Targeting stromal androgen receptor suppresses prolactin-driven benign prostatic hyperplasia (BPH)

Molecular Endocrinology

Volumn 27, Issue 10, 2013, Pages 1617-1631

  Lai, Kuo Pao ^a   Huang, Chiung Kuei ^a   Fang, Lei Ya ^a   Izumi, Kouji ^a   Lo, Chi Wen ^a   Wood, Ronald ^a   Kindblom, Jon ^c   Yeh, Shuyuan ^a   Chang, Chawnshang ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c SAHLGRENSKA ACADEMY AT UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANTINEOPLASTIC AGENT; ASC J9; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; PROBASIN; PROLACTIN; PROLACTIN RECEPTOR; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; HUMAN; HUMAN CELL; MALE; MICTURITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROSTATE SIZE; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STROMA CELL;

ANDROGEN-BINDING PROTEIN; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CURCUMIN; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLASTS; GENE EXPRESSION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, SMOOTH MUSCLE; ORGAN SIZE; PROLACTIN; PROSTATE; PROSTATIC HYPERPLASIA; PROTEOLYSIS; RECEPTORS, ANDROGEN; STAT3 TRANSCRIPTION FACTOR; STROMAL CELLS;

EID: 84884808807     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1207     Document Type: Article

References (64)

1. Barry MJ. Evaluation of symptoms and quality of life in men with benign prostatic hyperplasia. Urology. 2001;58:25-32; discussion 32.
2. Blanker MH, Bohnen AM, Groeneveld FP, Bernsen RM, Prins A, Ruud Bosch JL. Normal voiding patterns and determinants of increased diurnal and nocturnal voiding frequency in elderly men. J Urol. 2000;164:1201-1205.
3. Berry SJ, Coffey DS, Walsh PC, Ewing LL. The development of human benign prostatic hyperplasia with age. J Urol. 1984;132: 474-479.
4. Isaacs JT, Coffey DS. Etiology and disease process of benign prostatic hyperplasia. Prostate Suppl. 1989;2:33-50.
5. Weisser H, Krieg M. [Benign prostatic hyperplasia-the outcome of age-induced alteration of androgen-estrogen balance?]. Urologe A. 1997;36:3-9.
6. Huang X, Lee C. Regulation of stromal proliferation, growth arrest, differentiation and apoptosis in benign prostatic hyperplasia by TGF-beta. Front Biosci. 2003;8:s740-s749.
7. Lin VK, Wang SY, Vazquez DV, Xu C, Zhang S, Tang L. Prostatic stromal cells derived from benign prostatic hyperplasia specimens possess stem cell like property. Prostate. 2007;67:1265-1276.
8. Wang L, Yang JR, Yang LY, Liu ZT. Chronic inflammation in benign prostatic hyperplasia: implications for therapy. Med Hypotheses. 2008;70:1021-1023.
9. Hammond GL, Kontturi M, Maattala P, Puukka M, Vihko R. Serum FSH, LH and prolactin in normal males and patients with prostatic diseases. Clin Endocrinol (Oxf). 1977;7:129-135.
10. Ron M, Fich A, Shapiro A, Caine M, Ben-David M. Prolactin concentration in prostates with benign hypertrophy. Urology. 1981; 17:235-237.
11. Syms AJ, Harper ME, Griffiths K. The effect of prolactin on human BPH epithelial cell proliferation. Prostate. 1985;6:145-153.
12. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998;19:225-268.
13. Nevalainen MT, Valve EM, Ahonen T, Yagi A, Paranko J, Harkonen PL. Androgen-dependent expression of prolactin in rat prostate epithelium in vivo and in organ culture. FASEB J. 1997; 11:1297-1307.
14. Nevalainen MT, Valve EM, Ingleton PM, Harkonen PL. Expression and hormone regulation of prolactin receptors in rat dorsal and lateral prostate. Endocrinology. 1996;137:3078-3088.
15. Wennbo H, Kindblom J, Isaksson OG, Tornell J. Transgenic mice overexpressing the prolactin gene develop dramatic enlargement of the prostate gland. Endocrinology. 1997;138:4410-4415.
16. Kindblom J, Dillner K, Ling C, Tornell J, Wennbo H. Progressive prostate hyperplasia in adult prolactin transgenic mice is not dependent on elevated serum androgen levels. Prostate. 2002; 53:24-33.
17. Kindblom J, Dillner K, Sahlin L, et al. Prostate hyperplasia in a transgenic mouse with prostate-specific expression of prolactin. Endocrinology. 2003;144:2269-2278.
18. Yeh S, Tsai MY, Xu Q, et al. Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA. 2002;99:13498-13503.
19. Lai KP, Yamashita S, Vitkus S, Shyr CR, Yeh S, Chang C. Suppressed prostate epithelial development with impaired branching morphogenesis in mice lacking stromal fibromuscular androgen receptor. Mol Endocrinol. 2012;26:52-66.
20. Webber MM, Trakul N, Thraves PS, et al. A human prostatic stromal myofibroblast cell line WPMY-1: a model for stromalepithelial interactions in prostatic neoplasia. Carcinogenesis. 1999; 20:1185-1192.
21. Li Y, Li CX, Ye H, et al. Decrease in stromal androgen receptor associates with androgen-independent disease and promotes prostate cancer cell proliferation and invasion. J Cell Mol Med. 2008; 12:2790-2798.
22. Hayward SW, Dahiya R, Cunha GR, Bartek J, Deshpande N, Narayan P. Establishment and characterization of an immortalized but non-transformed human prostate epithelial cell line: BPH-1. In Vitro Cell Dev Biol Anim. 1995;31:14-24.
23. Wu CT, Altuwaijri S, Ricke WA, et al. Increased prostate cell proliferation and loss of cell differentiation in mice lacking prostate epithelial androgen receptor. Proc Natl Acad Sci USA. 2007;104: 12679-12684.
24. Leung YY, Schwarz EM, Silvers CR, Messing EM, Wood RW. Uroflow in murine urethritis. Urology. 2004;64:378-382.
25. Prins GS, Birch L, Greene GL. Androgen receptor localization in different cell types of the adult rat prostate. Endocrinology. 1991; 129:3187-3199.
26. El-Alfy M, Luu-The V, Huang XF, Berger L, Labrie F, Pelletier G. Localization of type 5 17 β-hydroxysteroid dehydrogenase, 3β-hydroxysteroid dehydrogenase, and androgen receptor in the human prostate by in situ hybridization and immunocytochemistry. Endocrinology. 1999;140:1481-1491.
27. Godoy A, Montecinos VP, Gray DR, et al. Androgen deprivation induces rapid involution and recovery of human prostate vasculature. Am J Physiol Endocrinol Metab. 2011;300:E263-E275.
28. Godoy A, Watts A, Sotomayor P, et al. Androgen receptor is causally involved in the homeostasis of the human prostate endothelial cell. Endocrinology. 2008;149:2959-2969.
29. Wang X, Lin WJ, Izumi K, et al. Increased infiltrated macrophages in benign prostatic hyperplasia (BPH): role of stromal androgen receptor in macrophage-induced prostate stromal cell proliferation. J Biol Chem. 2012;287:18376-18385.
30. Alonso-Magdalena P, Brossner C, Reiner A, et al. A role for epithelial-mesenchymal transition in the etiology of benign prostatic hyperplasia. Proc Natl Acad Sci USA. 2009;106:2859-2863.
31. Roehrborn CG. Pathology of benign prostatic hyperplasia. Int J Impot Res 2008;20(suppl 3):S11-S18.
32. de Jong TP, Klijn AJ. Urodynamic studies in pediatric urology. Nat Rev Urol. 2009;6:585-594.
33. Ahonen TJ, Harkonen PL, Rui H, Nevalainen MT. PRL signal transduction in the epithelial compartment of rat prostate maintained as long-term organ cultures in vitro. Endocrinology. 2002; 143:228-238.
34. Dagvadorj A, Kirken RA, Leiby B, Karras J, Nevalainen MT. Transcription factor signal transducer and activator of transcription 5 promotes growth of human prostate cancer cells in vivo. Clin Cancer Res. 2008;14:1317-1324.
35. Djakiew D, Delsite R, Pflug B, Wrathall J, Lynch JH, Onoda M. Regulation of growth by a nerve growth factor-like protein which modulates paracrine interactions between a neoplastic epithelial cell line and stromal cells of the human prostate. Cancer Res. 1991; 51:3304-3310.
36. Li Y, Zhang DY, Ren Q, et al. Regulation of a novel androgen receptor target gene, the cyclin B1 gene, through androgen-dependent E2F family member switching. Mol Cell Biol. 2012;32:2454-2466.
37. Chuang KH, Altuwaijri S, Li G, et al. Neutropenia with impaired host defense against microbial infection in mice lacking androgen receptor. J Exp Med. 2009;206:1181-1199.
38. Shuai K, Halpern J, ten Hoeve J, Rao X, Sawyers CL. Constitutive activation of STAT5 by the BCR-ABL oncogene in chronic myelogenous leukemia. Oncogene. 1996;13:247-254.
39. Gu L, Chiang KY, Zhu N, Findley HW, Zhou M. Contribution of STAT3 to the activation of survivin by GM-CSF in CD34+ cell lines. Exp Hematol. 2007;35:957-966.
40. Lin L, Amin R, Gallicano GI, et al. The STAT3 inhibitor NSC 74859 is effective in hepatocellular cancers with disrupted TGF-β signaling. Oncogene. 2009;28:961-972.
41. Yang ZZ, Grote DM, Ziesmer SC, et al. Soluble IL-2Rα facilitates IL-2-mediated immune responses and predicts reduced survival in follicular B-cell non-Hodgkin lymphoma. Blood. 2011;118:2809-2820.
42. Lai KP, Huang CK, Chang YJ, et al. New therapeutic approach to suppress castration-resistant prostate cancer using ASC-J9® via targeting androgen receptor in selective prostate cells. Am J Pathol. 2013;182:460-473.
43. Rohr HP, Bartsch G. Human benign prostatic hyperplasia: a stromal disease? New perspectives by quantitative morphology. Urology. 1980;16:625-633.
44. Cross NA, Reid SV, Harvey AJ, Jokonya N, Eaton CL. Opposing actions of TGFβ1 and FGF2 on growth, differentiation and extracellular matrix accumulation in prostatic stromal cells. Growth Factors. 2006;24:233-241.
45. Sciarra A, Mariotti G, Salciccia S, et al. Prostate growth and inflammation. J Steroid Biochem Mol Biol. 2008;108:254-260.
46. Gulley J, Figg WD, Dahut WL. Treatment options for androgenindependent prostate cancer. Clin Adv Hematol Oncol. 2003;1: 49-57.
47. Kramer G, Marberger M. Could inflammation be a key component in the progression of benign prostatic hyperplasia? Curr Opin Urol. 2006;16:25-29.
48. Mishra VC, Allen DJ, Nicolaou C, et al. Does intraprostatic inflammation have a role in the pathogenesis and progression of benign prostatic hyperplasia? BJU Int. 2007;100:327-331.
49. Delongchamps NB, de la Roza G, Chandan V, et al. Evaluation of prostatitis in autopsied prostates-is chronic inflammation more associated with benign prostatic hyperplasia or cancer? J Urol. 2008;179:1736-1740.
50. Royuela M, De Miguel MP, Bethencourt FR, Fraile B, Arenas MI, Paniagua R. IL-2, its receptors, and bcl-2 and bax genes in normal, hyperplastic and carcinomatous human prostates: immunohistochemical comparative analysis. Growth Factors. 2000;18:135-146.
51. Steiner GE, Stix U, Handisurya A, et al. Cytokine expression pattern in benign prostatic hyperplasia infiltrating T cells and impact of lymphocytic infiltration on cytokine mRNA profile in prostatic tissue. Lab Invest. 2003;83:1131-1146.
52. Giri D, Ittmann M. Interleukin-8 is a paracrine inducer of fibroblast growth factor 2, a stromal and epithelial growth factor in benign prostatic hyperplasia. Am J Pathol. 2001;159:139-147.
53. Handisurya A, Steiner GE, Stix U, et al. Differential expression of interleukin-15, a pro-inflammatory cytokine and T-cell growth factor, and its receptor in human prostate. Prostate. 2001;49:251-262.
54. Royuela M, de Miguel MP, Ruiz A, et al. Interferon-gamma and its functional receptors overexpression in benign prostatic hyperplasia and prostatic carcinoma: parallelism with c-myc and p53 expression. Eur Cytokine Netw. 2001;11:119-127.
55. Wang W, Bergh A, Damber JE. Chronic inflammation in benign prostate hyperplasia is associated with focal upregulation of cyclooxygenase-2, Bcl-2, and cell proliferation in the glandular epithelium. Prostate. 2004;61:60-72.
56. Hellstrom WJ, Giuliano F, Rosen RC. Ejaculatory dysfunction and its association with lower urinary tract symptoms of benign prostatic hyperplasia and BPH treatment. Urology. 2009;74:15-21.
57. Greco KA, McVary KT. The role of combination medical therapy in benign prostatic hyperplasia. Int J Impot Res. 2008;20(suppl 3): S33-S43.
58. Gravas S, Oelke M. Current status of 5α-reductase inhibitors in the management of lower urinary tract symptoms and BPH. World J Urol. 28:9-15.
59. Vela-Navarrete R. BPH α blocker therapy. J Urol (Paris). 1995; 101:26-28.
60. Kojima Y, Kubota Y, Sasaki S, Hayashi Y, Kohri K. Translational pharmacology in aging men with benign prostatic hyperplasia: molecular and clinical approaches to alpha1-adrenoceptors. Curr Aging Sci. 2009;2:223-239.
61. Steers WD. 5α-reductase activity in the prostate. Urology. 2001;58: 17-24; discussion 24.
62. Gur S, Kadowitz PJ, Hellstrom WJ. Guide to drug therapy for lower urinary tract symptoms in patients with benign prostatic obstruction: implications for sexual dysfunction. Drugs. 2008;68:209-229.
63. Imperato-McGinley J, Guerrero L, Gautier T, German JL, Peterson RE. Steroid 5α-reductase deficiency in man. An inherited form of male pseudohermaphroditism. Birth Defects Orig Artic Ser. 1975; 11:91-103.
64. Lee KL, Peehl DM. Molecular and cellular pathogenesis of benign prostatic hyperplasia. J Urol. 2004;172:1784-1791.