Increased expression of genes converting adrenal androgens to testosterone in castration-recurrent prostate cancer

Androgen Action in Prostate Cancer

Volumn , Issue , 2009, Pages 123-139

  Balk, Steven P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79951834640     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-69179-4_5     Document Type: Chapter

References (72)

1. Andersson, S., Geissler, W.M., Patel, S., and Wu, L. (1995). The molecular biology of androgenic 17 beta-hydroxysteroid dehydrogenases. J. Steroid Biochem. Mol. Biol. 53, 37-39.
2. Baek, S.H., Ohgi, K.A., Nelson, C.A., Welsbie, D., Chen, C., Sawyers, C.L., Rose, D.W., and Rosenfeld, M.G. (2006). Ligand-specific allosteric regulation of coactivator functions of androgen receptor in prostate cancer cells. Proc. Natl. Acad. Sci. U. S. A 103, 3100-3105.
3. Bauman, D.R., Steckelbroeck, S., Peehl, D.M., and Penning, T.M. (2006a). Transcript profiling of the androgen signal in normal prostate, benign prostatic hyperplasia, and prostate cancer. Endocrinology 147, 5806-5816.
4. Bauman, D.R., Steckelbroeck, S., Williams, M.V., Peehl, D.M., and Penning, T.M. (2006b). Identification of the major oxidative 3alpha-hydroxysteroid dehydrogenase in human prostate that converts 5alpha-androstane-3alpha, 17beta-diol to 5alpha-dihydrotestosterone: a potential therapeutic target for androgen-dependent disease. Mol. Endocrinol. 20, 444-458.
5. Belanger, A., Pelletier, G., Labrie, F., Barbier, O., and Chouinard, S. (2003). Inactivation of androgens by UDP-glucuronosyltransferase enzymes in humans. Trends Endocrinol. Metab. 14, 473-479.
6. Belanger, B., Belanger, A., Labrie, F., Dupont, A., Cusan, L., and Monfette, G. (1989). Comparison of residual C-19 steroids in plasma and prostatic tissue of human, rat and guinea pig after castration: unique importance of extratesticular androgens in men. J. Steroid Biochem. 32, 695-698.
7. Bjelfman, C., Soderstrom, T.G., Brekkan, E., Norlen, B.J., Egevad, L., Unge, T., Andersson, S., and Rane, A. (1997). Differential gene expression of steroid 5 alpha-reductase 2 in core needle biopsies from malignant and benign prostatic tissue. J. Clin. Endocrinol. Metab 82, 2210-2214.
8. Bonkhoff, H., Stein, U., Aumuller, G., and Remberger, K. (1996). Differential expression of 5 alpha-reductase isoenzymes in the human prostate and prostatic carcinomas. Prostate 29, 261-267.
9. Chen, C.D., Welsbie, D.S., Tran, C., Baek, S.H., Chen, R., Vessella, R., Rosenfeld, M.G., and Sawyers, C.L. (2004). Molecular determinants of resistance to antiandrogen therapy. Nat. Med. 10, 33-39.
10. Cheng, S., Brzostek, S., Lee, S.R., Hollenberg, A.N., and Balk, S.P. (2002). Inhibition of the dihydrotestosterone-activated androgen receptor by nuclear receptor corepressor. Mol. Endo-crinol. 16, 1492-1501.
11. Chouinard, S., Pelletier, G., Belanger, A., and Barbier, O. (2004). Cellular specific expression of the androgen-conjugating enzymes UGT2B15 and UGT2B17 in the human prostate epithelium. Endocr. Res. 30, 717-725.
12. Chouinard, S., Pelletier, G., Belanger, A., and Barbier, O. (2006). Isoform-specific regulation of uridine diphosphate-glucuronosyltransferase 2B enzymes in the human prostate: differential consequences for androgen and bioactive lipid inactivation. Endocrinology 147, 5431-5442.
13. Desmond, J.C., Mountford, J.C., Drayson, M.T., Walker, E.A., Hewison, M., Ride, J.P., Luong, Q. T., Hayden, R.E., Vanin, E.F., and Bunce, C.M. (2003). The aldo-keto reductase AKR1C3 is a novel suppressor of cell differentiation that provides a plausible target for the non-cyclooxy-genase-dependent antineoplastic actions of nonsteroidal anti-inflammatory drugs. Cancer Res. 63, 505-512.
14. Dufort, I., Rheault, P., Huang, X.F., Soucy, P., and Luu-The, V. (1999). Characteristics of a highly labile human type 5 17beta-hydroxysteroid dehydrogenase. Endocrinology 140, 568-574.
15. El Alfy, M., Luu-The, V., Huang, X.F., Berger, L., Labrie, F., and Pelletier, G. (1999). Localization of type 5 17beta-hydroxysteroid dehydrogenase, 3beta-hydroxysteroid dehydrogenase, and androgen receptor in the human prostate by in situ hybridization and immunocytochemis-try. Endocrinology 140, 1481-1491.
16. Elo, J.P., Akinola, L.A., Poutanen, M., Vihko, P., Kyllonen, A.P., Lukkarinen, O., and Vihko, R. (1996). Characterization of 17beta-hydroxysteroid dehydrogenase isoenzyme expression in benign and malignant human prostate. Int. J. Cancer 66, 37-41.
17. Ettinger, S.L., Sobel, R., Whitmore, T.G., Akbari, M., Bradley, D.R., Gleave, M.E., and Nelson, C. C. (2004). Dysregulation of sterol response element-binding proteins and downstream effectors in prostate cancer during progression to androgen independence. Cancer Res. 64, 2212-2221.
18. Fowler, J.E., Jr., Pandey, P., Seaver, L.E., and Feliz, T.P. (1995). Prostate specific antigen after gonadal androgen withdrawal and deferred flutamide treatment. J. Urol. 154, 448-453.
19. Fromont, G., Chene, L., Vidaud, M., Vallancien, G., Mangin, P., Fournier, G., Validire, P., Latil, A., and Cussenot, O. (2005). Differential expression of 37 selected genes in hormone-refractory prostate cancer using quantitative taqman real-time RT-PCR. Int. J. Cancer 114, 174-181.
20. Fung, K.M., Samara, E.N., Wong, C., Metwalli, A., Krlin, R., Bane, B., Liu, C.Z., Yang, J.T., Pitha, J.V., Culkin, D.J., Kropp, B.P., Penning, T.M., and Lin, H.K. (2006). Increased expression of type 2 3alpha-hydroxysteroid dehydrogenase/type 5 17beta-hydroxysteroid dehydro-genase (AKR1C3) and its relationship with androgen receptor in prostate carcinoma. Endocr. Relat. Cancer 13, 169-180.
21. Geller, J. (1985). Rationale for blockade of adrenal as well as testicular androgens in the treatment of advanced prostate cancer. Semin. Oncol. 12, 28-35.
22. Geller, J. and Albert, J. (1987). Effects of castration compared with total androgen blockade on tissue dihydrotestosterone (DHT) concentration in benign prostatic hyperplasia (BPH). Urol. Res. 15, 151-153.
23. Geller, J., Albert, J.D., Nachtsheim, D.A., and Loza, D. (1984). Comparison of prostatic cancer tissue dihydrotestosterone levels at the time of relapse following orchiectomy or estrogen therapy. J. Urol. 132, 693-696.
24. Gingras, S. and Simard, J. (1999). Induction of 3beta-hydroxysteroid dehydrogenase/isomerase type 1 expression by interleukin-4 in human normal prostate epithelial cells, immortalized keratinocytes, colon, and cervix cancer cell lines. Endocrinology 140, 4573-4584.
25. Guillemette, C., Hum, D.W., and Belanger, A. (1996). Regulation of steroid glucuronosyltransfer-ase activities and transcripts by androgen in the human prostatic cancer LNCaP cell line. Endocrinology 137, 2872-2879.
26. Harkonen, P., Torn, S., Kurkela, R., Porvari, K., Pulkka, A., Lindfors, A., Isomaa, V., and Vihko, P. (2003). Sex hormone metabolism in prostate cancer cells during transition to an androgen-independent state. J. Clin. Endocrinol. Metab. 88, 705-712.
27. Harrington, W.R., Sengupta, S., and Katzenellenbogen, B.S. (2006). Estrogen regulation of the glucuronidation enzyme UGT2B15 in estrogen receptor-positive breast cancer cells. Endocrinology 147, 3843-3850.
28. Heemers, H., Maes, B., Foufelle, F., Heyns, W., Verhoeven, G., and Swinnen, J.V. (2001). Androgens stimulate lipogenic gene expression in prostate cancer cells by activation of the sterol regulatory element-binding protein cleavage activating protein/sterol regulatory element-binding protein pathway. Mol. Endocrinol. 15, 1817-1828.
29. Hodgson, M.C., Astapova, I., Hollenberg, A.N., and Balk, S.P. (2007). Activity of androgen receptor antagonist bicalutamide in prostate cancer cells is independent of NCoR and SMRT corepressors. Cancer Res. 67, 8388-8395.
30. Holzbeierlein, J., Lal, P., LaTulippe, E., Smith, A., Satagopan, J., Zhang, L., Ryan, C., Smith, S., Scher, H., Scardino, P., Reuter, V., and Gerald, W.L. (2004). Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am. J. Pathol. 164, 217-227.
31. Iehle, C., Radvanyi, F., Gil Diez de, M., Ouafik, L.H., Gerard, H., Chopin, D., Raynaud, J.P., and Martin, P.M. (1999). Differences insteroid 5alpha-reductase iso-enzymes expression between normal and pathological human prostate tissue. J. Steroid Biochem. Mol. Biol. 68, 189-195.
32. Ji, Q., Chang, L., Stanczyk, F.Z., Ookhtens, M., Sherrod, A., and Stolz, A. (2007). Impaired dihydrotestosterone catabolism in human prostate cancer: critical role of AKR1C2 as a pre-receptor regulator of androgen receptor signaling. Cancer Res. 67, 1361-1369.
33. Ji, Q., Chang, L., VanDenBerg, D., Stanczyk, F.Z., and Stolz, A. (2003). Selective reduction of AKR1C2 in prostate cancer and its role in DHT metabolism. Prostate 54, 275-289.
34. Joyce, R., Fenton, M.A., Rode, P., Constantine, M., Gaynes, L., Kolvenbag, G., DeWolf, W., Balk, S., Taplin, M.E., and Bubley, G.J. (1998). High dose bicalutamide for androgen independent prostate cancer: effect of prior hormonal therapy. J. Urol. 159, 149-153.
35. Komoto, J., Yamada, T., Watanabe, K., and Takusagawa, F. (2004). Crystal structure of human prostaglandin F synthase (AKR1C3). Biochemistry 43, 2188-2198.
36. Krieg, M., Bartsch, W., Janssen, W., and Voigt, K.D. (1979). A comparative study of binding, metabolism and endogenous levels of androgens in normal, hyperplastic and carcinomatous human prostate. J. Steroid Biochem. 11, 615-624.
37. Labrie, F., Luu-The, V., Lin, S.X., Simard, J., and Labrie, C. (2000). Role of 17 beta-hydroxyster-oid dehydrogenases in sex steroid formation in peripheral intracrine tissues. Trends Endocri-nol. Metab. 11, 421-427.
38. Lin, H.K., Jez, J.M., Schlegel, B.P., Peehl, D.M., Pachter, J.A., and Penning, T.M. (1997). Expression and characterization of recombinant type 2 3 alpha-hydroxysteroid dehydrogenase (HSD) from human prostate: demonstration of bifunctional 3 alpha/17 beta-HSD activity and cellular distribution. Mol. Endocrinol. 11, 1971-1984.
39. Lin, H.K., Steckelbroeck, S., Fung, K.M., Jones, A.N., and Penning, T.M. (2004). Characterization of a monoclonal antibody for human aldo-keto reductase AKR1C3 (type 2 3alpha-hydroxys-teroid dehydrogenase/type 5 17beta-hydroxysteroid dehydrogenase); immunohistochemical detection in breast and prostate. Steroids 69, 795-801.
40. Luo, J., Dunn, T.A., Ewing, C.M., Walsh, P.C., and Isaacs, W.B. (2003). Decreased gene expression of steroid 5 alpha-reductase 2 in human prostate cancer: implications for finasteride therapy of prostate carcinoma. Prostate 57, 134-139.
41. Mahoney, E.M. and Harrison, J.H. (1972). Bilateral adrenalectomy for palliative treatment of prostatic cancer. J. Urol. 108, 936-938.
42. Masiello, D., Cheng, S., Bubley, G.J., Lu, M.L., and Balk, S.P. (2002). Bicalutamide functions as an androgen receptor antagonist by assembly of a transcriptionally inactive receptor. J. Biol. Chem. 277, 26321-26326.
43. Matsuura, K., Shiraishi, H., Hara, A., Sato, K., Deyashiki, Y., Ninomiya, M., and Sakai, S. (1998). Identification of a principal mRNA species for human 3alpha-hydroxysteroid dehydrogenase isoform (AKR1C3) that exhibits high prostaglandin D2 11-ketoreductase activity. J. Biochem. 124, 940-946.
44. Miyamoto, H., Yeh, S., Lardy, H., Messing, E., and Chang, C. (1998). Delta5-androstenediol is a natural hormone with androgenic activity in human prostate cancer cells. Proc. Natl. Acad. Sci. U. S. A 95, 11083-11088.
45. Mizokami, A., Koh, E., Fujita, H., Maeda, Y., Egawa, M., Koshida, K., Honma, S., Keller, E.T., and Namiki, M. (2004). The adrenal androgen androstenediol is present in prostate cancer tissue after androgen deprivation therapy and activates mutated androgen receptor. Cancer Res. 64, 765-771.
46. Mohler, J.L., Gregory, C.W., Ford, O.H., III, Kim, D., Weaver, C.M., Petrusz, P., Wilson, E.M., and French, F.S. (2004). The androgen axis in recurrent prostate cancer. Clin. Cancer Res. 10, 440-448.
47. Nishiyama, T., Hashimoto, Y., and Takahashi, K. (2004). The influence of androgen deprivation therapy on dihydrotestosterone levels in the prostatic tissue of patients with prostate cancer. Clin. Cancer Res. 10, 7121-7126.
48. Page, S.T., Lin, D.W., Mostaghel, E.A., Hess, D.L., True, L.D., Amory, J.K., Nelson, P.S., Matsumoto, A.M., and Bremner, W.J. (2006). Persistent intraprostatic androgen concentrations after medical castration in healthy men. J. Clin. Endocrinol. Metab 91, 3850-3856.
49. Pelletier, G., Luu-The, V., Tetu, B., and Labrie, F. (1999). Immunocytochemical localization of type 5 17beta-hydroxysteroid dehydrogenase in human reproductive tissues. J. Histochem. Cytochem. 47, 731-738.
50. Penning, T.M., Bauman, D.R., Jin, Y., and Rizner, T.L. (2007). Identification of the molecular switch that regulates access of 5alpha-DHT to the androgen receptor. Mol. Cell Endocrinol. 265-266, 77-82.
51. Penning, T.M., Burczynski, M.E., Jez, J.M., Hung, C.F., Lin, H.K., Ma, H., Moore, M., Palackal, N., and Ratnam, K. (2000). Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem. J. 351, 67-77.
52. Penning, T.M., Steckelbroeck, S., Bauman, D.R., Miller, M.W., Jin, Y., Peehl, D.M., Fung, K.M., and Lin, H.K. (2006). Aldo-keto reductase (AKR) 1C3: role in prostate disease and the development of specific inhibitors. Mol. Cell Endocrinol. 248, 182-191.
53. Ratnam, K., Ma, H., and Penning, T.M. (1999). The arginine 276 anchor for NADP(H) dictates fluorescence kinetic transients in 3 alpha-hydroxysteroid dehydrogenase, a representative aldo-keto reductase. Biochemistry 38, 7856-7864.
54. Rizner, T.L., Lin, H.K., Peehl, D.M., Steckelbroeck, S., Bauman, D.R., and Penning, T.M. (2003). Human type 3 3alpha-hydroxysteroid dehydrogenase (aldo-keto reductase 1C2) and androgen metabolism in prostate cells. Endocrinology 144, 2922-2932.
55. Russell, D.W. and Wilson, J.D. (1994). Steroid 5 alpha-reductase: two genes/two enzymes. Annu. Rev. Biochem. 63, 25-61.
56. Scher, H.I., Liebertz, C., Kelly, W.K., Mazumdar, M., Brett, C., Schwartz, L., Kolvenbag, G., Shapiro, L., and Schwartz, M. (1997). Bicalutamide for advanced prostate cancer: the natural versus treated history of disease. J. Clin. Oncol. 15, 2928-2938.
57. Shang, Y., Myers, M., and Brown, M. (2002). Formation of the androgen receptor transcription complex. Mol. Cell 9, 601-610.
58. Simard, J., Ricketts, M.L., Gingras, S., Soucy, P., Feltus, F.A., and Melner, M.H. (2005). Molecular biology of the 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family. Endocr. Rev. 26, 525-582.
59. Soderstrom, T.G., Bjelfman, C., Brekkan, E., Ask, B., Egevad, L., Norlen, B.J., and Rane, A. (2001). Messenger ribonucleic acid levels of steroid 5 alpha-reductase 2 in human prostate predict the enzyme activity. J. Clin. Endocrinol. Metab. 86, 855-858.
60. Stanbrough, M., Bubley, G.J., Ross, K., Golub, T.R., Rubin, M.A., Penning, T.M., Febbo, P.G., and Balk, S.P. (2006). Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 66, 2815-2825.
61. Steckelbroeck, S., Jin, Y., Gopishetty, S., Oyesanmi, B., and Penning, T.M. (2004). Human cytosolic 3alpha-hydroxysteroid dehydrogenases of the aldo-keto reductase superfamily display significant 3beta-hydroxysteroid dehydrogenase activity: implications for steroid hormone metabolism and action. J. Biol. Chem. 279, 10784-10795.
62. Swinnen, J.V., Ulrix, W., Heyns, W., and Verhoeven, G. (1997). Coordinate regulation of lipogenic gene expression by androgens: evidence for a cascade mechanism involving sterol regulatory element binding proteins. Proc. Natl. Acad. Sci. U. S. A 94, 12975-12980.
63. Thomas, L.N., Douglas, R.C., Vessey, J.P., Gupta, R., Fontaine, D., Norman, R.W., Thompson, I. M., Troyer, D.A., Rittmaster, R.S., and Lazier, C.B. (2003). 5alpha-reductase type 1 immu-nostaining is enhanced in some prostate cancers compared with benign prostatic hyperplasia epithelium. J. Urol. 170, 2019-2025.
64. Thomas, L.N., Lazier, C.B., Gupta, R., Norman, R.W., Troyer, D.A., O'Brien, S.P., and Ritt-master, R.S. (2005). Differential alterations in 5alpha-reductase type 1 and type 2 levels during development and progression of prostate cancer. Prostate 63, 231-239.
65. Thomas, L.N., Douglas, R.C., Lazier, C.B., Too, C.K., Rittmaster, R.S., and Tindall, D.J. (2007). Type 1 and Type 2 5alpha-reductase expression in the development and progression of prostate cancer. Eur. Urol. 53, 244-252.
66. Thompson, I.M., Goodman, P.J., Tangen, C.M., Lucia, M.S., Miller, G.J., Ford, L.G., Lieber, M. M., Cespedes, R.D., Atkins, J.N., Lippman, S.M., Carlin, S.M., Ryan, A., Szczepanek, C.M., Crowley, J.J., and Coltman, C.A., Jr. (2003). The influence of finasteride on the development of prostate cancer. N. Engl. J. Med. 349, 215-224.
67. Titus, M.A., Gregory, C.W., Ford, O.H., III, Schell, M.J., Maygarden, S.J., and Mohler, J.L. (2005a). Steroid 5alpha-reductase isozymes I and II in recurrent prostate cancer. Clin. Cancer Res. 11, 4365-4371.
68. Titus, M.A., Schell, M.J., Lih, F.B., Tomer, K.B., and Mohler, J.L. (2005b). Testosterone and dihydrotestosterone tissue levels in recurrent prostate cancer. Clin. Cancer Res. 11, 4653-4657.
69. Weihua, Z., Lathe, R., Warner, M., and Gustafsson, J.A. (2002). An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta, 17beta-diol, and CYP7B1, regulates prostate growth. Proc. Natl. Acad. Sci. U. S. A 99, 13589-13594.
70. Weihua, Z., Makela, S., Andersson, L.C., Salmi, S., Saji, S., Webster, J.I., Jensen, E.V., Nilsson, S., Warner, M., and Gustafsson, J.A. (2001). A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc. Natl. Acad. Sci. U. S. A 98, 6330-6335.
71. Wilson, J.D., Griffin, J.E., and Russell, D.W. (1993). Steroid 5 alpha-reductase 2 deficiency. Endocr. Rev. 14, 577-593.
72. Zhu, P., Baek, S.H., Bourk, E.M., Ohgi, K.A., Garcia-Bassets, I., Sanjo, H., Akira, S., Kotol, P.F., Glass, C.K., Rosenfeld, M.G., and Rose, D.W. (2006). Macrophage/Cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 124, 615-629.