Prostate development: Mechanisms for opposite effects of low and high doses of estrogenic chemicals

Endocrine Disruptors: Effects on Male and Female Reproductive Systems, Second Edition

Volumn , Issue , 2004, Pages 379-410

  Richter, Catherine A ^a   Timms, Barry G ^b   vom Saal, Frederick S ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 16444378551     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (141)

1. Pang, S., Chow, P., and Wong, T., The role of the seminal vesicles, coagulating glands and prostate on the fertility and fecundity of mice, J. Reprod. Fertil., 56, 129, 1979.
2. Zuckerman, S., The endocrine control of the prostate, Proc. R. Soc. Med., 29, 1557, 1936.
3. Franks, L.M., Benign nodular hyperplasia of the prostate: a review, Annals of the Royal College Surgeons of England, 14, 92, 1954.
4. Prins, G.S., Developmental estrogenization of the prostate gland, in Prostate: Basic and Clinical Aspects, Naz, R.K., CRC Press, Boca Raton, FL, 1997, pp. 247.
5. Gupta, C., Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals, Proc. Soc. Exp. Biol. Med., 224, 61, 2000.
6. Welshons, W.V. et al. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity, Environ. Health Perspect., 111, 994, 2003.
7. Nagel, S.C. et al. 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, 1997.
8. vom Saal, F.S. et al. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses, Proc. Natl. Acad. Sci. USA, 94, 2056, 1997.
9. Montano, M.M., Welshons, W.V., and vom Saal, F.S., Free estradiol in serum and brain uptake of estradiol during fetal and neonatal sexual differentiation in female rats, Biol. Reprod., 53, 1198, 1995.
10. Weir, H.K. et al. Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control, J. Natl. Cancer Inst., 95, 1276, 2003.
11. Verhamme, K.M. et al. Incidence and prevalence of lower urinary tract symptoms suggestive of benign prostatic hyperplasia in primary care-the Triumph project, Eur. Urol., 42, 323, 2002.
12. Burstein, S.R., The historical background of gerontology. III. The quest for rejuvenation, Geriatrics, 10, 536, 1955.
13. Medvei, V.C., A History of Endocrinology, MTP Press, Lancaster, PA, 1982.
14. Tisell, L.-E. and Salander, H., The lobes of the human prostate, Scand. J. Urol. Nephrol., 9, 185, 1975.
15. McNeal, J.E., Anatomy of the prostate: An historical survey of divergent views, The Prostate, 1, 3, 1980.
16. Timms, B.G., Anatomical perspectives of prostate development, in Prostate: Basic and Clinical Aspects, Naz, R.K., CRC Press, New York, 1997.
17. Lowsley, O.S., The development of the human prostate gland with reference to the development of other structures at the neck of the urinary bladder, Am. J. Anat., 13, 299, 1912.
18. McNeal, J.E., The prostate gland: Morphology and pathobiology, Monographs in Urology, 4, 1, 1983.
19. Timms, B.G., Mohs, T.J., and Didio, L.J.A., Ductal budding and branching patterns in the developing prostate, J. Urol., 151, 1427, 1994.
20. Takeda, H., Lasnitzki, I., and Mizuno, T., Analysis of prostatic bud induction by brief androgen treatment in the fetal rat urogenital sinus, J. Endocrinol., 110, 467, 1986.
21. Marker, P.C. et al. Hormonal, cellular, and molecular control of prostatic development, Dev. Biol., 253, 165, 2003.
22. Sugimura, Y., Cunha, G.R., and Donjacour, A.A., Morphogenesis of ductal networks in the mouse prostate, Biol. Reprod., 34, 961, 1986.
23. Lavoipierre, A.M., Ultrasound of the prostate and testicles, World J. Surg., 24, 198, 2000.
24. Sugimura, Y. et al. Whole-mount autoradiography study of DNA synthetic activity during postnatal development and androgen-induced regeneration in the mouse prostate, Biol. Reprod., 34, 985, 1986.
25. Sugimura, Y., Cunha, G.R., and Donjacour, A.A., Morphological and histological study of castration-induced degeneration and androgen-induced regeneration in the mouse prostate, Biol. Reprod., 34, 973, 1986.
26. Hayward, S.W. et al. Interactions between adult human prostatic epithelium and rat urogenital sinus mesenchyme in a tissue recombination model, Differentiation, 63, 131, 1998.
27. McNeal, J., Pathology of benign prostatic hyperplasia. Insight into etiology, Urol. Clin. North Am., 17, 477, 1990.
28. Price, D., Comparative aspects of development and structure in the prostate, Natl. Cancer Inst. Monogr., 12, 1, 1963.
29. McNeal, J.E., The anatomic heterogeneity of the prostate, in Models of Prostate Cancer, Coffey, D., Merchant, D., and Murphy, G., Liss, New York, 1980, pp. 149.
30. Hiraoka, Y. and Akimoto, M., Anatomy of the Prostate from Fetus to Adult-Origin of Benign Prostatic Hyperplasia, Urol. Res., 177, 1987.
31. Aumüller, G., Morphologic and regulatory aspects of prostatic function, Anat. Embryol., 179, 519, 1989.
32. Thomson, A.A. et al. The role of smooth muscle in regulating prostatic induction, Development, 129, 1905, 2002.
33. Adams, J.Y. et al. Expression of estrogen receptor beta in the fetal, neonatal, and prepubertal human prostate, Prostate, 52, 69, 2002.
34. Aboseif, S. et al. Mesenchymal reprogramming of adult human epithelial differentiation, Differentiation, 65, 113, 1999.
35. Block, E., Lew, M., and Klein, M., Studies on the inhibition of fetal androgen formation: Testosterone synthesis by fetal and newborn mouse testes in vitro, Endocrinol., 88, 41, 1971.
36. Wilson, J.D., George, F.W., and Griffin, J.E., The hormonal control of sexual development, Science, 211, 1278, 1981.
37. vom Saal, F.S., Sexual differentiation in litter bearing mammals: influence of sex of adjacent fetuses in utero, J. Anim. Sci., 67, 1824, 1989.
38. vom Saal, F.S., Montano, M.M., and Wang, M.H., Sexual differentiation in mammals, in Chemically Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection, Colborn, T. and Clement, C., Princeton Scientific Publishing Co., Princeton, NJ, 1992, pp. 17.
39. Roy, A.K. et al. Regulation of androgen action, Vitam. Horm., 55, 309, 1999.
40. Bardin, C.W. and Catterall, J.F., Testosterone: a major determinant of extragenital sexual dimorphism, Science, 211, 1285, 1981.
41. Dadras, S.S. et al. Inhibition of 5 a-reductase in rat prostate reveals differential regulation of androgen-response gene expression by testosterone and dihydrotestosterone, Gene Expr., 9, 183, 2001.
42. Cunha, G.R. and Chung, L.W., Stromal-epithelial interactions-I. Induction of prostatic phenotype in urothelium of testicular feminized (Tfm/y) mice, J. Steroid Biochem., 14, 1317, 1981.
43. Shannon, J.M. and Cunha, G.R., Autoradiographic localization of androgen binding in the developing mouse prostate, The Prostate, 4, 367, 1983.
44. Takeda, H. et al. Autoregulation of androgen receptor expression in rodent prostate: Immunohistochemical and in situ hybridization analysis, Biochem. Biophys. Res. Commun., 177, 488, 1991.
45. Davies, J.A., Do different branching epithelia use a conserved developmental mechanism?, Bioessays, 24, 937, 2002.
46. Gioeli, D. et al. Androgen receptor phosphorylation: Regulation and identification of the phosphorylation sites, J. Biol. Chem., 277, 29304, 2002.
47. Gupta, C., Modulation of androgen receptor (AR)-mediated transcriptional activity by EGF in the developing mouse reproductive tract primary cells, Mol. Cell. Endocrinol., 152, 169, 1999.
48. Thomson, A.A., Foster, B.A., and Cunha, G.R., Analysis of growth factor and receptor mRNA levels during development of the rat seminal vesicle and prostate, Development, 124, 2431, 1997.
49. Donjacour, A.A., Thomson, A.A., and Cunha, G.R., FGF-10 plays an essential role in the growth of the fetal prostate, Dev. Biol., 261, 39, 2003.
50. Thomson, A.A. and Cunha, G.R., Prostatic growth and development are regulated by FGF10, Development, 126, 3693, 1999.
51. Ruan, W.F. et al. Evidence that insulin-like growth factor I and growth hormone are required for prostate gland development, Endocrinol., 140, 1984, 1999.
52. Abbott, B.D. et al. Lack of expression of EGF and TGF-a in the fetal mouse alters formation of prostatic epithellial buds and influences the response to TCDD, Toxicol. Sci., 76, 427, 2003.
53. Itoh, N., Patel, U., and Skinner, M.K., Developmental and hormonal regulation of transforming growth factor-a and epidermal growth factor receptor gene expression in isolated prostatic epithelial and stromal cells, Endocrinol., 139, 1369, 1998.
54. Marker, P.C. et al. fucosyltransferase1 and H-type complex carbohydrates modulate epithelial cell proliferation during prostatic branching morphogenesis, Dev. Biol., 233, 95, 2001.
55. Ball, E.M.A. and Risbridger, G.P., New perspectives on growth factor-sex steroid interaction in the prostate, Cytokine Growth Factor Rev., 14, 5, 2003.
56. Itoh, N. et al. Developmental and hormonal regulation of transforming growth factor-ß1 (TGFß1), -2, and -3 gene expression in isolated prostatic epithelial and stromal cells: epidermal growth factor and TGFß interactions, Endocrinol., 139, 1378, 1998.
57. Lamm, M.L.G. et al. Mesenchymal factor bone morphogenetic protein 4 restricts ductal budding and branching morphogenesis in the developing prostate, Dev. Biol., 232, 301, 2001.
58. Kincl, F., Pi., A., and Lasso, L., Effects of estradiol benzoate treatment in the newborn male rat, Endocrinol., 72, 966, 1963.
59. Arai, Y., Nature of metaplasia in rat coagulating glands induced by neonatal treatment with estrogen, Endocrinology, 86, 918, 1970.
60. Rajfer, J. and Coffey, D.S., Sex steroid imprinting of the immature prostate, Invest. Urol., 16, 186 1978.
61. Rajfer, J. and Coffey, D.S., Effects of neonatal steroids on male sex tissues, Invest. Urol., 17, 3, 1979.
62. Vannier, B. and Raynaud, J.P., Long-term effects of prenatal oestrogen treatment on genital morphology and reproductive function in the rat, J. Reprod. Fertil., 59, 43, 1980.
63. Lung, B. and Cunha, G.R., Development of seminal vesicles and coagulating glands in neonatal mice. I. the morphogenetic effects of various hormonal conditions, The Anatomical Record, 199, 73, 1981.
64. Prins, G.S., Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression, Endocrinology, 130, 2401, 1992.
65. Prins, G.S. et al. Effects of neonatal estrogen exposure on prostatic secretory genes and their correlation with androgen receptor expression in the separate prostate lobes of the adult rat, Endocrinology, 132, 2387, 1993.
66. Santti, R. et al. Developmental estrogenization and prostatic neoplasia, The Prostate, 24, 67, 1994.
67. Baranao, J. et al. Effects of androgen treatment of the neonate on rat testis and sex accessory organs, Biol. Reprod., 25, 851, 1981.
68. Jarred, R.A. et al. Evidence that estrogens directly alter androgen-regulated prostate development, Endocrinology, 141, 3471, 2000.
69. Arai, Y., Chen, C.-Y., and Nishizuka, Y., Cancer development in male reproductive tract in rats given diethylstilbestrol at neonatal age, Jpn. J. Cancer Res., 69, 861, 1978.
70. McLachlan, J.A., Newbold, R.R., and Bullock, B., Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol, Science, 190, 991, 1975.
71. Driscoll, S.G. and Taylor, S.H., Effects of prenatal maternal estrogen on the male urogenital system, Obstet. Gynecol., 56, 537, 1980.
72. Martikainen, P. et al. Interaction of male and female sex hormones in cultured rat prostate, Prostate, 11, 291, 1987.
73. Newbold, R., Cellular and molecular effects of developmental exposure to diethylstilbestrol: Implications for other environmental estrogens, Environ. Health Perspect., 103, 83, 1995.
74. Swan, S.H. and vom Saal, F.S., Alterations in male reproductive development: The role of endocrine disrupting chemicals, in Endocrine Disruptors in the Environment, Metzler, M., Springer-Verlag, Heidelberg, 2001, pp. 131.
75. Nonneman, D.J. et al. Intrauterine position effects on steroid metabolism and steroid receptors of reproductive organs in male mice, Biol. Reprod., 47, 723, 1992.
76. Timms, B.G., Petersen, S.L., and vom Saal, F.S., Prostate gland growth during development is stimulated in both male and female rat fetuses by intrauterine proximity to female fetuses, J. Urol., 161, 1694, 1999.
77. Blacklock, N.J., The development and morphology of the prostate, in The Endocrinology of Prostate Tumours, Ghanadian, R., MTP Press, Lancaster, England, 1983, pp. 1.
78. Welshons, W.V. et al. Development of in vitro assays to predict activity of xenoestrogens in animals: fetal exposure to methoxychlor and other xenoestrogens increases adult prostate size in mice, Toxicol. Ind. Health, 15, 12, 1999.
79. Timms, B.G. et al. Estrogenic chemicals in plastic and oral contraceptives disrupt the fetal mouse prostate and urethra, Submitted, 2004.
80. Mawhinney, M. and Neubauer, B., Actions of estrogen in the male, Invest. Urol., 16, 409, 1979.
81. Jung-Testas, I. et al. Androgen and estrogen receptors in rat ventral prostate epithelium and stroma, Endocrinol., 109, 1287, 1981.
82. Cunha, G.R. et al. The endocrinology and developmental biology of the prostate, Endocr. Rev., 8, 338, 1987.
83. Cooke, P.S. et al. Estrogen Receptor Expression in Developing Epididymis, Efferent Ductules, and Other Male Reproductive Organs, Endocrinol., 128, 2874, 1992.
84. Kuiper, G.G.J.M. et al. Cloning of a novel estrogen receptor expressed in rat prostate and ovary, Proc. Natl. Acad. Sci. USA, 93, 5925, 1996.
85. Routhledge, E.J. et al. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) a and ERß, J. Biol. Chem., 46, 35986, 2000.
86. Salvatori, L. et al. Oestrogens and selective oestrogen receptor (ER) modulators regulate EGF receptor gene expression through human ER a and ß subtypes via an Sp1 site, Oncogene, 22, 4875, 2003.
87. Prins, G.S. et al. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor a: studies with aERKO and ßERKO mice, Cancer Res., 61, 6089, 2001.
88. Kumar, V.M., Leo, M.E., and Tindall, D.J., Modulation of androgen receptor transcriptional activity by the estrogen receptor, J. Androl., 15, 534, 1994.
89. Collins, A.T. et al. Androgen and oestrogen responsiveness of stromal cells derived from the human hyperplastic prostate: oestrogen regulation of the androgen receptor, J. Endocrinol., 143, 269, 1994.
90. Yeh, S. et al. From estrogen to androgen receptor: A new pathway for sex hormones in prostate, Proc. Natl. Acad. Sci. USA, 95, 5527, 1998.
91. Richter, C.A. and vom Saal, F.S., Dioxin interacts with estrogen and androgen response systems to disrupt prostate development, Organohalogen Compounds, 65, 63, 2003.
92. Richter, C.A. et al. Estradiol upregulates androgen receptor mRNA in fetal mouse urogenital sinus mesenchyme cells, Submitted, 2004.
93. Woodham, C., Birch, L., and Prins, G.S., Neonatal estrogen down-regulates prostatic androgen receptor through a proteosome-mediated protein degradation pathway, Endocrinol., 144, 4841, 2003.
94. Coser, K.R. et al. Global analysis of ligand sensitivity of estrogen inducible and suppressible genes in MCF7/BUS breast cancer cells by DNA microarray, Proc. Natl. Acad. Sci. USA, 100, 13994, 2003.
95. Bektic, J. et al. Identification of genes involved in estrogenic action in the human prostate using microarray analysis, Genomics, 83, 34, 2004.
96. Migliaccio, A. et al. Steroid-induced androgen receptor-oestradiol receptor ß-Src complex triggers prostate cancer cell proliferation, EMBO J., 19, 5406, 2000.
97. Lee, S.R. et al. AR and ER interaction with a p21-activated kinase (PAK6), Mol. Endocrinol., 16, 85, 2002.
98. Panet-Raymond, V. et al. Interactions between androgen and estrogen receptors and the effects on their transactivational properties, Mol. Cell. Endocrinol., 167, 139, 2000.
99. Adesanya-Famuyiwa, O.O. et al. Localization and sex steroid regulation of androgen receptor gene expression in rhesus monkey uterus, Obstet. Gynecol., 93, 265, 1999.
100. Esposito, T. et al. Regulation of androgen receptor mRNA expression in primary culture of Harderian gland cells: cross-talk between steroid hormones, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 132, 97, 2002.
101. Suzuki, K. et al. Synergistic effects of estrogen and androgen on the prostate: Effects of estrogen on androgen-and estrogen-receptors, BrdU uptake, immunohistochemical study of AR, and responses to antiandrogens, Prostate, 26, 151, 1995.
102. Gupta, C., The role of estrogen receptor, androgen receptor and growth factors in diethylstilbestrol-induced programming of prostate differentiation, Urol. Res., 28, 223, 2000.
103. Ignar-Trowbridge, D.M. et al. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor, Proc. Natl. Acad. Sci. USA, 89, 4658, 1992.
104. Trachtenberg, J., Hicks, L.L., and Walsh, P.C., Androgen-and estrogen-receptor content in spontaneous and experimentally induced canine prostatic hyperplasia, J. Clin. Invest., 65, 1051, 1980.
105. Roselli, C.E. and Fasasi, T.A., Estradiol increases the duration of nuclear receptor occupation in the preoptic area of the male rat treated with testosterone, J. Steroid Bochem. Mol. Biol., 42, 161, 1992.
106. Challis, J.R.G. and Lye, S.J., Parturition, in Physiology of Reproduction, Knobil, E., Neill, J., and Pfaff, D., Raven Press, New York, 1994, pp. 985.
107. Clark, J.H. and Mani, S.K., Actions of ovarian steroid hormones, in Physiology of Reproduction, Knobil, E., Neill, J., and Pfaff, D., Raven Press, New York, 1994, pp. 1011.
108. McPherson, S.J. et al. Elevated androgens and prolactin in aromatase-deficient mice cause enlargement, but not malignancy, of the prostate gland, Endocrinology, 142, 2458, 2001.
109. Colborn, T., vom Saal, F.S., and Soto, A.M., Developmental effects of endocrine disrupting chemicals in wildlife and humans, Environ. Health Perspect., 101, 378, 1993.
110. Kavlock, R.J. et al. Research needs for the risk assessment of health and environmental effects of endocrine disruptors: A report of the US EPA sponsored workshop, Environ. Health Perspect. Suppl., 104, 715, 1996.
111. Ralph, J.L. et al. Disruption of androgen regulation in the prostate by the environmental contaminant hexachlorobenzene, Environ. Health Perspect., 111, 461, 2003.
112. vom Saal, F.S. et al. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior, Toxicol. Ind. Health, 14, 239, 1998.
113. Howdeshell, K.L. et al. Exposure to bisphenol A advances puberty, Nature, 401, 763, 1999.
114. Stumpf, W.E., Narbaitz, R., and Sar, M., Estrogen receptors in the fetal mouse, J. Steroid Biochem., 12, 55, 1980.
115. Djoesland, O., Androgen metabolism by rat epididymis: effects of castration and antiandrogens, Steroids, 27, 47, 1976.
116. Tindall, V.J., French, F.S., and Nayfeh, S.N., Estradiol-17ß inhibition of androgen uptake and binding in epididymis of adult male rats in vivo: A comparison with cyproterone acetate, Steroids, 37, 257, 1981.
117. Wetherill, Y.B. et al. The xenoestrogen bisphenol A induces inappropriate androgen receptor activation and mitogenesis in prostate adenocarcinoma cells, Mol. Cancer Therap., 7, 515, 2002.
118. Schönfelder, G. et al. Parent bisphenol A accumulation in human maternal-fetalplacental unit, Environ. Health Perspect., 110, A703, 2002.
119. Thayer, K.A. et al. Altered reproductive organs in male mice exposed prenatally to sub-clinical doses of 17a-ethinyl estradiol, Hum. Reprod., 16, 988, 2001.
120. Soeffing, W.J. and Timms, B.G., Localization of androgen receptor and cell specific cytokeratins in basal cells of rat ventral prostate, J. Androl., 16, 197, 1995.
121. Zalko, D. et al. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD-1 mice, Environ. Health Perspect., 111, 309, 2003.
122. Richter, C.A. et al. Androgen receptor mRNA is upregulated by estrogen in mouse prostate primary cell culture, Toxicol. Sci., 72(S-1), 238, 2003.
123. Nagao, T. et al. Low-dose bisphenol A does not affect reproductive organs in estrogensensitive C57BL/6N mice exposed at the sexually mature, juvenile, or embryonic stage, Reprod. Toxicol., 16, 123, 2002.
124. Spearow, J.L. et al. Genetic variation in susceptibility to endocrine disruption by estrogen in mice, Science, 285, 1259, 1999.
125. Ramos, J.G. et al. Prenatal exposure to low doses of bisphenol A alters the periductal stroma and glandular cell function in the rat ventral prostate, Biol. Reprod., 65, 1271, 2001.
126. DeKlerk, D.P. et al. Comparison of spontaneous and experimentally induced canine prostatic hyperplasia, J. Clin. Invest., 64, 842, 1979.
127. Leav, I. et al. Biochemical alterations in sex hormone-induced hyperplasia and dysplasia of the dorsolateral prostates of Noble rats, J. Natl. Cancer Inst., 80, 1045, 1988.
128. Risbridger, G.P. et al. Oestrogens and prostate cancer, Endocrine-Related Cancer, 10, 187, 2003.
129. Noble, R.L., Prostate carcinoma of the Nb rat in relation to hormones, Int. Rev. Exp. Pathol., 23, 113, 1982.
130. Leav, I. et al. Androgen supported-estrogen enhancement of epithelial proliferation in the prostate of intact Noble rats, Prostate, 15, 23, 1989.
131. Ofner, P., Bosland, M., and Vena, R.L., Differential effects of diethystilbestrol and estradiol-17ß in combination with testosterone on rat prostate lobes, Toxicol. Appl. Pharmacol., 112, 300, 1992.
132. Ho, S.-M. et al. The conjoint actions of androgens and estrogens in the induction of proliferative lesions in the rat prostate, in Hormonal Carcinogenesis, Li, J.J., Li, S.A., and Nandi, S., Springer-Verlag, New York, 1992.
133. McNeal, J.E. and Bostwich, D.G., Intraductal dysplasia: A premalignant lesion of the prostate, Hum. Pathol., 17, 64, 1986.
134. Paulozzi, L.J., Erickson, J.D., and Jackson, R.J., Hypospadias trends in two US surveillance systems, Pediatrics, 100, 831, 1997.
135. Baskin, L.S., Himes, K., and Colborn, T., Hypospadias and endocrine disruption: Is there a connection?, Environ. Health Perspect., 109, 1175, 2001.
136. Carlsen, E. et al. Declining semen quality and incresaing incidence of testicular cancer: Is there a common cause?, Environ. Health Perspect., 103 (Suppl 7), 137, 1995.
137. Hass, G.P. and Sakr, W.A., Epidemiology of prostate cancer, CA. Cancer J. Clin., 47, 273, 1997.
138. Swan, S.H., Elkin, E.P., and Fenster, L., Have sperm densities declined: A reanalysis of global trend data, Environ. Health Perspect., 105, 1228, 1997.
139. Swan, S.H. et al. Semen quality in relation to biomarkers of pesticide exposure, Environ. Health Perspect., 111, 1478, 2003.
140. Allan, F.D., Essentials of Human Embryology, Oxford University Press, New York, 1960.
141. Timms, B.G., Peterson, R.E., and F.S., V.S., 2,3,7,8-Tetrachlorodibenzo-p-dioxin interacts with endogenous estradiol to disrupt prostate gland morphogenesis in male rat fetuses, Tox. Sci., 67, 264, 2002.