Elevated SGK1 predicts resistance of breast cancer cells to Akt inhibitors

Biochemical Journal

Volumn 452, Issue 3, 2013, Pages 499-508

  Sommer, Eeva M ^a   Dry, Hannah ^b   Cross, Darren ^b   Guichard, Sylvie ^b   Davies, Barry R ^b   Alessi, Dario R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Mammalian target of rapamycin (mTOR); N Myc downstream regulated gene 1 (NDRG1); Phosphoinositide 3 kinase (PI3K); Protein kinase inhibitor; Signal transduction inhibitor

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; AZD 5363; AZD 8055; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN KINASE B INHIBITOR; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER CELL; CANCER CELL; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; ONCOGENE C MYB; PHOSPHORYLATION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GROWTH INHIBITORS; HEK293 CELLS; HUMANS; IMMEDIATE-EARLY PROTEINS; MOLECULAR SEQUENCE DATA; PREDICTIVE VALUE OF TESTS; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SHEEP;

MAMMALIA;

EID: 84878389598     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130342     Document Type: Article

References (42)

1. Miller, T. W., Rexer, B. N., Garrett, J. T. and Arteaga, C. L. (2011) Mutations in the phosphatidylinositol 3-kinase pathway: role in tumor progression and therapeutic implications in breast cancer. Breast Cancer Res. 13, 224
2. Engelman, J. A. (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat. Rev. Cancer 9, 550-562
3. Liu, P., Cheng, H., Roberts, T. M. and Zhao, J. J. (2009) Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 8, 627-644
4. Engelman, J. A., Luo, J. and Cantley, L. C. (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7, 606-619 (Pubitemid 44100518)
5. Alessi, D. R., James, S. R., Downes, C. P., Holmes, A. B., Gaffney, P. R., Reese, C. B. and Cohen, P. (1997) Characterization of a 3-phosphoinositide- dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7, 261-269 (Pubitemid 27176852)
6. Sarbassov, D. D., Guertin, D. A., Ali, S. M. and Sabatini, D. M. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101 (Pubitemid 40262113)
7. 3-dependent mechanisms leading to resistance to PDK1 inhibitors. Biochem. J. 448, 285-295
8. Manning, B. D. and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274 (Pubitemid 46962095)
9. Webster, M. K., Goya, L. and Firestone, G. L. (1993) Immediate-early transcriptional regulation and rapid messenger-RNA turnover of a putative serine threonine protein-kinase. J. Biol. Chem. 268, 11482-11485 (Pubitemid 23168084)
10. Kobayashi, T., Deak, M., Morrice, N. and Cohen, P. (1999) Characterization of the structure and regulation of two novel isoforms of serum- and glucocorticoid-induced protein kinase. Biochem. J. 344, 189-197
11. Pearce, L. R., Komander, D. and Alessi, D. R. (2010) The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11, 9-22
12. Kobayashi, T. and Cohen, P. (1999) Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J. 339, 319-328 (Pubitemid 29209961)
13. Biondi, R. M., Kieloch, A., Currie, R. A., Deak, M. and Alessi, D. R. (2001) The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J. 20, 4380-4390 (Pubitemid 32772032)
14. Garcia-Martinez, J. M. and Alessi, D. R. (2008) mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 416, 375-385
15. Murray, J. T., Cummings, L. A., Bloomberg, G. B. and Cohen, P. (2005) Identification of different specificity requirements between SGK1 and PKBα. FEBS Lett. 579, 991-994 (Pubitemid 40248658)
16. Alessi, D. R., Caudwell, F. B., Andjelkovic, M., Hemmings, B. A. and Cohen, P. (1996) Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399,
17. Brunet, A., Park, J., Tran, H., Hu, L. S., Hemmings, B. A. and Greenberg, M. E. (2001) Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21, 952-965 (Pubitemid 32104742)
18. Yap, T. A., Yan, L., Patnaik, A., Fearen, I., Olmos, D., Papadopoulos, K., Baird, R. D., Delgado, L., Taylor, A., Lupinacci, L. et al. (2011) First-in-man clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors. J. Clin. Oncol. 29, 4688-4695
19. Webster, M. K., Goya, L., Ge, Y., Maiyar, A. C. and Firestone, G. L. (1993) Characterization of sgk, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol. Cell. Biol. 13, 2031-2040 (Pubitemid 23097682)
20. Pearce, L. R., Sommer, E. M., Sakamoto, K., Wullschleger, S. and Alessi, D. R. (2011) Protor-1 is required for efficient mTORC2-mediated activation of SGK1 in the kidney. Biochem. J. 436, 169-179
21. Davies, B. R., Greenwood, H., Dudley, P., Crafter, C., Yu, D.-H., Zhang, J., Li, J., Gao, B., Ji, Q., Maynard, J. et al. (2012) Preclinical pharmacology of AZD5363, an inhibitor of AKT: pharmacodynamics, antitumor activity, and correlation of monotherapy activity with genetic background. Mol. Cancer Ther. 11, 873-887
22. Najafov, A., Sommer, E. M., Axten, J. M., Deyoung, M. P. and Alessi, D. R. (2011) Characterization of GSK2334470, a novel and highly specific inhibitor of PDK1. Biochem. J. 433, 357-369
23. Kobayashi, T. and Cohen, P. (1999) Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J. 339, 319-328 (Pubitemid 29209961)
24. Dry, J. R., Pavey, S., Pratilas, C. A., Harbron, C., Runswick, S., Hodgson, D., Chresta, C., McCormack, R., Byrne, N., Cockerill, M. et al. (2010) Transcriptional pathway signatures predict MEK addiction and response to selumetinib (AZD6244). Cancer Res. 70, 2264-2273
25. Hirai, H., Sootome, H., Nakatsuru, Y., Miyama, K., Taguchi, S., Tsujioka, K., Ueno, Y., Hatch, H., Majumder, P. K., Pan, B. S. and Kotani, H. (2010) MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol. Cancer Ther. 9, 1956-1967
26. Murray, J. T., Campbell, D. G., Morrice, N., Auld, G. C., Shpiro, N., Marquez, R., Peggie, M., Bain, J., Bloomberg, G. B., Grahammer, F. et al. (2004) Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem. J. 384, 477-488 (Pubitemid 40018961)
27. García-Martínez, J. M. and Alessi, D. R. (2008) mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 416, 375-385
28. Koninki, K., Barok, M., Tanner, M., Staff, S., Pitkanen, J., Hemmila, P., Ilvesaro, J. and Isola, J. (2010) Multiple molecular mechanisms underlying trastuzumab and lapatinib resistance in JIMT-1 breast cancer cells. Cancer Lett. 294, 211-219
29. Brickley, D. R., Mikosz, C. A., Hagan, C. R. and Conzen, S. D. (2002) Ubiquitin modification of serum and glucocorticoid-induced protein kinase-1 (SGK-1). J. Biol. Chem. 277, 43064-43070 (Pubitemid 35285688)
30. 2+-channel Orai1/STIM1 by serum- and glucocorticoid-inducible kinase 1 (SGK1). FASEB J. 25, 2012-2021
31. Schmidt, E.-M., Kraemer, B. F., Borst, O., Muenzer, P., Schoenberger, T., Schmidt, C., Leibrock, C., Towhid, S. T., Seizer, P., Kuhl, D. et al. (2012) SGK1 sensitivity of platelet migration. Cell. Physiol. Biochem. 30, 259-268
32. Chresta, C. M., Davies, B. R., Hickson, I., Harding, T., Cosulich, S., Critchlow, S. E., Vincent, J. P., Ellston, R., Jones, D., Sini, P. et al. (2010) AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res. 70, 288-298
33. Kokame, K., Kato, H. and Miyata, T. (1996) Homocysteine-respondent genes in vascular endothelial cells identified by differential display analysis. GRP78/BiP and novel genes. J. Biol. Chem. 271, 29659-29665 (Pubitemid 26389590)
34. Zhou, D., Salnikow, K. and Costa, M. (1998) Cap43, a novel gene specifically induced by Ni2+ compounds. Cancer Res. 58, 2182-2189 (Pubitemid 28232906)
35. Kurdistani, S. K., Arizti, P., Reimer, C. L., Sugrue, M. M., Aaronson, S. A. and Lee, S. W. (1998) Inhibition of tumor cell growth by RTP/rit42 and its responsiveness to p53 and DNA damage. Cancer Res. 58, 4439-4444 (Pubitemid 28450049)
36. Park, H., Adams, M. A., Lachat, P., Bosman, F., Pang, S. C. and Graham, C. H. (2000) Hypoxia induces the expression of a 43-kDa protein (PROXY-1) in normal and malignant cells. Biochem. Biophys. Res. Commun. 276, 321-328
37. Shimono, A., Okuda, T. and Kondoh, H. (1999) N-myc-dependent repression of ndr1, a gene identified by direct subtraction of whole mouse embryo cDNAs between wild type and N-myc mutant. Mech. Dev. 83, 39-52 (Pubitemid 29302080)
38. Melotte, V., Qu, X., Ongenaert, M., van Criekinge, W., de Bruine, A. P., Baldwin, H. S. and van Engeland, M. (2010) The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications. FASEB J. 24, 4153-4166
39. Bandyopadhyay, S., Pai, S. K., Hirota, S., Hosobe, S., Takano, Y., Saito, K., Piquemal, D., Commes, T., Watabe, M., Gross, S. C. et al. (2004) Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene 23, 5675-5681 (Pubitemid 39093045)
40. Lang, F., Artunc, F. and Vallon, V. (2009) The physiological impact of the serum and glucocorticoid-inducible kinase SGK1. Curr. Opin. Nephrol. Hypertens. 18, 439-448
41. Wu, W., Chaudhuri, S., Brickley, D. R., Pang, D., Karrison, T. and Conzen, S. D. (2004) Microarray analysis reveals glucocorticoid-regulated survival genes that are associated with inhibition of apoptosis in breast epithelial cells. Cancer Res. 64, 1757-1764 (Pubitemid 38428699)
42. Bogusz, A. M., Brickley, D. R., Pew, T. and Conzen, S. D. (2006) A novel N-terminal hydrophobic motif mediates constitutive degradation of serum- and glucocorticoid-induced kinase-1 by the ubiquitin-proteasome pathway. FEBS J. 273, 2913-2928