DOI QR코드

DOI QR Code

Toxicological Mechanism of Endocrine Disrupting Chemicals: Is Estrogen Receptor Involved?

  • Jeung, Eui-Bae (Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary Medicine, Chungbuk National University) ;
  • Choi, Kyung-Chul (Laboratory of Veterinary Biochemistry and Immunology, College of Veterinary Medicine, Chungbuk National University)
  • 투고 : 2010.05.26
  • 심사 : 2010.06.24
  • 발행 : 2010.12.01

초록

Endocrine disrupting chemicals (EDCs) have been shown to interfere with physiological systems, i.e., adversely affecting hormone balance (endocrine system), or disrupting normal function, in the female and male reproductive organs. Although endocrine disruption is a global concern for human health, its impact and significance and the screening strategy for detecting these synthetic or man-made chemicals are not clearly understood in female and male reproductive functions. Thus, in this review, we summarize the interference of environmental EDCs on reproductive development and function, and toxicological mechanism(s) of EDCs in in vitro and in vivo models of male and female reproductive system. In addition, this review highlights the effect of exposure to multiple EDCs on reproductive functions, and brings attention to their toxicological mechanism(s) through estrogen receptors.

키워드

참고문헌

  1. Abney, T.O. and Myers, R.B. (1991). 17 beta-estradiol inhibition of Leydig cell regeneration in the ethane dimethylsulfonatetreated mature rat. J. Androl., 12, 295-304.
  2. Allen, D.L., Mitchner, N.A., Uveges, T.E., Nephew, K.P., Khan, S. and Ben-Jonathan, N. (1997). Cell-specific induction of c-fos expression in the pituitary gland by estrogen. Endocrinology, 138, 2128-2135. https://doi.org/10.1210/en.138.5.2128
  3. An, B.S., Choi, K.C., Kang, S.K., Hwang, W.S. and Jeung, E.B. (2003). Novel Calbindin-D(9k) protein as a useful biomarker for environmental estrogenic compounds in the uterus of immature rats. Reprod Toxicol., 17, 311-319. https://doi.org/10.1016/S0890-6238(03)00003-0
  4. Aranda, A. and Pascual, A. (2001). Nuclear hormone receptors and gene expression. Physiol. Rev., 81, 1269-1304. https://doi.org/10.1152/physrev.2001.81.3.1269
  5. Arnold, A.P. and Gorski, R.A. (1984). Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci., 7, 413-442. https://doi.org/10.1146/annurev.ne.07.030184.002213
  6. Bulayeva, N.N., Gametchu, B. and Watson, C.S. (2004). Quantitative measurement of estrogen-induced ERK 1 and 2 activation via multiple membrane-initiated signaling pathways. Steroids, 69, 181-192. https://doi.org/10.1016/j.steroids.2003.12.003
  7. Bulayeva, N.N., Wozniak, A.L., Lash, L.L. and Watson, C.S. (2005). Mechanisms of membrane estrogen receptor-alphamediated rapid stimulation of Ca2+ levels and prolactin release in a pituitary cell line. Am. J. Physiol. Endocrinol. Metab., 288, E388-397. https://doi.org/10.1152/ajpendo.00349.2004
  8. Charpentier, A.H., Bednarek, A.K., Daniel, R.L., Hawkins, K.A., Laflin, K.J., Gaddis, S., MacLeod, M.C. and Aldaz, C.M. (2000). Effects of estrogen on global gene expression: identification of novel targets of estrogen action. Cancer Res., 60, 5977-5983.
  9. Choi, K.C. and Jeung, E.B. (2003). The biomarker and endocrine disruptors in mammals. J. Reprod. Dev., 49, 337-345. https://doi.org/10.1262/jrd.49.337
  10. Cobb, M.H. and Goldsmith, E.J. (1995). How MAP kinases are regulated. J. Biol. Chem., 270, 14843-14846. https://doi.org/10.1074/jbc.270.25.14843
  11. Couse, J.F., Lindzey, J., Grandien, K., Gustafsson, J.A. and Korach, K.S. (1997). Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptorbeta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology, 138, 4613-4621. https://doi.org/10.1210/en.138.11.4613
  12. Crisp, T.M., Clegg, E.D., Cooper, R.L., Wood, W.P., Anderson, D.G., Baetcke, K.P., Hoffmann, J.L., Morrow, M.S., Rodier, D.J., Schaeffer, J.E., Touart, L.W., Zeeman, M.G. and Patel, Y.M. (1998). Environmental endocrine disruption: an effects assessment and analysis. Environ. Health Perspect, 106 Suppl 1, 11-56. https://doi.org/10.2307/3433911
  13. Dang, V.H., Choi, K.C., Hyun, S.H. and Jeung, E.B. (2007a). Analysis of gene expression profiles in the offspring of rats following maternal exposure to xenoestrogens. Reprod. Toxicol., 23, 42-54. https://doi.org/10.1016/j.reprotox.2006.08.010
  14. Dang, V.H., Choi, K.C., Hyun, S.H. and Jeung, E.B. (2007b). Induction of uterine calbindin-D9k through an estrogen receptor-dependent pathway following single injection with xenobiotic agents in immature rats. J. Toxicol. Environ. Health A, 70, 171-182. https://doi.org/10.1080/15287390600755257
  15. Dang, V.H., Choi, K.C. and Jeung, E.B. (2007c). Tetrabromodiphenyl ether (BDE 47) evokes estrogenicity and calbindin-D9k expression through an estrogen receptor-mediated pathway in the uterus of immature rats. Toxicol. Sci., 97, 504-511. https://doi.org/10.1093/toxsci/kfm051
  16. Dang, V.H., Nguyen, T.H., Choi, K.C. and Jeung, E.B. (2007d). A calcium-binding protein, calbindin-D9k, is regulated through an estrogen-receptor mediated mechanism following xenoestrogen exposure in the GH3 cell line. Toxicol. Sci., 98, 408-415. https://doi.org/10.1093/toxsci/kfm120
  17. Dang, V.H., Choi, K.C. and Jeung, E.B. (2009a). Estrogen receptors are involved in xenoestrogen induction of growth hormone in the rat pituitary gland. J. Reprod. Dev., 55, 206-213. https://doi.org/10.1262/jrd.20147
  18. Dang, V.H., Nguyen, T.H., Lee, G.S., Choi, K.C. and Jeung, E.B. (2009b). In vitro exposure to xenoestrogens induces growth hormone transcription and release via estrogen receptor-dependent pathways in rat pituitary GH3 cells. Steroids, 74, 707-714. https://doi.org/10.1016/j.steroids.2009.03.002
  19. Dang, V.H., Choi, K.C. and Jeung, E.B. (2010). Membrane-impermeable estrogen is involved in regulation of calbindin-D9k expression via non-genomic pathways in a rat pituitary cell line, GH3 cells. Toxicol. In Vitro, In press.
  20. Daston, G.P., Cook, J.C. and Kavlock, R.J. (2003). Uncertainties for endocrine disrupters: our view on progress. Toxicol. Sci., 74, 245-252. https://doi.org/10.1093/toxsci/kfg105
  21. Dos Santos, E.G., Dieudonne, M.N., Pecquery, R., Le Moal, V., Giudicelli, Y. and Lacasa, D. (2002). Rapid nongenomic E2 effects on p42/p44 MAPK, activator protein-1, and cAMP response element binding protein in rat white adipocytes. Endocrinology, 143, 930-940. https://doi.org/10.1210/en.143.3.930
  22. Ellerkmann, E., Nagy, G.M. and Frawley, L.S. (1991). Rapid augmentation of prolactin cell number and secretory capacity by an estrogen-induced factor released from the neurointermediate lobe. Endocrinology, 129, 838-842. https://doi.org/10.1210/endo-129-2-838
  23. Filardo, E.J. (2002). Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid. Biochem. Mol. Biol., 80, 231-238. https://doi.org/10.1016/S0960-0760(01)00190-X
  24. Filardo, E.J., Quinn, J.A., Frackelton, A.R., Jr. and Bland, K.I. (2002). Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol., 16, 70-84. https://doi.org/10.1210/me.16.1.70
  25. Frasor, J., Barnett, D.H., Danes, J.M., Hess, R., Parlow, A.F. and Katzenellenbogen, B.S. (2003). Response-specific and ligand dose-dependent modulation of estrogen receptor (ER) alpha activity by ERbeta in the uterus. Endocrinology, 144, 3159-3166. https://doi.org/10.1210/en.2002-0143
  26. Hall, J.M. and McDonnell, D.P. (2005). Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting. Mol. Interv., 5, 343-357. https://doi.org/10.1124/mi.5.6.7
  27. Hess, R.A., Bunick, D., Lee, K.H., Bahr, J., Taylor, J.A., Korach, K.S. and Lubahn, D.B. (1997). A role for oestrogens in the male reproductive system. Nature, 390, 509-512. https://doi.org/10.1038/37352
  28. Hong, E., Choi, K.-C. and Jeung, E.-B. (2003). Maternal-fetal transfer of endocrine disruptors in the induction of Calbindin-D9k mRNA and protein during pregnancy in rat model. Mol. Cell. Endocrinol., 212, 63-72. https://doi.org/10.1016/j.mce.2003.08.011
  29. Hoyer, P.B. (2001). Reproductive toxicology: current and future directions. Biochem. Pharmacol., 62, 1557-1564. https://doi.org/10.1016/S0006-2952(01)00814-0
  30. Katzenellenbogen, J.A. and Katzenellenbogen, B.S. (1996). Nuclear hormone receptors: ligand-activated regulators of transcription and diverse cell responses. Chem. Biol., 3, 529-536. https://doi.org/10.1016/S1074-5521(96)90143-X
  31. Keefer, D.A., Stumpf, W.E. and Petrusz, P. (1976). Quantitative autoradiographic assessment of 3H-estradiol uptake in immunocytochemically characterized pituitary cells. Cell. Tissue. Res., 166, 25-35. https://doi.org/10.1007/BF00215122
  32. Kelly, M.J. and Levin, E.R. (2001). Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab., 12, 152-156. https://doi.org/10.1016/S1043-2760(01)00377-0
  33. Kuiper, G.G., Enmark, E., Pelto-Huikko, M., Nilsson, S. and Gustafsson, J.A. (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA, 93, 5925-5930. https://doi.org/10.1073/pnas.93.12.5925
  34. Laws, S.C., Carey, S.A., Ferrell, J.M., Bodman, G.J. and Cooper, R.L. (2000). Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol. Sci., 54, 154-167. https://doi.org/10.1093/toxsci/54.1.154
  35. Leung, K.C., Johannsson, G., Leong, G.M. and Ho, K.K. (2004). Estrogen regulation of growth hormone action. Endocr. Rev., 25, 693-721. https://doi.org/10.1210/er.2003-0035
  36. Levin, E.R. (2005). Integration of the extranuclear and nuclear actions of estrogen. Mol. Endocrinol., 19, 1951-1959. https://doi.org/10.1210/me.2004-0390
  37. Levine, J.E. (1997). New concepts of the neuroendocrine regulation of gonadotropin surges in rats. Biol. Reprod., 56, 293-302. https://doi.org/10.1095/biolreprod56.2.293
  38. Lieberman, M.E., Maurer, R.A., Claude, P. and Gorski, J. (1982). Prolactin synthesis in primary cultures of pituitary cells: regulation by estradiol. Mol. Cell. Endocrinol., 25, 277-294. https://doi.org/10.1016/0303-7207(82)90084-3
  39. MacLusky, N.J. and Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science, 211, 1294-1302. https://doi.org/10.1126/science.6163211
  40. Marino, M., Acconcia, F. and Ascenzi, P. (2005). Estrogen receptor signalling: bases for drug actions. Curr. Drug. Targets. Immune. Endocr. Metabol. Disord., 5, 305-314. https://doi.org/10.2174/1568008054863763
  41. Marino, M., Galluzzo, P. and Ascenzi, P. (2006). Estrogen signaling multiple pathways to impact gene transcription. Curr. Genomics, 7, 497-508. https://doi.org/10.2174/138920206779315737
  42. Micevych, P.E. and Mermelstein, P.G. (2008). Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol. Neurobiol., 38, 66-77. https://doi.org/10.1007/s12035-008-8034-z
  43. Mitchner, N.A., Garlick, C., Steinmetz, R.W. and Ben-Jonathan, N. (1999). Differential regulation and action of estrogen receptors alpha and beta in GH3 cells. Endocrinology, 140, 2651-2658. https://doi.org/10.1210/en.140.6.2651
  44. Mosselman, S., Polman, J. and Dijkema, R. (1996). ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett., 392, 49-53. https://doi.org/10.1016/0014-5793(96)00782-X
  45. Nilsson, S., Makela, S., Treuter, E., Tujague, M., Thomsen, J., Andersson, G., Enmark, E., Pettersson, K., Warner, M. and Gustafsson, J.A. (2001). Mechanisms of estrogen action. Physiol. Rev., 81, 1535-1565. https://doi.org/10.1152/physrev.2001.81.4.1535
  46. Nishihara, E., Nagayama, Y., Inoue, S., Hiroi, H., Muramatsu, M., Yamashita, S. and Koji, T. (2000). Ontogenetic changes in the expression of estrogen receptor alpha and beta in rat pituitary gland detected by immunohistochemistry. Endocrinology, 141, 615-620. https://doi.org/10.1210/en.141.2.615
  47. Paech, K., Webb, P., Kuiper, G.G., Nilsson, S., Gustafsson, J., Kushner, P.J. and Scanlan, T.S. (1997). Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science, 277, 1508-1510. https://doi.org/10.1126/science.277.5331.1508
  48. Park, S.H., Kim, K.Y., An, B.S., Choi, J.H., Jeung, E.B., Leung, P.C. and Choi, K.C. (2009). Cell growth of ovarian cancer cells is stimulated by xenoestrogens through an estrogen-dependent pathway, but their stimulation of cell growth appears not to be involved in the activation of the mitogen-activated protein kinases ERK-1 and p38. J. Reprod. Dev., 55, 23-29. https://doi.org/10.1262/jrd.20094
  49. Pelletier, G., Liao, N., Follea, N. and Govindan, M.V. (1988). Distribution of estrogen receptors in the rat pituitary as studied by in situ hybridization. Mol. Cell. Endocrinol., 56, 29-33. https://doi.org/10.1016/0303-7207(88)90005-6
  50. Pujol, P., Rey, J.M., Nirde, P., Roger, P., Gastaldi, M., Laffargue, F., Rochefort, H. and Maudelonde, T. (1998). Differential expression of estrogen receptor-alpha and -beta messenger RNAs as a potential marker of ovarian carcinogenesis. Cancer. Res., 58, 5367-5373.
  51. Qin, C., Samudio, I., Ngwenya, S. and Safe, S. (2004). Estrogendependent regulation of ornithine decarboxylase in breast cancer cells through activation of nongenomic cAMP-dependent pathways. Mol. Carcinog., 40, 160-170. https://doi.org/10.1002/mc.20030
  52. Revelli, A., Massobrio, M. and Tesarik, J. (1998). Nongenomic actions of steroid hormones in reproductive tissues. Endocr. Rev., 19, 3-17. https://doi.org/10.1210/er.19.1.3
  53. Roy, D., Angelini, N.L. and Belsham, D.D. (1999). Estrogen directly respresses gonadotropin-releasing hormone (GnRH) gene expression in estrogen receptor-alpha (ERalpha)- and ERbeta-expressing GT1-7 GnRH neurons. Endocrinology, 140, 5045-5053. https://doi.org/10.1210/en.140.11.5045
  54. Sarkar, D.K., Kim, K.H. and Minami, S. (1992). Transforming growth factor-beta 1 messenger RNA and protein expression in the pituitary gland: its action on prolactin secretion and lactotropic growth. Mol. Endocrinol., 6, 1825-1833. https://doi.org/10.1210/me.6.11.1825
  55. Sharpe. (1998a). The roles of oestrogen in male. Trends Endocrinol. Metab., 9, 371-377. https://doi.org/10.1016/S1043-2760(98)00089-7
  56. Sharpe. (1998b). Environmental oestrogen and male infertility. Pure. Appl. Chem., 70, 1685-1701. https://doi.org/10.1351/pac199870091685
  57. Steinmetz, R., Brown, N.G., Allen, D.L., Bigsby, R.M. and Ben-Jonathan, N. (1997). The environmental estrogen bisphenol A stimulates prolactin release in vitro and in vivo. Endocrinology, 138, 1780-1786. https://doi.org/10.1210/en.138.5.1780
  58. Tinnanooru, P., Dang, V.H., Nguyen, T.H., Lee, G.S., Choi, K.C. and Jeung, E.B. (2008). Estrogen regulates the localization and expression of calbindin-D9k in the pituitary gland of immature male rats via the ERalpha-pathway. Mol. Cell. Endocrinol., 285, 26-33. https://doi.org/10.1016/j.mce.2008.01.011
  59. Tokunaga, E., Kimura, Y., Mashino, K., Oki, E., Kataoka, A., Ohno, S., Morita, M., Kakeji, Y., Baba, H. and Maehara, Y. (2006). Activation of PI3K/Akt signaling and hormone resistance in breast cancer. Breast Cancer, 13, 137-144. https://doi.org/10.2325/jbcs.13.137
  60. Toppari, J., Larsen, J.C., Christiansen, P., Giwercman, A., Grandjean, P., Guillette, L.J., Jr., Jegou, B., Jensen, T.K., Jouannet, P., Keiding, N., Leffers, H., McLachlan, J.A., Meyer, O., Muller, J., Rajpert-De Meyts, E., Scheike, T., Sharpe, R., Sumpter, J. and Skakkebaek, N.E. (1996). Male reproductive health and environmental xenoestrogens. Environ. Health Perspect, 104 Suppl 4, 741-803.
  61. Treeck, O., Pfeiler, G., Mitter, D., Lattrich, C., Piendl, G. and Ortmann, O. (2007). Estrogen receptor {beta}1 exerts antitumoral effects on SK-OV-3 ovarian cancer cells. J. Endocrinol., 193, 421-433. https://doi.org/10.1677/JOE-07-0087
  62. Turgeon, J.L. and Waring, D.W. (1981). Acute progesterone and 17 beta-estradiol modulation of luteinizing hormone secretion by pituitaries of cycling rats superfused in vitro. Endocrinology, 108, 413-419. https://doi.org/10.1210/endo-108-2-413
  63. Turner, R.T., Riggs, B.L. and Spelsberg, T.C. (1994). Skeletal effects of estrogen. Endocr. Rev., 15, 275-300.
  64. Vo, T.T., Jung, E.M., Dang, V.H., Jung, K., Baek, J., Choi, K.C. and Jeung, E.B. (2009a). Differential effects of flutamide and di-(2-ethylhexyl) phthalate on male reproductive organs in a rat model. J. Reprod. Dev., 55, 400-411. https://doi.org/10.1262/jrd.20220
  65. Vo, T.T., Jung, E.M., Dang, V.H., Yoo, Y.M., Choi, K.C., Yu, F.H. and Jeung, E.B. (2009b). Di-(2 ethylhexyl) phthalate and flutamide alter gene expression in the testis of immature male rats. Reprod. Biol. Endocrinol., 7, 104. https://doi.org/10.1186/1477-7827-7-104
  66. Waring, R.H. and Harris, R.M. (2005). Endocrine disrupters: a human risk? Mol. Cell. Endocrinol., 244, 2-9. https://doi.org/10.1016/j.mce.2005.02.007
  67. Watanabe, H., Suzuki, A., Kobayashi, M., Takahashi, E., Itamoto, M., Lubahn, D.B., Handa, H. and Iguchi, T. (2003). Analysis of temporal changes in the expression of estrogen-regulated genes in the uterus. J. Mol. Endocrinol., 30, 347-358. https://doi.org/10.1677/jme.0.0300347
  68. Watson, C.S., Bulayeva, N.N., Wozniak, A.L. and Alyea, R.A. (2007). Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids, 72, 124-134. https://doi.org/10.1016/j.steroids.2006.11.002
  69. Watters, J.J., Chun, T.Y., Kim, Y.N., Bertics, P.J. and Gorski, J. (2000). Estrogen modulation of prolactin gene expression requires an intact mitogen-activated protein kinase signal transduction pathway in cultured rat pituitary cells. Mol. Endocrinol., 14, 1872-1881. https://doi.org/10.1210/me.14.11.1872
  70. Williams, K., McKinnell, C., Saunders, P.T., Walker, M., Fisher, J.S., Turner, K.J., Atanassova, N. and Sharpe, M. (2001). Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Hum. Reprod. Update, 7, 236-247. https://doi.org/10.1093/humupd/7.3.236
  71. Wilson, M.E., Price, R.H., Jr. and Handa, R.J. (1998). Estrogen receptor-beta messenger ribonucleic acid expression in the pituitary gland. Endocrinology, 139, 5151-5156. https://doi.org/10.1210/en.139.12.5151

피인용 문헌

  1. Chlorinated biphenyls effect on estrogen-related receptor expression, steroid secretion, mitochondria ultrastructure but not on mitochondrial membrane potential in Leydig cells vol.369, pp.2, 2017, https://doi.org/10.1007/s00441-017-2596-x
  2. Computational prediction models for assessing endocrine disrupting potential of chemicals pp.1532-4095, 2018, https://doi.org/10.1080/10590501.2018.1537132