzyme expression and tended to reduce progesterone content of corpora lutea, as well as circulating progesterone in nonpregnant aged female offspring, Reprod Biol Endocrinol, 11, 34, 10.1186/1477-7827-11-34 · DOI
  35. Long, 2010, The effect of early to mid-gestational nutrient restriction on female offspring fertility and hypothalamic-pituitary-adrenal axis response to stress, J Anim Sci, 88, 2029, 10.2527/jas.2009-2568 · DOI
  36. Flegal, 2010, Prevalence and trends in obesity among US adults, 1999–2008, JAMA, 303, 235, 10.1001/jama.2009.2014 · DOI · Paper page
  37. Catalano, 2006, The short- and long-term implications of maternal obesity on the mother and her offspring, BJOG, 113, 1126, 10.1111/j.1471-0528.2006.00989.x · DOI
  38. Armitage, 2004, Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?, J Physiol, 561, 355, 10.1113/jphysiol.2004.072009 · DOI
  39. Palatianou, 2014, Long-term metabolic effects of high birth weight: a critical review of the literature, Horm Metab Res, 46, 911, 10.1055/s-0034-1395561 · DOI
  40. Alfaradhi, 2011, Developmental programming in response to maternal overnutrition, Front Genet, 2, 27, 10.3389/fgene.2011.00027 · DOI
  41. Vickers, 2012, Strategies for reversing the effects of metabolic disorders induced as a consequence of developmental programming, Front Physiol, 3, 242, 10.3389/fphys.2012.00242 · DOI
  42. Fisher, 2013, Is obesity still increasing among pregnant women? Prepregnancy obesity trends in 20 states, 2003–2009, Prev Med, 56, 372, 10.1016/j.ypmed.2013.02.015 · DOI
  43. Lake, 1997, Child to adult body mass index in the 1958 British birth cohort: associations with parental obesity, Arch Dis Child, 77, 376, 10.1136/adc.77.5.376 · DOI
  44. Laitinen, 2001, Family social class, maternal body mass index, childhood body mass index, and age at menarche as predictors of adult obesity, Am J Clin Nutr, 74, 287, 10.1093/ajcn/74.3.287 · DOI
  45. O'Reilly, 2013, The risk of maternal obesity to the long-term health of the offspring, Clin Endocrinol, 78, 9, 10.1111/cen.12055 · DOI
  46. Paliy, 2014, Excess body weight during pregnancy and offspring obesity: potential mechanisms, Nutrition, 30, 245, 10.1016/j.nut.2013.05.011 · DOI
  47. Lau, 2014, Maternal weight gain in pregnancy and risk of obesity among offspring: a systematic review, J Obes, 2014
  48. Kral, 2006, Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years, Pediatrics, 118, e1644, 10.1542/peds.2006-1379 · DOI
  49. Villamor, 2006, Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study, Lancet, 368, 1164, 10.1016/S0140-6736(06)69473-7 · DOI · Paper page
  50. Ainge, 2011, A systematic review on animal models of maternal high fat feeding and offspring glycaemic control, Int J Obes, 35, 325, 10.1038/ijo.2010.149 · DOI
  51. Long, 2010, Maternal obesity and increased nutrient intake before and during gestation in the ewe results in altered growth, adiposity, and glucose tolerance in adult offspring, J Anim Sci, 88, 3546, 10.2527/jas.2010-3083 · DOI
  52. McCurdy, 2009, Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates, J Clin Invest, 119, 323
  53. Sullivan, 2010, Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring, J Neurosci, 30, 3826, 10.1523/JNEUROSCI.5560-09.2010 · DOI
  54. Rattanatray, 2010, Impact of maternal periconceptional overnutrition on fat mass and expression of adipogenic and lipogenic genes in visceral and subcutaneous fat depots in the postnatal lamb, Endocrinology, 151, 5195, 10.1210/en.2010-0501 · DOI
  55. Giraudo, 2010, Maternal high fat feeding and gestational dietary restriction: effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice, Pharmacol Biochem Behav, 97, 121, 10.1016/j.pbb.2010.04.017 · DOI
  56. Dunkel Schetter, 2011, Psychological science on pregnancy: stress processes, biopsychosocial models, and emerging research issues, Annu Rev Psychol, 62, 531, 10.1146/annurev.psych.031809.130727 · DOI
  57. Li, 2010, Prenatal stress exposure related to maternal bereavement and risk of childhood overweight, PLoS One, 5, e11896, 10.1371/journal.pone.0011896 · DOI
  58. Dixon, 2012, Lifecourse approach to racial/ethnic disparities in childhood obesity, Adv Nutr, 3, 73, 10.3945/an.111.000919 · DOI · Paper page
  59. Harville, 2010, Disasters and perinatal health: a systematic review, Obstet Gynecol Surv, 65, 713, 10.1097/OGX.0b013e31820eddbe · DOI
  60. Vaiserman, 2015, Epigenetic programming by early-life stress: evidence from human populations, Dev Dyn, 244, 254, 10.1002/dvdy.24211 · DOI
  61. Keinan-Boker, 2015, Chronic health conditions in Jewish Holocaust survivors born during World War II, Isr Med Assoc J, 17, 206
  62. Beijers, 2014, Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis, Eur Child Adolesc Psychiatry, 23, 943, 10.1007/s00787-014-0566-3 · DOI
  63. Moisiadis, 2014, Glucocorticoids and fetal programming part 1: outcomes, Nat Rev Endocrinol, 10, 391, 10.1038/nrendo.2014.73 · DOI
  64. Entringer, 2013, Impact of stress and stress physiology during pregnancy on child metabolic function and obesity risk, Curr Opin Clin Nutr Metab Care, 16, 320, 10.1097/MCO.0b013e32835e8d80 · DOI
  65. Weinstock, 1997, Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis?, Neurosci Biobehav Rev, 21, 1, 10.1016/S0149-7634(96)00014-0 · DOI
  66. Huizink, 2004, Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?, Psychol Bull, 130, 115, 10.1037/0033-2909.130.1.115 · DOI · Paper page
  67. Welberg, 2001, Prenatal stress, glucocorticoids and the programming of the brain, J Neuroendocrinol, 13, 113, 10.1111/j.1365-2826.2001.00601.x · DOI · Paper page
  68. Veru, 2014, Prenatal maternal stress exposure and immune function in the offspring, Stress, 17, 133, 10.3109/10253890.2013.876404 · DOI
  69. Constantinof, Programming of stress pathways: a transgenerational perspective [published online ahead of print October 22, 2015], J Steroid Biochem Mol Biol
  70. Fowden, 2004, Endocrine mechanisms of intrauterine programming, Reproduction, 127, 515, 10.1530/rep.1.00033 · DOI
  71. Barnes, 1994, Ovarian hyperandrogynism as a result of congenital adrenal virilizing disorders: evidence for perinatal masculinization of neuroendocrine function in women, J Clin Endocrinol Metab, 79, 1328
  72. Silverman, 1993, Fetal hyperinsulinism in offspring of diabetic mothers. Association with the subsequent development of childhood obesity, Ann NY Acad Sci, 699, 36, 10.1111/j.1749-6632.1993.tb18835.x · DOI
  73. Steegers, 2010, Pre-eclampsia, Lancet, 376, 631, 10.1016/S0140-6736(10)60279-6 · DOI · Paper page
  74. Bar-Lev, 2012, Genetics of adrenocortical disease: an update, Curr Opin Endocrinol Diabetes Obes, 19, 159, 10.1097/MED.0b013e328352f013 · DOI
  75. Chen, 2010, Sex hormone-binding globulin genetic variation: associations with type 2 diabetes mellitus and polycystic ovary syndrome, Minerva Endocrinol, 35, 271
  76. Tempfer, 2004, Applications of polymorphisms and pharmacogenomics in obstetrics and gynecology, Pharmacogenomics, 5, 57, 10.1517/phgs.5.1.57.25687 · DOI
  77. Davis, 2012, Pre-eclampsia and offspring cardiovascular health: mechanistic insights from experimental studies, Clin Sci (Lond), 123, 53, 10.1042/CS20110627 · DOI
  78. Dumesic, 2014, Intrauterine environment and polycystic ovary syndrome, Semin Reprod Med, 32, 159, 10.1055/s-0034-1371087 · DOI
  79. Sir-Petermann, 2007, Early metabolic derangements in daughters of women with polycystic ovary syndrome, J Clin Endocrinol Metab, 92, 4637, 10.1210/jc.2007-1036 · DOI
  80. Aerts, 2006, Animal evidence for the transgenerational development of diabetes mellitus, Int J Biochem Cell Biol, 38, 894, 10.1016/j.biocel.2005.07.006 · DOI
  81. Padmanabhan, 2013, Animal models of the polycystic ovary syndrome phenotype, Steroids, 78, 734, 10.1016/j.steroids.2013.05.004 · DOI
  82. Cardoso, 2015, Steroidogenic versus metabolic programming of reproductive neuroendocrine, ovarian and metabolic dysfunctions, Neuroendocrinology, 102, 226, 10.1159/000381830 · DOI
  83. Heerwagen, 2010, Maternal obesity and fetal metabolic programming: a fertile epigenetic soil, Am J Physiol Regul Integr Comp Physiol, 299, R711, 10.1152/ajpregu.00310.2010 · DOI
  84. Poston, 2010, Developmental programming and diabetes - The human experience and insight from animal models, Best Pract Res Clin Endocrinol Metab, 24, 541, 10.1016/j.beem.2010.05.007 · DOI
  85. Berends, 2012, Early determinants of type-2 diabetes, Best Pract Res Clin Endocrinol Metab, 26, 569, 10.1016/j.beem.2012.03.002 · DOI
  86. Capra, 2013, The origins of health and disease: the influence of maternal diseases and lifestyle during gestation, Ital J Pediatr, 39, 7, 10.1186/1824-7288-39-7 · DOI
  87. Davis, 2014, 2014 consensus statement from the first Economics of Physical Inactivity Consensus (EPIC) conference (Vancouver), Br J Sports Med, 48, 947, 10.1136/bjsports-2014-093575 · DOI
  88. Owen, 2010, Sedentary behavior: emerging evidence for a new health risk, Mayo Clin Proc, 85, 1138, 10.4065/mcp.2010.0444 · DOI · Paper page
  89. Barnes, 2012, Obesity and sedentary lifestyles: risk for cardiovascular disease in women, Tex Heart Inst J, 39, 224
  90. Thorp, 2010, Deleterious associations of sitting time and television viewing time with cardiometabolic risk biomarkers: Australian Diabetes, Obesity and Lifestyle (AusDiab) study 2004–2005, Diabetes Care, 33, 327, 10.2337/dc09-0493 · DOI
  91. Mourtakos, 2015, Maternal lifestyle characteristics during pregnancy, and the risk of obesity in the offspring: a study of 5,125 children, BMC Pregnancy Childbirth, 15, 66, 10.1186/s12884-015-0498-z · DOI
  92. Mathias, 2014, Maternal diet, bioactive molecules, and exercising as reprogramming tools of metabolic programming, Eur J Nutr, 53, 711, 10.1007/s00394-014-0654-7 · DOI
  93. Ross, 2015, Developmental consequences of fetal exposure to drugs: what we know and what we still must learn, Neuropsychopharmacology, 40, 61, 10.1038/npp.2014.147 · DOI
  94. Ting, 2006, The effect of acute, chronic, and prenatal ethanol exposure on insulin sensitivity, Pharmacol Ther, 111, 346, 10.1016/j.pharmthera.2005.10.004 · DOI
  95. De Rycke, 2002, Epigenetic risks related to assisted reproductive technologies: risk analysis and epigenetic inheritance, Hum Reprod, 17, 2487, 10.1093/humrep/17.10.2487 · DOI
  96. De Geyter, 2006, Comparative birth weights of singletons born after assisted reproduction and natural conception in previously infertile women, Hum Reprod, 21, 705, 10.1093/humrep/dei378 · DOI
  97. Romundstad, 2008, Effects of technology or maternal factors on perinatal outcome after assisted fertilisation: a population-based cohort study, Lancet, 372, 737, 10.1016/S0140-6736(08)61041-7 · DOI
  98. Dahlen, 2013, The EPIIC hypothesis: intrapartum effects on the neonatal epigenome and consequent health outcomes, Med Hypotheses, 80, 656, 10.1016/j.mehy.2013.01.017 · DOI
  99. Bahrke, 1998, Anabolic-androgenic steroid abuse and performance-enhancing drugs among adolescents, Child Adolesc Psychiatr Clin N Am, 7, 821, 10.1016/S1056-4993(18)30214-1 · DOI
  100. Smithells, 1981, Oral contraceptives and birth defects, Dev Med Child Neurol, 23, 369, 10.1111/j.1469-8749.1981.tb02469.x · DOI
  101. Barbour, 2014, Unresolved controversies in gestational diabetes: implications on maternal and infant health, Curr Opin Endocrinol Diabetes Obes, 21, 264, 10.1097/MED.0000000000000080 · DOI
  102. Schneider, 2011, The effects of prenatal alcohol exposure on behavior: rodent and primate studies, Neuropsychol Rev, 21, 186, 10.1007/s11065-011-9168-8 · DOI
  103. Sjöblom, 2005, Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis, Endocrinology, 146, 2142, 10.1210/en.2004-1260 · DOI
  104. Zambrano, 2013, Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies, Nutr Rev, 71, S42, 10.1111/nure.12068 · DOI
  105. Nathanielsz, 2013, Interventions to prevent adverse fetal programming due to maternal obesity during pregnancy, Nutr Rev, 71, S78, 10.1111/nure.12062 · DOI
  106. Koletzko, 2014, The Power of Programming and the EarlyNutrition project: opportunities for health promotion by nutrition during the first thousand days of life and beyond, Ann Nutr Metab, 64, 187, 10.1159/000365017 · DOI
  107. Barua, 2015, Lifestyle, pregnancy and epigenetic effects, Epigenomics, 7, 85, 10.2217/epi.14.71 · DOI
  108. Diamanti-Kandarakis, 2009, Endocrine-disrupting chemicals: an Endocrine Society scientific statement, Endocr Rev, 30, 293, 10.1210/er.2009-0002 · DOI · Paper page
  109. Gore, 2015, EDC-2: The Endocrine Society's Second Scientific Statement on Endocrine-Disrupting Chemicals, Endocr Rev, 36, E1, 10.1210/er.2015-1010 · DOI · Paper page
  110. Kabir, 2015, A review on endocrine disruptors and their possible impacts on human health, Environ Toxicol Pharmacol, 40, 241, 10.1016/j.etap.2015.06.009 · DOI · Paper page
  111. Masuda, 1978, Transfer of polychlorinated biphenyls from mothers to foetuses and infants, Food Cosmet Toxicol, 16, 543, 10.1016/S0015-6264(78)80221-1 · DOI
  112. Ando, 1985, Transfer of polychlorinated biphenyls (PCBs) to newborn infants through the placenta and mothers' milk, Arch Environ Contam Toxicol, 14, 51, 10.1007/BF01055761 · DOI
  113. Woodruff, 2011, Bridging epidemiology and model organisms to increase understanding of endocrine disrupting chemicals and human health effects, J Steroid Biochem Mol Biol, 127, 108, 10.1016/j.jsbmb.2010.11.007 · DOI
  114. Harada, 1995, Minamata disease: methylmercury poisoning in Japan caused by environmental pollution, Crit Rev Toxicol, 25, 1, 10.3109/10408449509089885 · DOI
  115. Guo, 2004, Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans, Int Arch Occup Environ Health, 77, 153, 10.1007/s00420-003-0487-9 · DOI
  116. Chevalier, 2015, Endocrine disruptors: new players in the pathophysiology of type 2 diabetes?, Diabetes Metab, 41, 107, 10.1016/j.diabet.2014.09.005 · DOI
  117. Vom Saal, 2012, The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity, Mol Cell Endocrinol, 354, 74, 10.1016/j.mce.2012.01.001 · DOI
  118. Lesage, 2002, Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels, J Endocrinol, 174, 37, 10.1677/joe.0.1740037 · DOI
  119. Veiga-Lopez, 2011, Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep, Biol Reprod, 84, 87, 10.1095/biolreprod.110.086686 · DOI
  120. Beckett, 2014, Developmental programing: impact of testosterone on placental differentiation, Reproduction, 148, 199, 10.1530/REP-14-0055 · DOI
  121. Welberg, 2005, Chronic maternal stress inhibits the capacity to up-regulate placental 11β-hydroxysteroid dehydrogenase type 2 activity, J Endocrinol, 186, R7, 10.1677/joe.1.06374 · DOI
  122. Mairesse, 2007, Maternal stress alters endocrine function of the feto-placental unit in rats, Am J Physiol Endocrinol Metab, 292, E1526, 10.1152/ajpendo.00574.2006 · DOI · Paper page
  123. Lesage, 2004, Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat, J Endocrinol, 181, 291, 10.1677/joe.0.1810291 · DOI
  124. Vogt Isaksen, 2004, Maternal smoking, intrauterine growth restriction, and placental apoptosis, Pediatr Dev Pathol, 7, 433, 10.1007/s10024-004-0105-1 · DOI
  125. Padmanabhan, 2010, Developmental programming: impact of prenatal testosterone excess and postnatal weight gain on insulin sensitivity index and transfer of traits to offspring of overweight females, Endocrinology, 151, 595, 10.1210/en.2009-1015 · DOI
  126. Cardoso, 2016, Developmental programming: impact of gestational steroid and metabolic milieus on adiposity and insulin sensitivity in prenatal testosterone-treated female sheep, Endocrinology, 157, 522, 10.1210/en.2015-1565 · DOI
  127. Gorski, 2006, Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance, Am J Physiol Regul Integr Comp Physiol, 291, R768, 10.1152/ajpregu.00138.2006 · DOI
  128. Bouret, 2004, Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice, J Neurosci, 24, 2797, 10.1523/JNEUROSCI.5369-03.2004 · DOI
  129. Nakae, 2001, Distinct and overlapping functions of insulin and IGF-I receptors, Endocr Rev, 22, 818, 10.1210/edrv.22.6.0452 · DOI
  130. Forhead, 2009, The hungry fetus? Role of leptin as a nutritional signal before birth, J Physiol, 587, 1145, 10.1113/jphysiol.2008.167072 · DOI
  131. Wood, 2014, Estrogen in the fetus, 217, 10.1007/978-1-4939-1031-1_19 · DOI
  132. Bondesson, 2015, Estrogen receptor signaling during vertebrate development, Biochim Biophys Acta, 1849, 142, 10.1016/j.bbagrm.2014.06.005 · DOI
  133. Fowden, 2003, The insulin-like growth factors and feto-placental growth, Placenta, 24, 803, 10.1016/S0143-4004(03)00080-8 · DOI
  134. Bispham, 2003, Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development, Endocrinology, 144, 3575, 10.1210/en.2003-0320 · DOI · Paper page
  135. Holemans, 2004, Diet-induced obesity in the rat: a model for gestational diabetes mellitus, Am J Obstet Gynecol, 190, 858, 10.1016/j.ajog.2003.09.025 · DOI
  136. Abi Salloum, 2015, Developmental programming: exposure to testosterone excess disrupts steroidal and metabolic environment in pregnant sheep, Endocrinology, 156, 2323, 10.1210/en.2014-2006 · DOI
  137. Whyte, 2007, Maternal diet composition alters serum steroid and free fatty acid concentrations and vaginal pH in mice, J Endocrinol, 192, 75, 10.1677/JOE-06-0095 · DOI
  138. Takahashi, 1998, Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies, Psychoneuroendocrinology, 23, 571, 10.1016/S0306-4530(98)00024-9 · DOI
  139. Barrett, 2015, Stress and androgen activity during fetal development, Endocrinology, 156, 3435, 10.1210/en.2015-1335 · DOI
  140. Pasquali, 2006, Insulin-sensitizing agents in polycystic ovary syndrome, European J Endocrinol, 154, 763, 10.1530/eje.1.02156 · DOI
  141. Zulian, 2005, Spironolactone in the treatment of polycystic ovary syndrome: effects on clinical features, insulin sensitivity and lipid profile, J Endocrinol Invest, 28, 49, 10.1007/BF03345529 · DOI
  142. Ganie, 2013, Improved efficacy of low-dose spironolactone and metformin combination than either drug alone in the management of women with polycystic ovary syndrome (PCOS): a six-month, open-label randomized study, J Clin Endocrinol Metab, 98, 3599, 10.1210/jc.2013-1040 · DOI
  143. Coviello, 2006, Adolescent girls with polycystic ovary syndrome have an increased risk of the metabolic syndrome associated with increasing androgen levels independent of obesity and insulin resistance, J Clin Endocrinol Metab, 91, 492, 10.1210/jc.2005-1666 · DOI
  144. Corbould, 2008, Effects of androgens on insulin action in women: is androgen excess a component of female metabolic syndrome?, Diabetes Metab Res Rev, 24, 520, 10.1002/dmrr.872 · DOI
  145. Ji, 2016, Nutritional epigenetics with a focus on amino acids: implications for the development and treatment of metabolic syndrome, J Nutr Biochem, 27, 1, 10.1016/j.jnutbio.2015.08.003 · DOI
  146. Mennitti, 2015, Type of fatty acids in maternal diets during pregnancy and/or lactation and metabolic consequences of the offspring, J Nutr Biochem, 26, 99, 10.1016/j.jnutbio.2014.10.001 · DOI
  147. Valko, 2007, Free radicals and antioxidants in normal physiological functions and human disease, Int J Biochem Cell Biol, 39, 44, 10.1016/j.biocel.2006.07.001 · DOI · Paper page
  148. Luo, 2006, Tracing the origins of “fetal origins” of adult diseases: programming by oxidative stress?, Med Hypotheses, 66, 38, 10.1016/j.mehy.2005.08.020 · DOI
  149. Radaelli, 2003, Gestational diabetes induces placental genes for chronic stress and inflammatory pathways, Diabetes, 52, 2951, 10.2337/diabetes.52.12.2951 · DOI · Paper page
  150. Yan, 2010, Up-regulation of Toll-like receptor 4/nuclear factor-κB signaling is associated with enhanced adipogenesis and insulin resistance in fetal skeletal muscle of obese sheep at late gestation, Endocrinology, 151, 380, 10.1210/en.2009-0849 · DOI
  151. Bruce, 2009, Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression, Hepatology, 50, 1796, 10.1002/hep.23205 · DOI · Paper page
  152. Neier, 2015, Assessing human health risk to endocrine disrupting chemicals: a focus on prenatal exposures and oxidative stress, Endocr Disruptors, 3, e1069916, 10.1080/23273747.2015.1069916 · DOI
  153. Sen, 2010, Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats, Diabetes, 59, 3058, 10.2337/db10-0301 · DOI
  154. Godfrey, 2007, Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease, Pediatr Res, 61, 5R, 10.1203/pdr.0b013e318045bedb · DOI
  155. Lane, 2014, Fetal programming, epigenetics, and adult onset disease, Clin Perinatol, 41, 815, 10.1016/j.clp.2014.08.006 · DOI
  156. Perera, 2011, Prenatal environmental exposures, epigenetics, and disease, Reprod Toxicol, 31, 363, 10.1016/j.reprotox.2010.12.055 · DOI
  157. Bouchard, 2010, Leptin gene epigenetic adaptation to impaired glucose metabolism during pregnancy, Diabetes Care, 33, 2436, 10.2337/dc10-1024 · DOI
  158. Xu, 2014, Early embryonic androgen exposure induces transgenerational epigenetic and metabolic changes, Mol Endocrinol, 28, 1329, 10.1210/me.2014-1042 · DOI
  159. Stel, 2015, The role of epigenetics in the latent effects of early life exposure to obesogenic endocrine disrupting chemicals, Endocrinology, 156, 3466, 10.1210/en.2015-1434 · DOI
  160. Bell, 2016, Two-hit exposure to polychlorinated biphenyls at gestational and juvenile life stages: 2. Sex-specific neuromolecular effects in the brain, Mol Cell Endocrinol, 420, 125, 10.1016/j.mce.2015.11.024 · DOI
  161. Bayer, 1999, Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the “two hit hypothesis.”, J Psychiatr Res, 33, 543, 10.1016/S0022-3956(99)00039-4 · DOI · Paper page
  162. Abbott, 2013, Nonhuman primate models of polycystic ovary syndrome, Mol Cell Endocrinol, 373, 21, 10.1016/j.mce.2013.01.013 · DOI
  163. Padmanabhan, 2013, Sheep models of polycystic ovary syndrome phenotype, Mol Cell Endocrinol, 373, 8, 10.1016/j.mce.2012.10.005 · DOI
  164. Crews, 2007, Transgenerational epigenetic imprints on mate preference, Proc Natl Acad Sci USA, 104, 5942, 10.1073/pnas.0610410104 · DOI · Paper page
  165. Xin, 2015, Multigenerational and transgenerational effects of endocrine disrupting chemicals: a role for altered epigenetic regulation?, Semin Cell Dev Biol, 43, 66, 10.1016/j.semcdb.2015.05.008 · DOI
  166. Walker, 2011, Transgenerational neuroendocrine disruption of reproduction, Nat Rev Endocrinol, 7, 197, 10.1038/nrendo.2010.215 · DOI
  167. Painter, 2008, Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life, BJOG, 115, 1243, 10.1111/j.1471-0528.2008.01822.x · DOI · Paper page
  168. Skinner, 2008, What is an epigenetic transgenerational phenotype? F3 or F2, Reprod Toxicol, 25, 2, 10.1016/j.reprotox.2007.09.001 · DOI · Paper page
  169. Curley, 2011, Epigenetics and the origins of paternal effects, Horm Behav, 59, 306, 10.1016/j.yhbeh.2010.06.018 · DOI
  170. Pembrey, 2010, Male-line transgenerational responses in humans, Hum Fertil (Camb), 13, 268, 10.3109/14647273.2010.524721 · DOI
  171. Kaplan, 2011, The role of microbes in developmental immunologic programming, Pediatr Res, 69, 465, 10.1203/PDR.0b013e318217638a · DOI
  172. Manco, 2012, Gut microbiota and developmental programming of the brain: from evidence in behavioral endophenotypes to novel perspective in obesity, Front Cell Infect Microbiol, 2, 109, 10.3389/fcimb.2012.00109 · DOI
  173. Thompson, 2012, Developmental origins of obesity: early feeding environments, infant growth, and the intestinal microbiome, Am J Hum Biol, 24, 350, 10.1002/ajhb.22254 · DOI
  174. Ibáñez, 2003, Low-dose combination of flutamide, metformin and an oral contraceptive for non-obese, young women with polycystic ovary syndrome, Hum Reprod, 18, 57, 10.1093/humrep/deg056 · DOI

Cited by

Sorted by citations

See all 208

Metadata

Authors
Padmanabhan, V., Cardoso, R. C., & Puttabyatappa, M.
Affiliations
Department of Pediatrics, University of Michigan, Ann Arbor, Michigan 48109–5718
Venue
Endocrinology
Publisher
The Endocrine Society
Published
2016-02-09
Volume
157
Issue
4
Pages
1328-1340
ISSN
  • 0013-7227
  • 1945-7170
DOI
10.1210/en.2016-1003
Cited by
208
References
26
Language
en

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