Skeletal muscle atrophy: Potential therapeutic agents and their mechanisms of action

Pharmacological Research

Volumn 99, Issue , 2015, Pages 86-100

  Dutt, Vikas ^a   Gupta, Sanjeev ^a   Dabur, Rajesh ^b   Injeti, Elisha ^c   Mittal, Ashwani ^a  

^a KURUKSHETRA UNIVERSITY   (India)

^b MAHARSHI DAYANAND UNIVERSITY   (India)

^c CEDARVILLE UNIVERSITY   (United States)

Author keywords

Anti cytokines; Atrophy; Cachexia; Cox2 inhibitor; Eicosapentaenoic acid; Histone decetylase inhibitor; Megestrol acetate; Phosphodiesterase inhibitor; Resveratrol; Adrenoceptor agonists

Indexed keywords

ANAMORELIN; AVR 118; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; BIMAGRUMAB; CELECOXIB; CILOMILAST; CLENBUTEROL; CYCLOOXYGENASE 2 INHIBITOR; ENOBOSARM; FORMOTEROL; FORMOTEROL PLUS MEGESTROL; GHRELIN; GLPG 0492; ICOSAPENTAENOIC ACID; IMMUNOMODULATING AGENT; MEGESTROL ACETATE; MELOXICAM; PENTOXIFYLLINE; PHOSPHODIESTERASE INHIBITOR; PLACEBO; RAMATERCEPT; RESVERATROL; ROLIPRAM; SELECTIVE ANDROGEN RECEPTOR MODULATOR; THALIDOMIDE; TORBAFYLLINE; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; BIOLOGICAL PRODUCT; CYTOKINE; ENZYME INHIBITOR; MUSCLE PROTEIN;

ANTIINFLAMMATORY ACTIVITY; ARTHRITIS; ARTICLE; CACHEXIA; CHRONIC KIDNEY DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; DRUG STRUCTURE; DUCHENNE MUSCULAR DYSTROPHY; HUMAN; INCLUSION BODY MYOSITIS; MUSCLE ATROPHY; MUSCLE DENERVATION; MUSCLE MASS; MUSCLE REGENERATION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SARCOPENIA; SEPSIS; SKELETAL MUSCLE; SPINAL CORD INJURY; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; MUSCULAR ATROPHY; PATHOLOGY;

ADRENERGIC BETA-AGONISTS; ANIMALS; BIOLOGICAL PRODUCTS; CYTOKINES; ENZYME INHIBITORS; HUMANS; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY;

EID: 84930944230     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.05.010     Document Type: Review

References (160)

1. D.J. Glass Skeletal muscle hypertrophy and atrophy signalling pathways Int. J. Biochem. Cell Biol. 37 2005 1974 1984
2. E.E. Dupont-Versteegden Apoptosis in muscle atrophy: relevance to sarcopenia Exp. Gerontol. 40 2005 473 481
3. P. Zhang, X. Chen, and M. Fan Signaling mechanisms involved in disuse muscle atrophy Med. Hypotheses 69 2007 310 321
4. A.J. Murton, D. Constantin, and P.L. Greenhaff The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and trophy Biochim. Biophys. Acta 1782 2008 730 743
5. J.J. McCarthy, K.A. Esser, C.A. Peterson, and E.E. Dupont-Versteegden Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy Physiol. Genomics 39 2009 219 226
6. A. Kumar, S. Bhatnagar, and P.K. Paul TWEAK and TRAF6 regulate skeletal muscle atrophy Curr. Opin. Clin. Nutr. Metab. Care 15 2012 233 239
7. A. Mittal, S. Bhatnagar, A. Kumar, E. Lach-Trifilieff, S. Wauters, H. Li, D.Y. Makonchuk, D.J. Glass, and A. Kumar The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice J. Cell Biol. 188 2010 833 849
8. H. Li, S. Malhotra, and A. Kumar Nuclear factor-kappa B signaling in skeletal muscle atrophy J. Mol. Med. (Berl.) 86 2008 1113 1126
9. M. Llovera, N. Carbó, J. López-Soriano, C. García-Martínez, S. Busquets, B. Alvarez, N. Agell, P. Costelli, F.J. Lopez-Soriano, A. Celada, and J.M. Argiles Different cytokines modulate ubiquitin gene expression in rat skeletal muscle Cancer Lett. 133 1 1998 83 87
10. R.A. Frost, and C.H. Lang Protein kinase B/Akt: a nexus of growth factor and cytokine signalling in determining muscle mass J. Appl. Physiol. 103 2007 378 387
11. A. Bonetto, F. Penna, M. Muscaritoli, V.G. Minero, F. Rossi Fanelli, and F.M. Baccino Are antioxidants useful for treating skeletal muscle atrophy? Free Radic. Biol. Med. 47 2009 906 916
12. P. Bonaldo, and M. Sandri Cellular and molecular mechanisms of muscle atrophy Dis. Model. Mech. 6 2013 25 39
13. R. Joshi, N. Kadeer, S. Sheriff, L.A. Friend, J.H. James, and A. Balasubramaniam Phosphodiesterase (PDE) inhibitor torbafylline (HWA 448) attenuates burn-induced rat skeletal muscle proteolysis through the PDE4/cAMP/EPAC/PI3K/Akt pathway Mol. Cell Endocrinol. 393 2014 152 163
14. D.A. Goncalves, W.A. Silveira, E.C. Lira, F.A. Graça, S. Paula-Gomes, N.M. Zanon, I.C. Kettelhut, and L.C. Navegantes Clenbuterol suppresses proteasomal and lysosomal proteolysis and atrophy-related genes in denervated rat soleus muscles independently of Akt Am. J. Physiol. Endocrinol. Metab. 302 2012 E123 E133
15. S.K. Joshi, H.T. Kim, B.T. Feeley, and X. Liu Differential ubiquitin-proteasome and autophagy signaling following rotator cuff tears and suprascapular nerve injury J. Orthop. Res. 32 2014 138 144
16. E.M. Duncan, T.L. Muratore-Schroeder, R.G. Cook, B.A. Garcia, J. Shabanowitz, and D.F. Hunt Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation Cell 135 2008 284 294
17. H. Takahashi, K. Ishidoh, D. Muno, A. Ohwada, T. Nukiwa, E. Kominami, and S. Kira Cathepsin L activity is increased in alveolar macrophages and bronchoalveolar lavage fluid of smokers Am. Rev. Respir. Dis. 147 1993 1562 1568
18. R.B. Hunter, E. Stevenson, A. Koncarevic, H. Mitchell-Felton, D.A. Essig, and S.C. Kandarian Activation of an alternative NF-kappaB pathway in skeletal muscle during disuse atrophy FASEB J. 16 2002 529 538
19. J.N. Gordon, T.M. Trebble, R.D. Ellis, H.D. Duncan, T. Johns, and P.M. Goggin Thalidomide in the treatment of cancer cachexia: a randomised placebo controlled trial Gut 54 2005 540 545
20. L.G. Melstrom, K.A. Melstrom Jr., X.Z. Ding, and T.E. Adrian Mechanisms of skeletal muscle degradation and its therapy in cancer cachexia Histol. Histopathol. 22 2007 805 814
21. V.C. Vaughan, M. Sullivan-Gunn, E. Hinch, P. Martin, and P.A. Lewandowski Eicosapentaenoic acid and oxypurinol in the treatment of muscle wasting in a mouse model of cancer cachexia PLoS ONE 7 2012 e45900
22. I. Ronga, F. Gallucci, F. Riccardi, and G. Uomo Anorexia-cachexia syndrome in pancreatic cancer: recent advances and new pharmacological approach Adv. Med. Sci. 59 2014 1 6
23. C.R. Tan, P.M. Yaffee, L.H. Jamil, S.K. Lo, N. Nissen, and S.J. Pandol Pancreatic cancer cachexia: a review of mechanisms and therapeutics Front. Physiol. 5 2014 88
24. P. Magee, S. Pearson, and J. Allen The omega-3 fatty acid, eicosapentaenoic acid (EPA), prevents the damaging effects of tumour necrosis factor (TNF)-alpha during murine skeletal muscle cell differentiation Lipids Health Dis. 7 2008 24
25. Y. Liu, F. Chen, J. Odle, X. Lin, H. Zhu, H. Shi, Y. Hou, and J. Yin Fish oil increases muscle protein mass and modulates Akt/FOXO, TLR4, and NOD signaling in weanling piglets after lipopolysaccharide challenge J. Nutr. 143 2013 1331 1339
26. A.S. Whitehouse, H.J. Smith, J.L. Drake, and M.J. Tisdale Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid Cancer Res. 61 2001 3604 3609
27. M.J. Tisdale Pathogenesis of cancer cachexia J. Support Oncol. 1 2003 159 168
28. M.J. Tisdale The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting J. Support. Oncol. 3 2005 209 217
29. H.C. Olguin, and B.B. Olwin Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal Dev. Biol. 275 2004 375 388
30. E. Berardi, P. Aulino, I. Murfuni, A. Toschi, F. Padula, and B.M. Scicchitano Skeletal muscle is enriched in hematopoietic stem cells and not inflammatory cells in cachectic mice Neurol. Res. 30 2008 160 169
31. M. Tian, K.L. Kliewer, M.L. Asp, M.B. Stout, and M.A. Belury c9t11-Conjugated linoleic acid-rich oil fails to attenuate wasting in colon-26 tumor-induced late-stage cancer cachexia in male CD2F1 mice Mol. Nutr. Food Res. 55 2011 268 277
32. F. Penna, S. Busquets, F. Pin, M. Toledo, F.M. Baccino, F.J. López-Soriano, P. Costelli, and J.M. Argiles Combined approach to counteract experimental cancer cachexia: eicosapentaenoic acid and training exercise J. Cachexia Sarcopenia Muscle 2 2011 95 104
33. M. Li, Q. Zhu, C. Hu, J.P. Giesy, and Z. Kong Protective effects of eicosapentaenoic acid on genotoxicity and oxidative stress of cyclophosphamide in mice Environ. Toxicol. 26 2011 217 223
34. J. Khal, and M.J. Tisdale Downregulation of muscle protein degradation in sepsis by eicosapentaenoic acid (EPA) Biochem. Biophys. Res. Commun. 375 2008 238 240
35. J. Singh, N.K. Verma, S.M. Kansagra, B.N. Kate, and C.S. Dey Altered PPARgamma expression inhibits myogenic differentiation in C2C12 skeletal muscle cells Mol. Cell Biochem. 294 2007 163 171
36. A.F. Mauricio, E. Minatel, H.S. Neto, and M.J. Marques Effects of fish oil containing eicosapentaenoic acid and docosahexaenoic acid on dystrophic mdx mice Clin. Nutr. 32 2013 636 642
37. A. Jatoi, K. Rowland, C.L. Loprinzi, J.A. Sloan, S.R. Dakhil, N. MacDonald, B. Gagnon, P.J. Novotny, J.A. Mailliard, T.I. Bushey, S. Nair, B. Christensen, and North Central Cancer Treatment G An eicosapentaenoic acid supplement versus megestrol acetate versus both for patients with cancer-associated wasting: a North Central Cancer Treatment Group and National Cancer Institute of Canada collaborative effort J. Clin. Oncol. 22 2004 2469 2476
38. K.C. Fearon, M.D. Barber, A.G. Moses, S.H. Ahmedzai, G.S. Taylor, M.J. Tisdale, and G.D. Murray Double-blind, placebo-controlled, randomized study of eicosapentaenoic acid diester in patients with cancer cachexia J. Clin. Oncol. 24 2006 3401 3407
39. R.A. Murphy, E. Yeung, V.C. Mazurak, and M. Mourtzakis Influence of eicosapentaenoic acid supplementation on lean body mass in cancer cachexia Br. J. Cancer 105 2011 1469 1473
40. H.J. Smith, P. Mukerji, and M.J. Tisdale Attenuation of proteasome-induced proteolysis in skeletal muscle by {beta}-hydroxy-{beta}-methylbutyrate in cancer-induced muscle loss Cancer Res. 65 2005 277 283
41. H.L. Eley, S.T. Russell, J.H. Baxter, P. Mukerji, and M.J. Tisdale Signaling pathways initiated by beta-hydroxy-beta-methylbutyrate to attenuate the depression of protein synthesis in skeletal muscle in response to cachectic stimuli Am. J. Physiol. Endocrinol. Metab. 293 2007 E923 E931
42. K.K. Noh, K.W. Chung, Y.J. Choi, M.H. Park, E.J. Jang, C.H. Park, C. Yoon, N.D. Kim, M.K. Kim, and H.Y. Chung β-Hydroxy β-methylbutyrate improves dexamethasone-induced muscle atrophy by modulating the muscle degradation pathway in SD rat PLoS ONE 9 2014 e102947
43. A. Rahman, K. Wilund, P.J. Fitschen, K. Jeejeebhoy, R. Agarwala, and J.W. Drover Elderly persons with ICU-acquired weakness: the potential role for β-hydroxy-β-methylbutyrate (HMB) supplementation? J. Parenter. Enteral Nutr. 38 2013 567 575
44. P.E. May, A. Barber, J.T. D'Olimpio, A. Hourihane, and N.N. Abumrad Reversal of cancer-related wasting using oral supplementation with a combination of beta-hydroxy-beta-methylbutyrate, arginine, and glutamine Am. J. Surg. 183 2002 471 479
45. M.D. Girón, J.D. Vílchez, S. Shreeram, R. Salto, M. Manzano, and E. Cabrera β-Hydroxy-β-methylbutyrate (HMB) normalizes dexamethasone-induced autophagy-lysosomal pathway in skeletal muscle PLoS ONE 10 2015 e011752
46. S.E. Alway, S.L. Pereira, N.K. Edens, Y. Hao, and B.T. Bennett β-Hydroxy-β-methylbutyrate (HMB) enhances the proliferation of satellite cells in fast muscles of aged rats during recovery from disuse atrophy Exp. Gerontol. 48 2013 973 984
47. T.K. Sin, B.Y. Yung, and P.M. Siu Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance Cell Physiol. Biochem. 35 2015 541 552
48. N. Alamdari, Z. Aversa, E. Castillero, A. Gurav, V. Petkova, and S. Tizio Resveratrol prevents dexamethasone-induced expression of the muscle atrophy-related ubiquitin ligases atrogin-1 and MuRF1 in cultured myotubes through a SIRT1-dependent mechanism Biochem. Biophys. Res. Commun. 417 2012 528 533
49. D.T. Wang, Y. Yin, Y.J. Yang, P.J. Lv, Y. Shi, L. Lu, and L.B. Wei Resveratrol prevents TNF-α-induced muscle atrophy via regulation of Akt/mTOR/FoxO1 signaling in C2C12 myotubes Int. Immunopharmacol. 19 2014 206 213
50. S. Busquets, G. Fuste, E. Ametller, M. Olivan, M. Figueras, and P. Costelli Resveratrol does not ameliorate muscle wasting in different types of cancer cachexia models Clin. Nutr. 26 2007 239 244
51. L.D. Williams, G.A. Burdock, J.A. Edwards, M. Beck, and J. Bausch Safety studies conducted on high-purity trans-resveratrol in experimental animals Food Chem. Toxicol. 47 2009 2170 2182
52. K.H. Chen, M.L. Cheng, Y.H. Jing, D.T. Chiu, M.S. Shiao, and J.K. Chen Resveratrol ameliorates metabolic disorders and muscle wasting in streptozotocin-induced diabetic rats Am. J. Physiol. Endocrinol. Metab. 301 2011 E853 E863
53. I. Momken, L. Stevens, A. Bergouignan, D. Desplanches, F. Rudwill, and I. Chery Resveratrol prevents the wasting disorders of mechanical unloading by acting as a physical exercise mimetic in the rat FASEB J. 25 2011 3646 3660
54. S.M. Wyke, S.T. Russell, and M.J. Tisdale Induction of proteasome expression in skeletal muscle is attenuated by inhibitors of NF-kappaB activation Br. J. Cancer 91 2004 1742 1750
55. S. Shadfar, M.E. Couch, K.A. McKinney, L.J. Weinstein, X. Yin, and J.E. Rodríguez Oral resveratrol therapy inhibits cancer-induced skeletal muscle and cardiac atrophy in vivo Nutr. Cancer 63 2011 749 762
56. Y. Qi, J.Y. Shang, L.J. Ma, B.B. Sun, X.G. Hu, and B. Liu Inhibition of AMPK expression in skeletal muscle by systemic inflammation in COPD rats Respir. Res. 15 2014 156
57. D.J. Boocock, G.E. Faust, K.R. Pate, A.M. Schinas, V.A. Brown, and M.P. Ducharme Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent Cancer Epidemiol. Biomarkers Prev. 16 2007 1246 1252
58. F. Visioli The resveratrol fiasco Pharmacol. Res. 90 2014 87
59. N. Nagaya, T. Itoh, S. Murakami, H. Oya, M. Uematsu, and K. Miyatake Treatment of cachexia with ghrelin in patients with COPD Chest 128 2005 1187 1193
60. R. Barazzoni, X. Zhu, M. Deboer, R. Datta, M.D. Culler, and M. Zanetti Combined effects of ghrelin and higher food intake enhance skeletal muscle mitochondrial oxidative capacity and AKT phosphorylation in rats with chronic kidney disease Kidney Int. 77 2010 23 28
61. M. Nakazato, N. Murakami, and Y. Date A role for ghrelin in the central regulation of feeding Nature 409 2001 194 198
62. S. Reano, A. Graziani, and N. Filigheddu Acylated and unacylated ghrelin administration to blunt muscle wasting Curr. Opin. Clin. Nutr. Metab. Care 17 2014 236 240
63. S. Sheriff, N. Kadeer, R. Joshi, L.A. Friend, J.H. James, and A. Balasubramaniam Des-acyl ghrelin exhibits pro-anabolic and anti-catabolic effects on C2C12 myotubes exposed to cytokines and reduces burn-induced muscle proteolysis in rats Mol. Cell Endocrinol. 351 2012 286 295
64. H. Tsubouchi, S. Yanagi, A. Miura, N. Matsumoto, K. Kangawa, and M. Nakazato Ghrelin relieves cancer cachexia associated with the development of lung adenocarcinoma in mice Eur. J. Pharmacol. 743 2014 1 10
65. N. Nagaya, J. Moriya, Y. Yasumura, M. Uematsu, F. Ono, and W. Shimizu Effects of ghrelin administration on left ventricular function, exercise capacity, and muscle wasting in patients with chronic heart failure Circulation 110 2004 3674 3679
66. K. Koshinaka, K. Toshinai, A. Mohammad, K. Noma, M. Oshikawa, and H. Ueno Therapeutic potential of ghrelin treatment for unloading-induced muscle atrophy in mice Biochem. Biophys. Res. Commun. 412 2011 296 301
67. F. Strasser, T.A. Lutz, and M.T. Maeder Safety, tolerability and pharmacokinetics of intravenous ghrelin for cancer-related anorexia/cachexia: a randomised, placebo-controlled, doubleblind, double-crossover study Br. J. Cancer 98 2008 300 308
68. T. Akamizu, K. Takaya, and T. Irako Pharmacokinetics, safety, and endocrine and appetite effects of ghrelin administration in young healthy subjects Eur. J. Endocrinol. 150 2004 447 455
69. J.M. Garcia, J. Friend, and S. Allen Therapeutic potential of anamorelin, a novel, oral ghrelin mimetic, in patients with cancer-related cachexia: a multicenter, randomized, double-blind, crossover, pilot study Support. Care Cancer 21 2013 129 137
70. C. Pietra, Y. Takeda, N. Tazawa-Ogata, M. Minami, X. Yuanfeng, E.M. Duus, and R. Northrup Anamorelin HCl (ONO-7643), a novel ghrelin receptor agonist, for the treatment of cancer anorexia-cachexia syndrome: preclinical profile J. Cachexia Sarcopenia Muscle 5 2014 329 337
71. D.C. Currow, and A.P. Abernethy Anamorelin hydrochloride in the treatment of cancer anorexia-cachexia syndrome Future Oncol. 10 2014 789 802
72. B.A. Bondesen, S.T. Mills, K.M. Kegley, and G.K. Pavlath The COX-2 pathway is essential during early stages of skeletal muscle regeneration Am. J. Physiol. Cell Physiol. 287 2004 C475 C483
73. T.W. Davis, B.S. Zweifel, J.M. O'Neal, D.M. Heuvelman, A.L. Abegg, and T.O. Hendrich Inhibition of cyclooxygenase-2 by celecoxib reverses tumor-induced wasting J. Pharmacol. Exp. Ther. 308 2004 929 934
74. A.J. Baumgarten, H.H. Fiebig, and A.M. Burger Molecular analysis of xenograft models of human cancer cachexia - possibilities for therapeutic intervention Cancer Genomics Proteomics 4 2007 223 231
75. A.I. Martin, M.P. Nieto-Bona, E. Castillero, C. Fernandez-Galaz, M. Lopez-Menduina, and A.B. Gomez-Sanmiguel Effect of cyclooxygenase-2 inhibition by meloxicam, on atrogin-1 and myogenic regulatory factors in skeletal muscle of rats injected with endotoxin J. Physiol. Pharmacol. 63 2012 649 659
76. G. Mantovani, A. Macció, C. Madeddu, R. Serpe, G. Antoni, and E. Massa Phase II nonrandomized study of the efficacy and safety of COX-2 inhibitor celecoxib on patients with cancer cachexia J. Mol. Med. 88 2010 85 92
77. H.J. Hussey, and M.J. Tisdale Effect of the specific cyclooxygenase-2 inhibitor meloxicam on tumour growth and cachexia in a murine model Int. J. Cancer 87 2000 95 100
78. V. Lai, J. George, L. Richey, H.J. Kim, T. Cannon, C. Shores, and M. Couch Results of a pilot study of the effects of celecoxib on cancer cachexia in patients with cancer of the head, neck, and gastrointestinal tract Head Neck 30 2008 67 74
79. F.I. Romero, M.J. Martínez-Calatrava, O. Sánchez-Pernaute, O. Gualillo, R. Largo, and G. Herrero-Beaumont Pharmacological modulation by celecoxib of cachexia associated with experimental arthritis and atherosclerosis in rabbits Br. J. Pharmacol. 161 2010 1012 1022
80. M. Granado, A.I. Martín, M.A. Villanúa, and A. López-Calderón Experimental arthritis inhibits the insulin-like growth factor-I axis and induces muscle wasting through cyclooxygenase-2 activation Am. J. Physiol. Endocrinol. Metab. 292 2007 E1656 E1665
81. S.M. Senf, P.B. Sandesara, S.A. Reed, and A.R. Judge p300 acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle Am. J. Physiol. Cell Physiol. 300 2011 C1490 C1501
82. A.W. Beharry, P.B. Sandesara, B.M. Roberts, L.F. Ferreira, S.M. Senf, and A.R. Judge HDAC1 activates FoxO and is both sufficient and required for skeletal muscle atrophy J. Cell Sci. 127 Pt 7 2014 1441 1453
83. H. Tang, and D. Goldman Activity-dependent gene regulation in skeletal muscle is mediated by a histone deacetylase (HDAC)-Dach2-myogenin signal transduction cascade Proc. Natl. Acad. Sci. U. S. A. 103 2006 16977 16982
84. H. Tang, P. Macpherson, M. Marvin, E. Meadows, W.H. Klein, and X.J. Yang A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression Mol. Biol. Cell 20 2009 1120 1131
85. K.V. Bricceno, P.J. Sampognaro, J.P. Van Meerbeke, C.J. Sumner, H. Fischbeck, and B.G. Burnett Histone deacetylase inhibition suppresses myogenin-dependent atrogene activation in spinal muscular atrophy mice Hum. Mol. Genet. 21 2012 4448 4459
86. A.M. Avila, B.G. Burnett, A.A. Taye, F. Gabanella, M.A. Knight, and P. Hartenstein Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy J. Clin. Invest. 117 2007 659 671
87. A. Bonetto, F. Penna, V.G. Minero, P. Reffo, G. Bonelli, and F.M. Baccino Deacetylase inhibitors modulate the myostatin/follistatin axis without improving cachexia in tumor-bearing mice Curr. Cancer Drug Targets 9 2009 608 616
88. M.E. Benny Klimek, T. Aydogdu, M.J. Link, M. Pons, L.G. Koniaris, and T.A. Zimmers Acute inhibition of myostatin-family proteins preserves skeletal muscle in mouse models of cancer cachexia Biochem. Biophys. Res. Commun. 391 2010 1548 1554
89. G.C. Minetti, C. Colussi, R. Adami, C. Serra, C. Mozzetta, and V. Parente Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors Nat. Med. 12 2006 1147 1150
90. C. Colussi, C. Mozzetta, A. Gurtner, B. Illi, J. Rosati, and C. Gaetano HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment Proc. Natl. Acad. Sci. U. S. A. 105 2008 19183 19187
91. C. Colussi, A. Gurtner, J. Rosati, B. Illi, G. Ragone, and C. Gaetano Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy FASEB J. 23 2009 2131 2141
92. L. Combaret, T. Tilignac, A. Claustre, L. Voisin, D. Taillandier, and C. Obled Torbafylline (HWA 448) inhibits enhanced skeletal muscle ubiquitin-proteasome-dependent proteolysis in cancer and septic rats Biochem. J. 361 2002 185 192
93. F.C. Mei, J. Qiao, O.M. Tsygankova, J.L. Meinkoth, L.A. Quilliam, and X. Cheng Differential signalling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation J. Biol. Chem. 277 2002 11497 11504
94. 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 Cell Signal. 17 2005 1551 1559
95. S. Gerlo, P. Verdood, and R. Kooijman Modulation of cytokine production by cyclic adenosine monophosphate analogs in human leukocytes J. Interferon Cytokine Res. 30 2010 883 891
96. M. Metrich, M. Berthouze, E. Morel, B. Crozatier, A.M. Gomez, and F. Lezoualc'h Role of the cAMP-binding protein Epac in cardiovascular physiology and pathophysiology Pflugers Arch. 459 2010 535 546
97. D. Breuillé, M.C. Farge, F. Rose, M. Arnal, D. Attaix, and C. Obled Pentoxifylline decreases body weight loss and muscle protein wasting characteristics of sepsis Am. J. Physiol. 265 1993 E660 E666
98. 2+-dependent and ATP proteasome-dependent proteolysis in skeletal muscle from acutely diabetic rats Am. J. Physiol. Endocrinol. Metab. 292 2007 E702 E708
99. L. Combaret, C. Rallière, D. Taillandier, K. Tanaka, and D. Attaix Manipulation of the ubiquitin-proteasome pathway in cachexia: pentoxifylline suppresses the activation of 20S and 26S proteasomes in muscles from tumor-bearing rats Mol. Biol. Rep. 26 1999 95 101
100. J. Semmler, U. Gebert, T. Eisenhut, J. Moeller, M.M. Schönharting, and A. Alléra Xanthine derivatives: comparison between suppression of tumour necrosis factor-alpha production and inhibition of cAMP phosphodiesterase activity Immunology 78 1993 520 525
101. C. Deval, S. Mordier, C. Obled, D. Bechet, L. Combaret, and D. Attaix Identification of cathepsin L as a differentially expressed message associated with skeletal muscle wasting Biochem. J. 360 2001 143 150
102. B.T. Steffen, S.J. Lees, and F.W. Booth Anti-TNF treatment reduces rat skeletal muscle wasting in monocrotaline-induced cardiac cachexia J. Appl. Physiol. 105 2008 1985 1950 1958
103. R.T. Hinkle, E. Dolan, D.B. Cody, M.B. Bauer, and R.J. Isfort Phosphodiesterase 4 inhibition reduces skeletal muscle atrophy Muscle Nerve 32 2005 775 781
104. D.A. Goncalves, E.C. Lira, A.M. Baviera, P. Cao, N.M. Zanon, and Z. Arany Mechanisms involved in 3′,5′-cyclic adenosine monophosphate-mediated inhibition of the ubiquitin-proteasome system in skeletal muscle Endocrinology 150 2009 5395 5404
105. J.D. Knight, and R. Kothary The myogenic kinome: protein kinases critical to mammalian skeletal myogenesis Skelet. Muscle 1 2011 29
106. R. Stewart, L. Flechner, M. Montminy, and R. Berdeaux CREB is activated by muscle injury and promotes muscle regeneration PLoS ONE 6 2011 e24714
107. J.G. Ryall, and G.S. Lynch The potential and the pitfalls of beta-adrenoceptor agonists for the management of skeletal muscle wasting Pharmacol. Ther. 120 2008 219 232
108. Y. Quanjun, Y. Genjin, W. Lili, L. Bin, L. Jin, and Y. Qi Serum metabolic profiles reveal the effect of formoterol on cachexia in tumor-bearing mice Mol. Biosyst. 9 2013 3015 3025
109. O.R. Joassard, A. Amirouche, Y.S. Gallot, M.M. Desgeorges, J. Castells, and A.C. Durieux Regulation of Akt-mTOR, ubiquitin-proteasome and autophagy-lysosome pathways in response to formoterol administration in rat skeletal muscle Int. J. Biochem. Cell Biol. 45 2013 2444 2455
110. M. Toledo, J. Springer, S. Busquets, A. Tschirner, F.J. López-Soriano, and S.D. Anker Formoterol in the treatment of experimental cancer cachexia: effects on heart function J. Cachexia Sarcopenia Muscle 5 2014 315 320
111. B. D'Agostino, M. Polverino, G. Cirino, A. Lombardi, B. Grassi, and N. Sullo Exercise capacity and cytochrome oxidase activity in muscle mitochondria of COPD patients Respir. Med. 104 2010 83 90
112. N. Sullo, F. Roviezzo, M. Matteis, G. Spaziano, S. Del Gaudio, and A. Lombardi Skeletal muscle oxidative metabolism in an animal model of pulmonary emphysema: formoterol and skeletal muscle dysfunction Am. J. Respir. Cell Mol. Biol. 48 2013 198 203
113. 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 Res. 64 2004 6725 6731
114. S. Busquets, M. Toledo, E. Marmonti, M. Orpí, E. Capdevila, and A. Betancourt Formoterol treatment downregulates the myostatin system in skeletal muscle of cachectic tumour-bearing rats Oncol. Lett. 3 2012 185 189
115. C.A. Steelman, J.C. Recknor, D. Nettleton, and J.M. Reecy Transcriptional profiling of myostatin-knockout mice implicates Wnt signaling in postnatal skeletal muscle growth and hypertrophy FASEB J. 20 2006 580 582
116. C. McFarlane, E. Plummer, and M. Thomas Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-κB-independent. FoxO1-dependent mechanism J. Cell Physiol. 209 2006 501 514
117. D. Joulia-Ekaza, and G. Cabello The myostatin gene: physiology and pharmacological relevance Curr. Opin. Pharmacol. 7 2007 310 315
118. L.R. Rodino-Klapac, A.M. Haidet, J. Kota, C. Handy, B.K. Kaspar, and J.R. Mendell Inhibition of myostatin with emphasis on follistatin as a therapy for muscle disease Muscle Nerve 39 2009 283 296
119. H. Amthor, G. Nicholas, I. McKinnell, C.F. Kemp, M. Sharma, and R. Kambadur Follistatin complexes myostatin and antagonises myostatin-mediated inhibition of myogenesis Dev. Biol. 270 2004 19 30
120. E. Ametller, S. Busquets, G. Fuster, M.T. Figueras, M. Olivan, and C.C.F. de Oliveira Formoterol may activate rat muscle regeneration during cancer cachexia Insci. J. 1 2011 1 17
121. S.R. Jesinkey, M.C. Korrapati, K.A. Rasbach, C.C. Beeson, and R.G. Schnellmann Atomoxetine prevents dexamethasone-induced skeletal muscle atrophy in mice J. Pharmacol. Exp. Ther. 351 2014 663 673
122. J.G. Ryall, J.D. Schertzer, and G.S. Lynch Attenuation of age-related muscle wasting and weakness in rats after formoterol treatment: therapeutic implications for sarcopenia J. Gerontol. A: Biol. Sci. Med. Sci. 62 2007 813 823
123. J.D. Ma, S.F. Heavey, C. Revta, and E.J. Roeland Novel investigational biologics for the treatment of cancer cachexia Expert Opin. Biol. Ther. 14 2014 1113 1120
124. M. Llovera, N. Carbó, C. García-Martínez, P. Costelli, L. Tessitore, and F.M. Baccino Anti-TNF treatment reverts increased muscle ubiquitin gene expression in tumour-bearing rats Biochem. Biophys. Res. Commun. 221 1996 653 655
125. M. Granado, A.I. Martín, T. Priego, A. López-Calderón, and M.A. Villanúa Tumour necrosis factor blockade did not prevent the increase of muscular muscle RING finger-1 and muscle atrophy F-box in arthritic rats J. Endocrinol. 191 2006 319 326
126. J.N. Gordon, and P.M. Goggin Thalidomide and its derivatives: emerging from the wilderness Postgrad. Med. J. 79 2003 127 132
127. S. Joglekar, and M. Levin The promise of thalidomide: evolving indications Drugs Today (Barc) 40 2004 197 204
128. I. Kedar, W. Mermershtain, and H. Ivgi Thalidomide reduces serum C-reactive protein and interleukin-6 and induces response to IL-2 in a fraction of metastatic renal cell cancer patients who failed IL-2-based therapy Int. J. Cancer 110 2004 260 265
129. M. Stroud Thalidomide and cancer cachexia: old problem, new hope? Gut 54 2005 447 448
130. M. Davis, W. Lasheen, D. Walsh, F. Mahmoud, L. Bicanovsky, and R. Lagman A Phase II dose titration study of thalidomide for cancer-associated anorexia J. Pain Symptom Manage. 43 2012 78 86
131. K.H. Liu, L.M. Liao, L.S. Ro, Y.L. Wu, and T.S. Yeh Thalidomide attenuates tumor growth and preserves fast-twitch skeletal muscle fibers in cholangiocarcinoma rats Surgery 143 2008 375 383
132. R. Sartori, P. Gregorevic, and M. Sandri TGFβ and BMP signaling in skeletal muscle: potential significance for muscle-related disease Trends Endocrinol. Metab. 25 2014 464 471
133. G. Kaplan, S. Thomas, D.S. Fierer, K. Mulligan, P.A. Haslett, and W.J. Fesse Thalidomide for the treatment of AIDS-associated wasting AIDS Res. Hum. Retroviruses 16 2000 1345 1355
134. J. Fujita, J.R. Mestre, J.B. Zeldis, K. Subbaramaiah, and A.J. Dannenberg Thalidomide and its analogues inhibit lipopolysaccharide-mediated Iinduction of cyclooxygenase-2 Clin. Cancer Res. 7 2001 3349 3355
135. S. Dodson, V.E. Baracos, A. Jatoi, W.J. Evans, D. Cella, and J.T. Dalton Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies Annu. Rev. Med. 62 2011 265 279
136. T. Thum, and J. Springer Breakthrough in cachexia treatment through a novel selective androgen receptor modulator J. Cachexia Sarcopenia Muscle 2 2011 121 123
137. J.T. Dalton, K.G. Barnette, C.E. Bohl, M.L. Hancock, D. Rodriguez, and S.T. Dodson The selective androgen receptor modulator GTx-024 (enobosarm) improves lean body mass and physical function in healthy elderly men and postmenopausal women: results of a double-blind, placebo-controlled phase II trial J. Cachexia Sarcopenia Muscle 2 2011 153 161
138. A.S. Dobs, R.V. Boccia, C.C. Croot, N.Y. Gabrail, J.T. Dalton, and M.L. Hancock Effects of enobosarm on muscle wasting and physical function in patients with cancer: a double-blind, randomised controlled phase 2 trial Lancet Oncol. 14 2013 335 345
139. R. Blanqué, L. Lepescheux, M. Auberval, D. Minet, D. Merciris, and C. Cottereaux Characterization of GLPG0492, a selective androgen receptor modulator, in a mouse model of hindlimb immobilization BMC Musculoskelet. Disord. 15 2014 291
140. A. Cozzoli, R.F. Capogrosso, V.T. Sblendorio, M.M. Dinardo, C. Jagerschmidt, and F. Namour GLPG0492, a novel selective androgen receptor modulator, improves muscle performance in the exercised-mdx mouse model of muscular dystrophy Pharmacol. Res. 72 2013 9 24
141. M. Chasen, S.Z. Hirschman, and R. Bhargava Phase II study of the novel peptide-nucleic acid OHR118 in the management of cancer-related anorexia/cachexia J. Am. Med. Dir. Assoc. 12 2011 62 67
142. ClinicalTrials.gov. Open label study with OHR/AVR118 in advanced cancer patients with anorexia-cachexia. http://clinicaltrials.gov/ct2/show/NCT01206335.
143. G. Mantovani, C. Madeddu, and A. Macciò Drugs in development for treatment of patients with cancer-related anorexia and cachexia syndrome Drug Des. Dev. Ther. 7 2013 645 656 (article has retracted)
144. ClinicalTrials.gov. Pilot Study of APD209 in Cancer Cachexia http://clinicaltrials.gov/show/NCT00895726.
145. X. Zhou, J.L. Wang, J. Lu, Y. Song, K.S. Kwak, and Q. Jiao Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival Cell 142 2010 531 543
146. T.A. Zimmers, M.V. Davies, L.G. Koniaris, P. Haynes, A.F. Esquela, and K.N. Tomkinson Induction of cachexia in mice by systemically administered myostatin Science 296 2002 1486 1488
147. K. Patel, and H. Amthor The function of myostatin and strategies of myostatin blockade-new hope for therapies aimed at promoting growth of skeletal muscle Neuromuscul. Disord. 15 2005 117 126
148. S. Roth, and S. Walsh Myostatin: a therapeutic target for skeletal muscle wasting Curr. Opin. Clin. Nutr. Metab. Care 7 2004 259 263
149. S. Bogdanovich, T.O. Krag, E.R. Barton, L.D. Morris, L.A. Whittemore, and R.S. Ahima Functional improvement of dystrophic muscle by myostatin blockade Nature 420 2002 418 421
150. https://clinicaltrials.gov/ct2/show/NCT02250443.
151. https://clinicaltrials.gov/ct2/show/NCT01963598.
152. C.L. Donohoe, A.M. Ryan, and J.V. Reynolds Cancer cachexia: mechanisms and clinical implications Gastroenterol. Res. Pract. 2011 2011 601434
153. O. Kanat, E. Cubukcu, N. Avci, F. Budak, I. Ercan, and M. Canhoroz Comparison of three different treatment modalities in the management of cancer cachexia Tumori 99 2013 229 233
154. A. Pascual López, M. Roqué i Figuls, G. Urrútia Cuchi, E.G. Berenstein, B. Almenar Pasies, and M. Balcells Alegre Systematic review of megestrol acetate in the treatment of anorexia-cachexia syndrome J. Pain Symptom Manage 27 2004 360 369
155. A. Laviano, A. Inui, D.L. Marks, M.M. Meguid, C. Pichard, and F. Rossi Fanelli Neural control of the anorexia-cachexia syndrome Am. J. Physiol. Endocrinol. Metab. 295 2008 E1000-1008
156. T. Martins, R. Vitorino, D. Moreira-Gonçalves, F. Amado, J.A. Duarte, and R. Ferreira Recent insights on the molecular mechanisms and therapeutic approaches for cardiac cachexia Clin. Biochem. 47 2014 8 15
157. H.D. McCarthy, R.E. Crowder, S. Dryden, and G. Williams Megestrol acetate stimulates food and water intake in the rat: effects on regional hypothalamic neuropeptide Y concentrations Eur. J. Pharmacol. 265 1994 99 102
158. G. Mantovani, A. Macciò, E. Massa, and C. Madeddu Managing cancer-related anorexia/cachexia Drugs 61 2001 499 514
159. S. Busquets, R. Serpe, S. Sirisi, M. Toledo, J. Coutinho, and R. Martínez Megestrol acetate: its impact on muscle protein metabolism supports its use in cancer cachexia Clin. Nutr. 29 2010 733 737
160. S.W. Jones, R.J. Hill, P.A. Krasney, B. O'Conner, N. Peirce, and P.L. Greenhaff Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass FASEB J. 18 2004 1025 1027