Endocrine disruptors in utero cause ovarian damages linked to endometriosis

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 5, 2012, Pages 1724-1730

  Signorile, Pietro G ^a   Spugnini, Enrico P ^b   Citro, Gennaro ^b   Viceconte, Rosa ^a   Vincenzi, Bruno ^c   Baldi, Feliciano ^d   Baldi, Alfonso ^a,d  

^a Fondazione Italiana Endometriosi   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^d SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Bisphenol A; Endocrine Disruptor; Endometriosis; Infertility; Ovary; Precocious Menopause; Premature Ovarian Failure

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; FEMALE; FIRST PASS EFFECT; MOUSE; NONHUMAN; OVARY DISEASE; OVARY FOLLICLE; PHENOTYPE; PRENATAL EXPOSURE; ANIMAL; BAGG ALBINO MOUSE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; ENVIRONMENTAL EXPOSURE; OVARY; PREGNANCY;

ANIMALIA; MUS;

ANIMALS; ENDOCRINE DISRUPTORS; ENDOMETRIOSIS; FEMALE; MATERNAL EXPOSURE; MICE; MICE, INBRED BALB C; OVARY; PREGNANCY;

EID: 84860850264     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e493     Document Type: Article

References (53)

1. TK Jensen, T Sobotka, MA Hansen, AT Pedersen, W Lutz, NE Skakkebaek: Declining trends in conception rates in recent birth cohorts of native Danish women: a possible role of deteriorating male reproductive health. Int. J. Androl 30, 1-9 (2007))
2. BE Hamilton, SJ Ventura: Fertility and abortion rates in the United States, 1960-2002. Int. J. Androl 29, 34-45 (2006))
3. A Crain, SJ Janssen, TM Edwards, J Heindel, S Ho, P Hant, T Iguchi, A Juul, JA MacLachlan, J Schwartz, N Skakkebaek, AM Soto, S Swan, C Walker, TK Woodruff, TJ Woodruff, LC Giudice, LJ Guillette: Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil. Steril 90, 911-940 (2008))
4. J Toppari, JC Larsen, P Christiansen, A Giwercman, P Grandjean, LJ Jr Guillette, B Jégou, TK Jensen, P Jouannet, N Keiding, H Leffers, JA McLachlan, O Meyer, J Müller, E Rajpert-De Meyts, T Scheike, R Sharpe, J Sumpter, NE Skakkebaek: Male reproductive health and enviromental xenoestrogens. Environ Health Perspect 104 (S4), 741-803 (1996)) (Pubitemid 26290302)
5. AL Herbst, H Ulfelder, DC Poskanzer: Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N. Engl J Med 284, 878-881 (1971))
6. EPA. Endocrine Disruptor Screening and Testing Advisory Committee (EDSTAC), Final Report. Washington, DC:U.S. Enviromental Protection Agency, 1998.
7. CR Tyler, S Joblin, JP Sumpter: Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol 28, 319-361 (1998)) (Pubitemid 28389719)
8. JA McLachlan: Enviromental signalling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocrine Reviews 22, 319-341 (2001)) (Pubitemid 32554362)
9. KI Howdeshell, AK Hotchkiss, KA Thayer, JG Vandenbergh, FS vom Saal: Exposure to bisphenol A advances puberty. Nature 401, 763-764 (1999))
10. BS Rubin, MK Murray, DA Damassa, JC King, AM Soto: Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrus cyclicity, and plasma LH levels. Environ Health Perspect 109, 675-680 (2001)) (Pubitemid 32785423)
11. S Honma, A Suzuki, DL Buchanan, Y Katsu, H Watanabe, T Iguchi: Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 16, 117-122 (2002)) (Pubitemid 34457183)
12. CM Markey, PR Wadia, BS Rubin: Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol A in the female mouse genitalia tract. Biol Reprod 72, 1344-1351 (2005)) (Pubitemid 40696077)
13. G Schonfelder, K Friedrich, M Paul, I Chahoud: Developmental effects of prenatal exposure to bisphenol A on the uterus of rat offspring. Neoplasia 6, 584-594 (2004)) (Pubitemid 39411096)
14. RR Newbold, WN Jefferson, E Padilla Banks: Longterm adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 24, 253-258 (2007)) (Pubitemid 47393609)
15. RR Newbold, WJ Jefferson, E Padilla-Banks: Prenatal exposure to bisphenol A at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect 117, 879-885 (2009))
16. D Caserta, L Maranghi, A Mantovani, R Marci, F Maranghi, M Moscarini: Impact of endocrine disruptors chemicals in gynaecology. Hum Reprod Update 14, 59-72 (2008))
17. RR Newbold, EP Banks, B Bullock, WM Jefferson: Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res 61, 4325-4328 (2001)) (Pubitemid 32685752)
18. DL Davids, HL Bradlow, M Wolff, T Woodruff, DG Hoel, H Anton-Colver: Medical hypothesis: xenoestrogens as preventable causes of breast cancer. Environ Health Perspect 101, 372-377 (1993))
19. RR Newbold, E Padilla-Banks, RJ Snyder, TM Phillips, WM Jefferson: Developmental exposure to endocrine disruptors and the obesity epidemic. Reprod Toxicol 23, 290-296 (2007)) (Pubitemid 46628873)
20. B Sallout, M Walker: The fetal origin of adult disease. J Obstet Gynaecol 23, 555-560 (2003))
21. D Crews, JA McLachlan: Epigenetics, evolution, endocrine disruption, health, and disease. Endocrinology 147, S4-S10 (2006))
22. EC Doods, W Lawson: Synthetic estrogenic agents without the phenanthrene nucleus. Nature 137, 996 (1936))
23. E Burridge: Bisphenol A: product profile. Eur Chem News 20, 17 (2003))
24. Y Kawagoshi, Y Fujita, I Kishi, I Fukunaga: Estrogenic chemicals and estrogenic activity in leachate from municipal waste landfill determined by two-hybrid assay. J Enviromen Monitoring 5, 269-274 (2003)) (Pubitemid 36469516)
25. A Coors, PD Jones, JP Giesy, HT Ratte: Removal of estrogenic activity from municipal waste landfill leachate assessed with a bioassay based on reporter gene expression. Enviromen. Sci Technol 37, 3430-3434 (2003)) (Pubitemid 36935645)
26. PG Signorile, EP Spugnini, L Mita, P Mellone, A D'Avino, M Bianco, N Diano, L Caputo, F Rea, R Viceconte, M Portaccio, E Viggiano, G Citro, R Pierantoni, V Sica, B Vincenzi, DG Mita, F Baldi, A Baldi: Pre-natal exposure of mice to bisphenol A elicits an endometriosislike phenotype in female offspring. Gen Comp Endocrinol 168, 318-325 (2010))
27. LC Giudice, LC Kao: Endometriosis. The Lancet 364, 1789-1799 (2004)) (Pubitemid 39488065)
28. A Baldi, M Campioni, PG Signorile: Endometriosis: pathogenesis, diagnosis, therapy and association with cancer. Oncol Reports 19, 843-846 (2008)) (Pubitemid 351802649)
29. PG Signorile, M Campioni, B Vincenzi, A D'Avino, A Baldi: Rectovaginal septum endometriosis: an immunohistochemical analysis of 62 cases. In vivo 23, 459-464 (2009))
30. SE Bulun: Endometriosis. N Engl J Med 360, 268-279 (2009))
31. WG Foster: Endocrine toxicants including 2,3,7,8- terachlorodibenzo-P- dioxin (TCCD) and dioxin-like chemicals and endometriosis: there is a link. J Toxicol Environ Health 1, 177-187 (2008)) (Pubitemid 351451259)
32. SA Missmer, SE Hankinson, D Spiegelma, RL Barbieri, KB Michels, DJ Hunter: In utero exposure and the incidence of endometriosis. Fertil Steril 82, 1501-1508 (2004))
33. L Benaglia, E Somigliana, V Vighi, G Ragni, P Vercellini, L Fedele: Rate of severe ovarian damage following surgery for endometriomas. Hum Reprod 25, 678-682 (2010))
34. M Busacca, M Vignali: Endometrioma excision and ovarian reserve: a dangerous relation. J Minim Invasive Gynecol 16, 142-148 (2009))
35. CM Markey, PR Wadia, BS Rubin, C Sonnenschein, AM Soto: Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol Reprod 72, 1344-1351 (2005)) (Pubitemid 40696077)
36. NTP, 2008. CEHR brief on bisphenol A. Research Triangle Park, NC: National Toxicology Program.
37. W Volkel, M Kiranoglu, H Fromme: Determination of free and total bisphenol A in human urine to assess daily uptake as a basis for valid risk assessment. Toxicol Lett 179, 155-162 (2008))
38. SG Selevan, CA Kimmel, P Mendola: Identifying critical windows of exposure for children's health. Enviromen Health Perspect 108 (S3), 451-455 (2000)) (Pubitemid 30466172)
39. K Block, A Bardana, P Igarashi, HS Taylor: In utero diethylstibelstrol (DES) exposure alters Hox gene expression in the developing mullerian system. FASEB J 14, 1101-1108 (2000)) (Pubitemid 30350391)
40. CC Smith, HS Taylor: Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. Faseb J 21, 239-246 (2007)) (Pubitemid 46052562)
41. HS Taylor: Endocrine disruptors affect developmental programming of hox gene expression. Fertil Steril 89, e57- e58 (2008)) (Pubitemid 351749392)
42. H Du, HS Taylor: Molecular regulation of Mullerian development by HOX genes. Ann NY Acad Sci 1034, 152-165 (2004)) (Pubitemid 40362358)
43. SF Gilbert: Mechanisms for the enviromental regulation of gene expression: ecological aspects of animal development. J Biosci 30, 65-74 (2005)) (Pubitemid 40571501)
44. A Baldi, E Calia, A Ciampini, M Riccio, A Vetuschi, AM Persico, F Keller: Deafferentation-induced apoptosis of neurons in thalamic somatosensory nuclei of the newborn rat: critical period and rescue from cell death by peripherally applied neurotrophins. Eur J Neurosci 12, 2281-2290 (2000)) (Pubitemid 30497026)
45. R Badraoui, NB Abdelmoula, N Feki, H Ben Nasr, T Rebai: Endcorine disruption and ovarian morphometric responses in rats following exposure to tetradifon. Gen Comp Endocrinol 166, 268-272 (2010))
46. M Uzumcu, R Zachow: Developmental exposure to environmental endocrine disruptors: consequences within the ovary and on female reproductive function. Reprod Toxicol 23, 337-352 (2007)) (Pubitemid 46602924)
47. V Padmanabhan, HN Sarma, M Savabieasfahani, TL Steckler, A Veiga-Lopez: Developmental reprogramming of reproductive and metabolic dysfunction in sheep: native steroids vs. environmental steroid receptor modulators. Int J Androl 33, 394-404 (2010))
48. PG Signorile, F Baldi, R Bussani, M D'Armiento, M De Falco, A Baldi: Ectopic endometrium in human foetuses is a common event and sustains the theory of mullerianosis in the pathogenesis of endometriosis, a disease that predisposes to cancer. J Exp Clin Cancer Res 28, 49 (2009))
49. PG Signorile, F Baldi, R Bussani, M D'Armiento, M De Falco, M Boccellino, L Quagliuolo, A Baldi: New evidences sustaining the presence of endometriosis in the human foetus. Reprod Biomed Online 21, 142-147 (2010))
50. PG Signorile, A Baldi: Endometriosis: new concepts in the pathogenesis. Int J Biochem Cell Biol 42, 778-780 (2010))
51. KM Taylor, CA Gray, MM Joyce, MD Stewart, FW Bazer, TE Spencer: Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin. Biol Reprod 63, 1192-1204 (2000))
52. JA Jefferies, SJ Robboy, PC O'Brien, EJ Bergstralh, DR Labarthe, AB Barnes, KL Noller, PA Hatab, RH Kaufman, DE Townsend: Structural anomalies of the cervix and vagina in women enrolled in the Diethylstilbestrol Adenosis (DESAD) Project. Am J Obstet Gynecol 148, 59-66 (1984)) (Pubitemid 14218547)
53. LD Johnson, SG Driscoll, AT Hertig, PT Cole, RJ Nickerson: Vaginal adenosis in stillborns and neonates exposed to diethylstilbestrol and steroidal estrogens and progestin. Obstet Gynecol 53, 671-679 (1979)) (Pubitemid 9153534)