Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development

FASEB Journal

Volumn 21, Issue 1, 2007, Pages 239-246

  Smith, Caroline C ^a   Taylor, Hugh S ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bisphenol A; BPA; Endocrine disruption; HOX

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN; LUCIFERASE; TRANSCRIPTION FACTOR HOXA10; UNCLASSIFIED DRUG; XENOESTROGEN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDOCRINE DISEASE; ESTROGEN RESPONSIVE ELEMENT; FEMALE; GENE EXPRESSION; GENITAL SYSTEM; GESTATION PERIOD; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UTERUS;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; DNA PRIMERS; ENDOCRINE DISRUPTORS; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; PHENOLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UTERUS;

EID: 33845985271     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6635com     Document Type: Article

References (63)

1. Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L., and Feldman, D. (1993) Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132, 2279-2286
2. Coldham, N. G., Dave, M., Sivapathasundaram, S., McDonnell, D. P., Connor, C., and Sauer, M. J. (1997) Evaluation of a recombinant yeast cell estrogen screening assay. Environ. Health Perspect. 105, 734-742
3. Tinwell, H., Joiner, R., Pate, I., Soames, A., Foster, J., and Ashby, J. (2000) Uterotrophic activity of bisphenol A in the immature mouse. Regul. Toxicol. Pharmacol. 32, 118-126
4. Markey, C. M., Michaelson, C. L., Veson, E. C., Sonnenschein, C., Soto, and A. M. (2001) The mouse uterotrophic assay: a reevaluation of its validity in assessing the estrogenicity of bisphenol A. Environ. Health Perspect. 109, 55-60
5. Ashby, J., and Tinwell, H. (1998) Oestrogenic activity of Bisphenol A in the immature rat. Hum. Exp. Toxicol. 17, 598-599
6. Morrison, A. G., Callanan, J. J., Evans, N. P., Aldridge, T. C., and Sweeney, T. (2003) Effects of endocrine disrupting compounds on the pathology and oestrogen receptor alpha and beta distribution in the uterus and cervix of ewe lambs. Domest. Anim. Endocrinol. 25, 329-343
7. Steinmetz, R., Mitchner, N. A., Grant, A., Allen, D. L., Bigsby, R. M., and Ben-Jonathan, N. (1998) The xenoestrogen bisphenol A induces growth, differentiation, and c-fos gene expression in the female reproductive tract. Endocrinology 139, 2741-2747
8. Sugiura-Ogasawara, M., Ozaki, Y., Sonta, S. I., Makino, T., and Suzumori, K. (2005) Exposure to bisphenol A is associated with recurrent miscarriage. Hum. Reprod. 2005, 2325-2329
9. Howdeshell, K. L., Hotchkiss, A. K., Thayer, K. A., Vandenbergh, J. G., and vom Saal, F. S. (1999) Exposure to bisphenol A advances puberty. Nature 401, 763-764
10. Howdeshell, K. L., and vom Saal, F. S. (2000) Developmental exposure to Bisphenol A: interaction with endogenous estradiol during pregnancy in mice. Amer. Zool. 40, 429-437
11. Rubin, B. S., Murray, M. K., Damassa, D. A., King, J. C., and Soto, A. M. (2001) Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ. Health Perspect. 109, 675-680
12. Markey, C. M., Luque, E. H., Munoz De Toro, M., Sonnenschein, C., and Soto, A. M. (2001) In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol. Reprod. 65, 1215-1223
13. Munoz-de-Toro, M., Markey, C., Wadia, P. R., Luque, E. H., Rubin, B. S., Sonnenschein, C., and Soto, A. M. (2005) Perinatal exposure to Bisphenol A alters peripubertal mammary gland development in mice. Endocrinology 146, 4138-4147
14. Schonfelder, G., Flick, B., Mayr, E., Talsness, C., Paul, M., and Chahoud, I. (2002) In utero exposure to low doses of bisphenol A lead to long-term deleterious effects in the vagina. Neoplasia 4, 98-102
15. Suzuki, A., Sugihara, A., Uchida, K., Sato, T., Ohta, Y., Katsu, Y., Watanabe, H., and Iguchi, T. (2002) Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod. Toxicol. 16, 107-16
16. Markey, C. M., Wadia, P. R., Rubin, B. S., Sonnenschein, C., and Soto, A. M. (2005) Long-term effects of fetal exposure to low doses of the xenoestrogen bisphenol-A in the female mouse genital tract. Biol. Reprod. 72, 1344-51
17. Schonfelder, G., Friedrich, K., Paul, M., and Chahoud, I. (2004) Developmental effects of prenatal exposure to bisphenol a on the uterus of rat offspring. Neoplasia 6, 584-94
18. Al-Hiyasat, A. S., Darmani, H., and Elbetieha, A. M. (2002) Effects of bisphenol A on adult male mouse fertility. Eur. J. Oral Sci. 110, 163-167
19. Al-Hiyasat, A. S., Darmani, H., and Elbetieha, A. M. (2004) Leached components from dental composites and their effects on fertility of female mice. Eur. J. Oral Sci. 112, 267-272
20. Darmani, H., and Al-Hiyasat, A. S. (2004) Reproductive toxic effect of bisphenol A dimethacrylate in mice. J. Biomed. Mater Res. A. 69, 637-43
21. Darmani, H., and Al-Hiyasat, A. S. (2006) The effects of BIS-GMA and TEG-DMA on female mouse fertility. Dent. Mater. 22, 353-8
22. Hiroi, H., Tsutsumi, O., Takeuchi, T., Momoeda, M., Ikezuki, Y., Okamura, A., Yokota, H., and Taketani, Y. (2004) Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr. J. 51, 595-600
23. Fei, X., Chung, H., and Taylor, H. S. (2005) Methoxychlor disrupts uterine Hoxa10 gene expression. Endocrinology 146, 3445-51
24. Block, K., Kardana, A., Igarashi, P., and Taylor, H. S. (2000) In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing mullerian system. FASEB J. 14, 1101-1108
25. Akbas, G. E., Song, J., and Taylor, H. S. (2004) A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES). J. Mol. Biol. 340, 1013-1023
26. Ma, L., Benson, G. V., Lim, H., Dey, S. K., and Maas, R. L. (1998) Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev. Biol. 15, 141-154
27. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell 78, 191-201
28. Taylor, H. S., Vanden Heuvel, G. B., and Igarashi, P. (1997) A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol. Reprod. 57, 1338-1345
29. Couse, J. F., Dixon, D., Yates, M., Moore, A. B., Ma, L., Maas, R., and Korach, K. S. (2001) Estrogen receptor-alpha knockout mice exhibit resistance to the developmental effects of neonatal diethylstilbestrol exposure on the female reproductive tract. Dev. Biol. 238, 224-238
30. Littlefield, B. A., Gurpide, E., Markiewicz, L., McKinley, B., and Hochberg, R. B. (1990) A simple and sensitive microtiter plate estrogen bioassay based on stimulation of alkaline phosphatase in Ishikawa cells: estrogenic action of delta 5 adrenal steroids. Endocrinology 127, 2757-2762
31. Lessey, B. A., Ilesanmi, A. O., Castelbaum, A. J., Yuan, L., Somkuti, S. G., Chwalisz, K., and Satyaswaroop, P. G. (1996) Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): Progesterone-induced expression of the a-1 integrin. J. Steroid Biochem. Mol. Biol. 59, 31-39
32. Sarno, J. L., Kliman, H. J., and Taylor, H. S. (2005) HOXA10, Pbx2, and Meis1 protein expression in the human endometrium: formation of multimeric complexes on HOXA10 target genes. J. Clin. Endocrinol. Metab. 90, 522-528
33. Taylor, H. S., Igarashi, P., Olive, D. L., and Arici, A. (1999) Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium. J. Clin. Endocrinol. Metab. 84, 1129-1135
34. Taylor, H. S., Arici, A., Olive, D. L., and Igarashi, P. (1998) HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest. 101, 1379-1384
35. Sakkas, D., Lu, C., Zulfikaroglu, E., Neuber, E., and Taylor, H. S. (2003) A soluble molecule secreted by human blastocysts modulates regulation of HOXA10 expression in an epithelial endometrial cell line. Fertil. Steril. 80, 1169-1174
36. Lessey, B. A., Killam, A. P., Metzger, D. A., Haney, A. F., Greene, G. L., and McCarty, K. S., Jr., (1988) Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 67, 334-340
37. Budwit-Novotny, D. A., McCarty, K. S., Sr., Cox, E. B., Soper, J. R., Mutch, D. G., Creasman, W. T., Flowers, J. L., and McCarty, K. S., Jr. (1986) Immunohistochemical analyses of estrogen receptor in endometrial adenocarcinoma using a monoclonal antibody. Cancer Res. 46, 5419-5425
38. Troy, P. J., Daftary, G. S., Bagot, C. N., and Taylor, H. S. (2003) Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10. Mol. Cell. Biol. 23, 1-13
39. Herbst, A. L., Scully, R. E., and Robboy, S. J. (1975) The significance of adenosis and clear-cell adenocarcinoma of the genital tract in young females. J. Reprod. Med. 15, 5-11
40. Guillette, L. J., Jr., Brock, J. W., Rooney, A. A., and Woodward, A. R. (1999) Serum concentrations of various environmental contaminants and their relationship to sex steroid concentrations and phallus size in juvenile American alligators. Arch. Environ. Contam. Toxicol. 36, 447-455
41. Reijnders, P. J. (1986) Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324, 456-457
42. Ikezuki, Y., Tsutsumi, O., Takai, Y., Kamei, Y., and Taketani, Y. (2002) Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 17, 2839-2841
43. Tsutsumi, O. (2005) Assessment of human contamination of estrogenic endocrine-disrupting chemicals and their risk for human reproduction. J. Steroid Biochem. Mol Biol. 93, 325-30
44. Yamada, H., Furuta, I., Kato, E. H., Kataoka, S., Usuki, Y., Kobashi, G., Sata, F., Kishi, R., and Fujimoto, S. (2002) Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod. Toxicol. 16, 735-739
45. Lemmen, J. G., Arends, R. J., van der Saag, P. T., and van der Burg, B. (2004) In vivo imaging of activated estrogen receptors in utero by estrogens and bisphenol A. Environ. Health Perspect. 112, 1544-9
46. Nagel, S. C., vom Saal, F. S., Thayer, K. A., Dhar, M. G., Boechler, M., and Welshons, W. V. (1997) Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ. Health Perspect. 105, 70-76
47. Milligan, S. R., Khan, O., and Nash, M. (1998) Competitive binding of xenobiotic oestrogens to rat alpha-fetoprotein and to sex steroid binding proteins in human and rainbow trout (Oncorhynchus mykiss) plasma. Gen. Comp. Endocrinol. 112, 89-95
48. Satokata, I., Benson, G., and Maas, R. (1995) Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374, 460-463
49. Daftary, G. S., and Taylor, H. S. (2004) Pleiotropic effects of Hoxa10 on the functional development of peri-implantation endometrium. Mol. Reprod. Dev. 67, 8-14
50. Bagot, C. N., Kliman, H. J., and Taylor, H. S. (2001) Maternal Hoxa10 is required for pinopod formation in the development of mouse uterine receptivity to embryo implantation. Dev. Dyn. 222, 538-44
51. Bagot, C. N., Troy, P. J., and Taylor, H. S. (2000) Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Ther. 7, 1378-1384
52. Spencer, F., Chi, L., Zhu, M. X., Nixon, E., and Lemelle, C. (2002) Uterine molecular responses to bisphenol A treatment before and after decidual induction in pseudopregnant rats. Int. J. Hyg. Environ. Health. 204, 353-7
53. Pottenger, L. H., Domoradzki, J. Y., Markham, D. A., Hansen, S. C., Cagen, S. Z., and Waechter, J. M., Jr. (2000) The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol. Sci. 54, 3-18
54. Taylor, H. S., Bagot, C., Kardana, A., Olive, D., and Arici, A. (1999) HOX gene expression is altered in the endometrium of women with endometriosis. Hum. Reprod. 14, 1328-1331
55. Salih, S. M., and Taylor, H. S. (2004) HOXA10 gene expression in human fallopian tube and ectopic pregnancy. Am. J. Obstet. Gynecol. 190, 1404-1406
56. Daftary, G. S., Taylor, H. S. (2002) Hydrosalpinx fluid diminishes endometrial cell HOXA10 expression. Fertil. Steril. 78, 577-580
57. Cermik, D., Selam, B., and Taylor, H. S. (2003) Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 88, 238-243
58. Kelly, M., Daftary, G., and Taylor, H. S. (2006) An autoregulatory element maintains HOXA10 expression in endometrial epithelial cells. Am. J. Obstet. Gynecol. 194, 1100-1107
59. Bagot, C. N., Troy, P. J., and Taylor, H. S. (2000) Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Ther. 7, 1378-1384
60. Troy, P. J., Daftary, G. S., Bagot, C. N., and Taylor, H. S. (2003) Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10. Mol. Cell. Biol. 23, 1-13
61. Li, S., Ma, L., Chiang, T., Burow, M., Newbold, R. R., Negishi, M., Barrett, J. C., and McLachlan, J. A. (2001) Promoter CpG methylation of Hox-a10 and Hox-a11 in mouse uterus not altered upon neonatal diethylstilbestrol exposure. Mol. Carcinog. 32, 213-219
62. Li, E. (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662-673
63. Maffini, M. V., Rubin, B. S., Sonnenschein, C., and Soto, A. M. (2006) Endocrine disruptors and reproductive health: The case of bisphenol-A. Mol. Cell. Endocrinol. 25, 179-86