Regulation of Akt-mTOR, ubiquitin-proteasome and autophagy-lysosome pathways in response to formoterol administration in rat skeletal muscle

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 11, 2013, Pages 2444-2455

  Joassard, Olivier Roger ^a   Amirouche, Adel ^a   Gallot, Yann Simon ^a   Desgeorges, Marine Maud ^a   Castells, Josiane ^a   Durieux, Anne Cécile ^a   Berthon, Phanélie ^b   Freyssenet, Damien Gilles ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ DE SAVOIE   (France)

Author keywords

2 agonist; Akt mTOR pathway; Autophagy; Hypertrophy; MAFbx atrogin 1; Ubiquitin proteasome

Indexed keywords

ATROGIN 1; AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 13; AUTOPHAGY PROTEIN 5; CATHEPSIN B; CATHEPSIN L; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORMOTEROL; GAMMA AMINOBUTYRIC ACID RECEPTOR ASSOCIATED PROTEIN LIKE 1; INITIATION FACTOR 3; INITIATION FACTOR 4E BINDING PROTEIN 1; LIGHT CHAIN 3 BETA; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCLE RING FINGER 1 PROTEIN; MYOD PROTEIN; MYOSTATIN; PROTEASOME; PROTEIN; PROTEIN BCL 2; PROTEIN BNIP3; PROTEIN KINASE B; PROTEIN P62; PROTEIN S6; TRANSCRIPTION FACTOR EB; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN; UNC 51 LIKE KINASE1; UNCLASSIFIED DRUG; BETA 2 ADRENERGIC RECEPTOR; ETHANOLAMINE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOSERINE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; GASTROCNEMIUS MUSCLE; LIGHT CHAIN; LYSOSOME; MALE; MASS; MUSCLE HYPERTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE; TREATMENT DURATION; TREATMENT RESPONSE; ANIMAL; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYPERTROPHY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; WISTAR RAT;

EUKARYOTA; RATTUS;

ANIMALS; AUTOPHAGY; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ETHANOLAMINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HYPERTROPHY; LYSOSOMES; MALE; MUSCLE, SKELETAL; PHOSPHORYLATION; PHOSPHOSERINE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA-2; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UBIQUITIN;

EID: 84883497000     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.07.019     Document Type: Article

References (71)

1. T. Abo, R.H. Iida, S. Kaneko, T. Suga, H. Yamada, and Y. Hamada IGF and myostatin pathways are respectively induced during the earlier and the later stages of skeletal muscle hypertrophy induced by clenbuterol, a beta(2)-adrenergic agonist Cell Biochemistry and Function 2012
2. E.T. Agbenyega, and A.C. Wareham Effect of clenbuterol on skeletal muscle atrophy in mice induced by the glucocorticoid dexamethasone Comparative Biochemistry and Physiology Part A: Physiology 102 1992 141 145
3. J.Y. Altarejos, and M. Montminy CREB and the CRTC co-activators: sensors for hormonal and metabolic signals Nature Reviews Molecular Cell Biology 12 2011 141 151
4. A. Amirouche, A.C. Durieux, S. Banzet, N. Koulmann, R. Bonnefoy, and C. Mouret Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle Endocrinology 150 2009 286 294
5. A.M. Baviera, N.M. Zanon, L.C. Navegantes, and I.C. Kettelhut Involvement of cAMP/Epac/PI3K-dependent pathway in the antiproteolytic effect of epinephrine on rat skeletal muscle Molecular Cell Endocrinology 315 2010 104 112
6. F. Beitzel, P. Gregorevic, J.G. Ryall, D.R. Plant, M.N. Sillence, and G.S. Lynch Beta2-adrenoceptor agonist fenoterol enhances functional repair of regenerating rat skeletal muscle after injury Journal of Applied Physiology 96 2004 1385 1392 (Pubitemid 38392675)
7. R. Berdeaux, N. Goebel, L. Banaszynski, H. Takemori, T. Wandless, and G.D. Shelton SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes Nature Medicine 13 2007 597 603 (Pubitemid 46828484)
8. P. Berthon, S. Duguez, F.B. Favier, A. Amirouche, L. Feasson, and L. Vico Regulation of ubiquitin-proteasome system, caspase enzyme activities, and extracellular proteinases in rat soleus muscle in response to unloading Pflugers Archiv 454 2007 625 633 (Pubitemid 46872895)
9. S.C. Bodine, E. Latres, S. Baumhueter, V.K. Lai, L. Nunez, and B.A. Clarke Identification of ubiquitin ligases required for skeletal muscle atrophy Science 294 2001 1704 1708 (Pubitemid 33104839)
10. S.C. Bodine, T.N. Stitt, M. Gonzalez, W.O. Kline, G.L. Stover, and R. Bauerlein Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo Nature Cell Biology 3 2001 1014 1019 (Pubitemid 34428747)
11. J.J. Brault, J.G. Jespersen, and A.L. Goldberg Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy Journal of Biological Chemistry 285 2010 19460 19471
12. E.O. Brennesvik, C. Ktori, J. Ruzzin, E. Jebens, P.R. Shepherd, and J. Jensen Adrenaline potentiates insulin-stimulated PKB activation via cAMP and Epac: implications for cross talk between insulin and adrenaline Cellular Signalling 17 2005 1551 1559 (Pubitemid 41253994)
13. V.A. Bricout, B.D. Serrurier, and A.X. Bigard Clenbuterol treatment affects myosin heavy chain isoforms and MyoD content similarly in intact and regenerated soleus muscles Acta Physiologica Scandinavica 180 2004 271 280 (Pubitemid 38299638)
14. S. Busquets, M.T. Figueras, G. Fuster, V. Almendro, R. Moore-Carrasco, and E. Ametller Anticachectic effects of formoterol: a drug for potential treatment of muscle wasting Cancer Research 64 2004 6725 6731 (Pubitemid 39297935)
15. M. Cazzola, D. Spina, and M.G. Matera The use of bronchodilators in stable chronic obstructive pulmonary disease Pulmonary Pharmacology and Therapeutics 10 1997 129 144 (Pubitemid 29094856)
16. A.E. Chen, D.D. Ginty, and C.M. Fan Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins Nature 433 2005 317 322
17. B.A. Clarke, D. Drujan, M.S. Willis, L.O. Murphy, R.A. Corpina, and E. Burova The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle Cell Metabolism 6 2007 376 385 (Pubitemid 350011998)
18. S. Cohen, J.J. Brault, S.P. Gygi, D.J. Glass, D.M. Valenzuela, and C. Gartner During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation Journal of Cell Biology 185 2009 1083 1095
19. Y. Daaka, L.M. Luttrell, and R.J. Lefkowitz Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A Nature 390 1997 88 91 (Pubitemid 27494762)
20. J. de Rooij, F.J. Zwartkruis, M.H. Verheijen, R.H. Cool, S.M. Nijman, and A. Wittinghofer Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP Nature 396 1998 474 477 (Pubitemid 28553318)
21. A.C. Durieux, A. Amirouche, S. Banzet, N. Koulmann, R. Bonnefoy, and M. Pasdeloup Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression Endocrinology 148 2007 3140 3147 (Pubitemid 46996985)
22. P.W. Emery, N.J. Rothwell, M.J. Stock, and P.D. Winter Chronic effects of beta 2-adrenergic agonists on body composition and protein synthesis in the rat Bioscience Reports 4 1984 83 91 (Pubitemid 14143396)
23. J.M. Enserink, A.E. Christensen, J. de Rooij, M. van Triest, F. Schwede, and H.G. Genieser A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK Nature Cell Biology 4 2002 901 906 (Pubitemid 35331366)
24. J. Fielitz, M.S. Kim, J.M. Shelton, S. Latif, J.A. Spencer, and D.J. Glass Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3 Journal of Clinical Investigation 117 2007 2486 2495 (Pubitemid 47494350)
25. S.M. Gehrig, R. Koopman, T. Naim, C. Tjoakarfa, and G.S. Lynch Making fast-twitch dystrophic muscles bigger protects them from contraction injury and attenuates the dystrophic pathology American Journal of Pathology 176 2010 29 33
26. T. Geng, P. Li, X. Yin, and Z. Yan PGC-1alpha promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice American Journal of Pathology 178 2011 1738 1748
27. H. Gilson, O. Schakman, S. Kalista, P. Lause, K. Tsuchida, and J.P. Thissen Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin American Journal of Physiology Endocrinology and Metabolism 297 2009 E157 E164
28. C. Handschin, J. Rhee, J. Lin, P.T. Tarr, and B.M. Spiegelman An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle Proceedings of the National Academy of Sciences of the United States of America 100 2003 7111 7116 (Pubitemid 36706401)
29. L.S. Harrington, G.M. Findlay, A. Gray, T. Tolkacheva, S. Wigfield, and H. Rebholz The TSC1-2 tumor suppressor controls insulin-PI3 K signaling via regulation of IRS proteins Journal of Cell Biology 166 2004 213 223 (Pubitemid 38988774)
30. W.P. Hausdorff, M. Bouvier, B.F. O'Dowd, G.P. Irons, M.G. Caron, and R.J. Lefkowitz Phosphorylation sites on two domains of the beta 2-adrenergic receptor are involved in distinct pathways of receptor desensitization Journal of Biological Chemistry 264 1989 12657 12665 (Pubitemid 19191160)
31. S. Iezzi, M. Di Padova, C. Serra, G. Caretti, C. Simone, and E. Maklan Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin Developmental Cell 6 2004 673 684 (Pubitemid 38579351)
32. O.R. Joassard, A.C. Durieux, and D.G. Freyssenet β2-adrenergic agonists and the treatment of skeletal muscle wasting disorders International Journal of Biochemistry and Cell Biology 2013 10.1016/j.biocel.2013.06.025
33. H. Kawasaki, G.M. Springett, N. Mochizuki, S. Toki, M. Nakaya, and M. Matsuda A family of cAMP-binding proteins that directly activate Rap1 Science 282 1998 2275 2279 (Pubitemid 29004080)
34. V. Kedar, H. McDonough, R. Arya, H.H. Li, H.A. Rockman, and C. Patterson Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I Proceedings of the National Academy of Sciences of the United States of America 101 2004 18135 18140 (Pubitemid 40054086)
35. W.O. Kline, F.J. Panaro, H. Yang, and S.C. Bodine Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol Journal of Applied Physiology 102 2007 740 747 (Pubitemid 46220906)
36. R. Koopman, S.M. Gehrig, B. Leger, J. Trieu, S. Walrand, and K.T. Murphy Cellular mechanisms underlying temporal changes in skeletal muscle protein synthesis and breakdown during chronic {beta}-adrenoceptor stimulation in mice Journal of Physiology 588 2010 4811 4823
37. J. Lagirand-Cantaloube, N. Offner, A. Csibi, M.P. Leibovitch, S. Batonnet-Pichon, and L.A. Tintignac The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy Embo Journal 27 2008 1266 1276 (Pubitemid 351574748)
38. S. Lokireddy, C. McFarlane, X. Ge, H. Zhang, S.K. Sze, and M. Sharma Myostatin induces degradation of sarcomeric proteins through a Smad3 signaling mechanism during skeletal muscle wasting Molecular Endocrinology 25 2011 1936 1949
39. P.A. MacLennan, and R.H. Edwards Effects of clenbuterol and propranolol on muscle mass, evidence that clenbuterol stimulates muscle beta-adrenoceptors to induce hypertrophy Biochemical Journal 264 1989 573 579 (Pubitemid 20024530)
40. C. Mammucari, G. Milan, V. Romanello, E. Masiero, R. Rudolf, and P. Del Piccolo FoxO3 controls autophagy in skeletal muscle in vivo Cell Metabolism 6 2007 458 471 (Pubitemid 350163055)
41. A.C. McPherron, A.M. Lawler, and S.J. Lee Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member Nature 387 1997 83 90 (Pubitemid 27202654)
42. H. Nakatogawa, Y. Ichimura, and Ohsumi Y. Atg8 a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion Cell 130 2007 165 178 (Pubitemid 47031316)
43. L.C. Navegantes, N.M. Resano, A.M. Baviera, R.H. Migliorini, and I.C. Kettelhut Effect of sympathetic denervation on the rate of protein synthesis in rat skeletal muscle American Journal of Physiology Endocrinology and Metabolism 286 2004 E642 E647
44. L.C. Navegantes, N.M. Resano, R.H. Migliorini, and I.C. Kettelhut Role of adrenoceptors and cAMP on the catecholamine-induced inhibition of proteolysis in rat skeletal muscle American Journal of Physiology Endocrinology and Metabolism 279 2000 E663 E668
45. L.C. Navegantes, N.M. Resano, R.H. Migliorini, and I.C. Kettelhut Catecholamines inhibit Ca(2+)-dependent proteolysis in rat skeletal muscle through beta(2)-adrenoceptors and cAMP American Journal of Physiology Endocrinology and Metabolism 281 2001 E449 E454
46. M.A. Pearen, S.A. Myers, S. Raichur, J.G. Ryall, G.S. Lynch, and G.E. Muscat The orphan nuclear receptor, NOR-1, a target of beta-adrenergic signaling, regulates gene expression that controls oxidative metabolism in skeletal muscle Endocrinology 149 2008 2853 2865 (Pubitemid 351724495)
47. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Research 29 2001 e45
48. C. Polge, A.E. Heng, M. Jarzaguet, S. Ventadour, A. Claustre, and L. Combaret Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1 Faseb Journal 25 2011 3790 3802
49. C. Rommel, S.C. Bodine, B.A. Clarke, R. Rossman, L. Nunez, and T.N. Stitt Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways Nature Cell Biology 3 2001 1009 1013 (Pubitemid 34428746)
50. N.J. Rothwell, M.J. Stock, and D.K. Sudera Changes in tissue blood flow and beta-receptor density of skeletal muscle in rats treated with the beta2-adrenoceptor agonist clenbuterol British Journal of Pharmacology 90 1987 601 607 (Pubitemid 17022608)
51. J.G. Ryall, P. Gregorevic, D.R. Plant, and M.N. Sillence Lynch GS. Beta 2-agonist fenoterol has greater effects on contractile function of rat skeletal muscles than clenbuterol American Journal of Physiology Regulatory Integrative and Comparative Physiology 283 2002 R1386 R1394
52. J.G. Ryall, D.R. Plant, P. Gregorevic, and M.N. Sillence Lynch GS. Beta 2-agonist administration reverses muscle wasting and improves muscle function in aged rats Journal of Physiology 555 2004 175 188 (Pubitemid 38313069)
53. J.G. Ryall, M.N. Sillence, and G.S. Lynch Systemic administration of beta2-adrenoceptor agonists, formoterol and salmeterol, elicit skeletal muscle hypertrophy in rats at micromolar doses British Journal of Pharmacology 147 2006 587 595
54. M. Sandri, J. Lin, C. Handschin, W. Yang, Z.P. Arany, and S.H. Lecker PGC-1{alpha} protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription Proceedings of the National Academy of Sciences of the United States of America 103 2006 16260 16265 (Pubitemid 44715184)
55. M. Sandri, C. Sandri, A. Gilbert, C. Skurk, E. Calabria, and A. Picard Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 117 2004 399 412 (Pubitemid 38534545)
56. A. Seibold, B. Williams, Z.F. Huang, J. Friedman, R.H. Moore, and B.J. Knoll Localization of the sites mediating desensitization of the beta(2)-adrenergic receptor by the GRK pathway Molecular Pharmacology 58 2000 1162 1173
57. S.K. Shenoy, M.T. Drake, C.D. Nelson, D.A. Houtz, K. Xiao, and S. Madabushi beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor Journal of Biological Chemistry 281 2006 1261 1273
58. H. Shi, C. Zeng, A. Ricome, K.M. Hannon, A.L. Grant, and D.E. Gerrard Extracellular signal-regulated kinase pathway is differentially involved in beta-agonist-induced hypertrophy in slow and fast muscles American Journal of Physiology Cell Physiology 292 2007 C1681 C1689
59. A.A. Sneddon, M.I. Delday, J. Steven, and C.A. Maltin Elevated IGF-II mRNA and phosphorylation of 4E-BP1 and p70(S6k) in muscle showing clenbuterol-induced anabolism American Journal of Physiology Endocrinology and Metabolism 281 2001 E676 E682
60. T.N. Stitt, D. Drujan, B.A. Clarke, F. Panaro, Y. Timofeyva, and W.O. Kline The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors Molecular Cell 14 2004 395 403 (Pubitemid 38591410)
61. Y. Suzuki, T. Shen, M. Poyard, M. Best-Belpomme, J. Hanoune, and N. Defer Expression of adenylyl cyclase mRNAs in the denervated and in the developing mouse skeletal muscle American Journal of Physiology 274 1998 C1674 C1685
62. L.A. Tintignac, J. Lagirand, S. Batonnet, V. Sirri, M.P. Leibovitch, and S.A. Leibovitch Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase Journal of Biological Chemistry 280 2005 2847 2856 (Pubitemid 40189393)
63. A. Tzatsos, and K.V. Kandror Nutrients suppress phosphatidylinositol 3-kinase/Akt signaling via raptor-dependent mTOR-mediated insulin receptor substrate 1 phosphorylation Molecular and Cellular Biology 26 2006 63 76
64. J.A. van Noord, J.J. Smeets, J.A. Raaijmakers, A.M. Bommer, and F.P. Maesen Salmeterol versus formoterol in patients with moderately severe asthma: onset and duration of action European Respiratory Journal 9 1996 1684 1688 (Pubitemid 26271155)
65. H. Weidberg, E. Shvets, T. Shpilka, F. Shimron, V. Shinder, and Z.L.C3 Elazar GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis Embo Journal 29 2010 1792 1802
66. T. Wenz, S.G. Rossi, R.L. Rotundo, B.M. Spiegelman, and C.T. Moraes Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging Proceedings of the National Academy of Sciences of the United States of America 106 2009 20405 20410
67. Z. Xie, U. Nair, and D.J. Klionsky Atg8 controls phagophore expansion during autophagosome formation Molecular Biology of the Cell 19 2008 3290 3298
68. T. Yimlamai, S.L. Dodd, S.E. Borst, and S. Park Clenbuterol induces muscle-specific attenuation of atrophy through effects on the ubiquitin-proteasome pathway Journal of Applied Physiology 99 2005 71 80 (Pubitemid 40934466)
69. R.J. Zeman, R. Ludemann, and J.D. Etlinger Clenbuterol, a beta 2-agonist, retards atrophy in denervated muscles American Journal of Physiology 252 1987 E152 E155
70. J. Zhao, J.J. Brault, A. Schild, P. Cao, M. Sandri, and S. Schiaffino FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells Cell Metabolism 6 2007 472 483 (Pubitemid 350163056)
71. W.Z. Zhu, M. Zheng, W.J. Koch, R.J. Lefkowitz, B.K. Kobilka, and R.P. Xiao Dual modulation of cell survival and cell death by beta(2)-adrenergic signaling in adult mouse cardiac myocytes Proceedings of the National Academy of Sciences of the United States of America 98 2001 1607 1612 (Pubitemid 32165546)