A cell-autonomous role for the glucocorticoid receptor in skeletal muscle atrophy induced by systemic glucocorticoid exposure

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 10, 2012, Pages

  Watson, Monica L ^a   Baehr, Leslie M ^a   Reichardt, Holger M ^b   Tuckermann, Jan P ^c   Bodine, Sue C ^a,d   David Furlow, J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c FRITZ LIPMANN INSTITUTE   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Denervation; Dexamethasone; Muscle atrophy F box; Muscle RING finger 1; Nutritional deprivation

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MUSCLE RING FINGER 1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLS; CONTROLLED STUDY; FEMALE; GENE; GENE CONTROL; GENE DELETION; GENE EXPRESSION; KNOCKOUT MOUSE; LEG MUSCLE; MAFBX GENE; MOUSE; MURF1 GENE; MUSCLE ATROPHY; MUSCLE DENERVATION; NERVE LESION; NONHUMAN; NUTRITION; PRIORITY JOURNAL; SCIATIC NERVE; SKELETAL MUSCLE; STARVATION;

ANIMALS; CALORIC RESTRICTION; CARRIER PROTEINS; DEXAMETHASONE; GLUCOCORTICOIDS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MUSCLE DENERVATION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PHOSPHOPROTEINS; RECEPTORS, GLUCOCORTICOID; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84861118898     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00512.2011     Document Type: Article

References (64)

1. Baehr LM, Furlow JD, Bodine SC. Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J Physiol 589: 4759-4776, 2011.
2. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schütz G, Schibler U. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289: 2344-2347, 2000.
3. Barel M, Perez OA, Giozzet VA, Rafacho A, Bosqueiro JR, do Amaral SL. Exercise training prevents hyperinsulinemia, muscular glycogen loss and muscle atrophy induced by dexamethasone treatment. Eur J Appl Physiol 108: 999-1007, 2010.
4. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
5. Boyle MP, Brewer JA, Funatsu M, Wozniak DF, Tsien JZ, Izumi Y, Muglia LJ. Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc Natl Acad Sci USA 102: 473-478, 2005.
6. Brewer JA, Khor B, Vogt SK, Muglia LM, Fujiwara H, Haegele KE, Sleckman BP, Muglia LJ. T-cell glucocorticoid receptor is required to suppress COX-2-mediated lethal immune activation. Nat Med 9: 1318-1322, 2003.
7. Brüning JC, Michael MD, Winnay JN, Hayashi T, Hörsch D, Accili D, Goodyear LJ, Kahn CR. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2: 559-569, 1998.
8. Buren J, Lai YC, Lundgren M, Eriksson JW, Jensen J. Insulin action and signalling in fat and muscle from dexamethasone-treated rats. Arch Biochem Biophys 474: 91-101, 2008.
9. Cho JE, Fournier M, Da X, Lewis MI. Time course expression of Foxo transcription factors in skeletal muscle following corticosteroid administration. J Appl Physiol 108: 137-145, 2010.
10. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasonetreated skeletal muscle. Cell Metab 6: 376-385, 2007.
11. Cole TJ, Blendy JA, Monaghan AP, Krieglstein K, Schmid W, Aguzzi A, Fantuzzi G, Hummler E, Unsicker K, Schütz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev 9: 1608-1621, 1995.
12. Dardevet D, Sornet C, Grizard J. Glucocorticoid-induced insulin resistance of protein synthesis is independent of the rapamycin-sensitive pathways in rat skeletal muscle. J Endocrinol 162: 77-85, 1999.
13. Desler MM, Jones SJ, Smith CW, Woods TL. Effects of dexamethasone and anabolic agents on proliferation and protein synthesis and degradation in C2C12 myogenic cells. J Anim Sci 74: 1265-1273, 1996.
14. Dumas JF, Simard G, Roussel D, Douay O, Foussard F, Malthiery Y, Ritz P. Mitochondrial energy metabolism in a model of undernutrition induced by dexamethasone. Br J Nutr 90: 969-977, 2003.
15. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 151: 4811-4819, 2010.
16. Gesina E, Tronche F, Herrera P, Duchene B, Tales W, Czernichow P, Breant B. Dissecting the role of glucocorticoids on pancreas development. Diabetes 53: 2322-2329, 2004.
17. Goldberg AL. Protein turnover in skeletal muscle. II. Effects of denervation and cortisone on protein catabolism in skeletal muscle. J Biol Chem 244: 3223-3229, 1969.
18. Hasselgren PO. Glucocorticoids and muscle catabolism. Curr Opin Clin Nutr Metab Care 2: 201-205, 1999.
19. Hobler SC, Tiao G, Fischer JE, Monaco J, Hasselgren PO. Sepsisinduced increase in muscle proteolysis is blocked by specific proteasome inhibitors. Am J Physiol Regul Integr Comp Physiol 274: R30-R37, 1998.
20. Hong DH, Forsberg NE. Effects of dexamethasone on protein degradation and protease gene expression in rat L8 myotube cultures. Mol Cell Endocrinol 108: 199-209, 1995.
21. Hu Z, Lee IH, Wang X, Sheng H, Zhang L, Du J, Mitch WE. PTEN expression contributes to the regulation of muscle protein degradation in diabetes. Diabetes 56: 2449-2456, 2007.
22. Hu Z, Wang H, Leed IH, Du J, Mitch WE. Endogenous glucocorticoids and impaired insulin signaling are both required to stimulate muscle wasting under pathophysiological conditions in mice. J Clin Invest 119: 3059-3069, 2009.
23. Kellendonk C, Eiden S, Kretz O, Schutz G, Schmidt I, Tronche F, Simon E. Inactivation of the GR in the nervous system affects energy accumulation. Endocrinology 143: 2333-2340, 2002.
24. Kellendonk C, Opherk C, Anlag K, Schutz G, Tronche F. Hepatocytespecific expression of Cre recombinase. Genesis 26: 151-153, 2000.
25. Kelly EJ, Sandgren EP, Brinster RL, Palmiter RD. A pair of adjacent glucocorticoid response elements regulate expression of two mouse metallothionein genes. Proc Natl Acad Sci USA 94: 10045-10050, 1997.
26. Kimball SR, Jefferson LS. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. J Biol Chem 285: 29027-29032, 2010.
27. Lewis MI, Bodine SC, Kamangar N, Xu X, Da X, Fournier M. Effect of severe short-term malnutrition on diaphragm muscle signal transduction pathways influencing protein turnover. J Appl Physiol 100: 1799-1806, 2006.
28. Logie JJ, Ali S, Marshall KM, Heck MM, Walker BR, Hadoke PW. Glucocorticoid-mediated inhibition of angiogenic changes in human endothelial cells is not caused by reductions in cell proliferation or migration. PLoS One 5: e14476, 2010.
29. Ma K, Mallidis C, Bhasin S, Mahabadi V, Artaza J, Gonzalez-Cadavid N, Arias J, Salehian B. Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am J Physiol Endocrinol Metab 285: E363-E371, 2003.
30. May RC, Kelly RA, Mitch WE. Metabolic acidosis stimulates protein degradation in rat mucle by glucocorticoid-dependent mechanism. J Clin Invest 77: 614-621, 1986.
31. Meisler N, Shull S, Xie R, Long GL, Absher M, Connolly JP, Cutroneo KR. Glucocorticoids coordinately regulate type I collagen pro alpha 1 promoter activity through both the glucocorticoid and transforming growth factor beta response elements: a novel mechanism of glucocorticoid regulation of eukaryotic genes. J Cell Biochem 59: 376-388, 1995.
32. Mitch WE, Bailey JL, Wang X, Jurkovitz C, Newby D, Price SR. Evaluation of signals activating ubiquitin-proteasome proteolysis in a model of muscle wasting. Am J Physiol Cell Physiol 276: C1132-C1138, 1999.
33. Moresi V, Williams AH, Meadows E, Flynn JM, Potthoff MJ, McAnally J, Shelton JM, Backs J, Klein WH, Richardson JA, Bassel-Duby R, Olson EN. Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143: 35-45, 2010.
34. Muir JL, Pfister HP. Corticosterone and prolactin responses to predictable and unpredictable novelty stress in rats. Physiol Behav 37: 285-288, 1986.
35. O'Sullivan U, Gluckman PD, Breier BH, Woodall S, Siddiqui RA, McCutcheon SN. Insulin-like growth factor-1 (IGF-1) in mice reduces weight loss during starvation. Endocrinology 125: 2793-2794, 1989.
36. Opherk C, Tronche F, Kellendonk C, Kohlmüller D, Schulze A, Schmid W, Schütz G. Inactivation of the glucocorticoid receptor in hepatocytes leads to fasting hypoglycemia and ameliorates hyperglycemia in streptozotocin-induced diabetes mellitus. Mol Endocrinol 18: 1346-1353, 2004.
37. Park YS, Ha Choi Y, Park CH, Kim KT. Nongenomic glucocorticoid effects on activity-dependent potentiation of catecholamine release in chromaffin cells. Endocrinology 149: 4921-4927, 2008.
38. Rao RH. Adaptations in glucose homeostasis during chronic nutritional deprivation in rats: hepatic resistance to both insulin and glucagon. Metabolism 44: 817-824, 1995.
39. Rauch A, Seitz S, Baschant U, Schilling AF, Illing A, Stride B, Kirilov M, Mandic V, Takacz A, Schmidt-Ullrich R, Ostermay S, Schinke T, Spanbroek R, Zaiss MM, Angel PE, Lerner UH, David JP, Reichardt HM, Amling M, Schütz G, Tuckermann JP. Glucocorticoids suppress bone formation by attenuating osteoblast differentiation via the monomeric glucocorticoid receptor. Cell Metab 11: 517-531, 2010.
40. Riso EM, Ahtikoski A, Alev K, Kaasik P, Pehme A, Seene T. Relationship between extracellular matrix, contractile apparatus, muscle mass and strength in case of glucocorticoid myopathy. J Steroid Biochem Mol Biol 108: 117-120, 2008.
41. Rooman R, Koster G, Bloemen R, Gresnigt R, van Buul-Offers SC. The effect of dexamethasone on body and organ growth of normal and IGF-II-transgenic mice. J Endocrinol 163: 543-552, 1999.
42. Ruff RL, Martyn D, Gordon AM. Glucocorticoid-induced atrophy is not due to impaired excitability of rat muscle. Am J Physiol Endocrinol Metab 243: E512-E521, 1982.
43. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412, 2004.
44. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55-89, 2000.
45. Schoepe S, Schäcke H, Bernd A, Zöller N, Asadullah K. Identification of novel in vitro test systems for the determination of glucocorticoid receptor ligand-induced skin atrophy. Skin Pharmacol Physiol 23: 139-151, 2010.
46. Seene T. Turnover of skeletal muscle contractile proteins in glucocorticoid myopathy. J Steroid Biochem Mol Biol 50: 1-4, 1994.
47. Shah OJ, Kimball SR, Jefferson LS. Acute attenuation of translation initiation and protein synthesis by glucocorticoids in skeletal muscle. Am J Physiol Endocrinol Metab 278: E76-E82, 2000.
48. Smith IJ, Alamdari N, O'Neal P, Gonnella P, Aversa Z, Hasselgren PO. Sepsis increases the expression and activity of the transcription factor Forkhead Box O 1 (FOXO1) in skeletal muscle by a glucocorticoiddependent mechanism. Int J Biochem Cell Biol 42: 701-711, 2010.
49. So AY, Bernal TU, Pillsbury ML, Yamamoto KR, Feldman BJ. Glucocorticoid regulation of the circadian clock modulates glucose homeostasis. Proc Natl Acad Sci USA 106: 17582-17587, 2009.
50. Sterling KM Jr, Harris MJ, Mitchell JJ, DiPetrillo TA, Delaney GL, Cutroneo KR. Dexamethasone decreases the amounts of type I procollagen mRNAs in vivo and in fibroblast cell cultures. J Biol Chem 258: 7644-7647, 1983.
51. Stojanovska L, Rosella G, Proietto J. Evolution of dexamethasoneinduced insulin resistance in rats. Am J Physiol Endocrinol Metab 258: E748-E756, 1990.
52. Sun L, Trausch-Azar JS, Muglia LJ, Schwartz AL. Glucocorticoids differentially regulate degradation of MyoD and Id1 by N-terminal ubiquitination to promote muscle protein catabolism. Proc Natl Acad Sci USA 3339-3344, 2008.
53. Tillis CC, Huang HW, Bi W, Pan S, Bruce SR, Alcorn JL. Glucocorticoid regulation of human pulmonary surfactant protein-B (SP-B) mRNA stability is independent of activated glucocorticoid receptor. Am J Physiol Lung Cell Mol Physiol 300: L940-L950, 2011.
54. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103, 1999.
55. Tronche F, Opherk C, Moriggl R, Kellendonk C, Reimann A, Schwake L, Reichardt HM, Stangl K, Gau D, Hoeflich A, Beug H, Schmid W, Schütz G. Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth. Genes Dev 18: 492-497, 2004.
56. Tuckermann JP, Kleiman A, Moriggl R, Spanbroek R, Neumann A, Illing A, Clausen BE, Stride B, Forster I, Habenicht AJ, Reichardt HM, Tronche F, Schmid W, Schutz G. Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. J Clin Invest 117: 1381-1390, 2007.
57. Tulipano G, Taylor JE, Halem HA, Datta R, Dong JZ, Culler MD, Bianchi I, Cocchi D, Giustina A. Glucocorticoid inhibition of growth in rats: partial reversal with the full-length ghrelin analog BIM-28125. Pituitary 10: 267-274, 2007.
58. Verhees KJ, Schols AM, Kelders MC, Op den Kamp CM, van der Velden JL, Langen RC. Glycogen synthase kinase-3β is required for the induction of skeletal muscle atrophy. Am J Physiol Cell Physiol 301: C995-C1007, 2011.
59. 2 -activated, and ubiquitin-proteasome proteolytic pathways. J Clin Invest 97: 1610-1617, 1996.
60. Waddell D, Baehr L, Van Den Brandt J, Johnsen S, Reichardt H, Furlow J, Bodine S. The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 295: E785-E797, 2008.
61. Wang H, Kubica N, Ellisen LW, Jefferson LS, Kimball SR. Dexamethasone represses signaling through the mammalian target of rapamycin in muscle cells by enhancing expression of REDD1. J Biol Chem 281: 39128-39134, 2006.
62. Weinstein RS, Wan C, Liu Q, Wang Y, Almeida M, O'Brien CA, Thostenson J, Roberson PK, Boskey AL, Clemens TL, Manolagas SC. Endogenous glucocorticoids decrease skeletal angiogenesis, vascularity, hydration, and strength in aged mice. Aging Cell 9: 147-161, 2010.
63. Wing SS, Haas AL, Goldberg AL. Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem J 307: 639-645, 1995.
64. Zhao W, Qin W, Pan J, Wu Y, Bauman WA, Cardozo C. Dependence of dexamethasone-induced Akt/FOXO1 signaling, upregulation of MAFbx, and protein catabolism upon the glucocorticoid receptor. Biochem Biophys Res Commun 378: 668-672, 2009.