BMC Medicine | Full text | Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity

  • Skinner MK, Manikkam M, Guerrero-Bosagna C: Epigenetic transgenerational actions of environmental factors in disease etiology.

    Trends Endocrinol Metab 2010, 21:214-222. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Jirtle RL, Skinner MK: Environmental epigenomics and disease susceptibility.

    Nat Rev Genet 2007, 8:253-262. PubMed Abstract | Publisher Full Text

  • Skinner MK: Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability.

    Epigenetics 2011, 6:838-842. PubMed Abstract | Publisher Full Text

  • Anway MD, Cupp AS, Uzumcu M, Skinner MK: Epigenetic transgenerational actions of endocrine disruptors and male fertility.

    Science 2005, 308:1466-1469. PubMed Abstract | Publisher Full Text

  • Anway MD, Leathers C, Skinner MK: Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease.

    Endocrinology 2006, 147:5515-5523. PubMed Abstract | Publisher Full Text

  • Stouder C, Paoloni-Giacobino A: Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm.

    Reproduction 2010, 139:373-379. PubMed Abstract | Publisher Full Text

  • Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK: Transgenerational Actions of Environmental Compounds on Reproductive Disease and Epigenetic Biomarkers of Ancestral Exposures.

    PLoS ONE 2012, 7:e31901. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Nilsson EE, Schindler R, Savenkova MI, Skinner MK: Inhibitory actions of anti-Mullerian hormone (AMH) on ovarian primordial follicle assembly.

    PLoS ONE 2011, 6:e20087. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Bruner-Tran KL, Osteen KG: Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations.

    Reprod Toxicol 2011, 31:344-350. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S: Methyl donor supplementation prevents transgenerational amplification of obesity.

    Int J Obes (Lond) 2008, 32:1373-1379. Publisher Full Text

  • Hauser MT, Aufsatz W, Jonak C, Luschnig C: Transgenerational epigenetic inheritance in plants.

    Biochim Biophys Acta 1809, 2011:459-468.

  • Ruden DM, Lu X: Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila.

    Curr Genomics 2008, 9:500-508. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, Lim JP, Benayoun BA, Shi Y, Brunet A: Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans.

    Nature 2011, 479:365-371. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Pembrey ME: Male-line transgenerational responses in humans.

    Hum Fertil (Camb) 2010, 13:268-271. Publisher Full Text

  • Guimaraes RM, Asmus CI, Meyer A: DDT reintroduction for malaria control: the cost-benefit debate for public health.

    Cad Saude Publica 2007, 23:2835-2844. PubMed Abstract | Publisher Full Text

  • Sadasivaiah S, Tozan Y, Breman JG: Dichlorodiphenyltrichloroethane (DDT) for indoor residual spraying in Africa: how can it be used for malaria control?

    Am J Trop Med Hyg 2007, 77:249-263. PubMed Abstract | Publisher Full Text

  • Davies K: Strategies for eliminating and reducing persistent bioaccumulative toxic substances: common approaches, emerging trends, and level of success.

    J Environ Health 2006, 69:9-15. PubMed Abstract

  • Enayati A, Hemingway J: Malaria management: past, present, and future.

    Annu Rev Entomol 2010, 55:569-591. PubMed Abstract | Publisher Full Text

  • van den Berg H: Global status of DDT and its alternatives for use in vector control to prevent disease.

    Environ Health Perspect 2009, 117:1656-1663. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Aneck-Hahn NH, Schulenburg GW, Bornman MS, Farias P, de Jager C: Impaired semen quality associated with environmental DDT exposure in young men living in a malaria area in the Limpopo Province, South Africa.

    J Androl 2007, 28:423-434. PubMed Abstract | Publisher Full Text

  • Hauser R, Singh NP, Chen Z, Pothier L, Altshul L: Lack of an association between environmental exposure to polychlorinated biphenyls and p, p?-DDE and DNA damage in human sperm measured using the neutral comet assay.

    Hum Reprod 2003, 18:2525-2533. PubMed Abstract | Publisher Full Text

  • ATSDR: Agency for Toxic Substances and Diseases Registry (ATSDR)/US Public Health Service, Toxicological Profile for 4,4?-DDT, 4,4?-DDE, 4, 4?-DDD (Update). Atlanta, GA: ATSDR; 1994. PubMed Abstract

  • Longnecker MP, Klebanoff MA, Zhou H, Brock JW: Association between maternal serum concentration of the DDT metabolite DDE and preterm and small-for-gestational-age babies at birth.

    Lancet 2001, 358:110-114. PubMed Abstract | Publisher Full Text

  • Jaga K, Brosius D: Pesticide exposure: human cancers on the horizon.

    Rev Environ Health 1999, 14:39-50. PubMed Abstract

  • Hamlin HJ, Guillette LJ Jr: Birth defects in wildlife: the role of environmental contaminants as inducers of reproductive and developmental dysfunction.

    Syst Biol Reprod Med 2010, 56:113-121. PubMed Abstract | Publisher Full Text

  • Eskenazi B, Chevrier J, Rosas LG, Anderson HA, Bornman MS, Bouwman H, Chen A, Cohn BA, de Jager C, Henshel DS, Leipzig F, Leipzig JS, Lorenz EC, Snedeker SM, Stapleton D: The Pine River statement: human health consequences of DDT use.

    Environ Health Perspect 2009, 117:1359-1367. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Valvi D, Mendez MA, Martinez D, Grimalt JO, Torrent M, Sunyer J, Vrijheid M: Prenatal concentrations of polychlorinated biphenyls, DDE, and DDT and overweight in children: a prospective birth cohort study.

    Environ Health Perspect 2012, 120:451-457. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • McAllister EJ, Dhurandhar NV, Keith SW, Aronne LJ, Barger J, Baskin M, Benca RM, Biggio J, Boggiano MM, Eisenmann JC, Elobeid M, Fontaine KR, Gluckman P, Hanlon EC, Katzmarzyk P, Pietrobelli A, Redden DT, Ruden DM, Wang C, Waterland RA, Wright SM, Allison DB: Ten putative contributors to the obesity epidemic.

    Crit Rev Food Sci Nutr 2009, 49:868-913. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Caballero B: The global epidemic of obesity: an overview.

    Epidemiol Rev 2007, 29:1-5. PubMed Abstract | Publisher Full Text

  • Trasande L, Attina TM, Blustein J: Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents.

    JAMA 2012, 308:1113-1121. PubMed Abstract | Publisher Full Text

  • Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner M: Plastics derived endocrine disruptors (BPA, DEHP and DBP) Induce epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations.

    PLoS ONE 2013, 8:e55387. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Tracey R, Manikkam M, Guerrero-Bosagna C, Skinner M: Hydrocarbon (Jet Fuel JP-8) induces epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations.

    Reprod Toxicol 2013, 36:104-116. PubMed Abstract | Publisher Full Text

  • Janesick A, Blumberg B: Obesogens, stem cells and the developmental programming of obesity.

    Int J Androl 2012, 35:437-448. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Sabin MA, Werther GA, Kiess W: Genetics of obesity and overgrowth syndromes.

    Best Pract Res Clin Endocrinol Metab 2011, 25:207-220. PubMed Abstract | Publisher Full Text

  • Phan-Hug F, Beckmann JS, Jacquemont S: Genetic testing in patients with obesity.

    Best Pract Res Clin Endocrinol Metab 2012, 26:133-143. PubMed Abstract | Publisher Full Text

  • Waterland RA: Is epigenetics an important link between early life events and adult disease?

    Horm Res 2009, 71:13-16. PubMed Abstract | Publisher Full Text

  • Anderson PJ, Critchley JA, Chan JC, Cockram CS, Lee ZS, Thomas GN, Tomlinson B: Factor analysis of the metabolic syndrome: obesity vs insulin resistance as the central abnormality.

    Int J Obes Relat Metab Disord 2001, 25:1782-1788. PubMed Abstract | Publisher Full Text

  • Ferrannini E, Haffner SM, Mitchell BD, Stern MP: Hyperinsulinaemia: the key feature of a cardiovascular and metabolic syndrome.

    Diabetologia 1991, 34:416-422. PubMed Abstract | Publisher Full Text

  • Franks S: Polycystic ovary syndrome.

    N Engl J Med 1995, 333:853-861. PubMed Abstract | Publisher Full Text

  • Lauenborg J, Mathiesen E, Hansen T, Glumer C, Jorgensen T, Borch-Johnsen K, Hornnes P, Pedersen O, Damm P: The prevalence of the metabolic syndrome in a Danish population of women with previous gestational diabetes mellitus is three-fold higher than in the general population.

    J Clin Endocrinol Metab 2005, 90:4004-4010. PubMed Abstract | Publisher Full Text

  • Chen SH, He F, Zhou HL, Wu HR, Xia C, Li YM: Relationship between nonalcoholic fatty liver disease and metabolic syndrome.

    J Dig Dis 2011, 12:125-130. PubMed Abstract | Publisher Full Text

  • Akahoshi T, Uematsu A, Akashiba T, Nagaoka K, Kiyofuji K, Kawahara S, Hattori T, Kaneita Y, Yoshizawa T, Takahashi N, Uchiyama M, Hashimoto S: Obstructive sleep apnoea is associated with risk factors comprising the metabolic syndrome.

    Respirology 2010, 15:1122-1126. PubMed Abstract | Publisher Full Text

  • Mathew AV, Okada S, Sharma K: Obesity related kidney disease.

    Curr Diabetes Rev 2011, 7:41-49. PubMed Abstract | Publisher Full Text

  • Kasturi SS, Tannir J, Brannigan RE: The metabolic syndrome and male infertility.

    J Androl 2008, 29:251-259. PubMed Abstract | Publisher Full Text

  • Rahmanpour H, Jamal L, Mousavinasab SN, Esmailzadeh A, Azarkhish K: Association between polycystic ovarian syndrome, overweight, and metabolic syndrome in adolescents.

    J Pediatr Adolesc Gynecol 2012, 25:208-212. PubMed Abstract | Publisher Full Text

  • Motta AB: The role of obesity in the development of polycystic ovary syndrome.

    Curr Pharm Des 2012, 18:2482-2491. PubMed Abstract | Publisher Full Text

  • Beard J: DDT and human health.

    Sci Total Environ 2006, 355:78-89. PubMed Abstract | Publisher Full Text

  • Nilsson EE, Anway MD, Stanfield J, Skinner MK: Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease.

    Reproduction 2008, 135:713-721. PubMed Abstract | Publisher Full Text

  • Xie F, Zhang R, Yang C, Xu Y, Wang N, Sun L, Liu J, Wei R, Ai J: Long-term neuropeptide Y administration in the periphery induces abnormal baroreflex sensitivity and obesity in rats.

    Cell Physiol Biochem 2012, 29:111-120. PubMed Abstract | Publisher Full Text

  • Phillips LK, Prins JB: The link between abdominal obesity and the metabolic syndrome.

    Curr Hypertens Rep 2008, 10:156-164. PubMed Abstract | Publisher Full Text

  • National Task Force on the Prevention and Treatment of Obesity: Overweight, obesity, and health risk.

    Arch Intern Med 2000, 160:898-904. PubMed Abstract | Publisher Full Text

  • Anway MD, Skinner MK: Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease.

    Prostate 2008, 68:517-529. PubMed Abstract | Publisher Full Text

  • Taylor JA, Richter CA, Ruhlen RL, vom Saal FS: Estrogenic environmental chemicals and drugs: mechanisms for effects on the developing male urogenital system.

    J Steroid Biochem Mol Biol 2011, 127:83-95. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Meredith S, Dudenhoeffer G, Jackson K: Classification of small type B/C follicles as primordial follicles in mature rats.

    J Reprod Fertil 2000, 119:43-48. PubMed Abstract | Publisher Full Text

  • Tateno H, Kimura Y, Yanagimachi R: Sonication per se is not as deleterious to sperm chromosomes as previously inferred.

    Biol Reprod 2000, 63:341-346. PubMed Abstract | Publisher Full Text

  • Ward WS, Kimura Y, Yanagimachi R: An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development.

    Biol Reprod 1999, 60:702-706. PubMed Abstract | Publisher Full Text

  • Guerrero-Bosagna C, Settles M, Lucker B, Skinner M: Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome.

    PLoS ONE 2010, 5:e13100. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Guillette LJ Jr, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR: Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida.

    Environ Health Perspect 1994, 102:680-688. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Crews D, Gillette R, Scarpino SV, Manikkam M, Savenkova MI, Skinner MK: Epigenetic transgenerational inheritance of altered stress responses.

    Proc Natl Acad Sci U S A 2012, 109:9143-9148. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova M, Skinner M: Environmentally induced epigenetic transgenerational inheritance of ovarian disease.

    PLoS ONE 2012, 7:e36129. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • McGrowder DA, Jackson LA, Crawford TV: Prostate cancer and metabolic syndrome: is there a link?

    Asian Pac J Cancer Prev 2012, 13:1-13. PubMed Abstract | Publisher Full Text

  • Nelson RA, Bremer AA: Insulin resistance and metabolic syndrome in the pediatric population.

    Metab Syndr Relat Disord 2010, 8:1-14. PubMed Abstract | Publisher Full Text

  • Rose DP, Haffner SM, Baillargeon J: Adiposity, the metabolic syndrome, and breast cancer in African-American and white American women.

    Endocr Rev 2007, 28:763-777. PubMed Abstract | Publisher Full Text

  • Wisse BE: The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity.

    J Am Soc Nephrol 2004, 15:2792-2800. PubMed Abstract | Publisher Full Text

  • Cao J, Rebuli ME, Rogers J, Todd KL, Leyrer SM, Ferguson SA, Patisaul HB: Prenatal bisphenol a exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala.

    Toxicol Sci 2013, 133:157-173. PubMed Abstract | Publisher Full Text

  • McMillen IC, Rattanatray L, Duffield JA, Morrison JL, MacLaughlin SM, Gentili S, Muhlhausler BS: The early origins of later obesity: pathways and mechanisms.

    Adv Exp Med Biol 2009, 646:71-81. PubMed Abstract | Publisher Full Text

  • Massiera F, Barbry P, Guesnet P, Joly A, Luquet S, Moreilhon-Brest C, Mohsen-Kanson T, Amri EZ, Ailhaud G: A Western-like fat diet is sufficient to induce a gradual enhancement in fat mass over generations.

    J Lipid Res 2010, 51:2352-2361. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Dunn GA, Bale TL: Maternal high-fat diet effects on third-generation female body size via the paternal lineage.

    Endocrinology 2011, 152:2228-2236. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Gambineri A, Pelusi C, Vicennati V, Pagotto U, Pasquali R: Obesity and the polycystic ovary syndrome.

    Int J Obes Relat Metab Disord 2002, 26:883-896. PubMed Abstract | Publisher Full Text

  • Martinez-Bermejo E, Luque-Ramirez M, Escobar-Morreale HF: Obesity and the polycystic ovary syndrome.

    Minerva Endocrinol 2007, 32:129-140. PubMed Abstract

  • Doyle TJ, Bowman JL, Windell VL, McLean DJ, Kim KH: Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice.

    Biol Reprod 2013, 88:112. PubMed Abstract | Publisher Full Text

  • Maric-Bilkan C: Obesity and diabetic kidney disease.

    Med Clin North Am 2013, 97:59-74. PubMed Abstract | Publisher Full Text

  • Mlambo SS, van Vuren JH, Barnhoorn IE, Bornman MS: Histopathological changes in the reproductive system (ovaries and testes) of Oreochromis mossambicus following exposure to DDT.

    Environ Toxicol Pharmacol 2009, 28:133-139. PubMed Abstract | Publisher Full Text

  • Cohn BA, Cirillo PM, Christianson RE: Prenatal DDT exposure and testicular cancer: a nested case?control study.

    Arch Environ Occup Health 2010, 65:127-134. PubMed Abstract | Publisher Full Text | PubMed Central Full Text

  • Hart R, Hickey M, Franks S: Definitions, prevalence and symptoms of polycystic ovaries and polycystic ovary syndrome.

    Best Pract Res Clin Obstet Gynaecol 2004, 18:671-683. PubMed Abstract | Publisher Full Text

  • Ozucelik DN, Karcioglu O, Topacoglu H, Fowler JR: Toxicity following unintentional DDT ingestion.

    J Toxicol Clin Toxicol 2004, 42:299-303. PubMed Abstract | Publisher Full Text

  • Carson R: Silent Spring. Houghton Mifflin: Greenburg; 1963.

  • Rogan WJ, Chen A: Health risks and benefits of bis(4-chlorophenyl)-1,1,1-trichloroethane (DDT).

    Lancet 2005, 366:763-773. PubMed Abstract | Publisher Full Text

  • http://www.biomedcentral.com/1741-7015/11/228#sec7