Signalling pathways regulating muscle mass in ageing skeletal muscle. the role of the IGF1-Akt-mTOR-FoxO pathway

Biogerontology

Volumn 14, Issue 3, 2013, Pages 303-323

  Sandri, M ^a,b,g   Barberi, L ^c   Bijlsma, A Y ^d,e   Blaauw, B ^a,b   Dyar, K A ^a   Milan, G ^a   Mammucari, C ^b   Meskers, C G M ^e   Pallafacchina, G ^b,f   Paoli, A ^b   Pion, D ^j   Roceri, M ^j   Romanello, V ^a   Serrano, A L ⁱ   Toniolo, L ^b   Larsson, L ^g,h   Maier, A B ^d   Munoz Canoves P ⁱ   Musaro A ^c   Pende, M ^j   Reggiani, C ^b,f   Rizzuto, R ^b,f   Schiaffino, S ^a,f   more..

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f CNR   (Italy)

^g UPPSALA UNIVERSITY   (Sweden)

^h PENNSYLVANIA STATE UNIVERSITY   (United States)

ⁱ UNIVERSITAT POMPEU FABRA   (Spain)

^j UNIVERSITÉ PARIS DESCARTES   (France)

more..

Author keywords

Ageing; Akt; FoxO; IGF1; mTOR; Sarcopenia

Indexed keywords

ATROGIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MYOSTATIN; PROTEIN KINASE B; PROTEIN S6; SOMATOMEDIN C; TRANSCRIPTION FACTOR FOXO;

ADULT; AGED; AGING; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; COHORT ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME INACTIVATION; FEMALE; HUMAN; HUMAN TISSUE; LIFESPAN; LONGEVITY; MAJOR CLINICAL STUDY; MALE; MOUSE; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SARCOPENIA; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, ANIMAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; PROTO-ONCOGENE PROTEINS C-AKT; SARCOPENIA; SERPIN E2; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TOR SERINE-THREONINE KINASES; UBIQUITIN-PROTEIN LIGASES; YOUNG ADULT;

EID: 84881253436     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-013-9432-9     Document Type: Article

References (80)

1. Aguilar V, Alliouachene S, Sotiropoulos A, Sobering A, Athea Y, Djouadi F, Miraux S, Thiaudiere E, Foretz M, Viollet B, Diolez P, Bastin J, Benit P, Rustin P, Carling D, Sandri M, Ventura-Clapier R, Pende M (2007) S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 5:476-487
2. Anderson SB, Goldberg AL, Whitman M (2008) Identification of a novel pool of extracellular pro-myostatin in skeletal muscle. J Biol Chem 283:7027-7035
3. Bartfeld NS, Pasquale EB, Geltosky JE, Languino LR (1993) The alpha v beta 3 integrin associates with a 190-kDa protein that is phosphorylated on tyrosine in response to platelet-derived growth factor. J Biol Chem 268:17270-17276
4. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476:341-345
5. Bentzinger CF, Romanino K, Cloetta D, Lin S, Mascarenhas JB, Oliveri F, Xia J, Casanova E, Costa CF, Brink M, Zorzato F, Hall MN, Ruegg MA (2008) Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8:411-424
6. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L (2010) Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab 11:35-46
7. Blaauw B, Mammucari C, Toniolo L, Agatea L, Abraham R, Sandri M, Reggiani C, Schiaffino S (2008) Akt activation prevents the force drop induced by eccentric contractions in dystrophin-deficient skeletal muscle. Hum Mol Genet 17:3686-3696
8. Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C, Masiero E, Abraham R, Sandri M, Schiaffino S, Reggiani C (2009) Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 23:3896-3905
9. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014-1019
10. Brocca L, Cannavino J, Coletto L, Biolo G, Sandri M, Bottinelli R, Pellegrino MA (2012) The time course of the adaptations of human muscle proteome to bed rest and the underlying mechanisms. J Physiol 590:5211-5230
11. Carmeliet P, Kieckens L, Schoonjans L, Ream B, van Nuffelen A, Prendergast G, Cole M, Bronson R, Collen D, Mulligan RC (1993) Plasminogen activator inhibitor-1 gene-deficient mice. I. Generation by homologous recombination and characterization. J Clin Invest 92(6):2746-2755
12. Corpas E, Harman SM, Blackman MR (1993) Human growth hormone and human ageing. Endocr Rev 14:20-39
13. Courey AJ, Horowitz JC, Kim KK, Koh TJ, Novak ML, Subbotina N, Warnock M, Xue B, Cunningham AK, Lin Y, Goldklang MP, Simon RH, Lawrence DA, Sisson TH (2011) The vitronectin-binding function of PAI-1 exacerbates lung fibrosis in mice. Blood 118:2313-2321
14. De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336-340
15. Demontis F, Perrimon N (2010) FOXO/4E-BP signalling in drosophila muscles regulates organism-wide proteostasis during ageing. Cell 143:813-825
16. Deng G, Royle G, Wang S, Crain K, Loskutoff DJ (1996) Structural and functional analysis of the plasminogen activator inhibitor-1 binding motif in the somatomedin B domain of vitronectin. J Biol Chem 271:12716-12723
17. Fay WP (2004) Plasminogen activator inhibitor 1, fibrin, and the vascular response to injury. Trends Cardiovasc Med 14:196-202
18. Gaugler M, Brown A, Merrell E, DiSanto-Rose M, Rathmacher JA, Reynolds TH (2011) PKB signalling and atrogene expression in skeletal muscle of aged mice. J Appl Physiol 111:192-199
19. Grieshammer U, Sassoon D, Rosenthal N (1992) A transgene target for positional regulators marks early rostrocaudal specification of myogenic lineages. Cell 69:79-93
20. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214-226
21. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H, Barnett J, Leslie NR, Cheng S, Shepherd PR, Gout I, Downes CP, Lamb RF (2004) The TSC1-2 tumor suppressor controls insulin-PI3 K signaling via regulation of IRS proteins. J Cell Biol 166:213-223
22. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392-395
23. Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590
24. Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J, Hamilton JA, Ouchi N, Lebrasseur NK, Walsh K (2008) Fast/Glycolytic muscle fibre growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab 7:159-172
25. Kallman DA, Plato CC, Tobin JD (1990) The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol 45:M82-M88
26. Katewa SD, Kapahi P (2011) Role of TOR signaling in aging and related biological processes in Drosophila melanogaster. Exp Gerontol 46:382-390
27. Kenyon CJ (2010a) The genetics of ageing. Nature 464:504-512
28. Kenyon C (2010b) A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann N Y Acad Sci 1204:156-162
29. Kim JS, Cross JM, Bamman MM (2005) Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women. Am J Physiol Endocrinol Metab 288:E1110-E1119
30. Kim JS, Petrella JK, Cross JM, Bamman MM (2007) Load-mediated downregulation of myostatin mRNA is not sufficient to promote myofibre hypertrophy in humans: a cluster analysis. J Appl Physiol 103:1488-1495
31. Koh TJ, Bryer SC, Pucci AM, Sisson TH (2005) Mice deficient in plasminogen activator inhibitor-1 have improved skeletal muscle regeneration. Am J Physiol Cell Physiol 289:C217-C223
32. Lai KM, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AN, Yancopoulos GD, Glass DJ (2004) Conditional activation of akt in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24:9295-9304
33. Lamberts SW, van den Beld AW, van der Lely AJ (1997) The endocrinology of ageing. Science 278:419-424
34. Lamming DW, Ye L, Katajisto P, Goncalves MD, Saitoh M, Stevens DM, Davis JG, Salmon AB, Richardson A, Ahima RS, Guertin DA, Sabatini DM, Baur JA (2012) Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335:1638-1643
35. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149:274-293
36. Larsson L, Ansved T, Edstrom L, Gorza L, Schiaffino S (1991) Effects of age on physiological, immunohistochemical and biochemical properties of fast-twitch single motor units in the rat. J Physiol 443:257-275
37. Lee SJ (2004) Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20:61-86
38. Lee SJ, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98:9306-9311
39. Lionikas A, Blizard DA, Vandenbergh DJ, Glover MG, Stout JT, Vogler GP, McClearn GE, Larsson L (2003) Genetic architecture of fast- and slow-twitch muscle weight in 200-day old mice of the C56BL/6J and DBA/2J lineage. Physiol Genomics 16:141-152
40. Lionikas A, Blizard DA, Gerhard GS, Vandenbergh DJ, Stout JT, Vogler GP, McClearn GE, Larsson L (2005) Genetic determinants of weight of fast- and slow-twitch skeletal muscle in 500-day-old mice of the C57BL/6J and DBA/2J lineage. Physiol Genomics 21:184-192
41. Lionikas A, Blizard DA, Vandenbergh DJ, Stout JT, Vogler GP, McClearn GE, Larsson L (2006) Genetic determinants of weight of fast- and slow-twitch skeletal muscles in old mice. Mamm Genome 17:615-628
42. Lokireddy S, McFarlane C, Ge X, Zhang H, Sze SK, Sharma M, Kambadur R (2011) Myostatin induces degradation of sarcomeric proteins through a Smad3 signalling mechanism during skeletal muscle wasting. Mol Endocrinol 25:1936-1949
43. Lopez-Alemany R, Redondo JM, Nagamine Y, Munoz-Canoves P (2003) Plasminogen activator inhibitor type-1 inhibits insulin signalling by competing with alpha v beta3 integrin for vitronectin binding. Eur J Biochem 270:814-821
44. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458-471
45. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC (2002) Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 10:151-162
46. Marcell TJ, Harman SM, Urban RJ, Metz DD, Rodgers BD, Blackman MR (2001) Comparison of GH, IGF-I, and testosterone with mRNA of receptors and myostatin in skeletal muscle in older men. Am J Physiol Endocrinol Metab 281:E1159-E1164
47. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M (2009) Autophagy is required to maintain muscle mass. Cell Metab 10:507-515
48. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209:501-514
49. McKay BR, Ogborn DI, Bellamy LM, Tarnopolsky MA, Parise G (2012) Myostatin is associated with age-related human muscle stem cell dysfunction. FASEB J 26:2509-2521
50. McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94:12457-12461
51. McPherron AC, Lawler AM, Lee S-J (1997) Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387:83-90
52. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL, Rosenthal N (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27:195-200
53. Nagamine Y (2008) Transcriptional regulation of the plasminogen activator inhibitor type 1 - with an emphasis on negative regulation. Thromb Haemost 100:1007-1013
54. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, Sonenberg N, Kelly PA, Sotiropoulos A, Pende M (2005) Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 7:286-294
55. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci USA 99:9213-9218
56. Pallafacchina G, Blaauw B, Schiaffino S (2012) Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr Metab Cardiovasc Dis. doi: 10.1016/j.numecd.2012.02.002
57. Peterson CM, Johannsen DL, Ravussin E (2012) Skeletal muscle mitochondria and ageing: a review. J Ageing Res 2012:194821
58. Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, Liu ZX, Dong J, Mustard KJ, Hawley SA, Befroy D, Pypaert M, Hardie DG, Young LH, Shulman GI (2007) Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 5:151-156
59. Risson V, Mazelin L, Roceri M, Sanchez H, Moncollin V, Corneloup C, Richard-Bulteau H, Vignaud A, Baas D, Defour A, Freyssenet D, Tanti JF, Marchand-Brustel Y, Ferrier B, Conjard-Duplany A, Romanino K, Bauche S, Hantai D, Mueller M, Kozma SC, Thomas G, Ruegg MA, Ferry A, Pende M, Bigard X, Koulmann N, Schaeffer L, Gangloff YG (2009) Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187:859-874
60. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, Scorrano L, Rudolf R, Sandri M (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29:1774-1785
61. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3:1009-1013
62. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM (2007) PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25:903-915
63. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) FoxO transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399-412
64. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103:16260-16265
65. Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, Abraham R, Sandri M (2009) Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol 296:C1248-C1257
66. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skeletal Muscle 1:4
67. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. doi: 10.1111/febs.12253
68. Scicchitano BM, Rizzuto E, Musarò A (2009) Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1. Aging (Albany NY) 1:451-457
69. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al Qassab H, Carmignac D, Ramadani F, Woods A, Robinson IC, Schuster E, Batterham RL, Kozma SC, Thomas G, Carling D, Okkenhaug K, Thornton JM, Partridge L, Gems D, Withers DJ (2009) Ribosomal protein S6 kinase 1 signalling regulates mammalian life span. Science 326:140-144
70. Shavlakadze T, Winn N, Rosenthal N, Grounds MD (2005) Reconciling data from transgenic mice that overexpress IGF-I specifically in skeletal muscle. Growth Horm IGF Res 15:4-18
71. Shaw RJ, Bardeesy N, Manning BD, Lopez L, Kosmatka M, Depinho RA, Cantley LC (2004) The LKB1 tumor suppressor negatively regulates mTOR signalling. Cancer Cell 6:91-99
72. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408
73. Suelves M, Vidal B, Ruiz V, Baeza-Raja B, Diaz-Ramos A, Cuartas I, Lluis F, Parra M, Jardi M, Lopez-Alemany R, Serrano AL, Munoz-Canoves P (2005) The plasminogen activation system in skeletal muscle regeneration: antagonistic roles of urokinase-type plasminogen activator (uPA) and its inhibitor (PAI-1). Front Biosci 10:2978-2985
74. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ (2009) Myostatin reduces Akt/TORC1/p70S6 K signalling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296:C1258-C1270
75. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431:200-205
76. Velasco B, Cacicedo L, Escalada J, Lopez-Fernandez J, Sanchez-Franco F (1998) Growth hormone gene expression and secretion in ageing rats is age dependent and not age-associated weight increase related. Endocrinology 139:1314-1320
77. Vilchez D, Morantte I, Liu Z, Douglas PM, Merkwirth C, Rodrigues AP, Manning G, Dillin A (2012) RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489:263-268
78. Vuori K, Ruoslahti E (1994) Association of insulin receptor substrate-1 with integrins. Science 266:1576-1578
79. Winbanks CE, Weeks KL, Thomson RE, Sepulveda PV, Beyer C, Qian H, Chen JL, Allen JM, Lancaster GI, Febbraio MA, Harrison CA, McMullen JR, Chamberlain JS, Gregorevic P (2012) Follistatin-mediated skeletal muscle hypertrophy is regulated by Smad3 and mTOR independently of myostatin. J Cell Biol 197:997-1008
80. Yakar S, Liu JL, Stannard B, Butler A, Accili D et al (1999) Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci USA 96:7324-7329