Overexpression of glucocorticoid receptor β enhances myogenesis and reduces catabolic gene expression

International Journal of Molecular Sciences

Volumn 17, Issue 2, 2016, Pages

  Hinds, Terry D ^a   Peck, Bailey ^b   Shek, Evan ^b   Stroup, Steven ^b   Hinson, Jennifer ^b   Arthur, Susan ^b   Marino, Joseph S ^b  

^a MEDICAL COLLEGE OF OHIO   (United States)

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

Author keywords

Atrophy 6; Dexamethasone 9; Glucocorticoid receptor 2; Glucocorticoid receptor 3; GR 5; GR 4; MAFbx 7; MuRF1 8; Myogenesis

Indexed keywords

DEXAMETHASONE; F BOX PROTEIN; GLUCOCORTICOID RECEPTOR BETA; INSULIN; MUSCLE RING FINGER 1 PROTEIN; MYOSIN HEAVY CHAIN; RETINOIC ACID; TRANSCRIPTION FACTOR FKHRL1; GLUCOCORTICOID RECEPTOR; ISOPROTEIN; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CATABOLISM; GENE EXPRESSION; MOUSE; MTT ASSAY; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE MASS; MYOBLAST; MYOTUBE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG EFFECTS; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SKELETAL MUSCLE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DEXAMETHASONE; ENERGY METABOLISM; GENE EXPRESSION; GENE EXPRESSION REGULATION; INSULIN; MICE; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MYOBLASTS; PROTEIN ISOFORMS; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER;

EID: 84958559619     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17020232     Document Type: Article

References (54)

1. Ferrando, A.A.; Wolfe, R.R. Restoration of hormonal action and muscle protein. Crit. Care Med. 2007, 35, S630-S634.
2. Fitts, R.H.; Romatowski, J.G.; Peters, J.R.; Paddon-Jones, D.; Wolfe, R.R.; Ferrando, A.A. The deleterious effects of bed rest on human skeletal muscle fibers are exacerbated by hypercortisolemia and ameliorated by dietary supplementation. Am. J. Physiol. Cell. Physiol. 2007, 293, C313-C320.
3. Hanaoka, B.Y.; Peterson, C.A.; Horbinski, C.; Crofford, L.J. Implications of glucocorticoid therapy in idiopathic inflammatory myopathies. Nat. Rev. Rheumatol. 2012, 8, 448-457.
4. Miller, B.S.; Ignatoski, K.M.; Daignault, S.; Lindland, C.; Gauger, P.G.; Doherty, G.M.; Wang, S.C. A quantitative tool to assess degree of sarcopenia objectively in patients with hypercortisolism. Surgery 2011, 150, 1178-1185.
5. Cohen, S.; Nathan, J.A.; Goldberg, A.L. Muscle wasting in disease: Molecular mechanisms and promising therapies. Nat. Rev. Drug Discov. 2015, 14, 58-74.
6. Gross, K.L.; Cidlowski, J.A. Tissue-specific glucocorticoid action: A family affair. Trends Endocrinol. Metab. 2008, 19, 331-339.
7. Heitzer, M.D.; Wolf, I.M.; Sanchez, E.R.; Witchel, S.F.; DeFranco, D.B. Glucocorticoid receptor physiology. Rev. Endocr. Metab. Disord. 2007, 8, 321-330.
8. Schakman, O.; Kalista, S.; Barbe, C.; Loumaye, A.; Thissen, J.P. Glucocorticoid-induced skeletal muscle atrophy. Int. J. Biochem. Cell Biol. 2013, 45, 2163-2172.
9. Hinds, T.D., Jr.; Ramakrishnan, S.; Cash, H.A.; Stechschulte, L.A.; Heinrich, G.; Najjar, S.M.; Sanchez, E.R. Discovery of glucocorticoid receptor-β in mice with a role in metabolism. Mol. Endocrinol. 2010, 24, 1715-1727.
10. Oakley, R.H.; Jewell, C.M.; Yudt, M.R.; Bofetiado, D.M.; Cidlowski, J.A. The dominant negative activity of the human glucocorticoid receptor isoform: Specificity and mechanisms of action. J. Biol. Chem. 1999, 274, 27857-27866.
11. Oakley, R.H.; Sar, M.; Cidlowski, J.A. The human glucocorticoid receptor β isoform-Expression, biochemical properties, and putative function. J. Biol. Chem. 1996, 271, 9550-9559.
12. Whorwood, C.B.; Donovan, S.J.; Wood, P.J.; Phillips, D.I. Regulation of glucocorticoid receptor α and β isoforms and type I 11β-hydroxysteroid dehydrogenase expression in human skeletal muscle cells: A key role in the pathogenesis of insulin resistance? J. Clin. Endocrinol. Metab. 2001, 86, 2296-2308.
13. Leung, D.Y.; Hamid, Q.; Vottero, A.; Szefler, S.J.; Surs, W.; Minshall, E.; Chrousos, G.P.; Klemm, D.J. Association of glucocorticoid insensitivity with increased expression of glucocorticoid receptor β. J. Exp. Med. 1997, 186, 1567-1574.
14. Goleva, E.; Li, L.B.; Eves, P.T.; Strand, M.J.; Martin, R.J.; Leung, D.Y. Increased glucocorticoid receptor β alters steroid response in glucocorticoid-insensitive asthma. Am. J. Respir. Crit. Care Med. 2006, 173, 607-616.
15. Sousa, A.R.; Lane, S.J.; Cidlowski, J.A.; Staynov, D.Z.; Lee, T.H. Glucocorticoid resistance in asthma is associated with elevated in vivo expression of the glucocorticoid receptor β-isoform. J. Allergy Clin. Immunol. 2000, 105, 943-950.
16. Longui, C.A.; Vottero, A.; Adamson, P.C.; Cole, D.E.; Kino, T.; Monte, O.; Chrousos, G.P. Low glucocorticoid receptor α/β ratio in T-cell lymphoblastic leukemia. Horm. Metab. Res. 2000, 32, 401-406.
17. Piotrowska, H.; Jagodzinski, P.P. 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. 2009, 40, 156-162.
18. Webster, J.C.; Oakley, R.H.; Jewell, C.M.; Cidlowski, J.A. 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. USA 2001, 98, 6865-6870.
19. Kino, T.; Su, Y.A.; Chrousos, G.P. Human glucocorticoid receptor isoform β: Recent understanding of its potential implications in physiology and pathophysiology. Cell. Mol. Life Sci. 2009, 66, 3435-3448.
20. Stechschulte, L.A.; Wuescher, L.; Marino, J.S.; Hill, J.W.; Eng, C.; Hinds, T.D., Jr. Glucocorticoid receptor β stimulates Akt1 growth pathway by attenuation of PTEN. J. Biol. Chem. 2014, 289, 17885-17894.
21. Yin, Y.; Zhang, X.; Li, Z.; Deng, L.; Jiao, G.; Zhang, B.; Xie, P.; Mu, H.; Qiao, W.; Zou, J. Glucocorticoid receptor β regulates injury-mediated astrocyte activation and contributes to glioma pathogenesis via modulation of β-catenin/TCF transcriptional activity. Neurobiol. Dis. 2013, 59, 165-176.
22. Ligr, M.; Li, Y.; Logan, S.K.; Taneja, S.; Melamed, J.; Lepor, H.; Garabedian, M.J.; Lee, P. Mifepristone inhibits GRβ coupled prostate cancer cell proliferation. J. Urol. 2012, 188, 981-988.
23. Bentzinger, C.F.; Wang, Y.X.; Rudnicki, M.A. Building muscle: Molecular regulation of myogenesis. Cold Spring Harb. Perspect. Biol. 2012, 4, doi:10.1101/cshperspect.a008342.
24. Charge, S.B.; Rudnicki, M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 2004, 84, 209-238.
25. Rotwein, P.; Wilson, E.M. Distinct actions of Akt1 and Akt2 in skeletal muscle differentiation. J. Cell. Physiol. 2009, 219, 503-511.
26. Mandl, A.; Sarkes, D.; Carricaburu, V.; Jung, V.; Rameh, L. Serum withdrawal-induced accumulation of phosphoinositide 3-kinase lipids in differentiating 3T3-L6 myoblasts: Distinct roles for SHIP2 and PTEN. Mol. Cell. Biol. 2007, 27, 8098-8112.
27. Qin, W.; Pan, J.; Qin, Y.; Lee, D.N.; Bauman, W.A.; Cardozo, C. Identification of functional glucocorticoid response elements in the mouse Foxo1 promoter. Biochem. Biophys. Res. Commun. 2014, 450, 979-983.
28. Zheng, B.; Ohkawa, S.; Li, H.; Roberts-Wilson, T.K.; Price, S.R. Foxo3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB J. 2010, 24, 2660-2669.
29. Waddell, D.S.; Baehr, L.M.; van den Brandt, J.; Johnsen, S.A.; Reichardt, H.M.; Furlow, J.D.; Bodine, S.C. The glucocorticoid receptor and Foxo1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am. J. Physiol. Endocrinol. Metab. 2008, 295, E785-E797.
30. Watson, M.L.; Baehr, L.M.; Reichardt, H.M.; Tuckermann, J.P.; Bodine, S.C.; Furlow, J.D. A cell-autonomous role for the glucocorticoid receptor in skeletal muscle atrophy induced by systemic glucocorticoid exposure. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E1210-E1220.
31. 12myotubes. J. Cell. Biochem. 2008, 105, 353-364.
32. Baehr, L.M.; Furlow, J.D.; Bodine, S.C. Muscle sparing in muscle ring finger 1 null mice: Response to synthetic glucocorticoids. J. Physiol. 2011, 589, 4759-4776.
33. Seene, T.; Kaasik, P.; Pehme, A.; Alev, K.; Riso, E.M. The effect of glucocorticoids on the myosin heavy chain isoforms' turnover in skeletal muscle. J. Steroid Biochem. Mol. Biol. 2003, 86, 201-206.
34. Bodine, S.C.; Latres, E.; Baumhueter, S.; Lai, V.K.; Nunez, L.; Clarke, B.A.; Poueymirou, W.T.; Panaro, F.J.; Na, E.; Dharmarajan, K.; et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294, 1704-1708.
35. Lecker, S.H.; Jagoe, R.T.; Gilbert, A.; Gomes, M.; Baracos, V.; Bailey, J.; Price, S.R.; Mitch, W.E.; Goldberg, A.L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 2004, 18, 39-51.
36. Castillero, E.; Alamdari, N.; Lecker, S.H.; Hasselgren, P.O. Suppression of atrogin-1 and MuRF1 prevents dexamethasone-induced atrophy of cultured myotubes. Metabolism 2013, 62, 1495-1502.
37. Filipovic, D.; Pirkmajer, S.; Mis, K.; Mars, T.; Grubic, Z. Expression of glucocorticoid receptors in the regenerating human skeletal muscle. Physiol. Res. 2011, 60 (Suppl. S1), S147-S154.
38. Patel, R.; Williams-Dautovich, J.; Cummins, C.L. Minireview: New molecular mediators of glucocorticoid receptor activity in metabolic tissues. Mol. Endocrinol. 2014, 28, 999-1011.
39. Schacke, H.; Docke, W.D.; Asadullah, K. Mechanisms involved in the side effects of glucocorticoids. Pharmacol. Ther. 2002, 96, 23-43.
40. Asensio, C.; Muzzin, P.; Rohner-Jeanrenaud, F. Role of glucocorticoids in the physiopathology of excessive fat deposition and insulin resistance. Int. J. Obes. 2004, 28 (Suppl. S4), S45-S52.
41. Kuo, T.; Harris, C.A.; Wang, J.C. Metabolic functions of glucocorticoid receptor in skeletal muscle. Mol. Cell. Endocrinol. 2013, 380, 79-88.
42. Zhao, W.; Qin, W.; Pan, J.; Wu, Y.; Bauman, W.A.; Cardozo, C. Dependence of dexamethasone-induced Akt/Foxo1 signaling, upregulation of MAFbx, and protein catabolism upon the glucocorticoid receptor. Biochem. Biophys. Res. Commun. 2009, 378, 668-672.
43. Shimizu, N.; Yoshikawa, N.; Ito, N.; Maruyama, T.; Suzuki, Y.; Takeda, S.; Nakae, J.; Tagata, Y.; Nishitani, S.; Takehana, K.; et al. Crosstalk between glucocorticoid receptor and nutritional sensor mtor in skeletal muscle. Cell Metab. 2011, 13, 170-182.
44. Giorgino, F.; Almahfouz, A.; Goodyear, L.J.; Smith, R.J. Glucocorticoid regulation of insulin receptor and substrate IRS-1 tyrosine phosphorylation in rat skeletal muscle in vivo. J. Clin. Investig. 1993, 91, 2020-2030.
45. Hu, Z.; Wang, H.; Lee, I.H.; Du, J.; Mitch, W.E. Endogenous glucocorticoids and impaired insulin signaling are both required to stimulate muscle wasting under pathophysiological conditions in mice. J. Clin. Investig. 2009, 119, 3059-3069.
46. Kuo, T.; Lew, M.J.; Mayba, O.; Harris, C.A.; Speed, T.P.; Wang, J.C. Genome-wide analysis of glucocorticoid receptor-binding sites in myotubes identifies gene networks modulating insulin signaling. Proc. Natl. Acad. Sci. USA 2012, 109, 11160-11165.
47. Gomes, A.V.; Waddell, D.S.; Siu, R.; Stein, M.; Dewey, S.; Furlow, J.D.; Bodine, S.C. Upregulation of proteasome activity in muscle ring finger 1-null mice following denervation. FASEB J. 2012, 26, 2986-2999.
48. Tintignac, L.A.; Lagirand, J.; Batonnet, S.; Sirri, V.; Leibovitch, M.P.; Leibovitch, S.A. Degradation of myod mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 2005, 280, 2847-2856.
49. Jogo, M.; Shiraishi, S.; Tamura, T.A. Identification of MAFbx as a myogenin-engaged F-box protein in SCF ubiquitin ligase. FEBS Lett. 2009, 583, 2715-2719.
50. Marino, J.S.; Hinds, T.D., Jr.; Potter, R.A.; Ondrus, E.; Onion, J.L.; Dowling, A.; McLoughlin, T.J.; Sanchez, E.R.; Hill, J.W. Suppression of protein kinase C theta contributes to enhanced myogenesis in vitro via IRS1 and ERK1/2 phosphorylation. BMC Cell Biol. 2013, 14, doi:10.1186/1471-2121-14-39.
51. Clarke, B.A.; Drujan, D.; Willis, M.S.; Murphy, L.O.; Corpina, R.A.; Burova, E.; Rakhilin, S.V.; Stitt, T.N.; Patterson, C.; Latres, E.; et al. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 2007, 6, 376-385.
52. Cohen, S.; Brault, J.J.; Gygi, S.P.; Glass, D.J.; Valenzuela, D.M.; Gartner, C.; Latres, E.; Goldberg, A.L. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J. Cell Biol. 2009, 185, 1083-1095.
53. Spencer, J.A.; Eliazer, S.; Ilaria, R.L., Jr.; Richardson, J.A.; Olson, E.N. Regulation of microtubule dynamics and myogenic differentiation by MuRF, a striated muscle ring-finger protein. J. Cell Biol. 2000, 150, 771-784.
54. John, K.; Marino, J.S.; Sanchez, E.R.; Hinds, T.D., Jr. The glucocorticoid receptor: Cause or cure for obesity? Am. J. Physiol. Endocrinol. Metab. 2015, doi:10.1152/ajpendo.00478.2015.