Impaired dihydrotestosterone catabolism in human prostate cancer: Critical role of AKR1C2 as a pre-receptor regulator of androgen receptor signaling

Cancer Research

Volumn 67, Issue 3, 2007, Pages 1361-1369

  Ji, Qing ^a   Chang, Lilly ^a   Stanczyk, Frank Z ^a   Ookhtens, Murad ^a   Sherrod, Andy ^a   Stolz, Andrew ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Hoffman Medical Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANEDIOL; ANDROSTANOLONE; METRIBOLONE;

AKR1C1 GENE; AKR1C2 GENE; ARTICLE; CATABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

20-HYDROXYSTEROID DEHYDROGENASES; AGED; DIHYDROTESTOSTERONE; HUMANS; HYDROXYSTEROID DEHYDROGENASES; MALE; MIDDLE AGED; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 33847024000     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-1593     Document Type: Article

References (50)

1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000;50:7-33.
2. Isaacs JT. Role of androgens in prostatic cancer. Vitam Horm 1994;49:433-502.
3. Huggins C, Hodges CV. Studies on prostate cancer 1. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. Cancer Res 1941;1:293-7.
4. Ross RK, Pike MC, Coetzee GA et al. Androgen metabolism and prostate cancer: establishing a model of genetic susceptibility. Cancer Res 1998;58:4497-504.
5. Feigelson HS, Ross RK, Yu MC, Coetzee GA, Reichardt JK, Henderson BE. Genetic susceptibility to cancer from exogenous and endogenous exposures. J Cell Biochem Suppl 1996;25:15-22.
6. Russell DW, Berman DM, Bryant JT, et al. The molecular genetics of steroid 5 alpha-reductases. Recent Prog Horm Res 1994;49:275-84.
7. Thompson IM, Goodman PJ, Tangen CM, et al. The influence of finasteride on the development of prostate cancer. N Engl J Med 2003;349:215-24.
8. Galbraith SM, Duchesne GM. Androgens and prostate cancer: biology, pathology and hormonal therapy. Eur J Cancer 1997;33:545-54.
9. Chen CD, Welsbie DS, Tran C, et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004;10:33-9.
10. Penning TM, Burczynski ME, Jez JM, et al. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-1C4) 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 2000;351:67-77.
11. Ji Q, Chang L, Van Den Berg D, Stanczyk FZ, Stolz A. Selective reduction of AKR1C2 in prostate cancer and its role in DHT metabolism. Prostate 2003;54:275-89.
12. Deyashiki Y, Taniguchi H, Amano T, Nakayama T, Hara A, Sawada H. Structural and functional comparison of two human liver dihydrodiol dehydrogenases associated with 3 alpha-hydroxysteroid dehydrogenase activity. Biochem J 1992;282:741-6.
13. Khanna M, Qin KN, Wang RW, Cheng KC. Substrate specificity, gene structure, and tissue-specific distribution of multiple human 3 alpha-hydroxysteroid dehydrogenases. J Biol Chem 1995;270:20162-8.
14. Stolz A, Sugiyama Y, Kuhlenkamp J, Kaplowitz N. Identification and purification of a 36 kDa bile acid binder in human hepatic cytosol. FEBS Lett 1984;177:31-5.
15. Penning TM. Molecular endocrinology of hydroxysteroid dehydrogenases. Endocr Rev 1997;18:281-305.
16. Steckelbroeck S, Jin Y, Gopishetty S, Oyesanmi B, Penning TM. 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 2004;279:10784-95.
17. Dufort I, Labrie F, Luu-The V. Human types 1 and 3 alpha-hydroxysteroid dehydrogenases: differential lability and tissue distribution. J Clin Endocrinol Metab 2001;86:841-86.
18. Serafini P, Ablan F, Lobo RA. 5 alptia-Reductase activity in the genital skin of hirsute women. J Clin Endocrinol Metab 1985;60:349-55.
19. O'Donnell L, Stanton PG, Wreford NG, Robertson DM, McLachlan RI. Inhibition of 5 alpha-reductase activity impairs the testosterone-dependent restoration of spermiogenesis in adult rats. Endocrinology 1996;137:2703-10.
20. Ji Q, Aoyama C, Nien YD, et al. Selective loss of AKR1C1 and AKR1C2 in breast cancer and their potential effect on progesterone signaling. Cancer Res 2004;64:7610-7.
21. Ji Q, Liu PI, Elshimali Y, Stolz A. Frequent loss of estrogen and progesterone receptors in human prostatic tumors determined by quantitative real-time PCR. Mol Cell Endocrinol 2005;229:103-10.
22. Jia L, Kim J, Shen H, Clark PE, Tilley WD, Coetzee GA. Androgen receptor activity at the prostate specific antigen locus: steroidal and non-steroidal mechanisms. Mol Cancer Res 2003;1:385-92.
23. Fung KM, Samara EN, Wong C, et al. Increased expression of type 2 3alpha-hydroxysteroid dehydrogenase/type 5 17beta-hydroxysteroid dehydrogenase (AKR1C3) and its relationship with androgen receptor in prostate carcinoma. Endocr Relat Cancer 2006;13:169-80.
24. Lin HK, Steckelbroeck S, Fung KM, Jones AN, Penning TM. Characterization of a monoclonal antibody for human aldo-keto reductase AKR1C3 (type 2 3alphahydroxysteroid dehydrogenase/type 5 17beta-hydroxysteroid dehydrogenase); immunohistochemical detection in breast and prostate. Steroids 2004;69:795-801.
25. El-Alfy M, Luu-The V, Huang XF, Berger L, Labrie F, Pelletier G. Localization of type 5 17beta-hydroxysteroid dehydrogenase, 3beta-hydroxysteroid dehydrogenase, and androgen receptor in the human prostate by in situ hybridization and immunocytochemistry. Endocrinology 1999;140:1481-91.
26. Pelletier G, Luu-The V, Tetu B, Labrie F. Immunocytochemical localization of type 5 17beta-hydroxysteroid dehydrogenase in human reproductive tissues. J Histochem Cytochem 1999;47:731-8.
27. Nakamura Y, Suzuki T, Nakabayashi M, et al. In situ androgen producing enzymes in human prostate cancer. Endocr Relat Cancer 2005;12:101-7.
28. Oudes AJ, Campbell DS, Sorensen CM, Walashek LS, True LD, Liu AY. Transcriptomes of human prostate cells. BMC Genomics 2006;7:92.
29. Luo J, Dunn TA, Ewing CM, Walsh PC, Isaacs WB. Decreased gene expression of steroid 5 alpha-reductase 2 in human prostate cancer: implications for finasteride therapy of prostate carcinoma. Prostate 2003;57:134-9.
30. Ljung G, Norberg M, Holmberg L, Busch C, Nilsson S. Characterization of residual tumor cells following radical radiation therapy for prostatic adenocarcinoma; immunohistochemical expression of prostate-specific antigen, prostatic acid phosphatase, and cytokeratin 8. Prostate 1997;31:91-7.
31. Takikawa H, Stolz A, Kaplowitz N. Cyclical oxidation-reduction of the C3 position on bile acids catalyzed by rat hepatic 3 alpha-hydroxysteroid dehydrogenase. I. Studies with the purified enzyme, isolated rat hepatocytes, and inhibition by indomethacin. J Clin Invest 1987;80:852-60.
32. Tan J, Sharief Y, Hamil KG, et al. Dehydroepiandrosterone activates mutant androgen receptors expressed in the androgen-dependent human prostate cancer xenograft CWR22 and LNCaP cells. Mol Endocrinol 1997;11:450-9.
33. Kahmann S, Vassen L, Klein-Hitpass L. Synergistic enhancement of PRB-mediated RU486 and R5020 agonist activities through cyclic adenosine 3′,5′-monophosphate represents a delayed primary response. Mol Endocrinol 1998;12:278-89.
34. Kimura K, Markowski M, Bowen C, Gelmann EP. Androgen blocks apoptosis of hormone-dependent prostate cancer cells. Cancer Res 2001;61:5611-8.
35. Berchem GJ, Bosseler M, Sugars LY, Voeller HJ, Zeitlin S, Gelmann EP. Androgens induce resistance to bcl-2-mediated apoptosis in LNCaP prostate cancer cells. Cancer Res 1995;55:735-8.
36. Huang H, Cheville JC, Pan Y, Roche PC, Schmidt LJ, Tindall DJ. PTEN induces chemosensitivity in PTEN-mutated prostate cancer cells by suppression of Bcl-2 expression. J Biol Chem 2001;276:38830-6.
37. Huang H, Regan KM, Wang F, et al. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci U S A 2005;102:1649-54.
38. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001;1:34-45.
39. Zegarra-Moro OL, Schmidt LJ, Huang H, Tindall DJ. Disruption of androgen receptor function inhibits proliferation of androgen-refractory prostate cancer cells. Cancer Res 2002;62:1008-13.
40. Mohler JL, Gregory CW, Ford OH, 3rd, et al. The androgen axis in recurrent prostate cancer. Clin Cancer Res 2004;10:440-8.
41. Mohler JL, Gaston KE, Moore DT, et al. Racial differences in prostate androgen levels in men with clinically localized prostate cancer. J Urol 2004;1712277-80.
42. Krieg M, Bartsch W, Janssen W, Voigt KD. A comparative study of binding, metabolism and endogenous levels of androgens in normal, hyperplastic and carcinomatous human prostate. J Steroid Biochem 1979;11:615-24.
43. Makridakis N, Ross RK, Pike MC, et al. A prevalent missense substitution that modulates activity of prostatic steroid 5alpha-reductase. Cancer Res 1997;57:1020-2.
44. Bauman DR, Steckelbroeck S, Peehl DM, Penning TM. Transcript profiling of the androgen signal in normal prostate, benign prostatic hyperplasia and prostate cancer. Endocrinology 2006;147:5806-16.
45. Mizokami A, Koh E, Fujita H, et al. The adrenal androgen androstenediol is present in prostate cancer tissue after androgen deprivation therapy and activates mutated androgen receptor. Cancer Res 2004;64:765-71.
46. Labrie F, Dupont A, Simard J, Luu-The V, Belanger A. Intracrinology: the basis for the rational design of endocrine therapy at all stages of prostate cancer. Eur Urol 1993;24:94-105.
47. Nishiyama T, Hashimoto Y, Takahashi K. The influence of androgen deprivation therapy on dihydrotestosterone levels in the prostatic tissue of patients with prostate cancer. Clin Cancer Res 2004;10:7121-6.
48. Gao J, Arnold JT, Isaacs JT. Conversion from a paracrine to an autocrine mechanism of androgen-stimulated growth during malignant transformation of prostatic epithelial cells. Cancer Res 2001;61:5038-44.
49. Litvinov IV, De Marzo AM, Isaacs JT. Is the Achilles' heel for prostate cancer therapy a gain of function in androgen receptor signaling? J Clin Endocrinol Metab 2003;88:2972-82.
50. Koehler KF, Helguero LA, Haldosen LA, Warner M, Gustafsson JA. Reflections on the discovery and significance of estrogen receptor beta. Endocr Rev 2005;26:465-78.