Glucocorticoid receptor β stimulates Akt1 growth pathway by attenuation of pten

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17885-17894

  Stechschulte, Lance A ^a   Wuescher, Leah ^a   Marino, Joseph S ^b   Hill, Jennifer W ^a   Eng, Charis ^c,d   Hinds Jr , Terry D ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH;

ALTERNATIVE SPLICING; CANCER PATIENTS; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOIDS; INSULIN SIGNALING; INSULIN TREATMENT; LIGAND BINDING DOMAIN; PTEN EXPRESSION;

INSULIN;

GLUCOCORTICOID RECEPTOR ALPHA; GLUCOCORTICOID RECEPTOR BETA; INSULIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN AKT1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GROWTH REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

AKT; CELL GROWTH; CELL PROLIFERATION; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HORMONE RECEPTOR; INSULIN; PHOSPHATASE AND TENSIN HOMOLOG (PTEN);

3T3-L1 CELLS; ANIMALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSULIN; MICE; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 84903461857     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.544072     Document Type: Article

References (50)

1. Gericke, A., Munson, M., and Ross, A. H. (2006) Regulation of the PTEN phosphatase. Gene 374, 1-9 (Pubitemid 43737118)
2. Goswami, A., Ranganathan, P., and Rangnekar, V. M. (2006) The phosphoinositide 3-kinase/Akt1/Par-4 axis: a cancer-selective therapeutic target. Cancer Res. 66, 2889-2892
3. Hers, I., Vincent, E. E., and Tavaré, J. M. (2011) Akt signalling in health and disease. Cell. Signalling 23, 1515-1527
4. Wang, Z., and Garabedian, M. J. (2003) Modulation of glucocorticoid receptor transcriptional activation, phosphorylation, and growth inhibition by p27Kip1. J. Biol. Chem. 278, 50897-50901 (Pubitemid 38020320)
5. Zheng, Y. C., Izumi, K., Li, Y., Ishiguro, H., and Miyamoto, H. (2012) Contrary Regulation of Bladder Cancer Cell Proliferation and Invasion by Dexamethasone-Mediated Glucocorticoid Receptor Signals. Mol. Cancer Ther. 11, 2621-2632
6. Ni, Z., Tang, J., Cai, Z., Yang, W., Zhang, L., Chen, Q., Zhang, L., and Wang, X. (2011)Anew pathway of glucocorticoid action for asthma treatment through the regulation of PTEN expression. Respir. Res. 12, 47
7. Rivers, C., Levy, A., Hancock, J., Lightman, S., and Norman, M. (1999) Insertion of an amino acid in the DNA-binding domain of the glucocorticoid receptor as a result of alternative splicing. J. Clin. Endocrinol. Metab. 84, 4283-4286 (Pubitemid 30644231)
8. Ray, D. W., Davis, J. R., White, A., and Clark, A. J. (1996) Glucocorticoid receptor structure and function in glucocorticoid-resistant small cell lung carcinoma cells. Cancer Res. 56, 3276-3280 (Pubitemid 26242976)
9. Sapolsky, R. M., Romero, L. M., and Munck, A. U. (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Rev. 21, 55-89 (Pubitemid 32266068)
10. Vegiopoulos, A., and Herzig, S. (2007) Glucocorticoids, metabolism and metabolic diseases. Mol. Cell. Endocrinol. 275, 43-61 (Pubitemid 47259280)
11. Hinds, T. D., Jr., Ramakrishnan, S., Cash, H. A., Stechschulte, L. A., Heinrich, G., Najjar, S. M., and Sanchez, E. R. (2010) Discovery of glucocorticoid receptor-β in mice with a role in metabolism. Mol. Endocrinol. 24, 1715-1727
12. Rogatsky, I., Trowbridge, J. M., and Garabedian, M. J. (1997) Glucocorticoid receptor-mediated cell cycle arrest is achieved through distinct cell-specific transcriptional regulatory mechanisms. Mol. Cell. Biol. 17, 3181-3193 (Pubitemid 27215033)
13. Yemelyanov, A., Czwornog, J., Chebotaev, D., Karseladze, A., Kulevitch, E., Yang, X., and Budunova, I. (2007) Tumor suppressor activity of glucocorticoid receptor in the prostate. Oncogene 26, 1885-1896 (Pubitemid 46474637)
14. Zhu, X. Y., Liu, Y. J., Lu, J., and Xu, R. B. (2004) Knockdown of glucocorticoid receptor expression by RNA interference promotes cell proliferation in murine macrophage RAW264.7 cells. J. Steroid Biochem. Mol. Biol. 92, 375-382 (Pubitemid 40187155)
15. Kino, T., and Chrousos, G. P. (2001) Glucocorticoid and mineralocorticoid resistance/hypersensitivity syndromes. J. Endocrinol. 169, 437-445 (Pubitemid 32536976)
16. Strickland, I., Kisich, K., Hauk, P. J., Vottero, A., Chrousos, G. P., Klemm, D. J., and Leung, D. Y. (2001) High constitutive glucocorticoid receptor β in human neutrophils enables them to reduce their spontaneous rate of cell death in response to corticosteroids. J. Exp. Med. 193, 585-593 (Pubitemid 32539555)
17. Webster, J. C., Oakley, R. H., Jewell, C. M., and Cidlowski, J. A. (2001) Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative β isoform: a mechanism for the generation of glucocorticoid resistance. Proc. Natl. Acad. Sci. U. S. A. 98, 6865-6870 (Pubitemid 32538308)
18. Leung, D. Y., Hamid, Q., Vottero, A., Szefler, S. J., Surs, W., Minshall, E., Chrousos, G. P., and Klemm, D. J. (1997) Association of glucocorticoid insensitivity with increased expression of glucocorticoid receptor β. J. Exp. Med. 186, 1567-1574 (Pubitemid 27479816)
19. Longui, C. A., Vottero, A., Adamson, P. C., Cole, D. E., Kino, T., Monte, O., and Chrousos, G. P. (2000) Low glucocorticoid receptor α/β ratio in T-cell lymphoblastic leukemia. Horm. Metab. Res. 32, 401-406
20. Piotrowski, P., Burzynski, M., Lianeri, M., Mostowska, M., Wudarski, M., Chwalinska-Sadowska, H., and Jagodzinski, P. P. (2007) Glucocorticoid receptor β splice variant expression in patients with high and low activity of systemic lupus erythematosus. Folia histochemica et cytobiologica/Polish Academy of Sciences, Polish Histochemical and Cytochemical Society 45, 339-342 (Pubitemid 351193607)
21. Kino, T., Manoli, I., Kelkar, S., Wang, Y., Su, Y. A., and Chrousos, G. P. (2009) Glucocorticoid receptor (GR) β has intrinsic, GRα-independent transcriptional activity. Biochem. Biophys. Res. Commun. 381, 671-675
22. Wang, Y., Romigh, T., He, X., Tan, M. H., Orloff, M. S., Silverman, R. H., Heston, W. D., and Eng, C. (2011) Differential regulation of PTEN expression by androgen receptor in prostate and breast cancers. Oncogene 30, 4327-4338
23. Periyasamy, S., Hinds, T., Jr., Shemshedini, L., Shou, W., and Sanchez, E. R. (2010) FKBP51 and Cyp40 are positive regulators of androgen-dependent prostate cancer cell growth and the targets of FK506 and cyclosporin A. Oncogene 29, 1691-1701
24. Oakley, R. H., Webster, J. C., Sar, M., Parker, C. R., Jr., and Cidlowski, J. A. (1997) Expression and subcellular distribution of the β-isoform of the human glucocorticoid receptor. Endocrinology 138, 5028-5038 (Pubitemid 27460944)
25. Oakley, R. H., Sar, M., and Cidlowski, J. A. (1996) The human glucocorticoid receptor β isoform. Expression, biochemical properties, and putative function. J. Biol. Chem. 271, 9550-9559
26. Yang, Z. Z., Tschopp, O., Hemmings-Mieszczak, M., Feng, J., Brodbeck, D., Perentes, E., and Hemmings, B. A. (2003) Protein kinase B α/Akt1 regulates placental development and fetal growth. J. Biol. Chem. 278, 32124-32131 (Pubitemid 37048402)
27. Garcia-Cao, I., Song, M. S., Hobbs, R. M., Laurent, G., Giorgi, C., de Boer, V. C., Anastasiou, D., Ito, K., Sasaki, A. T., Rameh, L., Carracedo, A., Vander Heiden, M. G., Cantley, L. C., Pinton, P., Haigis, M. C., and Pandolfi, P. P. (2012) Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 149, 49-62
28. Nuutinen, U., Postila, V., Mättö, M., Eeva, J., Ropponen, A., Eray, M., Riikonen, P., and Pelkonen, J. (2006) Inhibition of PI3-kinase-Akt pathway enhances dexamethasone-induced apoptosis in a human follicular lymphoma cell line. Exp. Cell Res. 312, 322-330 (Pubitemid 41814841)
29. Zhang, C., Ryu, Y. K., Chen, T. Z., Hall, C. P., Webster, D. R., and Kang, M. H. (2012) Synergistic activity of rapamycin and dexamethasone in vitro and in vivo in acute lymphoblastic leukemia via cell-cycle arrest and apoptosis. Leukemia Res. 36, 342-349
30. Vazquez-Tello, A., Halwani, R., Hamid, Q., and Al-Muhsen, S. (2013) Glucocorticoid receptor-β up-regulation and steroid resistance induction by IL-17 and IL-23 cytokine stimulation in peripheral mononuclear cells. J. Clin. Immunol. 33, 466-478
31. DuBois, D. C., Sukumaran, S., Jusko, W. J., and Almon, R. R. (2013) Evidence for a glucocorticoid receptor β splice variant in the rat and its physiological regulation in liver. Steroids 78, 312-320
32. Skeen, J. E., Bhaskar, P. T., Chen, C. C., Chen, W. S., Peng, X. D., Nogueira, V., Hahn-Windgassen, A., Kiyokawa, H., and Hay, N. (2006) Akt deficiency impairs normal cell proliferation and suppresses oncogenesis in a p53-independent and mTORC1-dependent manner. Cancer Cell 10, 269-280 (Pubitemid 44512190)
33. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., 3rd, Kaestner, K. H., Bartolomei, M. S., Shulman, G. I., and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB β). Science 292, 1728-1731 (Pubitemid 32506248)
34. Fischer-Posovszky, P., Tews, D., Horenburg, S., Debatin, K. M., and Wabitsch, M. (2012) Differential function of Akt1 and Akt2 in human adipocytes. Mol. Cell. Endocrinol. 358, 135-143
35. Easton, R. M., Cho, H., Roovers, K., Shineman, D. W., Mizrahi, M., Forman, M. S., Lee, V. M., Szabolcs, M., de Jong, R., Oltersdorf, T., Ludwig, T., Efstratiadis, A., and Birnbaum, M. J. (2005) Role for Akt3/protein kinase Bγ in attainment of normal brain size. Mol. Cell. Biol. 25, 1869-1878 (Pubitemid 40280150)
36. Hollander, M. C., Maier, C. R., Hobbs, E. A., Ashmore, A. R., Linnoila, R. I., and Dennis, P. A. (2011) Akt1 deletion prevents lung tumorigenesis by mutant K-ras. Oncogene 30, 1812-1821
37. Xia, C., Meng, Q., Cao, Z., Shi, X., and Jiang, B. H. (2006) Regulation of angiogenesis and tumor growth by p110α and AKT1 via VEGF expression. J. Cell. Physiol. 209, 56-66 (Pubitemid 44318667)
38. Luo, C., Yi, B., Bai, L., Xia, Y., Wang, G., Qian, G., and Feng, H. (2010) Suppression of Akt1 phosphorylation by adenoviral transfer of the PTEN gene inhibits hypoxia-induced proliferation of rat pulmonary arterial smooth muscle cells. Biochem. Biophys. Res. Commun. 397, 486-492
39. Piovan, E., Yu, J., Tosello, V., Herranz, D., Ambesi-Impiombato, A., Da Silva, A. C., Sanchez-Martin, M., Perez-Garcia, A., Rigo, I., Castillo, M., Indraccolo, S., Cross, J. R., de Stanchina, E., Paietta, E., Racevskis, J., Rowe, J. M., Tallman, M. S., Basso, G., Meijerink, J. P., Cordon-Cardo, C., Califano, A., and Ferrando, A. A. (2013) Direct reversal of glucocorticoid resistance by AKT inhibition in acute lymphoblastic leukemia. Cancer Cell 24, 766-776
40. Oakley, R. H., Jewell, C. M., Yudt, M. R., Bofetiado, D. M., and Cidlowski, J. A. (1999) The dominant negative activity of the human glucocorticoid receptor β isoform. Specificity and mechanisms of action. J. Biol. Chem. 274, 27857-27866
41. Kelly, A., Bowen, H., Jee, Y. K., Mahfiche, N., Soh, C., Lee, T., Hawrylowicz, C., and Lavender, P. (2008) The glucocorticoid receptor β isoform can mediate transcriptional repression by recruiting histone deacetylases. J. Allergy Clin. Immunol. 121, 203-208.e1
42. Varricchio, L., Masselli, E., Alfani, E., Battistini, A., Migliaccio, G., Vannucchi, A. M., Zhang, W., Rondelli, D., Godbold, J., Ghinassi, B., Whitsett, C., Hoffman, R., and Migliaccio, A. R. (2011) The dominant negative β isoform of the glucocorticoid receptor is uniquely expressed in erythroid cells expanded from polycythemia vera patients. Blood 118, 425-436
43. Trapp, T., Rupprecht, R., Castrén, M., Reul, J. M., and Holsboer, F. (1994) Heterodimerization between mineralocorticoid and glucocorticoid receptor: a new principle of glucocorticoid action in the CNS. Neuron 13, 1457-1462
44. Liu, W., Wang, J., Sauter, N. K., and Pearce, D. (1995) Steroid receptor heterodimerization demonstrated in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 92, 12480-12484 (Pubitemid 26014093)
45. Ligr, M., Li, Y., Logan, S. K., Taneja, S., Melamed, J., Lepor, H., Garabedian, M. J., and Lee, P. (2012) Mifepristone inhibits GRβ coupled prostate cancer cell proliferation. J. Urol. 188, 981-988
46. Zhu, J., Gong, J. Y., Goodman, O. B., Jr., Cartegni, L., Nanus, D. M., and Shen, R. (2007) Bombesin attenuates pre-mRNA splicing of glucocorticoid receptor by regulating the expression of serine-arginine protein p30c (SRp30c) in prostate cancer cells. Biochim. Biophys. Acta 1773, 1087-1094 (Pubitemid 46898675)
47. Piotrowska, H., and Jagodzinski, P. P. (2009) Glucocorticoid receptor α and β variant expression is associated with ASF/SF2 splicing factor upregulation in HT-29 colon cancer and MCF-7 breast carcinoma cells. Arch. Med. Res. 40, 156-162
48. Piotrowska, H., and Jagodzinski, P. P. (2007) Trichostatin A, sodium butyrate, and 5-aza-2′-deoxycytidine alter the expression of glucocorticoid receptor α and β isoforms in Hut-78 T- and Raji B-lymphoma cell lines. Biomed. Pharmacother. 61, 451-454 (Pubitemid 47239342)
49. Psarra, A. M., Solakidi, S., Trougakos, I. P., Margaritis, L. H., Spyrou, G., and Sekeris, C. E. (2005) Glucocorticoid receptor isoforms in human hepatocarcinoma HepG2 and SaOS-2 osteosarcoma cells: presence of glucocorticoid receptor α in mitochondria and of glucocorticoid receptor β in nucleoli. Int. J. Biochem. Cell Biol. 37, 2544-2558 (Pubitemid 41400324)
50. Solakidi, S., Psarra, A. M., and Sekeris, C. E. (2007) Differential distribution of glucocorticoid and estrogen receptor isoforms: localization of GRβ and ERα in nucleoli and GRα and ERβ in the mitochondria of human osteosarcoma SaOS-2 and hepatocarcinoma HepG2 cell lines. JMNI 7, 240-245 (Pubitemid 350252832)