SGK3 Is an androgen-inducible kinase promoting prostate cancer cell proliferation through activation of p70 S6 kinase and up-regulation of cyclin D1

Molecular Endocrinology

Volumn 28, Issue 6, 2014, Pages 935-948

  Wang, Yuanzhong ^a   Zhou, Dujin ^a   Chen, Shiuan ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; ESTROGEN RECEPTOR; GLUCOCORTICOID INDUCIBLE KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; S6 KINASE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG; ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; CCND1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; SGK3 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; GENE LOCUS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; BINDING SITE; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; PROSTATE TUMOR; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

ANDROGENS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D1; DIHYDROTESTOSTERONE; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, ANDROGEN; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84901920546     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2013-1339     Document Type: Article

References (53)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11-30.
2. Green SM, Mostaghel EA, Nelson PS. Androgen action and metabolism in prostate cancer. Mol Cell Endocrinol. 2012;360:3-13.
3. Labrie F. Blockade of testicular and adrenal androgens in prostate cancer treatment. Nat Rev Urol. 2011;8:73-85.
4. Sharifi N. Minireview: Androgen metabolism in castration-resistant prostate cancer. Mol Endocrinol. 2013;27:708-714.
5. Heinlein CA, Chang C. Androgen receptor in prostate cancer. Endocr Rev. 2004;25:276-308.
6. Dehm SM, Tindall DJ. Androgen receptor structural and functional elements: role and regulation in prostate cancer. Mol Endocrinol. 2007;21:2855-2863.
7. Bennett NC, Gardiner RA, Hooper JD, Johnson DW, Gobe GC. Molecular cell biology of androgen receptor signalling. Int J Biochem Cell Biol. 2010;42:813-827.
8. Kobayashi T, Deak M, Morrice N, Cohen P. Characterization of the structure and regulation of two novel isoforms of serum-and glucocorticoid-induced protein kinase. Biochem J. 1999;344(Pt 1): 189-197.
9. Bruhn MA, Pearson RB, Hannan RD, Sheppard KE. Second AKT: the rise of SGK in cancer signalling. Growth Factors. 2010;28:394-408.
10. + exchanger NHE3 by glucocorticoids. Mol Biol Cell. 2011;22: 3812-3825.
11. Yao LJ, McCormick JA, Wang J, et al. Novel role for SGK3 in glucose homeostasis revealed in SGK3/Akt2 double-null mice. Mol Endocrinol. 2011;25:2106-2118.
12. Vasudevan KM, Barbie DA, Davies MA, et al. AKT-independent signaling downstream of oncogenic PIK3CA mutations in human cancer. Cancer Cell. 2009;16:21-32.
13. Bruhn MA, Pearson RB, Hannan RD, Sheppard KE. AKT-independent PI3-K signaling in cancer-emerging role for SGK3. Cancer Manag Res. 2013;5:281-292.
14. Wang Y, Zhou D, Phung S, Masri S, Smith D, Chen S. SGK3 is an estrogen-inducible kinase promoting estrogen-mediated survival of breast cancer cells. Mol Endocrinol. 2011;25:72-82.
15. Sherk AB, Frigo DE, Schnackenberg CG, et al. Development of a small-molecule serum-and glucocorticoid-regulated kinase-1 antagonist and its evaluation as a prostate cancer therapeutic. Cancer Res. 2008;68:7475-7483.
16. DePrimo SE, Diehn M, Nelson JB, et al. Transcriptional programs activated by exposure of human prostate cancer cells to androgen. Genome Biol. 2002;3:RESEARCH0032.
17. Cairns P, Okami K, Halachmi S, et al. Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res. 1997;57: 4997-5000.
18. Whang YE, Wu X, Suzuki H, et al. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci USA. 1998;95: 5246-5250.
19. Sarker D, Reid AH, Yap TA, de Bono JS. Targeting the PI3K/AKT pathway for the treatment of prostate cancer. Clin Cancer Res. 2009;15:4799-4805.
20. Carver BS, Chapinski C, Wongvipat J, et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell. 2011;19:575-586.
21. Zhou D, Shen R, Ye JJ, et al. Nuclear receptor coactivator PNRC2 regulates energy expenditure and adiposity. J Biol Chem. 2008;283: 541-553.
22. Green AR, Young P, Krivinskas S, et al. The expression of ERα, ERβ and PR in lobular carcinoma in situ of the breast determined using laser microdissection and real-time PCR. Histopathology. 2009;54:419-427.
23. Zhou D, Quach KM, Yang C, Lee SY, Pohajdak B, Chen S. PNRC: a proline-rich nuclear receptor coregulatory protein that modulates transcriptional activation of multiple nuclear receptors including orphan receptors SF1 (steroidogenic factor 1) and ERRα1 (estrogen related receptor α-1). Mol Endocrinol. 2000;14:986-998.
24. Zhou D, Masri S, Ye JJ, Chen S. Transcriptional regulation of the mouse PNRC2 promoter by the nuclear factor Y (NFY) and E2F1. Gene. 2005;361:89-100.
25. Perets R, Kaplan T, Stein I, et al. Genome-wide analysis of androgen receptor targets reveals COUP-TF1 as a novel player in human prostate cancer. PLoS One. 2012;7:e46467.
26. Denayer S, Helsen C, Thorrez L, Haelens A, Claessens F. The rules of DNA recognition by the androgen receptor. Mol Endocrinol. 2010;24:898-913.
27. Tewari AK, Yardimci GG, Shibata Y, et al. Chromatin accessibility reveals insights into androgen receptor activation and transcriptional specificity. Genome Biol. 2012;13:R88.
28. Wang Q, Li W, Liu XS, et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol Cell. 2007;27:380-392.
29. Lau KM, LaSpina M, Long J, Ho SM. Expression of estrogen receptor (ER)-α and ER-β in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Res. 2000;60:3175-3182.
30. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM. mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell. 2008;30:701-711.
31. Dai F, Yu L, He H, et al. Human serum and glucocorticoid-inducible kinase-like kinase (SGKL) phosphorylates glycogen syntheses kinase 3 beta (GSK-3β) at serine-9 through direct interaction. Biochem Biophys Res Commun. 2002;293:1191-1196.
32. Liu M, Chen L, Chan TH, et al. Serum and glucocorticoid kinase 3 at 8q13.1 promotes cell proliferation and survival in hepatocellular carcinoma. Hepatology. 2012;55:1754-1765.
33. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998;12:3499-3511.
34. Grewe M, Gansauge F, Schmid RM, Adler G, Seufferlein T. Regulation of cell growth and cyclin D1 expression by the constitutively active FRAP-p70s6K pathway in human pancreatic cancer cells. Cancer Res. 1999;59:3581-3587.
35. Xu Y, Chen SY, Ross KN, Balk SP. Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins. Cancer Res. 2006;66:7783-7792.
36. Akar U, Ozpolat B, Mehta K, et al. Targeting p70S6K prevented lung metastasis in a breast cancer xenograft model. Mol Cancer Ther. 2010;9:1180-1187.
37. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci USA. 1998;95:1432-1437.
38. Tessier M, Woodgett JR. Serum and glucocorticoid-regulated protein kinases: variations on a theme. J Cell Biochem. 2006;98:1391-1407.
39. Shanmugam I, Cheng G, Terranova PF, Thrasher JB, Thomas CP, Li B. Serum/glucocorticoid-induced protein kinase-1 facilitates androgen receptor-dependent cell survival. Cell Death Differ. 2007; 14:2085-2094.
40. Massie CE, Lynch A, Ramos-Montoya A, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011;30:2719-2733.
41. 2-induced proliferation and PSA production in human prostate cancer cells. Prostate. 2007;67:1152-1162.
42. Panet-Raymond V, Gottlieb B, Beitel LK, Pinsky L, Trifiro MA. Interactions between androgen and estrogen receptors and the effects on their transactivational properties. Mol Cell Endocrinol. 2000;167:139-150.
43. Slusarz A, Jackson GA, Day JK, et al. Aggressive prostate cancer is prevented in ERαKO mice and stimulated in ERαKO TRAMP mice. Endocrinology. 2012;153:4160-4170.
44. Ricke WA, McPherson SJ, Bianco JJ, Cunha GR, Wang Y, Risbridger GP. Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor α signaling. FASEB J. 2008;22:1512-1520.
45. Dey P, Strom A, Gustafsson JA. Estrogen receptor β upregulates FOXO3a and causes induction of apoptosis through PUMA in prostate cancer [published online ahead of print September 30, 2013]. Oncogene. doi: 10.1038/onc.2013.384.
46. Maggiolini M, Recchia AG, Carpino A, et al. Oestrogen receptor beta is required for androgen-stimulated proliferation of LNCaP prostate cancer cells. J Mol Endocrinol. 2004;32:777-791.
47. Migliaccio A, Castoria G, Di Domenico M, et al. Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. EMBO J. 2000;19:5406-5417.
48. Capra M, Nuciforo PG, Confalonieri S, et al. Frequent alterations in the expression of serine/threonine kinases in human cancers. Cancer Res. 2006;66:8147-8154.
49. Speers C, Tsimelzon A, Sexton K, et al. Identification of novel kinase targets for the treatment of estrogen receptor-negative breast cancer. Clin Cancer Res. 2009;15:6327-6340.
50. Xu J, Wan M, He Q, et al. SGK3 is associated with estrogen receptor expression in breast cancer. Breast Cancer Res Treat. 2012;134: 531-541.
51. Xu J, Liao L, Qin J, Xu J, Liu D, Songyang Z. Identification of Flightless-I as a substrate of the cytokine-independent survival kinase CISK. J Biol Chem. 2009;284:14377-14385.
52. Wang Y, Xu W, Zhou D, Neckers L, Chen S. Coordinated regulation of serum-and glucocorticoid-inducible kinase 3 by a C-terminal hydrophobic motif and Hsp90-Cdc37 chaperone complex. J Biol Chem. 2014;289:4815-4826.
53. Liu D, Yang X, Songyang Z. Identification of CISK, a new member of the SGK kinase family that promotes IL-3-dependent survival. Curr Biol. 2000;10:1233-1236.