Dioxin (TCDD) Induces Epigenetic Transgenerational Inheritance of Adult Onset Disease and Sperm Epimutations

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Manikkam, Mohan ^a   Tracey, Rebecca ^a   Guerrero Bosagna, Carlos ^a   Skinner, Michael K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIOXIN; DNA;

ANIMAL EXPERIMENT; ARTICLE; CLINICAL OBSERVATION; CONTROLLED STUDY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE; HISTOPATHOLOGY; HUMAN; IMMUNOPRECIPITATION; KIDNEY DISEASE; MALE; MUTATION; NONHUMAN; ONSET AGE; OVARY FOLLICLE; OVARY POLYCYSTIC DISEASE; PROMOTER REGION; PROSTATE DISEASE; PUBERTY; RAT; SEX DETERMINATION; SPERM;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; MALE; OVARIAN FOLLICLE; PROSTATIC DISEASES; RATS; SPERMATOZOA; TETRACHLORODIBENZODIOXIN;

ANIMALIA; RATTUS;

EID: 84866874968     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046249     Document Type: Article

References (73)

1. Skinner MK, Manikkam M, Guerrero-Bosagna C, (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21: 214-222.
2. Anway MD, Cupp AS, Uzumcu M, Skinner MK, (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
3. Reik W, Dean W, Walter J, (2001) Epigenetic reprogramming in mammalian development. Science 293: 1089-1093.
4. Guerrero-Bosagna C, Settles M, Lucker B, Skinner M, (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 5: e13100.
5. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK, (2012) Transgenerational Actions of Environmental Compounds on Reproductive Disease and Epigenetic Biomarkers of Ancestral Exposures. PLoS ONE 7: e31901.
6. Spaulding SW, (2011) The possible roles of environmental factors and the aryl hydrocarbon receptor in the prevalence of thyroid diseases in Vietnam era veterans. Curr Opin Endocrinol Diabetes Obes 18: 315-320.
7. IOM (2010) Veterans and Agent Orange Update 2010. Washington D.C.: The National Academies Press.
8. York G, Mick H (2008) Last Ghost of the Vietnam War. The Globe and Mail. Toronto, ON Canada: Phillip Crawley.
9. Eskenazi B, Mocarelli P, Warner M, Needham L, Patterson DG Jr, et al. (2004) Relationship of serum TCDD concentrations and age at exposure of female residents of Seveso, Italy. Environ Health Perspect 112: 22-27.
10. Ni HG, Zeng H, Tao S, Zeng EY, (2010) Environmental and human exposure to persistent halogenated compounds derived from e-waste in China. Environ Toxicol Chem 29: 1237-1247.
11. Guo YL, Hsu PC, Hsu CC, Lambert GH, (2000) Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 356: 1240-1241.
12. Carpenter DO, (2006) Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health 21: 1-23.
13. Baccarelli A, Giacomini SM, Corbetta C, Landi MT, Bonzini M, et al. (2008) Neonatal thyroid function in Seveso 25 years after maternal exposure to dioxin. PLoS Med 5: e161.
14. Courtney KD, Moore JA, (1971) Teratology studies with 2,4,5-trichlorophenoxyacetic acid and 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 20: 396-403.
15. van Leeuwen FX, Feeley M, Schrenk D, Larsen JC, Farland W, et al. (2000) Dioxins: WHO's tolerable daily intake (TDI) revisited. Chemosphere 40: 1095-1101.
16. Huang L, Huang R, Ran XR, Liu HY, Zhang Y, et al. (2011) Three-generation experiment showed female C57BL/6J mice drink drainage canal water containing low level of TCDD-like activity causing high pup mortality. J Toxicol Sci 36: 713-724.
17. Gray LE, Ostby JS, Kelce WR, (1997) A dose-response analysis of the reproductive effects of a single gestational dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male Long Evans Hooded rat offspring. Toxicol Appl Pharmacol 146: 11-20.
18. Gehrs BC, Riddle MM, Williams WC, Smialowicz RJ, (1997) Alterations in the developing immune system of the F344 rat after perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin: II. Effects on the pup and the adult. Toxicology 122: 229-240.
19. Skinner MK, (2008) What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 25: 2-6.
20. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner M (2012) Plastics Derived Endocrine Disruptors (BPA, DEHP and DBP) Induce Epigenetic Transgenerational Inheritance of Adult-Onset Disease and Sperm Epimutations. Submitted.
21. Salian S, Doshi T, Vanage G, (2009) Perinatal exposure of rats to Bisphenol A affects the fertility of male offspring. Life Sci 85: 742-752.
22. Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova M, et al. (2012) Environmentally Induced Epigenetic Transgenerational Inheritance of Ovarian Disease. PLoS ONE 7: e36129.
23. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner M (2012) Pesticide and Insect Repellent Mixture (Permethrin and DEET) Induces Epigenetic Transgenerational Inheritance of Disease and Sperm Epimutations. Reproductive Toxicology (Submitted).
24. Tracey R, Manikkam M, Guerrero-Bosagna C, Skinner M (2012) Hydrocarbon (Jet Fuel JP-8) Induces Epigenetic Transgenerational Inheritance of Adult-Onset Disease and Sperm Epimutations. Reproductive Toxicology (Submitted).
25. Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S, (2008) Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 32: 1373-1379.
26. Hauser MT, Aufsatz W, Jonak C, Luschnig C, (2011) Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta 1809: 459-468.
27. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, et al. (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479: 365-371.
28. Ruden DM, Lu X, (2008) Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila. Curr Genomics 9: 500-508.
29. Guerrero-Bosagna C, Covert T, Haque MM, Settles M, Nilsson EE, et al. (2012) Epigenetic Transgenerational Inheritance of Vinclozolin Induced Mouse Adult Onset Disease and Associated Sperm Epigenome Biomarkers. Reproductive Toxicology (Provisionally Accepted).
30. Pembrey ME, (2010) Male-line transgenerational responses in humans. Hum Fertil (Camb) 13: 268-271.
31. Bruner-Tran KL, Osteen KG, (2011) Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol 31: 344-350.
32. Anway MD, Leathers C, Skinner MK, (2006) Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147: 5515-5523.
33. Tsukimori K, Uchi H, Mitoma C, Yasukawa F, Chiba T, et al. (2012) Maternal exposure to high levels of dioxins in relation to birth weight in women affected by Yusho disease. Environ Int 38: 79-86.
34. Couture LA, Abbott BD, Birnbaum LS, (1990) A critical review of the developmental toxicity and teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: recent advances toward understanding the mechanism. Teratology 42: 619-627.
35. Mustafa A, Holladay S, Witonsky S, Zimmerman K, Manari A, et al. (2011) Prenatal TCDD causes persistent modulation of the postnatal immune response, and exacerbates inflammatory disease, in 36-week-old lupus-like autoimmune SNF1 mice. Birth Defects Res B Dev Reprod Toxicol 92: 82-94.
36. Lu CF, Wang YM, Peng SQ, Zou LB, Tan DH, et al. (2009) Combined effects of repeated administration of 2,3,7,8-tetrachlorodibenzo-p-dioxin and polychlorinated biphenyls on kidneys of male rats. Arch Environ Contam Toxicol 57: 767-776.
37. Nishimura N, Matsumura F, Vogel CF, Nishimura H, Yonemoto J, et al. (2008) Critical role of cyclooxygenase-2 activation in pathogenesis of hydronephrosis caused by lactational exposure of mice to dioxin. Toxicol Appl Pharmacol 231: 374-383.
38. Vujovic S, (2009) Aetiology of premature ovarian failure. Menopause Int 15: 72-75.
39. Hart R, Hickey M, Franks S, (2004) Definitions, prevalence and symptoms of polycystic ovaries and polycystic ovary syndrome. Best Pract Res Clin Obstet Gynaecol 18: 671-683.
40. Gao X, Petroff BK, Rozman KK, Terranova PF, (2000) Gonadotropin-releasing hormone (GnRH) partially reverses the inhibitory effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on ovulation in the immature gonadotropin-treated rat. Toxicology 147: 15-22.
41. Li X, Johnson DC, Rozman KK, (1995) Reproductive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female rats: ovulation, hormonal regulation, and possible mechanism(s). Toxicol Appl Pharmacol 133: 321-327.
42. Moran FM, Tarara R, Chen J, Santos S, Cheney A, et al. (2001) Effect of dioxin on ovarian function in the cynomolgus macaque (M. fascicularis). Reprod Toxicol 15: 377-383.
43. Flaws JA, Sommer RJ, Silbergeld EK, Peterson RE, Hirshfield AN, (1997) In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induces genital dysmorphogenesis in the female rat. Toxicol Appl Pharmacol 147: 351-362.
44. Gray LE Jr, Ostby JS, (1995) In utero 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters reproductive morphology and function in female rat offspring. Toxicol Appl Pharmacol 133: 285-294.
45. Heimler I, Trewin AL, Chaffin CL, Rawlins RG, Hutz RJ, (1998) Modulation of ovarian follicle maturation and effects on apoptotic cell death in Holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod Toxicol 12: 69-73.
46. Gao X, Son DS, Terranova PF, Rozman KK, (1999) Toxic equivalency factors of polychlorinated dibenzo-p-dioxins in an ovulation model: validation of the toxic equivalency concept for one aspect of endocrine disruption. Toxicol Appl Pharmacol 157: 107-116.
47. Kociba RJ, Keeler PA, Park CN, Gehring PJ, (1976) 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): results of a 13-week oral toxicity study in rats. Toxicol Appl Pharmacol 35: 553-574.
48. Roby KF, (2001) Alterations in follicle development, steroidogenesis, and gonadotropin receptor binding in a model of ovulatory blockade. Endocrinology 142: 2328-2335.
49. Roby K, (2000) Mechanisms of TCDD-mediated inhibition of ovulation [Abstract] Biol Reprod. 62: 284.
50. Salisbury TB, Marcinkiewicz JL, (2002) In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,4,7,8-pentachlorodibenzofuran reduces growth and disrupts reproductive parameters in female rats. Biol Reprod 66: 1621-1626.
51. Silbergeld EK, Mattison DR, (1987) Experimental and clinical studies on the reproductive toxicology of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Am J Ind Med 11: 131-144.
52. Son DS, Ushinohama K, Gao X, Taylor CC, Roby KF, et al. (1999) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) blocks ovulation by a direct action on the ovary without alteration of ovarian steroidogenesis: lack of a direct effect on ovarian granulosa and thecal-interstitial cell steroidogenesis in vitro. Reprod Toxicol 13: 521-530.
53. Umbreit TH, Hesse EJ, Gallo MA, (1987) Reproductive toxicity in female mice of dioxin-contaminated soils from a 2,4,5-trichlorophenoxyacetic acid manufacturing site. Arch Environ Contam Toxicol 16: 461-466.
54. Mattison DR, (1980) Morphology of oocyte and follicle destruction by polycyclic aromatic hydrocarbons in mice. Toxicol Appl Pharmacol 53: 249-259.
55. Davis BJ, McCurdy EA, Miller BD, Lucier GW, Tritscher AM, (2000) Ovarian tumors in rats induced by chronic 2,3,7,8-tetrachlorodibenzo-p-dioxin treatment. Cancer Res 60: 5414-5419.
56. Eskenazi B, Warner M, Marks AR, Samuels S, Gerthoux PM, et al. (2005) Serum dioxin concentrations and age at menopause. Environ Health Perspect 113: 858-862.
57. Xu N, Azziz R, Goodarzi MO (2010) Epigenetics in polycystic ovary syndrome: a pilot study of global DNA methylation. Fertil Steril 94: 781-783 e781.
58. Xu N, Kwon S, Abbott DH, Geller DH, Dumesic DA, et al. (2011) Epigenetic mechanism underlying the development of polycystic ovary syndrome (PCOS)-like phenotypes in prenatally androgenized rhesus monkeys. PLoS ONE 6: e27286.
59. DiVall SA, Radovick S, (2009) Endocrinology of female puberty. Curr Opin Endocrinol Diabetes Obes 16: 1-4.
60. Jacobson-Dickman E, Lee MM, (2009) The influence of endocrine disruptors on pubertal timing. Curr Opin Endocrinol Diabetes Obes 16: 25-30.
61. Kakeyama M, Sone H, Tohyama C, (2008) Perinatal exposure of female rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin induces central precocious puberty in the offspring. J Endocrinol 197: 351-358.
62. Traggiai C, Stanhope R, (2003) Disorders of pubertal development. Best Pract Res Clin Obstet Gynaecol 17: 41-56.
63. Warner M, Samuels S, Mocarelli P, Gerthoux PM, Needham L, et al. (2004) Serum dioxin concentrations and age at menarche. Environ Health Perspect 112: 1289-1292.
64. Wolff MS, Britton JA, Russo JC (2005) TCDD and puberty in girls. Environ Health Perspect 113: A17; author reply A18.
65. Jirtle RL, Skinner MK, (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8: 253-262.
66. Nilsson EE, Anway MD, Stanfield J, Skinner MK, (2008) Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 135: 713-721.
67. Stouder C, Paoloni-Giacobino A, (2010) Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 139: 373-379.
68. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, et al. (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441: 469-474.
69. Wagner KD, Wagner N, Ghanbarian H, Grandjean V, Gounon P, et al. (2008) RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 14: 962-969.
70. Nilsson EE, Schindler R, Savenkova MI, Skinner MK, (2011) Inhibitory actions of Anti-Mullerian Hormone (AMH) on ovarian primordial follicle assembly. PLoS ONE 6: e20087.
71. Meredith S, Dudenhoeffer G, Jackson K, (2000) Classification of small type B/C follicles as primordial follicles in mature rats. J Reprod Fertil 119: 43-48.
72. Tateno H, Kimura Y, Yanagimachi R, (2000) Sonication per se is not as deleterious to sperm chromosomes as previously inferred. Biol Reprod 63: 341-346.
73. Ward WS, Kimura Y, Yanagimachi R, (1999) An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biol Reprod 60: 702-706.