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Cited by 451Effects and risks of endocrine disrupting chemicalsToxic Organic Pollutants ImpactAdipokines, Inflammation, and Metabolic Diseases

The DOI matches its Crossref record; 13 of the 13 references it cites were found in a registry or an index.

Endocrine disruptors and obesity

Heindel, Jerrold J., Newbold, Retha, Schug, Thaddeus T.·2015·Nature Reviews Endocrinology
DOI 10.1038/nrendo.2015.163
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Abstract

The increasing incidence of obesity is a serious global public health challenge. Although the obesity epidemic is largely fueled by poor nutrition and lack of exercise, certain chemicals have been shown to potentially have a role in its aetiology. A substantial body of evidence suggests that a subclass of endocrine-disrupting chemicals (EDCs), which interfere with endocrine signalling, can disrupt hormonally regulated metabolic processes, especially if exposure occurs during early development. These chemicals, so-called 'obesogens' might predispose some individuals to gain weight despite their efforts to limit caloric intake and increase levels of physical activity. This Review discusses the role of EDCs in the obesity epidemic, the latest research on the obesogen concept, epidemiological and experimental findings on obesogens, and their modes of action. The research reviewed here provides knowledge that health scientists can use to inform their research and decision-making processes.

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  • Additional evidence indicates other possible causes and contributors to obesity, including genetic, epigenetic, foodborne, sleep deprivation and circadian dysrhythmia, psychological stress, endocrine disruptors, medications, and intrauterine and intergenerational effects.

    “Additional evidence is now also available indicating other possible causes and contributors to obesity, including genetic84 and epigenetic factors85, foodborne factors86, sleep deprivation and circadian dysrhythmia87, psychological stress, endocrine disruptors, medications, and intrauterine and intergenerational effects.”

    From Joint international consensus statement for ending stigma of obesity (2020) · cites this paper as [85]

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Research works printed but not linked: 126

  1. Hebert, J. R., Allison, D. B., Archer, E., Lavie, C. J. & Blair, S. N. Scientific decision making, policy decisions, and the obesity pandemic. Mayo Clin. Proc. 88, 593–604 (2013). · DOI
  2. Pulgaron, E. R. & Delamater, A. M. Obesity and type 2 diabetes in children: epidemiology and treatment. Curr. Diab. Rep. 14, 508 (2014). · DOI
  3. Sturm, R. The effects of obesity, smoking, and drinking on medical problems and costs. Health Aff. (Millwood) 21, 245–253 (2002). · DOI
  4. Calkins, K. & Devaskar, S. U. Fetal origins of adult disease. Curr. Probl. Pediatr. Adolesc. Health Care 41, 158–176 (2011). · DOI · Paper page
  5. Das, U. N. Obesity: genes, brain, gut, and environment. Nutrition 26, 459–473 (2010). · DOI
  6. Maric, G. et al. The role of gut hormones in appetite regulation (review). Acta Physiol. Hung. 101, 395–407 (2014). · DOI
  7. Lanthier, N. & Leclercq, I. A. Adipose tissues as endocrine target organs. Best Pract. Res. Clin. Gastroenterol. 28, 545–558 (2014). · DOI
  8. Sohn, J. W. Network of hypothalamic neurons that control appetite. BMB Rep. 48, 229–233 (2015). · DOI
  9. Barker, D. J., Winter, P. D., Osmond, C., Margetts, B. & Simmonds, S. J. Weight in infancy and death from ischaemic heart disease. Lancet 2, 577–580 (1989). · DOI · Paper page
  10. Diamanti-Kandarakis, E. et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. 30, 293–342 (2009). · DOI · Paper page
  11. Casals-Casas, C. & Desvergne, B. Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 73, 135–162 (2011). · DOI · Paper page
  12. Baillie-Hamilton, P. F. Chemical toxins: a hypothesis to explain the global obesity epidemic. J. Altern Complement. Med. 8, 185–192 (2002). · DOI
  13. Zoeller, R. T. et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 153, 4097–5110 (2012). · DOI
  14. Regnier, S. M. & Sargis, R. M. Adipocytes under assault: environmental disruption of adipose physiology. Biochim. Biophys. Acta 1842, 520–533 (2014). · DOI
  15. Grün, F. & Blumberg, B. Endocrine disrupters as obesogens. Mol. Cell. Endocrinol. 304, 19–29 (2009). · DOI
  16. Heindel, J. J. et al. Parma consensus statement on metabolic disruptors. Environ. Health 14, 54 (2015). · DOI
  17. Newbold, R. R. Developmental exposure to endocrine-disrupting chemicals programs for reproductive tract alterations and obesity later in life. Am. J. Clin. Nutr. 94, 1939S–1942S (2011). · DOI
  18. Janesick, A. & Blumberg, B. Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity. Birth Defects Res. C Embryo Today 93, 34–50 (2011). · DOI
  19. Barouki, R., Gluckman, P. D., Grandjean, P., Hanson, M. & Heindel, J. J. Developmental origins of non-communicable disease: implications for research and public health. Environ. Health 11, 42 (2012). · DOI
  20. Gluckman, P. D. & Hanson, M. A. Living with the past: evolution, development, and patterns of disease. Science 305, 1733–1736 (2004). · DOI
  21. Gluckman, P. D., Hanson, M. A., Beedle, A. S. & Raubenheimer, D. Fetal and neonatal pathways to obesity. Front. Horm. Res. 36, 61–72 (2008). · DOI
  22. Kirchner, S., Kieu, T., Chow, C., Casey, S. & Blumberg, B. Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Mol. Endocrinol. 24, 526–539 (2010). · DOI
  23. Pittenger, M. F. et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143–147 (1999). · DOI · Paper page
  24. Vaiserman, A. Early-life exposure to endocrine disrupting chemicals and later-life health outcomes: an epigenetic bridge? Aging Dis. 5, 419–429 (2014).
  25. Adriani, W., Seta, D. D., Dessi-Fulgheri, F., Farabollini, F. & Laviola, G. Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to D-amphetamine in rats perinatally exposed to bisphenol A. Environ. Health Perspect. 111, 395–401 (2003). · DOI
  26. Bernal, A. J. & Jirtle, R. L. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res. A Clin. Mol. Teratol. 88, 938–944 (2010). · DOI
  27. Skinner, M. K., Manikkam, M. & Guerrero-Bosagna, C. Epigenetic transgenerational actions of endocrine disruptors. Reprod. Toxicol. 31, 337–343 (2011). · DOI
  28. Desai, M., Jellyman, J. K. & Ross, M. G. Epigenomics, gestational programming and risk of metabolic syndrome. Int. J. Obes. (Lond.) 39, 633–641 (2015). · DOI
  29. Murphy, S. K. & Jirtle, R. L. Imprinting evolution and the price of silence. Bioessays 25, 577–588 (2003). · DOI
  30. Colaneri, A. et al. A minimal set of tissue-specific hypomethylated CpGs constitute epigenetic signatures of developmental programming. PLoS ONE 8, e72670 (2013). · DOI
  31. Remely, M., de la Garza, A. L., Magnet, U., Aumueller, E. & Haslberger, A. G. Obesity: epigenetic regulation—recent observations. Biomol. Concepts 6, 163–175 (2015). · DOI
  32. Waterland, R. A. Epigenetic mechanisms affecting regulation of energy balance: many questions, few answers. Annu. Rev. Nutr. 34, 337–355 (2014). · DOI
  33. Grun, F. et al. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol. Endocrinol. 20, 2141–2155 (2006). · DOI
  34. Lane, R. H. Fetal programming, epigenetics, and adult onset disease. Clin. Perinatol. 41, 815–831 (2014). · DOI
  35. McGowan, P. O. & Roth, T. L. Epigenetic pathways through which experiences become linked with biology. Dev. Psychopathol. 27, 637–648 (2015). · DOI
  36. Chamorro-Garcia, R. & Blumberg, B. Transgenerational effects of obesogens and the obesity epidemic. Curr. Opin. Pharmacol. 19, 153–158 (2014). · DOI
  37. Thayer, K. A., Heindel, J. J., Bucher, J. R. & Gallo, M. A. Role of environmental chemicals in diabetes and obesity: a National Toxicology Program workshop review. Environ. Health Perspect. 120, 779–789 (2012). · DOI
  38. Kupfer, D. J., Coble, P. A. & Rubinstein, D. Changes in weight during treatment for depression. Psychosom. Med. 41, 535–544 (1979). · DOI
  39. Shim, W. S. et al. The long-term effects of rosiglitazone on serum lipid concentrations and body weight. Clin. Endocrinol. (Oxf.) 65, 453–459 (2006). · DOI
  40. Chamorro-Garcia, R. et al. Transgenerational inheritance of prenatal obesogen exposure Environ. Health Perspect. 121, 359–366 (2012). · DOI
  41. Oken, E., Levitan, E. B. & Gillman, M. W. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int. J. Obes. (Lond.) 32, 201–210 (2008). · DOI · Paper page
  42. Irigaray, P. et al. Benzo[a]pyrene impairs β-adrenergic stimulation of adipose tissue lipolysis and causes weight gain in mice. A novel molecular mechanism of toxicity for a common food pollutant. FEBS J. 273, 1362–1372 (2006). · DOI
  43. Backes, C. H., Nelin, T., Gorr, M. W. & Wold, L. E. Early life exposure to air pollution: how bad is it? Toxicol. Lett. 216, 47–53 (2013). · DOI
  44. Vadillo-Ortega, F. et al. Air pollution, inflammation and preterm birth: a potential mechanistic link. Med. Hypotheses 82, 219–224 (2014). · DOI · Paper page
  45. Rundle, A. et al. Association of childhood obesity with maternal exposure to ambient air polycyclic aromatic hydrocarbons during pregnancy. Am. J. Epidemiol. 175, 1163–1172 (2012). · DOI
  46. McConnell, R. et al. Does near-roadway air pollution contribute to childhood obesity? Pediatr. Obes. http://dx.doi.org/10.1111/ijpo.12016 (2015). · DOI
  47. Jerrett, M. et al. Traffic-related air pollution and obesity formation in children: a longitudinal, multilevel analysis. Environ. Health 13, 49 (2014). · DOI
  48. Bolton, J. L. et al. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J. 26, 4743–4754 (2012). · DOI
  49. Zheng, Z. et al. Exposure to ambient particulate matter induces a NASH-like phenotype and impairs hepatic glucose metabolism in an animal model. J. Hepatol. 58, 148–154 (2013). · DOI
  50. Sun, Q. et al. Ambient air pollution exaggerates adipose inflammation and insulin resistance in a mouse model of diet-induced obesity. Circulation 119, 538–546 (2009). · DOI
  51. Kannan, K., Senthilkumar, K. & Giesy, J. P. Occurrence of butyltin compounds in human blood. Environ. Sci. Technol. 33, 1776–1779 (1999). · DOI
  52. Kanayama, T., Kobayashi, N., Mamiya, S., Nakanishi, T. & Nishikawa, J. Organotin compounds promote adipocyte differentiation as agonists of the peroxisome proliferator-activated receptor γ/retinoid X receptor pathway. Mol. Pharmacol. 67, 766–774 (2005). · DOI
  53. Pereira-Fernandes, A. et al. Toxicogenomics in the 3T3-L1 cell line, a new approach for screening of obesogenic compounds. Toxicol. Sci. 140, 352–363 (2014). · DOI
  54. Inadera, H. Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals. Environ. Health Prev. Med. 18, 185–197 (2013). · DOI
  55. Watt, J. & Schlezinger, J. J. Structurally-diverse, PPARγ-activating environmental toxicants induce adipogenesis and suppress osteogenesis in bone marrow mesenchymal stromal cells. Toxicology 331, 66–77 (2015). · DOI
  56. Blumberg, B. Obesogens, stem cells and the maternal programming of obesity. J. Dev. Orig. Health Dis. 2, 3–8 (2011). · DOI
  57. Kirchner, S., Kieu, T., Chow, C., Casey, S. & Blumberg, B. Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Mol. Endocrinol. 24, 526–539 (2010). · DOI
  58. Grun, F. & Blumberg, B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signalling. Endocrinology 147, S50–S55 (2006). · DOI
  59. Chamorro-Garcia, R. et al. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ. Health Perspect. 121, 359–366 (2013). · DOI
  60. Zuo, Z. et al. Tributyltin causes obesity and hepatic steatosis in male mice. Environ. Toxicol. 26, 79–85 (2011). · DOI
  61. Vandenberg, L. N., Maffini, M. V., Sonnenschein, C., Rubin, B. S. & Soto, A. M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 30, 75–95 (2009). · DOI
  62. Oppeneer, S. J. & Robien, K. Bisphenol A exposure and associations with obesity among adults: a critical review. Public Health Nutr. 18, 1847–1863 (2015). · DOI
  63. Le Corre, L., Besnard, P. & Chagnon, M. C. BPA, an energy balance disruptor. Crit. Rev. Food Sci. Nutr. 55, 769–777 (2015). · DOI
  64. Mirmira, P. & Evans-Molina, C. Bisphenol A, obesity, and type 2 diabetes mellitus: genuine concern or unnecessary preoccupation? Transl Res. 164, 13–21 (2014). · DOI
  65. Lakind, J. S., Goodman, M. & Mattison, D. R. Bisphenol A and indicators of obesity, glucose metabolism/type 2 diabetes and cardiovascular disease: a systematic review of epidemiologic research. Crit. Rev. Toxicol. 44, 121–150 (2014). · DOI
  66. Li, D. K. et al. Urine bisphenol-A level in relation to obesity and overweight in school-age children. PLoS ONE 8, 1–6 (2013).
  67. Trasande, L., Attina, T. M. & Blustein, J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 308, 1113–1121 (2012). · DOI
  68. Harley, K. G. et al. Prenatal and early childhood bisphenol A concentrations and behavior in school-aged children. Environ. Res. 126, 43–50 (2013). · DOI
  69. Troisi, J. et al. Placental concentrations of bisphenol A and birth weight from births in the Southeastern U.S. Placenta 35, 947–952 (2014). · DOI · Paper page
  70. Miao, M., Yuan, W., Zhu, G., He, X. & Li, D. K. In utero exposure to bisphenol-A and its effect on birth weight of offspring. Reprod. Toxicol. 32, 64–68 (2011). · DOI
  71. Braun, J. M. et al. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ. Health Perspect. 119, 131–137 (2010). · DOI · Paper page
  72. Masuno, H. et al. Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. J. Lipid Res. 43, 676–684 (2002). · DOI
  73. Angle, B. M. et al. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod. Toxicol. 42, 256–268 (2013). · DOI
  74. Mackay, H. et al. Organizational effects of perinatal exposure to bisphenol-A and diethylstilbestrol on arcuate nucleus circuitry controlling food intake and energy expenditure in male and female CD-1 mice. Endocrinology 154, 1465–1475 (2013). · DOI
  75. Olea, N. et al. Estrogenicity of resin-based composites and sealants used in dentistry. Environ. Health Perspect. 104, 298–305 (1996). · DOI
  76. Rubin, B. S. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J. Steroid Biochem. Mol. Biol. 127, 27–34 (2011). · DOI
  77. Masuno, H., Iwanami, J., Kidani, T., Sakayama, K. & Honda, K. Bisphenol A accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. Toxicol. Sci. 84, 319–327 (2005). · DOI
  78. Chamorro-Garcia, R. et al. Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor γ-independent mechanism. Environ. Health Perspect. 120, 984–989 (2012). · DOI
  79. Anderson, O. S. et al. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J. 27, 1784–1792 (2013). · DOI
  80. Kendig, E. L. et al. Estrogen-like disruptive effects of dietary exposure to bisphenol A or 17α-ethinyl estradiol in CD1 mice. Int. J. Toxicol. 31, 537–550 (2012). · DOI
  81. Mirmira, P. & Evans-Molina, C. Bisphenol A, obesity, and type 2 diabetes mellitus: genuine concern or unnecessary preoccupation? Transl Res. 164, 13–21 (2014). · DOI
  82. Boucher, J. G., Boudreau, A., Ahmed, S. & Atlas, E. Effects of bisphenol A β-D-glucuronide (BPA-G) on adipogenesis in human and murine preadipocytes. Environ. Health Perspect. http://dx.doi.org/10.1289/ehp.1409143 (2015). · DOI
  83. Trasande, L. Further limiting bisphenol A in food uses could provide health and economic benefits. Health Aff. (Millwood) 33, 316–323 (2014). · DOI
  84. Legler, J. et al. Obesity, diabetes, and associated costs of exposure to endocrine-disrupting chemicals in the European Union. J. Clin. Endocrinol. Metab. 100, 1278–1288 (2015). · DOI
  85. Stapleton, H. M., Eagle, S., Sjodin, A. & Webster, T. F. Serum PBDEs in a North Carolina toddler cohort: associations with handwipes, house dust, and socioeconomic variables. Environ. Health Perspect. 120, 1049–1054 (2012). · DOI
  86. Schecter, A., Papke, O., Joseph, J. E. & Tung, K. C. Polybrominated diphenyl ethers (PBDEs) in U.S. computers and domestic carpet vacuuming: possible sources of human exposure. J. Toxicol. Environ. Health A 68, 501–513 (2005). · DOI
  87. Hallgren, S., Sinjari, T., Hakansson, H. & Darnerud, P. O. Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch. Toxicol. 75, 200–208 (2001). · DOI
  88. Hoppe, A. A. & Carey, G. B. Polybrominated diphenyl ethers as endocrine disruptors of adipocyte metabolism. Obesity (Silver Spring) 15, 2942–2950 (2007). · DOI
  89. van der Ven, L. T. et al. A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicol. Sci. 94, 281–292 (2006). · DOI
  90. van der Ven, L. T. et al. A 28-day oral dose toxicity study enhanced to detect endocrine effects of a purified technical pentabromodiphenyl ether (pentaBDE) mixture in Wistar rats. Toxicology 245, 109–122 (2008). · DOI
  91. Chao, H. R., Wang, S. L., Lee, W. J., Wang, Y. F. & Papke, O. Levels of polybrominated diphenyl ethers (PBDEs) in breast milk from central Taiwan and their relation to infant birth outcome and maternal menstruation effects. Environ. Int. 33, 239–245 (2007). · DOI
  92. Herbstman, J. B. et al. Birth delivery mode modifies the associations between prenatal polychlorinated biphenyl (PCB) and polybrominated diphenyl ether (PBDE) and neonatal thyroid hormone levels. Environ. Health Perspect. 116, 1376–1382 (2008). · DOI
  93. Legler, J. et al. The OBELIX project: early life exposure to endocrine disruptors and obesity. Am. J. Clin. Nutr. 94, 1933S–1938S (2011). · DOI
  94. Erkin-Cakmak, A. et al . In utero and childhood polybrominated diphenyl ether exposures and body mass at age 7 years: the CHAMACOS study. Environ. Health Perspect. 123, 636–642 (2015). · DOI
  95. Suvorov, A., Battista, M. C. & Takser, L. Perinatal exposure to low-dose 2,2′,4,4′-tetrabromodiphenyl ether affects growth in rat offspring: what is the role of IGF-1? Toxicology. 260, 126–131 (2009). · DOI
  96. Patisaul, H. B. et al. Accumulation and endocrine disrupting effects of the flame retardant mixture Firemaster® 550 in rats: an exploratory assessment. J. Biochem. Mol. Toxicol. 27, 124–136 (2013). · DOI
  97. Belcher, S. M., Cookman, C. J., Patisaul, H. B. & Stapleton, H. M. In vitro assessment of human nuclear hormone receptor activity and cytotoxicity of the flame retardant mixture FM 550 and its triarylphosphate and brominated components. Toxicol. Lett. 228, 93–102 (2014). · DOI
  98. Pillai, H. K. et al. Ligand binding and activation of PPARγ by Firemaster® 550: effects on adipogenesis and osteogenesis in vitro. Environ. Health Perspect. 122, 1225–1232 (2014). · DOI
  99. Bourez, S. et al. The dynamics of accumulation of PCBs in cultured adipocytes vary with the cell lipid content and the lipophilicity of the congener. Toxicol. Lett. 216, 40–46 (2013). · DOI
  100. Elobeid, M. A., Brock, D. W., Allison, D. B., Padilla, M. A. & Ruden, D. M. Endocrine disruptors and obesity: an examination of selected persistent organic pollutants in the NHANES 1999–2002 data. Int. J. Environ. Res. Public Health 7, 2988–3005 (2010). · DOI
  101. Cupul-Uicab, L. A., Klebanoff, M. A., Brock, J. W. & Longnecker, M. P. Prenatal exposure to persistent organochlorines and childhood obesity in the U.S. Collaborative Perinatal Project. Environ. Health Perspect. 121, 1103–1109 (2013). · DOI
  102. Tang-Peronard, J. L. et al. Association between prenatal polychlorinated biphenyl exposure and obesity development at ages 5 and 7 y: a prospective cohort study of 656 children from the Faroe Islands. Am. J. Clin. Nutr. 99, 5–13 (2014). · DOI
  103. Heudorf, U., Mersch-Sundermann, V. & Angerer, J. Phthalates: toxicology and exposure. Int. J. Hyg. Environ. Health 210, 623–634 (2007). · DOI
  104. Hannon, P. R. & Flaws, J. A. The effects of phthalates on the ovary. Front. Endocrinol. 6, 8 (2015). · DOI
  105. Cai, H. et al. Human urinary/seminal phthalates or their metabolite levels and semen quality: a meta-analysis. Environ. Res. 142, 486–494 (2015). · DOI
  106. Hao, C., Cheng, X., Guo, J., Xia, H. & Ma, X. Perinatal exposure to diethyl-hexyl-phthalate induces obesity in mice. Front. Biosci. (Elite Ed.) 5, 725–733 (2013). · DOI
  107. Hao, C., Cheng, X., Xia, H. & Ma, X. The endocrine disruptor mono-(2-ethylhexyl) phthalate promotes adipocyte differentiation and induces obesity in mice. Biosci. Rep. 32, 619–629 (2012). · DOI
  108. Schmidt, J. S., Schaedlich, K., Fiandanese, N., Pocar, P. & Fischer, B. Effects of di(2-ethylhexyl) phthalate (DEHP) on female fertility and adipogenesis in C3H/N. mice. Environ. Health Perspect. 120, 1123–1129 (2012). · DOI
  109. Biemann, R., Fischer, B. & Navarrete Santos, A. Adipogenic effects of a combination of the endocrine-disrupting compounds bisphenol A, diethylhexylphthalate, and tributyltin. Obes. Facts 7, 48–56 (2014). · DOI
  110. Feige, J. N. et al. The endocrine disruptor monoethyl-hexyl-phthalate is a selective peroxisome proliferator-activated receptor γ modulator that promotes adipogenesis. J. Biol. Chem. 282, 19152–19166 (2007). · DOI
  111. Hurst, C. H. & Waxman, D. J. Activation of PPARα and PPARγ by environmental phthalate monoesters. Toxicol. Sci. 74, 297–308 (2003). · DOI
  112. Biemann, R. et al. Endocrine disrupting chemicals affect the adipogenic differentiation of mesenchymal stem cells in distinct ontogenetic windows. Biochem. Biophys. Res. Commun. 417, 747–52 (2012). · DOI
  113. Ferguson, K. K., O'Neill, M. S. & Meeker, J. D. Environmental contaminant exposures and preterm birth: a comprehensive review. J. Toxicol. Environ. Health Part B Crit. Rev. 16, 69–113 (2013). · DOI
  114. Barry, V., Darrow, L. A., Klein, M., Winquist, A. & Steenland, K. Early life perfluorooctanoic acid (PFOA) exposure and overweight and obesity risk in adulthood in a community with elevated exposure. Environ. Res. 132, 62–69 (2014). · DOI
  115. Ngo, H. T., Hetland, R. B., Sabaredzovic, A., Haug, L. S. & Steffensen, I. L. In utero exposure to perfluorooctanoate (PFOA) or perfluorooctane sulfonate (PFOS) did not increase body weight or intestinal tumorigenesis in multiple intestinal neoplasia (Min/+) mice. Environ. Res. 132, 251–263 (2014). · DOI
  116. Guerrero-Bosagna, C. & Skinner, M. K. Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol. Cell. Endocrinol. 354, 3–8 (2012). · DOI · Paper page
  117. Nilsson, E. et al. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE 7, e36129 (2012). · DOI
  118. Skinner, M. K. et al. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med. 11, 228 (2013). · DOI
  119. Tracey, R., Manikkam, M., Guerrero-Bosagna, C. & Skinner, M. K. Hydrocarbons (jet fuel JP-8) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. Reprod. Toxicol. 36, 104–116 (2013). · DOI
  120. Manikkam, M., Tracey, R., Guerrero-Bosagna, C. & Skinner, M. K. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS ONE 8, e55387 (2013). · DOI
  121. Manikkam, M., Tracey, R., Guerrero-Bosagna, C. & Skinner, M. K. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod. Toxicol. 34, 708–719 (2012). · DOI
  122. Aiken, C. E. & Ozanne, S. E. Transgenerational developmental programming. Hum. Reprod. Update 20, 63–75 (2014). · DOI
  123. Heard, E. & Martienssen, R. A. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95–109 (2014). · DOI · Paper page
  124. Tang, W. W. et al. A unique gene regulatory network resets the human germline epigenome for development. Cell 161, 1453–1467 (2015). · DOI · Paper page
  125. Daxinger, L. & Whitelaw, E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 20, 1623–1628 (2010). · DOI
  126. Heindel, J. J. & Schug, T. T. The perfect storm for obesity. Obesity (Silver Spring) 21, 1079–1080 (2013). · DOI

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Metadata

Authors
Heindel, J. J., Newbold, R., & Schug, T. T.
Affiliations
  • National Institute of Environmental Health Sciences (US)
  • National Institutes of Health (US)
Corresponding author
Heindel, Jerrold J.
ORCID
Heindel, Jerrold J.
Venue
Nature Reviews Endocrinology
Publisher
Springer Science and Business Media LLC
Published
2015-09-22
Volume
11
Issue
11
Pages
653-661
ISSN
  • 1759-5029 (ISSN-L)
  • 1759-5037
DOI
10.1038/nrendo.2015.163
OpenAlex
W2205803035
Cited by
451
References
13
Citations by year
2026: 16 · 2025: 46 · 2024: 40 · 2023: 46 · 2022: 35 · 2021: 47 · 2020: 58 · 2019: 46 · 2018: 49 · 2017: 37 · 2016: 26 · 2015: 1
FWCI
3.42
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Reviews Endocrinology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Keywords
obesogens, endocrine disruptors, obesity, obesity epidemic, mechanism of action, hormone signaling, metabolic regulation, early life exposure, obesity etiology, environmental chemicals
MeSH terms
Adult, Environmental Exposure, Environmental Pollutants, Female, Humans, Obesity, Pregnancy, Smoking, Adipogenesis, Endocrine Disruptors

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.

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