Estrogen receptor β activation impairs prostatic regeneration by inducing apoptosis in murine and human stem/progenitor enriched cell populations

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Hussain, Shirin ^a   Lawrence, Mitchell G ^a   Taylor, Renea A ^a   Lo, Camden Yeung Wah ^a   BioResource, A P C ^a   Frydenberg, Mark ^a   Ellem, Stuart J ^a   Furic, Luc ^a   Risbridger, Gail P ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA AGONIST; HORMONE RECEPTOR STIMULATING AGENT; PROTEIN P63; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; ANIMAL CELL; APOPTOSIS; ARTICLE; ATROPHY; BASAL CELL; CASTRATION RESISTANT PROSTATE CANCER; CELL DEATH; CELL LOSS; CELL POPULATION; CELL RENEWAL; CLONOGENESIS; CONTROLLED STUDY; DEPLETION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROSTATE DISEASE; RECEPTOR UPREGULATION; STEM CELL; TARGET CELL; TISSUE REGENERATION;

ANIMALS; APOPTOSIS; CASTRATION; CELL PROLIFERATION; CLONE CELLS; ESTROGEN RECEPTOR BETA; HUMANS; MALE; MICE; MICE, INBRED C57BL; PROSTATE; REGENERATION; STEM CELLS;

MURINAE;

EID: 84863694293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040732     Document Type: Article

References (45)

1. Huggins C, Hodges CV, (1941) Studies on prostatic cancer. The effect of castration, of estrogen and of androgen interaction on serum phosphatases in metastatic carcinoma of the prostate. Cancer Res 1: 293-297.
2. Goldenberg SL, Fenster HN, Perler Z, McLoughlin MG, (1983) Disseminated intravascular coagulation in carcinoma of prostate: role of estrogen therapy. Urology 22: 130-132.
3. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA, (1996) Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 93: 5925-5930.
4. Harris HA, (2006) Estrogen receptor-β: Recent lessons from in vivo studies. Mol Endocrinol.
5. Thomas C, Gustafsson JA, (2011) The different roles of ER subtypes in cancer biology and therapy. Nature reviews Cancer 11: 597-608.
6. Hillisch A, Peters O, Kosemund D, Muller G, Walter A, et al. (2004) Dissecting physiological roles of estrogen receptor alpha and beta with potent selective ligands from structure-based design. Mol Endocrinol 18: 1599-1609.
7. McPherson SJ, Ellem SJ, Simpson ER, Patchev V, Fritzemeier KH, et al. (2007) Essential role for estrogen receptor beta in stromal-epithelial regulation of prostatic hyperplasia. Endocrinology 148: 566-574.
8. McPherson SJ, Hussain S, Balanathan P, Hedwards SL, Niranjan B, et al. (2010) Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen independent and TNFalpha mediated. Proc Natl Acad Sci U S A 107: 3123-3128.
9. Risbridger GP, Frydenberg M, Hayward SW, Clark PE, Appu S, (2010) Endocrinology of the Prostate. In: Groot LJD, editors. editor. de Groots Textbook of Endocrinolgy 6th Edition. 6th ed.
10. Taylor RA, Toivanen R, Risbridger G, (2010) Stem cells in prostate cancer- treating the root of the problem. Endocr Relat Cancer.
11. Risbridger GP, Davis ID, Birrell SN, Tilley W, (2010) Breast and prostate cancer: more similar than different. Nature Review Cancer 10: 205-212.
12. Goldstein AS, Huang J, Guo C, Garraway IP, Witte ON, (2010) Identification of a cell of origin for human prostate cancer. Science 329: 568-571.
13. English HF, Santen RJ, Isaacs JT, (1987) Response of glandular versus basal rat ventral prostatic epithelial cells to androgen withdrawal and replacement. Prostate 11: 229-242.
14. Lawson DA, Zong Y, Memarzadeh S, Xin L, Huang J, et al. (2010) Basal epithelial stem cells are efficient targets for prostate cancer initiation. Proc Natl Acad Sci U S A 107: 2610-2615.
15. Xin L, Lukacs RU, Lawson DA, Cheng D, Witte ON, (2007) Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 25: 2760-2769.
16. Lukacs RU, Goldstein AS, Lawson DA, Cheng D, Witte ON, (2010) Isolation, cultivation and characterization of adult murine prostate stem cells. Nat Protoc 5: 702-713.
17. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON, (2007) Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci U S A 104: 181-186.
18. Wang Y, Hayward S, Cao M, Thayer K, Cunha G, (2001) Cell differentiation lineage in the prostate. Differentiation 68: 270-279.
19. Bianco JJ, Handelsman DJ, Pedersen JS, Risbridger GP, (2002) Direct response of the murine prostate gland and seminal vesicles to estradiol. Endocrinology 143: 4922-4933.
20. McPherson S, Wang H, Jones M, Pedersen J, Iismaa T, et al. (2001) Elevated androgens and prolactin in aromatase deficient (ArKO) mice cause enlargement but not malignancy of the prostate gland. Endocrinology 142: 2458-2467.
21. Bianco JJ, McPherson SJ, Wang H, Prins GS, Risbridger GP, (2006) Transient neonatal estrogen exposure to estrogen-deficient mice (aromatase knockout) reduces prostate weight and induces inflammation in late life. Am J Pathol 168: 1869-1878.
22. Bianco J, Handelsman DJ, Pedersen J, (2002) Direct response of the murine prostate gland and seminal vesicles to estradiol. Endocrinology 143: 4922-4933.
23. Leav I, Lau K, Adams J, McNeal J, Taplin M, et al. (2001) Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol 159: 79-92.
24. Zhou Q, Nie R, Prins GS, Saunders PT, Katzenellenbogen BS, et al. (2002) Localization of androgen and estrogen receptors in adult male mouse reproductive tract. Journal of andrology 23: 870-881.
25. Pelletier G, Labrie C, Labrie F, (2000) Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol 165: 359-370.
26. Imamov O, Morani A, Shim GJ, Omoto Y, Thulin-Andersson C, et al. (2004) Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc Natl Acad Sci U S A 101: 9375-9380.
27. Jefferson WN, Couse JF, Banks EP, Korach KS, Newbold RR, (2000) Expression of estrogen receptor beta is developmentally regulated in reproductive tissues of male and female mice. Biol Reprod 62: 310-317.
28. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, et al. (2004) CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117: 3539-3545.
29. Goldstein AS, Lawson DA, Cheng D, Sun W, Garraway IP, et al. (2008) Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc Natl Acad Sci U S A 105: 20882-20887.
30. Lukacs RU, Memarzadeh S, Wu H, Witte ON, (2010) Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell 7: 682-693.
31. Mulholland DJ, Xin L, Morim A, Lawson D, Witte O, et al. (2009) Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res 69: 8555-8562.
32. English HF, Drago JR, Santen RJ, (1985) Cellular response to androgen depletion and repletion in the rat ventral prostate: autoradiography and morphometric analysis. Prostate 7: 41-51.
33. Evans GS, Chandler JA, (1987) Cell proliferation studies in the rat prostate: II. The effects of castration and androgen-induced regeneration upon basal and secretory cell proliferation. Prostate 11: 339-351.
34. Wang X, Kruithof-de Julio M, Economides KD, Walker D, Yu H, et al. (2009) A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 461: 495-500.
35. Liu J, Pascal LE, Isharwal S, Metzger D, Ramos Garcia R, et al. (2011) Regenerated luminal epithelial cells are derived from pre-existing luminal epithelial cells in adult mouse prostate. Molecular endocrinology.
36. Uzgare AR, Xu Y, Isaacs JT, (2004) In vitro culturing and characteristics of transit amplifying epithelial cells from human prostate tissue. J Cell Biochem 91: 196-205.
37. Mak P, Leav I, Pursell B, Bae D, Yang X, et al. (2010) ERβ impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 17: 319-332.
38. Isaacs JT, (1984) Antagonistic effect of androgen on prostatic cell death. Prostate 5: 545-557.
39. Isaacs JT, (1987) Control of cell proliferation and cell death in the normal and neoplastic prostate: A stem cell model. In: Rodgers C, Coffey D, Cunha GR, Grayhack J, Hinman FJ, editors. pp. 85-94 editors. Benign Prostatic Hyperplasia. Washington, DC: Government Printing Office.
40. Isaacs J, (1987) Control of cell proliferation and cell death in the normal and neoplastic prostate: a stem cell model. In: Rodgers C, Coffey D, Cunha G, Greyhack J, Jr FH, editors. pp. 88-94 editors. Benign Prostatic Hyperplasia, NIH publication #87-2881. Washington DC: US Department of Health and Human Services.
41. de Marzo AM, Nelson WG, Meeker AK, Coffey DS, (1998) Stem cell features of benign and malignant prostate epithelial cells. J Urol 160: 2381-2392.
42. Kurita T, Medina RT, Mills AA, Cunha GR, (2004) Role of p63 and basal cells in the prostate. Development 131: 4955-4964.
43. Leong KG, Wang BE, Johnson L, Gao WQ, (2008) Generation of a prostate from a single adult stem cell. Nature 456: 804-808.
44. Choi N, Zhang B, Zhang L, Ittmann M, Xin L, (2012) Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer cell 21: 253-265.
45. Schleipen B, Hertrampf T, Fritzemeier KH, Kluxen FM, Lorenz A, et al. (2011) ERβ:-specific agonists and genistein inhibit proliferation and induce apoptosis in the large and small intestine. Carcinogenesis 32: 1675-1683.