Molecular mechanisms and signaling pathways of angiotensin II-induced muscle wasting: Potential therapeutic targets for cardiac cachexia

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 10, 2013, Pages 2322-2332

  Yoshida, Tadashi ^a   Tabony, A Michael ^a   Galvez, Sarah ^a   Mitch, William E ^b   Higashi, Yusuke ^a   Sukhanov, Sergiy ^a   Delafontaine, Patrice ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Angiotensin II; Cachexia; Congestive heart failure; Skeletal muscle

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONIST; ATROGIN 1; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CAPTOPRIL; CORTICOTROPIN RELEASING FACTOR; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOCORTICOID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; MYOSTATIN; NEUROPEPTIDE Y; OREXIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; S6 KINASE; SERUM AMYLOID A; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN C; TRANSCRIPTION FACTOR FOXO; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3;

BODY WEIGHT; CACHEXIA; CELL DIFFERENTIATION; CELL ENERGY; CHRONIC KIDNEY DISEASE; CONGESTIVE HEART FAILURE; DECREASED APPETITE; DENERVATION; ENDOTHELIUM CELL; ENERGY BALANCE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FATTY ACID OXIDATION; FOOD INTAKE; GASTROCNEMIUS MUSCLE; HEART INFARCTION; HUMAN; HYPERTENSION; LATERAL HYPOTHALAMUS; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE HYPERTROPHY; MUSCLE REGENERATION; MUSCLE STRENGTH; MYOBLAST; MYOTUBE; NERVE CELL; NONHUMAN; OBESITY; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SKELETAL MUSCLE; VASCULAR SMOOTH MUSCLE; WEIGHT REDUCTION;

RODENTIA;

5-AMINOIMIDAZOLE-4-CARBOXAMIDE RIBONUCLEOTIDE; ACE; AGOUTI-RELATED PROTEIN; AGRP; AICAR; AMP-ACTIVATED KINASE; AMPK; ANG II; ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR; ANGIOTENSIN-CONVERTING ENZYME; AT1R; CACHEXIA; CHF; CONGESTIVE HEART FAILURE; CORTICOTROPIN-RELEASING HORMONE; CRH; END-STAGE RENAL DISEASE; ERK; ESRD; EXTRACELLULAR SIGNAL-REGULTED KINASE; GLUCOCORTICOID RECEPTOR; GR; IGF-1; IL-6; INSULIN RECEPTOR SUBSTARTE; INSULIN-LIKE GROWTH FACTOR-1; INTERLEUKIN-6; IRS-1; MAMMALIAN TARGET OF RAPAMYCIN; MAPK; MITOGEN-ACTIVATED KINASE; MTOR; NEUROPEPTIDE Y; NPY; PHOSPHOINOSITIDE 3-KINASE; PI3K; POMC; PROOPIOMELANOCORTIN; REACTIVE OXYGEN SPECIES; ROS; SAA; SERUM AMYLOID A; SKELETAL MUSCLE; TGF-Β; THYROTROPIN-RELEASING HORMONE; TNF-Α; TRANSFORMING GROWTH FACTOR-Β; TRH; TUMOR NECROSIS FACTOR-Α; UBIQUITIN PROTEASOME SYSTEM; UPS;

ANGIOTENSIN II; ANIMALS; CACHEXIA; HEART DISEASES; HUMANS; MOLECULAR TARGETED THERAPY; MUSCLE, SKELETAL; MUSCULAR ATROPHY; SIGNAL TRANSDUCTION;

EID: 84885189913     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.05.035     Document Type: Review

References (129)

1. Aguilar V, Alliouachene S, Sotiropoulos A., Sobering A, Athea Y, Djouadi F., et al S6 Kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 2007 Jun; 5(6):476-87.
2. Anker SD, Negassa A, Coats AJS, Afzal R, Poole-Wilson PA, Cohn J.N., et al Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-converting-enzyme inhibitors: an observational study. Lancet 2003 Mar 29; 361(9363):1077-83.
3. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373-99.
4. Argilés J.M., López-Soriano FJ, Busquets S. Novel approaches to the treatment of cachexia. Drug Discov Today 2008 Jan; 13(1-2):73-8.
5. Attaix D, Baracos VE MAFbx/Atrogin-1 expression is a poor index of muscle proteolysis. Curr Opin Clin Nutr Metab Care 2010 May; 13(3):223-4.
6. Attaix D, Ventadour S, Codran A., Béchet D, Taillandier D., Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 2005; 41:173-86.
7. Auclair D, Garrel DR, Zerouala A.C., Ferland LH Activation of the ubiquitin pathway in rat skeletal muscle by catabolic doses of glucocorticoids. Am J Physiol Cell Physiol 1997 Mar 1; 271(3):C1007-16.
8. Barton ER, Morris L, Musarò A, Rosenthal N, Sweeney HL. Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice. J Cell Biol 2002 Apr 1; 157(1):137-48.
9. Bedair HS, Karthikeyan T, Quintero A, Li Y, Huard J. Angiotensin II receptor blockade administered after injury improves muscle regeneration and decreases fibrosis in normal skeletal muscle. Am J Sports Med 2008 Aug; 36(8):1548-54.
10. Bodine SC, Latres E, Baumhueter S., Lai VK, Nunez L, Clarke BA, et al Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001 Nov 23; 294(5547):1704-8.
11. Bodine SC, Stitt TN, Gonzalez M, Kline W.O., Stover GL, Bauerlein R, et al Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 2001 Nov; 3(11):1014-9.
12. Brack AS, Conboy MJ, Roy S, Lee M., Kuo CJ, Keller C, et al Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007 Aug 10; 317(5839):807-10.
13. Brink M, Price SR, Chrast J, Bailey J.L., Anwar A., Mitch WE, et al Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I. Endocrinology 2001 Apr; 142(4):1489-96.
14. Brink M, Wellen J, Delafontaine P. Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J Clin Invest 1996 Jun 1; 97(11):2509-16.
15. Burks TN, Andres-Mateos E, Marx R., Mejias R, van Erp C, Simmers JL, et al Losartan restores skeletal muscle remodeling and protects against disuse atrophy in sarcopenia. Sci Transl Med 2011 May 11; 3(82), 82ra37.
16. Cabello-Verrugio C., Acuña MJ, Morales M.G., Becerra A., Simon F, Brandan E. Fibrotic response induced by angiotensin-II requires NAD(P)H oxidase-induced reactive oxygen species (ROS) in skeletal muscle cells. Biochem Biophys Res Comm 2011 Jul; 410(3):665-70.
17. Cabello-Verrugio C., Cordova G, Salas J.D., Angiotensin II role in skeletal muscle atrophy. Curr Protein Pept Sci 2012 Sep 1; 13(6):560-9.
18. Cai D, Frantz JD, Tawa N.E., Melendez PA, Oh B-C, Lidov HGW, et al IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 2004 Oct 15; 119(2):285-98.
19. Carlson ME, Hsu M, Conboy IM Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008 Jul 24; 454(7203):528-32.
20. Chai W, Wang W, Dong Z., Cao W, Liu Z. Angiotensin II receptors modulate muscle microvascular and metabolic responses to insulin in vivo. Diabetes 2011 Nov; 60(11):2939-46.
21. Chai W, Wang W, Liu J., Barrett EJ, Carey RM, Cao W, et al Angiotensin II type 1 and type 2 receptors regulate basal skeletal muscle microvascular volume and glucose use. Hypertension 2010 Feb; 55(2):523-30.
22. Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature 2012 Oct 18; 490(7420):355-60.
23. Clarke BA, Drujan D, Willis M.S., Murphy LO, Corpina RA, Burova E, et al The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 2007 Nov; 6(5):376-85.
24. Cohen S, Brault JJ, Gygi S.P., Glass DJ, Valenzuela DM, Gartner C, et al During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 2009 Jun 15; 185(6):1083-95.
25. Cohn RD, van Erp C, Habashi JP, Soleimani A.A., Klein EC, Lisi MT, et al Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med 2007 Feb; 13(2):204-10
26. Coirault C, Hagège A, Chemla D, Fratacci MD, Guérot C, Lecarpentier Y. Angiotensin converting enzyme inhibitor therapy improves respiratory muscle strength in patients with heart failure. Chest 2001 Jun; 119(6):1755-60.
27. Coleman ME, DeMayo F, Yin K.C., Lee HM, Geske R, Montgomery C, et al Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 1995 May 19; 270(20):12109-16.
28. Collins CA, Zammit PS, Ruiz A.P., Morgan JE, Partridge TA A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 2007 Apr; 25(4):885-94.
29. Conboy IM, Conboy MJ, Smythe G.M., Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003 Nov 28; 302(5650):1575-7.
30. Conboy IM, Conboy MJ, Wagers A.J., Girma ER, Weissman IL, Rando TA Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005 Feb 17; 433(7027):760-4.
31. Conboy IM, Rando TA The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002 Sep; 3(3):397-409.
32. Csibi A, Cornille K, Leibovitch M.P., Poupon A., Tintignac LA, Sanchez AMJ, et al The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS ONE 2010; 5(2):e8994.
33. Csibi A, Leibovitch MP, Cornille K, Tintignac L.A., Leibovitch SA MAFbx/Atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J Biol Chem 2009 Feb 13; 284(7):4413-21.
34. Dalla Libera L., Ravara B, Angelini A., Rossini K, Sandri M, Thiene G., et al Beneficial effects on skeletal muscle of the angiotensin II type 1 receptor blocker irbesartan in experimental heart failure. Circulation 2001 May 1; 103(17):2195-200.
35. de Gasparo M., Catt KJ, Inagami T, Wright J.W., Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 2000 Sep; 52(3):415-72.
36. de Kloet A.D., Krause EG, Kim D-H, Sakai RR, Seeley R.J., Woods SC The effect of angiotensin-converting enzyme inhibition using captopril on energy balance and glucose homeostasis. Endocrinology 2009 Sep; 150(9):4114-23.
37. Di Bari M., van de Poll-Franse LV, Onder G, Kritchevsky SB, Newman A, Harris TB, et al. Antihypertensive medications and differences in muscle mass in older persons: the health, aging and body composition study. J Am Geriatr Soc 2004 Jun; 52(6):961-6.
38. Doehner W, Haehling von S, Anker SD, Lainscak M. Neurohormonal activation and inflammation in chronic cardiopulmonary disease: a brief systematic review. Wien Klin Wochenschr 2009 Jun; 121(9-10):293-6.
39. Elbaz M, Yanay N, Aga-Mizrachi S, Brunschwig Z., Kassis I, Ettinger K, et al Losartan, a therapeutic candidate in congenital muscular dystrophy: studies in the dy(2J)/dy(2J) mouse. Ann Neurol 2012 May; 71(5):699-708.
40. Fearon KCH, Glass DJ, Guttridge DC Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab 2012 Aug; 16(2):153-66.
41. Folli F, Kahn CR, Hansen H, Bouchie J.L., Feener EP Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J Clin Invest 1997 Nov 1; 100(9):2158-69.
42. Fujita J, Tsujinaka T, Ebisui C, Yano M, Shiozaki H, Katsume A, et al. Role of interleukin-6 in skeletal muscle protein breakdown and cathepsin activity in vivo. Eur Surg Res 1996; 28(5):361-6.
43. Gayan-Ramirez G., Vanderhoydonc F, Verhoeven G., Decramer M. Acute treatment with corticosteroids decreases IGF-1 and IGF-2 expression in the rat diaphragm and gastrocnemius. Am J RespirCrit Care Med 1999 Jan; 159(1):283-9.
44. Giovannini S, Cesari M, Marzetti E., Leeuwenburgh C, Maggio M, Pahor M. Effects of ACE-inhibition on IGF-1 and IGFBP-3 concentrations in older adults with high cardiovascular risk profile. J Cachexia Sarcopenia Muscle 2010 May 5; 14(6):457-60.
45. Glass D, Roubenoff R. Recent advances in the biology and therapy of muscle wasting. Ann NY Acad Sci 2010 Nov; 1211:25-36.
46. Goodman MN. Interleukin-6 induces skeletal muscle protein breakdown in rats. Proc Soc Exp Biol Med 1994 Feb; 205(2):182-5.
47. Grady EF, Sechi LA, Griffin C.A., Schambelan M., Kalinyak JE Expression of AT2 receptors in the developing rat fetus. J Clin Invest 1991 Sep; 88(3):921-33.
48. Graziani G, Badalamenti S, Del Bo A, Marabini M, Gazzano G, Como G, et al Abnormal hemodynamics and elevated angiotensin II plasma levels in polydipsic patients on regular hemodialysis treatment. Kidney Int 1993 Jul; 44(1):107-14.
49. Haehling von S., Lainscak M, Springer J., Anker SD Cardiac cachexia: a systematic overview. Pharmacol Ther 2009 Mar; 121(3):227-52.
50. Hambrecht R, Schulze PC, Gielen S, Linke A., Möbius-Winkler S, Yu J, et al. Reduction of insulin-like growth factor-I expression in the skeletal muscle of noncachectic patients with chronic heart failure. J Am Coll Cardiol 2002 Apr 3; 39(7): 1175-81.
51. Heineke J, Auger-Messier M, Xu J., Sargent M, York A, Welle S., et al Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation 2010 Jan 26; 121(3):419-25.
52. Hu Z, Wang H, Lee I.H., 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 2009 Sep 14; 119(10):3059-69.
53. Jin D, Takai S, Sakaguchi M., Okamoto Y, Muramatsu M, Miyazaki M. An antiarrhythmic effect of a chymase inhibitor after myocardial infarction. J Pharmacol Exp Ther 2004 May; 309(2):490-7.
54. Johnston APW, Baker J, Bellamy L.M., McKay BR, De Lisio M, Parise G. Regulation of muscle satellite cell activation and chemotaxis by angiotensin II. PLoS ONE 2010; 5(12):e15212.
55. Johnston APW, Baker J, De Lisio M, Parise G. Skeletal muscle myoblasts possess a stretch-responsive local angiotensin signalling system. J Renin Angiotensin Aldosterone Syst 2011 Jun; 12(2):75-84.
56. Kaneto H, Katakami N, Matsuhisa M., Matsuoka T-A. Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Inflamm 2010; 2010:453892.
57. Kimura S, Zhang G-X, Nishiyama A, Shokoji T., Yao L, Fan Y-Y, et al Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 2005 Mar; 45(3):438-44.
58. Lagirand-Cantaloube J., Cornille K, Csibi A., Batonnet-Pichon S, Leibovitch MP, Leibovitch SA Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS ONE 2009; 4(3):e4973.
59. Lagirand-Cantaloube J., Offner N, Csibi A., Leibovitch MP, Batonnet-Pichon S, Tintignac LA, et al. The initiation factor eIF3-f is a major target for Atrogin1/MAFbx function in skeletal muscle atrophy. EMBOJ 2008 Mar 20; 27(8):1266-76.
60. Lecker SH. Ubiquitin-protein ligases in muscle wasting: multiple parallel pathways? CurrOpin Clin Nutr Metab Care 2003 May; 6(3):271-5.
61. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEBJ 2004 Jan; 18(1):39-51.
62. Leclerc GM, Leclerc GJ, Fu G, Barredo JC AMPK-induced activation of Akt by AICAR is mediated by IGF-1R dependent and independent mechanisms in acute lymphoblastic leukemia. J Mol Signal 2010; 5:15.
63. Lenkei Z, Palkovits M, Corvol P., Llorens-Cortes C. Expression of angiotensin type-1 (AT1) and type-2 (AT2) receptor mRNAs in the adult rat brain: a functional neuroanatomical review. Front Neuroendocrinol 1997 Oct; 18(4):383-439.
64. Lütken SC, Kim SW, Jonassen T, Marples D, Knepper MA, Kwon T-H, et al. Changes of renal AQP2, ENaC, and NHE3 in experimentally induced heart failure: response to angiotensin II AT1 receptor blockade. Am J Physiol Renal Physiol 2009 Dec; 297(6):F1678-88.
65. Masson S, Latini R, Bevilacqua M., Vago T, Sessa F, Torri M., et al Within-patient variability of hormone and cytokine concentrations in heart failure. Pharmacol Res 1998 Mar; 37(3):213-7.
66. McCroskery S, Thomas M, Maxwell L., Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 2003 Sep 15; 162(6):1135-47.
67. Meinen S, Lin S, Rüegg MA. Angiotensin II type 1 receptor antagonists alleviate muscle pathology in the mouse model for laminin-alpha2-deficient congenital muscular dystrophy (MDC1A). Skeletal Muscle 2012 Sep 3; 2(1):18.
68. Miller DS, Villalobos AR, Pritchard JB. Organic cation transport in rat choroid plexus cells studied by fluorescence microscopy. Am J Physiol 1999 Apr; 276(4 Pt 1):C955-68.
69. 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 1999 May; 276(5 Pt 1):C1132-8.
70. Morales MG, Vazquez Y, Acuña MJ, Rivera JC, Simon F, Salas JD, et al. Angiotensin II-induced pro-fibrotic effects require p38MAPK activity and transforming growth factor beta 1 expression in skeletal muscle cells. Int J Biochem Cell Biol 2012 Nov; 44(11):1993-2002.
71. Muller FL, Song W, Jang Y.C., Liu Y., Sabia M, Richardson A, et al Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am J Physiol Regul Integr Comp Physiol 2007 Sep; 293(3): R1159-68.
72. - mice enhances muscle function despite reducing muscle mass but compromises repair after injury. Am J Physiol Regul Integr Comp Physiol 2012 Aug; 303(3):R321-31.
73. Musaro A, McCullagh K, Paul A., Houghton L, Dobrowolny G, Molinaro M., et al Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 2001 Feb; 27(2):195-200.
74. Nakashima K, Yakabe Y. AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 2007 Jul; 71(7):1650-6.
75. Narici MV, Maffulli N. Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 2010; 95:139-59.
76. Onder G, Liperoti R, Russo A., Capoluongo E, Minucci A, Lulli P., et al Use of ACE inhibitors is associated with elevated levels of IGFBP-3 among hypertensive older adults: results from the IlSIRENTE study. Eur J Clin Pharmacol 2007 Apr; 63(4):389-95.
77. Onder G, Penninx BWJH, Balkrishnan R, Fried L.P., Chaves PHM, Williamson J, et al Relation between use of angiotensin-converting enzyme inhibitors and muscle strength and physical function in older women: an observational study. Lancet 2002 Mar 16; 359(9310):926-30.
78. Pallafacchina G, Calabria E, Serrano A.L., Kalhovde JM, Schiaffino S. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci USA 2002 Jul 9; 99(14):9213-8.
79. Peng X-D, Xu P-Z, Chen ML, Hahn-Windgassen A, Skeen J, Jacobs J, et al. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev 2003 Jun 1; 17(11):1352-65.
80. Porter JP, Anderson JM, Robison R.J., Phillips AC Effect of central angiotensin II on body weight gain in young rats. Brain Res 2003 Jan 3; 959(1):20-8.
81. Porter JP, Potratz KR. Effect of intracerebroventricular angiotensin II on body weight and food intake in adult rats. Am J Physiol Regul Integr Comp Physiol 2004 Aug; 287(2):R422-8.
82. Powers SK, Smuder AJ, Judge AR. Oxidative stress and disuse muscle atrophy: cause or consequence? CurrOpin Clin Nutr Metab Care 2012 May; 15(3):240-5.
83. Pueyo ME, Gonzalez W, Nicoletti A., Savoie F, Arnal JF, Michel JB Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. Arterioscler Thromb Vasc Biol 2000 Mar; 20(3):645-51.
84. Qi J-S, Minor L.K., Smith C., Hu B, Yang J, Andrade-Gordon P, et al Characterization of functional urotensin II receptors in human skeletal muscle myoblasts: comparison with angiotensin II receptors. Peptides 2005 Apr; 26(4):683-90.
85. Rabinovsky ED, Gelir E, Gelir S., Lui H, Kattash M, DeMayo F.J., et al Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEBJ 2003 Jan; 17(1):53-5.
86. Roig E, Perez-Villa F, Morales M., Jiménez W, Orús J, Heras M., et al Clinical implications of increased plasma angiotensin II despite ACE inhibitor therapy in patients with congestive heart failure. Eur Heart J 2000 Jan; 21(1):53-7.
87. Rommel C, Bodine SC, Clarke B.A., Rossman R., Nunez L, Stitt TN, et al Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 2001 Nov; 3(11):1009-13.
88. Rommel C, Clarke BA, Zimmermann S, Nunez L., Rossman R, Reid K, et al Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 1999 Nov 26; 286(5445):1738-41.
89. Russell ST, Eley H, Tisdale MJ Role of reactive oxygen species in protein degradation in murine myotubes induced by proteolysis-inducing factor and angiotensin II. Cell Signal 2007 Aug; 19(8):1797-806.
90. Russell ST, Wyke SM, Tisdale MJ Mechanism of induction of muscle protein degradation by angiotensin II. Cell Signal 2006 Jul; 18(7):1087-96.
91. Sacco A, Doyonnas R, Kraft P., Vitorovic S, Blau HM Self-renewal and expansion of single transplanted muscle stem cells. Nature 2008 Nov 27; 456(7221):502-6.
92. Sanders PM, Russell ST, Tisdale MJ Angiotensin II directly induces muscle protein catabolism through the ubiquitin-proteasome proteolytic pathway and may play a role in cancer cachexia. Br J Cancer 2005 Aug 22; 93(4):425-34.
93. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 2008 Jun; 23:160-70.
94. Schakman O, Gilson H, de Coninck V, Lause P, Verniers J, Havaux X, et al. Insulin-like growth factor-I gene transfer by electroporation prevents skeletal muscle atrophy in glucocorticoid-treated rats. Endocrinology 2005 Apr; 146(4):1789-97.
95. Schulze PC, Fang J, Kassik K.A., Gannon J., Cupesi M, MacGillivray C, et al Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ Res 2005 Sep 2; 97(5):418-26.
96. Schulze PC, Gielen S, Adams V., Linke A, Möbius-Winkler S, Erbs S, et al. Muscular levels of proinflammatory cytokines correlate with a reduced expression of insulinlike growth factor-I in chronic heart failure. Basic Res Cardiol 2003 Jul; 98(4):267-74.
97. Semprun-Prieto L.C., Sukhanov S, Yoshida T., Rezk BM, Gonzalez-Villalobos RA, Vaughn C, et al Angiotensin II induced catabolic effect and muscle atrophy are redox dependent. Biochem Biophys Res Comm 2011 Jun 3; 409(2):217-21.
98. Sharma M, Kambadur R, Matthews K.G., Somers WG, Devlin GP, Conaglen JV, et al Myostatin, a transforming growth factor-beta superfamily member, is expressed in heart muscle and isupregulated in cardiomyocytes after infarct. J Cell Physiol 1999 Jul; 180(1):1-9.
99. Shyu KG, Lu MJ, Wang B.W., Sun HY, Chang H. Myostatin expression in ventricular myocardium in a rat model of volume-overload heart failure. Eur J Clin Invest 2006 Oct; 36(10):713-9.
100. Simões e Silva AC, Diniz JSS, Pereira RM, Pinheiro SVB, Santos RAS. Circulating renin Angiotensin system in childhood chronic renal failure: marked increase of Angiotensin-(1-7) inend-stage renaldisease. PediatrRes 2006 Dec; 60(6):734-9.
101. Song Y-H, Li Y., Du J, Mitch WE, Rosenthal N, Delafontaine P. Muscle-specific expression of IGF-1 blocks angiotensin II-induced skeletal muscle wasting. J Clin Invest 2005 Feb; 115(2):451-8.
102. Stegbauer J, Coffman TM. New insights into angiotensin receptor actions: from blood pressure to aging. CurrOpin Nephrol Hypertens 2011 Jan; 20(1):84-8.
103. Stevens-Lapsley J.E., Ye F, Liu M., Borst SE, Conover C, Yarasheski KE, et al Impact of viral-mediated IGF-I gene transfer on skeletal muscle following cast immobilization. Am J Physiol Endocrinol Metab 2010 Nov; 299(5):E730-40.
104. Sumukadas D, Witham MD, Struthers A.D., McMurdo MET. Effect of perindopril on physical function in elderly people with functional impairment: a randomized controlled trial. CMAJ 2007 Oct 9; 177(8):867-74.
105. Tabony AM, Yoshida T, Galvez S., Higashi Y, Sukhanov S, Chandrasekar B., et al Angiotensin IIupregulates protein phosphatase 2Caand inhibits AMP-activated protein kinase signaling and energy balance leading to skeletal muscle wasting. Hypertension 2011 Oct; 58(4):643-9.
106. Tan BH, Fearon KC Cachexia: prevalence and impact in medicine. Curr Opin Clin Nutr Metab Care 2008 Jul; 11(4):400-7.
107. Tatsumi R. Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim SciJ 2010 Feb; 81(1):11-20.
108. Tintignac LA, Lagirand J, Batonnet S., Sirri V, Leibovitch MP, Leibovitch SA Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem 2005 Jan 28; 280(4):2847-56.
109. Tisdale MJ. Mechanisms of cancer cachexia. Physiol Rev 2009 Apr; 89(2): 381-410.
110. Trendelenburg AU, Meyer A, Rohner D., Boyle J, Hatakeyama S, Glass DJ Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 2009 Jun; 296(6):C1258-70.
111. Tsujinaka T, Fujita J, Ebisui C., Yano M, Kominami E, Suzuki K., et al Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J Clin Invest 1996 Jan 1; 97(1):244-9.
112. Tsutsumi K, Strömberg C, Viswanathan M., Saavedra JM Angiotensin-II receptor subtypes in fetal tissue of the rat: autoradiography, guanine nucleotide sensitivity, and association with phosphoinositide hydrolysis. Endocrinology 1991 Aug; 129(2):1075-82.
113. van der Meer SFT, Jaspers RT, Jones DA, Degens H. Time-course of changes in the myonuclear domain during denervation in young-adult and old rat gastrocnemius muscle. Muscle Nerve 2011 Feb; 43(2):212-22.
114. Velloso LA, Folli F, Perego L., Saad MJA. The multi-faceted cross-talk between the insulin and angiotensin II signaling systems. Diabetes Metab Res Rev 2006 Mar; 22(2):98-107.
115. Ventadour S, Attaix D. Mechanisms of skeletal muscle atrophy. Curr Opin Clin Nutr Metab Care 2006 Nov; 18(6):631-5.
116. Wang B-W, Chang H., Kuan P, Shyu KG Angiotensin II activates myostatin expression in cultured rat neonatal cardiomyocytes via p38 MAP kinase and myocyte enhance factor 2 pathway. J Endocrinology 2008 Apr; 197(1):85-93.
117. Wang Y, Pessin JE Mechanisms for fiber-type specificity of skeletal muscle atrophy. Curr Opin Clin Nutr Metab Care 2013 May; 16(3):243-50.
118. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GME, Clark SE, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006 Nov 17; 281(46):35137-46.
119. Werner C, Pöss J, Böhm M. Optimal antagonism of the Renin-Angiotensin-aldosterone system: do we need dual or triple therapy? Drugs 2010 Jul 9; 70(10):1215-30.
120. Whitehead NP, Yeung EW, Froehner S.C., Allen DG Skeletal muscle NADPH oxidase is increased and triggers stretch-induced damage in the mdx mouse. PLoS ONE 2010; 5(12):e15354.
121. Wing SS, Goldberg AL Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am J Physiol 1993 Apr; 264(4 Pt 1):E668-76.
122. Yablonka-Reuveni Z., Day K. Skeletal muscle stem cells in the spotlight: the satellite cell. Regenerating the Heart. Springer; 2011. p. 173-200.
123. Yamamoto R, Akazawa H, Fujihara H., Ozasa Y, Yasuda N, Ito K., et al Angiotensin II type 1 receptor signaling regulates feeding behavior through anorexigenic corticotropin-releasing hormone in hypothalamus. J Biol Chem 2011 Jun 17; 286(24):21458-65.
124. Yoshida T, Semprun-Prieto L, Sukhanov S., Delafontaine P. IGF-1 prevents ANG II-induced skeletal muscle atrophy via Akt- and Foxo-dependent inhibition of the ubiquitin ligase atrogin-1 expression. Am J Physiol Heart Circ Physiol 2010 May; 298(5):H1565-70.
125. Yoshida T, Semprun-Prieto L, Wainford R.D., Sukhanov S., Kapusta DR, Delafontaine P. Angiotensin II reduces food intake by altering orexigenic neuropeptide expression in the mouse hypothalamus. Endocrinology 2012 Mar; 153(3):1411-20.
126. Zhang L, Du J, Hu Z., Han G, Delafontaine P, Garcia G., et al IL-6 and serum amyloid A synergy mediates angiotensin II-induced muscle wasting. J Am Soc Nephrol 2009 Mar; 20(3):604-12.
127. Zhao W, Swanson SA, Ye J, Li X., Shelton JM, Zhang W, et al Reactive oxygen species impair sympathetic vasoregulation in skeletal muscle in angiotensin II-dependent hypertension. Hypertension 2006 Oct; 48(4):637-43.
128. Zimmers TA, Davies MV, Koniaris L.G., Haynes P., Esquela AF, Tomkinson KN, et al Induction of cachexia in mice by systemically administered myostatin. Science 2002 May 24; 296(5572):1486-8.
129. Zoll J, Monassier L, Garnier A., N'Guessan B, Mettauer B, Veksler V., et al ACE inhibition prevents myocardial infarction-induced skeletal muscle mitochondrial dysfunction. J Appl Physiol 2006 Aug; 101(2):385-91.