Glucocorticoid-induced apoptosis and cellular mechanisms of myopathy

Journal of Steroid Biochemistry and Molecular Biology

Volumn 117, Issue 1-3, 2009, Pages 1-7

  Dirks Naylor, Amie J ^a   Griffiths, Carrie L ^a  

^a WINGATE UNIVERSITY   (United States)

Author keywords

Atrophy; Cell death; Mitochondria; Oxidative stress; Skeletal muscle

Indexed keywords

CASPASE 3; CASPASE 8; CERAMIDE; FAS ANTIGEN; GLUCOCORTICOID; MUSCLE PROTEIN; PROTEASOME; SOMATOMEDIN C;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; CORTICOSTEROID INDUCED MYOPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; INFLAMMATORY DISEASE; INSULIN RESISTANCE; MITOCHONDRION; MUSCLE ATROPHY; MYOPATHY; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CERAMIDES; GLUCOCORTICOIDS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INSULIN-LIKE GROWTH FACTOR I; MITOCHONDRIA, MUSCLE; MODELS, BIOLOGICAL; MUSCULAR DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION;

EID: 70249089025     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2009.05.014     Document Type: Review

References (67)

1. Seale J.P., and Compton M.R. Side-effects of corticosteroid agents. Med. J. Aust. 144 (1986) 139-142
2. Zoorob R.J., and Cender D. A different look at corticosteroids. Am. Fam. Physician 58 (1998) 443-450
3. Covar R.A., Leung D.Y., McCormick D., Steelman J., Zeitler P., and Spahn J.D. Risk factors associated with glucocorticoid-induced adverse effects in children with severe asthma. J. Allergy Clin. Immunol. 106 (2000) 651-659
4. Bowyer S.L., LaMothe M.P., and Hollister J.R. Steroid myopathy: incidence and detection in a population with asthma. J. Allergy Clin. Immunol. 76 (1985) 234-242
5. Mastagllia F. Drug induced myopathies. Pract. Neurol. 6 (2006) 4-13
6. Owczarek J., Jasinska M., and Orszulak-Michalak D. Drug-induced myopathies. An overview of the possible mechanisms. Pharmacol. Rep. 57 (2005) 23-34
7. Lee M.C., Lee J.S., Lee M.J., Lee J.H., and Kim H.I. Fas mediates apoptosis in steroid-induced myopathy of rats. Neuropathol. Appl. Neurobiol. 27 (2001) 396-402
8. Lee M.C., Wee G.R., and Kim J.H. Apoptosis of skeletal muscle on steroid-induced myopathy in rats. J. Nutr. 135 (2005) 1806S-1808S
9. Lim J.H., Kim D.Y., and Bang M.S. Effects of exercise and steroid on skeletal muscle apoptosis in the mdx mouse. Muscle Nerve 30 (2004) 456-462
10. Orzechowski A., Jank M., Gajkowska B., Sadkowski T., and Godlewskia M.M. A novel antioxidant-inhibited dexamethasone-mediated and caspase-3-independent muscle cell death. Ann. N.Y. Acad. Sci. 1010 (2003) 205-208
11. Oshima Y., Kuroda Y., Kunishige M., Matsumoto T., and Mitsui T. Oxidative stress-associated mitochondrial dysfunction in corticosteroid-treated muscle cells. Muscle Nerve 30 (2004) 49-54
12. Singleton J.R., Baker B.L., and Thorburn A. Dexamethasone inhibits insulin-like growth factor signaling and potentiates myoblast apoptosis. Endocrinology 141 (2000) 2945-2950
13. Lepine S., Lakatos B., Courageot M.P., Le Stunff H., Sulpice J.C., and Giraud F. Sphingosine contributes to glucocorticoid-induced apoptosis of thymocytes independently of the mitochondrial pathway. J. Immunol. 173 (2004) 3783-3790
14. Marchetti M.C., Di Marco B., Cifone G., Migliorati G., and Riccardi C. Dexamethasone-induced apoptosis of thymocytes: role of glucocorticoid receptor-associated Src kinase and caspase-8 activation. Blood 101 (2003) 585-593
15. Tonomura N., McLaughlin K., Grimm L., Goldsby R.A., and Osborne B.A. Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J. Immunol. 170 (2003) 2469-2478
16. Laane E., Panaretakis T., Pokrovskaja K., Buentke E., Corcoran M., Soderhall S., Heyman M., Mazur J., Zhivotovsky B., Porwit A., and Grander D. Dexamethasone-induced apoptosis in acute lymphoblastic leukemia involves differential regulation of Bcl-2 family members. Haematologica 92 (2007) 1460-1469
17. Conradie M.M., de Wet H., Kotze D.D., Burrin J.M., Hough F.S., and Hulley P.A. Vanadate prevents glucocorticoid-induced apoptosis of osteoblasts in vitro and osteocytes in vivo. J. Endocrinol. 195 (2007) 229-240
18. Davis M.C., McColl K.S., Zhong F., Wang Z., Malone M.H., and Distelhorst C.W. Dexamethasone-induced inositol 1,4,5-trisphosphate receptor elevation in murine lymphoma cells is not required for dexamethasone-mediated calcium elevation and apoptosis. J. Biol. Chem. (2008)
19. Lepine S., Sulpice J.C., and Giraud F. Signaling pathways involved in glucocorticoid-induced apoptosis of thymocytes. Crit. Rev. Immunol. 25 (2005) 263-288
20. Hoijman E., Rocha Viegas L., Keller Sarmiento M.I., Rosenstein R.E., and Pecci A. Involvement of Bax protein in the prevention of glucocorticoid-induced thymocytes apoptosis by melatonin. Endocrinology 145 (2004) 418-425
21. Hegardt C., Andersson G., and Oredsson S.M. Spermine prevents cytochrome c release in glucocorticoid-induced apoptosis in mouse thymocytes. Cell Biol. Int. 27 (2003) 115-121
22. Chauhan D., Hideshima T., Rosen S., Reed J.C., Kharbanda S., and Anderson K.C. Apaf-1/cytochrome c-independent and Smac-dependent induction of apoptosis in multiple myeloma (MM) cells. J. Biol. Chem. 276 (2001) 24453-24456
23. Hakem R., Hakem A., Duncan G.S., Henderson J.T., Woo M., Soengas M.S., Elia A., de la Pompa J.L., Kagi D., Khoo W., Potter J., Yoshida R., Kaufman S.A., Lowe S.W., Penninger J.M., and Mak T.W. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94 (1998) 339-352
24. Kuida K., Haydar T.F., Kuan C.Y., Gu Y., Taya C., Karasuyama H., Su M.S., Rakic P., and Flavell R.A. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94 (1998) 325-337
25. Yin X.M., Wang K., Gross A., Zhao Y., Zinkel S., Klocke B., Roth K.A., and Korsmeyer S.J. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400 (1999) 886-891
26. Micheau O., Solary E., Hammann A., and Dimanche-Boitrel M.T. Fas ligand-independent, FADD-mediated activation of the Fas death pathway by anticancer drugs. J. Biol. Chem. 274 (1999) 7987-7992
27. Gilson H., Schakman O., Combaret L., Lause P., Grobet L., Attaix D., Ketelslegers J.M., and Thissen J.P. Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148 (2007) 452-460
28. 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., Pan Z.Q., Valenzuela D.M., DeChiara T.M., Stitt T.N., Yancopoulos G.D., and Glass D.J. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294 (2001) 1704-1708
29. Mitch W.E., and Goldberg A.L. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335 (1996) 1897-1905
30. 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., and Glass D.J. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 6 (2007) 376-385
31. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., and Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117 (2004) 399-412
32. Yang Y., Fang S., Jensen J.P., Weissman A.M., and Ashwell J.D. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 288 (2000) 874-877
33. Hirsch T., Dallaporta B., Zamzami N., Susin S.A., Ravagnan L., Marzo I., Brenner C., and Kroemer G. Proteasome activation occurs at an early, premitochondrial step of thymocyte apoptosis. J. Immunol. 161 (1998) 35-40
34. Dallaporta B., Pablo M., Maisse C., Daugas E., Loeffler M., Zamzami N., and Kroemer G. Proteasome activation as a critical event of thymocyte apoptosis. Cell Death Differ. 7 (2000) 368-373
35. He H., Qi X.M., Grossmann J., and Distelhorst C.W. c-Fos degradation by the proteasome. An early, Bcl-2-regulated step in apoptosis. J. Biol. Chem. 273 (1998) 25015-25019
36. Gil-Gomez G., Berns A., and Brady H.J. A link between cell cycle and cell death: Bax and Bcl-2 modulate Cdk2 activation during thymocyte apoptosis. EMBO J. 17 (1998) 7209-7218
37. Grassilli E., Benatti F., Dansi P., Giammarioli A.M., Malorni W., Franceschi C., and Desiderio M.A. Inhibition of proteasome function prevents thymocyte apoptosis: involvement of ornithine decarboxylase. Biochem. Biophys. Res. Commun. 250 (1998) 293-297
38. Sun L., Trausch-Azar J.S., Muglia L.J., and Schwartz A.L. Glucocorticoids differentially regulate degradation of MyoD and Id1 by N-terminal ubiquitination to promote muscle protein catabolism. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 3339-3344
39. Tanaka K., Pracyk J.B., Takeda K., Yu Z.X., Ferrans V.J., Deshpande S.S., Ozaki M., Hwang P.M., Lowenstein C.J., Irani K., and Finkel T. Expression of Id1 results in apoptosis of cardiac myocytes through a redox-dependent mechanism. J. Biol. Chem. 273 (1998) 25922-25928
40. Siu P.M., and Alway S.E. Id2 and p53 participate in apoptosis during unloading-induced muscle atrophy. Am. J. Physiol. Cell Physiol. 288 (2005) C1058-1073
41. Jen Y., Weintraub H., and Benezra R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev. 6 (1992) 1466-1479
42. Sun L., Trausch-Azar J.S., Ciechanover A., and Schwartz A.L. Ubiquitin-proteasome-mediated degradation, intracellular localization, and protein synthesis of MyoD and Id1 during muscle differentiation. J. Biol. Chem. 280 (2005) 26448-26456
43. Schakman O., Gilson H., de Coninck V., Lause P., Verniers J., Havaux X., Ketelslegers J.M., and Thissen J.P. Insulin-like growth factor-I gene transfer by electroporation prevents skeletal muscle atrophy in glucocorticoid-treated rats. Endocrinology 146 (2005) 1789-1797
44. Fournier M., Huang Z.S., Li H., Da X., Cercek B., and Lewis M.I. Insulin-like growth factor I prevents corticosteroid-induced diaphragm muscle atrophy in emphysematous hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 (2003) R34-43
45. Tomas F.M. The anti-catabolic efficacy of insulin-like growth factor-I is enhanced by its early administration to rats receiving dexamethasone. J. Endocrinol. 157 (1998) 89-97
46. Bark T.H., McNurlan M.A., Lang C.H., and Garlick P.J. Increased protein synthesis after acute IGF-I or insulin infusion is localized to muscle in mice. Am. J. Physiol. 275 (1998) E118-123
47. Musaro A., Giacinti C., Borsellino G., Dobrowolny G., Pelosi L., Cairns L., Ottolenghi S., Cossu G., Bernardi G., Battistini L., Molinaro M., and Rosenthal N. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 1206-1210
48. Franke T.F., Kaplan D.R., and Cantley L.C. PI3K: downstream AKTion blocks apoptosis. Cell 88 (1997) 435-437
49. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., and Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 282 (1998) 1318-1321
50. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., and Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999) 857-868
51. Buren J., Lai Y.C., Lundgren M., Eriksson J.W., and Jensen J. Insulin action and signalling in fat and muscle from dexamethasone-treated rats. Arch. Biochem. Biophys. (2008)
52. Saad M.J., Folli F., Kahn J.A., and Kahn C.R. Modulation of insulin receptor, insulin receptor substrate-1, and phosphatidylinositol 3-kinase in liver and muscle of dexamethasone-treated rats. J. Clin. Invest. 92 (1993) 2065-2072
53. Holland W.L., Brozinick J.T., Wang L.P., Hawkins E.D., Sargent K.M., Liu Y., Narra K., Hoehn K.L., Knotts T.A., Siesky A., Nelson D.H., Karathanasis S.K., Fontenot G.K., Birnbaum M.J., and Summers S.A. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab. 5 (2007) 167-179
54. Straczkowski M., Kowalska I., Nikolajuk A., Dzienis-Straczkowska S., Kinalska I., Baranowski M., Zendzian-Piotrowska M., Brzezinska Z., and Gorski J. Relationship between insulin sensitivity and sphingomyelin signaling pathway in human skeletal muscle. Diabetes 53 (2004) 1215-1221
55. Chavez J.A., Knotts T.A., Wang L.P., Li G., Dobrowsky R.T., Florant G.L., and Summers S.A. A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids. J. Biol. Chem. 278 (2003) 10297-10303
56. Chavez J.A., and Summers S.A. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch. Biochem. Biophys. 419 (2003) 101-109
57. Baron A.D., Brechtel G., Wallace P., and Edelman S.V. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am. J. Physiol. 255 (1988) E769-774
58. Strle K., Broussard S.R., McCusker R.H., Shen W.H., Johnson R.W., Freund G.G., Dantzer R., and Kelley K.W. Proinflammatory cytokine impairment of insulin-like growth factor I-induced protein synthesis in skeletal muscle myoblasts requires ceramide. Endocrinology 145 (2004) 4592-4602
59. Hyde R., Hajduch E., Powell D.J., Taylor P.M., and Hundal H.S. Ceramide down-regulates System A amino acid transport and protein synthesis in rat skeletal muscle cells. FASEB J. 19 (2005) 461-463
60. Phillips D.C., Hunt J.T., Moneypenny C.G., Maclean K.H., McKenzie P.P., Harris L.C., and Houghton J.A. Ceramide-induced G2 arrest in rhabdomyosarcoma (RMS) cells requires p21Cip1/Waf1 induction and is prevented by MDM2 overexpression. Cell Death Differ. 14 (2007) 1780-1791
61. Calatayud C.A., Pasquini L.A., Pasquini J.M., and Soto E.F. Involvement of the ubiquitin-mediated proteolytic system in the signaling pathway induced by ceramide in primary astrocyte cultures. Dev. Neurosci. 27 (2005) 397-407
62. Turpin S.M., Lancaster G.I., Darby I., Febbraio M.A., and Watt M.J. Apoptosis in skeletal muscle myotubes is induced by ceramides and is positively related to insulin resistance. Am. J. Physiol. Endocrinol. Metab. 291 (2006) E1341-1350
63. Novelli M., Pocai A., Chiellini C., Maffei M., and Masiello P. Free fatty acids as mediators of adaptive compensatory responses to insulin resistance in dexamethasone-treated rats. Diab. Metab. Res. Rev. 24 (2008) 155-164
64. Mitsui T., Azuma H., Nagasawa M., Iuchi T., Akaike M., Odomi M., and Matsumoto T. Chronic corticosteroid administration causes mitochondrial dysfunction in skeletal muscle. J. Neurol. 249 (2002) 1004-1009
65. Yu J., Novgorodov S.A., Chudakova D., Zhu H., Bielawska A., Bielawski J., Obeid L.M., Kindy M.S., and Gudz T.I. JNK3 signaling pathway activates ceramide synthase leading to mitochondrial dysfunction. J. Biol. Chem. (2007)
66. Marolda M., Palma V., Camporeale F.S., Carandente M., Cioffi M., Orsini A.V., and Gentile A. Steroid myopathy: clinical and immunohistochemical study of a case. Ital. J. Neurol. Sci. 12 (1991) 409-413
67. Du J., Wang X., Miereles C., Bailey J.L., Debigare R., Zheng B., Price S.R., and Mitch W.E. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J. Clin. Invest. 113 (2004) 115-123