Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T09:03:42.597Z Has data issue: false hasContentIssue false
  • English
  • Français

Early-life estrogens and prostate cancer in an animal model

Published online by Cambridge University Press:  09 November 2010

G. S. Prins  and
S.-M. Ho
G. S. Prins*
Affiliation:
Departments of Urology and Physiology, University of Illinois at Chicago, Illinois, USA
S.-M. Ho
Affiliation:
Department of Environmental Health, University of Cincinnati, Ohio, USA
*
*Address for correspondence: G. S. Prins, PhD, Department of Urology, University of Illinois at Chicago, 820 S Wood St, MC955, Chicago, IL 60612, USA. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

While early-life estrogens are thought to play a physiologic role in prostate gland development, inappropriate estrogenic exposures either in dose, type or temporally can reprogram the prostate gland and increase susceptibility to abnormal prostate growth with aging including carcinogenesis. This review discusses the evidence for developmental estrogenic reprogramming that leads to adult prostate disease in a rat model. We propose that estrogen imprinting of the prostate is mediated through both structural reorganization of the gland early in life and epigenomic reprogramming that permits life-long memory of the inappropriate developmental exposures including heightened sensitivity to rising estradiol levels with aging. Complex interactions between early epigenetic programming and later-life experiences results in an emergence of multiple epigenomic outcomes, with some contributing to carcinogenesis with aging.

Keywords

bisphenol Aestrogenestrogenizationprostate developmentreprogramming
Type
Reviews
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 6 , December 2010 , pp. 365 - 370
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Prins, GS, Putz, O. Molecular signaling pathways that regulate prostate gland development. Differentiation. 2008; 6, 641–659.CrossRefGoogle Scholar
2. Ekbom, A, Hsieh, CC, Lipworth, L, et al. Perinatal characteristics in relation to incidence of and mortality from prostate cancer. Br Med J. 1996; 313, 337–341.CrossRefGoogle ScholarPubMed
3. Driscoll, SG, Taylor, SH. Effects of prenatal maternal estrogen on the male urogenital system. Obstet Gynecol. 1980; 56, 537–542.Google ScholarPubMed
4. Arai, Y, Chen, CY, Nishizuka, Y. Cancer development in male reproductive tract in rats given diethylstilbestrol at neonatal age. Gann. 1978; 69, 861–862.Google ScholarPubMed
5. Prins, GS. Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology. 1992; 130, 3703–3714.CrossRefGoogle ScholarPubMed
6. Prins, GS, Birch, L, Habermann, H, et al. Influence of neonatal estrogens on rat prostate development. Reprod Fertil Dev. 2001; 13, 241–252.CrossRefGoogle ScholarPubMed
7. Prins, GS, Huang, L, Birch, L, Pu, Y. The role of estrogens in normal and abnormal development of the prostate gland. Annals of the New York Academy of Sciences. 2006; 1089, 1–13.CrossRefGoogle ScholarPubMed
8. Prins, GS. Developmental estrogenization of the prostate gland. In Prostate: Basic and Clinical Aspects (ed. Naz RK), 1997: Chapter 10; pp. 247–265. C. R. C. Press, Boca Raton.Google Scholar
9. Putz, O, Schwartz, CB, Kim, S, LeBlanc, GA, Cooper, RL, Prins, GS. Neonatal low- and high-dose exposure to estradiol benzoate in the male rat: I. Effects on the prostate gland. Biol Reprod. 2001; 65, 1496–1505.CrossRefGoogle Scholar
10. Bosland, MC. Chemical and hormonal induction of prostate cancer in animal models. Urol Oncol. 1996; 2, 103–110.CrossRefGoogle ScholarPubMed
11. Ho, SM, Tang, WY, Belmonte, J, Prins, GS. Developmental exposure estradiol and bisphenol A (BPA) increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant (PDE4D4) in the rat prostate. Cancer Res. 2006; 66, 5624–5632.CrossRefGoogle Scholar
12. Prins, GS, Ye, SH, Birch, L, Ho, SM, Kannan, K. Serum Bisphenol A pharmacokinetics and prostatic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Repro Toxicology. 2010; online Oct 6.Google ScholarPubMed
13. Prins, GS, Birch, L. Neonatal estrogen exposure up-regulates estrogen receptor expression in the developing and adult rat prostate lobes. Endocrinology. 1997; 138, 1801–1809.CrossRefGoogle ScholarPubMed
14. Prins, GS, Marmer, M, Woodham, C, et al. Estrogen receptor-b messenger ribonucleic acid ontogeny in the prostate of normal and neonatally estrogenized rats. Endocrinology. 1998; 139, 874–883.CrossRefGoogle Scholar
15. Prins, GS, Birch, L, Couse, JF, Choi, I, Katzenellenbogen, B, Korach, KS. Estrogen imprinting of the developing prostate gland in mediated through stromal estrogen receptor a: studies with aERKO and bERKO mice. Cancer Res. 2001; 61, 6089–6097.Google Scholar
16. Pu, Y, Huang, L, Prins, GS. Sonic Hedgehog-patched-Gli signaling in the developing rat prostate gland: lobe-specific suppression by neonatal estrogens reduces ductal growth and branching. Dev Biol. 2004; 273, 257–275.CrossRefGoogle ScholarPubMed
17. Timms, BG, Howdeshell, KL, Barton, L, Bradley, S, Richter, CA, vom Saal, FS. Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. PNAS. 2005; 102, 7014–7019.CrossRefGoogle ScholarPubMed
18. Chang, WY, Wilson, MJ, Birch, L, Prins, GS. Neonatal estrogen stimulates proliferation of periductal fibroblasts and alters the extracellular matrix composition in the rat prostate. Endocrinology. 1999; 140, 405–415.CrossRefGoogle ScholarPubMed
19. Putz, O, Schwartz, CB, LeBlanc, GA, Cooper, RL, Prins, GS. Neonatal low- and high-dose exposure to estradiol benzoate in the male rat: II. Effects on male puberty and the reproductive tract. Biol Reprod. 2001; 65, 1506–1517.CrossRefGoogle ScholarPubMed
20. Prins, GS, Woodham, C, Lepinske, M, Birch, L. 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. 1993; 132, 2387–2398.CrossRefGoogle ScholarPubMed
21. Gilleran, JP, Putz, O, De Jong, M, et al. The role of prolactin in the prostatic inflammatory response to neonatal estrogen. Endocrinology. 2003; 144, 2046–2054.CrossRefGoogle ScholarPubMed
22. Woodham, C, Birch, L, Prins, GS. Neonatal estrogens down regulate prostatic androgen receptor levels through a proteosome-mediated protein degradation pathway. Endocrinology. 2003; 144, 4841–4850.CrossRefGoogle ScholarPubMed
23. Huang, L, Pu, Y, Alam, S, Birch, L, Prins, GS. Estrogenic regulation of signaling pathways and homeobox genes during rat prostate development. J Androl. 2004; 25, 330–337.CrossRefGoogle ScholarPubMed
24. Huang, L, Pu, Y, Birch, L, Prins, GS. Posterior Hox gene expression and differential androgen regulation in the developing and adult rat prostate lobes. Endocrinology. 2007; 148, 1235–1245.CrossRefGoogle ScholarPubMed
25. Huang, L, Pu, Y, Hu, WY, et al. The role of Wnt5a in prostate gland development. Dev Biol. 2009; 358, 188–199.CrossRefGoogle Scholar
26. Huang, L, Pu, Y, Alam, S, Birch, L, Prins, GS. The role of Fgf10 signaling in branching morphogenesis and gene expression in the rat prostate gland: lobe-specific supression by neonatal estrogens. Dev Biol. 2005; 278, 396–414.CrossRefGoogle Scholar
27. Prins, GS, Birch, L, Tang, WY, Ho, SM. Developmental estrogen exposures predispose to prostate carcinogenesis with aging. Reprod Toxicol. 2007; 23, 374–382.CrossRefGoogle ScholarPubMed