Sarcopenia of aging: Underlying cellular mechanisms and protection by calorie restriction

BioFactors

Volumn 35, Issue 1, 2009, Pages 28-35

  Marzetti, Emanuele ^a,b   Lees, Hazel Anne ^a   Wohlgemuth, Stephanie Eva ^a   Leeuwenburgh, Christiaan ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

Apoptosis; Autophagy; Iron; Mitochondria; Oxidative stress

Indexed keywords

HEMOGLOBIN; IRON; MITOCHONDRIAL DNA;

ALZHEIMER DISEASE; APOPTOSIS; AUTOPHAGY; BIOGENESIS; CALORIC RESTRICTION; CELL DEATH; CELL PROTECTION; DNA DAMAGE; DNA SYNTHESIS; DRUG METABOLISM; ELECTRON TRANSPORT; HUMAN; MITOCHONDRIAL RESPIRATION; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; OXYGEN TRANSPORT; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; STEROIDOGENESIS; AGING; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

AGING; ANIMALS; APOPTOSIS; CALORIC RESTRICTION; HUMANS; MITOCHONDRIA, MUSCLE; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; MUSCULAR ATROPHY; OXIDATIVE STRESS;

EID: 65549136627     PISSN: 09516433     EISSN: None     Source Type: Journal    
DOI: 10.1002/biof.5     Document Type: Review

References (102)

1. Fisher, A. L. (2004) Of worms and women: sarcopenia and its role in disability and mortality. J. Am. Geriatr. Soc. 52, 1185-1190.
2. Szulc, P., Beck, T. J., Marchand, F., and Delmas, P. D. (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men-the MINOS study. J. Bone Miner. Res. 20, 721-729.
3. Rantanen, T., Guralnik, J. M., Foley, D., Masaki, K., Leveille, S., Curb, J. D., and White, L. (1999) Midlife hand grip strength as a predictor of old age disability. JAMA 281, 558-560.
4. Metter, E. J., Talbot, L. A., Schrager, M., and Conwit, R. (2002) Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J. Gerontol. A Biol. Sci. Med. Sci. 57, B359-B365.
5. Iannuzzi-Sucich, M., Prestwood, K. M., andKenny, A. M. (2002) Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J. Gerontol. A Biol. Sci. Med. Sci. 57, M772-M777.
6. Roubenoff, R. (2004) Sarcopenic obesity: the confluence of two epidemics. Obes. Res. 12, 887-888.
7. Vandervoort, A. A. (2002) Aging of the human neuromuscular system. Muscle Nerve 25, 17-25.
8. Faulkner, J. A., Brooks, S. V., and Zerba, E. (1995) Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. J. Gerontol. A Biol. Sci. Med. Sci. 50, 124-129.
9. Lees, S. J., Rathbone, C. R., and Booth, F. W. (2006) Age-associated decrease in muscle precursor cell differentiation. Am. J. Physiol. Cell Physiol. 290, C609-C615.
10. Szulc, P., Duboeuf, F., Marchand, F., and Delmas, P. D. (2004) Hormonal and lifestyle determinants of appendicular skeletal muscle mass in men: the MINOS study. Am. J. Clin. Nutr. 80, 496-503.
11. Visser, M., Pahor, M., Taaffe, D. R., Goodpaster, B. H., Simonsick, E. M., Newman, A. B., Nevitt, M., and Harris, T. B. (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J. Gerontol. A Biol. Sci. Med. Sci. 57, M326-M332.
12. Dreyer, H. C. and Volpi, E. (2005) Role of protein and amino acids in the pathophysiology and treatment of sarcopenia. J. Am. Coll. Nutr. 24, 140S-145S.
13. Larsson, L., Sjodin, B., and Karlsson, J. (1978) Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years. Acta Physiol. Scand. 103, 31-39.
14. Usuki, F., Yasutake, A., Umehara, F., and Higuchi, I. (2004) Beneficial effects of mild lifelong dietary restriction on skeletal muscle: prevention of age-related mitochondrial damage, morphological changes, and vulnerability to a chemical toxin. Acta Neuropathol. 108, 1-9.
15. Kim, J. H., Kwak, H. B., Leeuwenburgh, C., and Lawler, J. M. (2008) Lifelong exercise and mild (8%) caloric restriction attenuate ageinduced alterations in plantaris muscle morphology, oxidative stress, and IGF-1 in the Fischer-344 rat. Exp. Gerontol. 43, 317-329.
16. Payne, A. M., Dodd, S. L., and Leeuwenburgh, C. (2003) Life-long calorie restriction in Fischer 344 rats attenuates age-related loss in skeletal muscle-specific force and reduces extracellular space. J. Appl. Physiol. 95, 2554-2562.
17. Marzetti, E., Wohlgemuth, S. E., Lees, H. A., Chung, H. Y., Giovannini, S., and Leeuwenburgh, C. (2008) Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech. Ageing Dev. 129, 542-549.
18. Hofer, T., Marzetti, E., Xu, J., Seo, A. Y., Gulec, S., Knutson, M. D., Leeuwenburgh, C., and Dupont-Versteegden, E. E. (2008) Increased iron content and RNA oxidative damage in skeletal muscle with aging and disuse atrophy. Exp. Gerontol. 43, 563-570.
19. Hiona, A. and Leeuwenburgh, C. (2008) The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp. Gerontol. 43, 24-33.
20. Chung, L. and Ng, Y. C. (2006) Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. Biochim. Biophys. Acta 1762, 103-109.
21. Dirks, A. and Leeuwenburgh, C. (2002) Apoptosis in skeletal muscle with aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R519-R527.
22. Marzetti, E., Groban, L., Wohlgemuth, S. E., Lees, H. A., Lin, M., Jobe, H., Giovannini, S., Leeuwenburgh, C., and Carter, C. S. (2008) Effects of short-term GH supplementation and treadmill exercise training on physical performance and skeletal muscle apoptosis in old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R558-R567.
23. Phillips, T. and Leeuwenburgh, C. (2005) Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J. 19, 668-670.
24. Pistilli, E. E., Siu, P. M., and Alway, S. E. (2006) Molecular regulation of apoptosis in fast plantaris muscles of aged rats. J. Gerontol. A Biol. Sci. Med. Sci. 61, 245-255.
25. Siu, P. M., Pistilli, E. E., Butler, D. C., and Alway, S. E. (2005) Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am. J. Physiol. Cell Physiol. 288, C338-C349.
26. Dirks, A. J., Hofer, T., Marzetti, E., Pahor, M., and Leeuwenburgh, C. (2006) Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle. Ageing Res. Rev. 5, 179-195. (Pubitemid 43786295)
27. Drew, B., Phaneuf, S., Dirks, A., Selman, C., Gredilla, R., Lezza, A., Barja, G., and Leeuwenburgh, C. (2003) Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R474-R480.
28. Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., and Nair, K. S. (2005) Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. USA 102, 5618-5623.
29. Wanagat, J., Cao, Z., Pathare, P., and Aiken, J. M. (2001) Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J. 15, 322-332.
30. Cao, Z., Wanagat, J., McKiernan, S. H., and Aiken, J. M. (2001) Mitochondrial DNA deletion mutations are concomitant with ragged red regions of individual, aged muscle fibers: analysis by laser-capture microdissection. Nucleic Acids Res. 29, 4502-4508.
31. Bua, E., Johnson, J., Herbst, A., Delong, B., McKenzie, D., Salamat, S., and Aiken, J. M. (2006) Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum. Genet. 79, 469-480.
32. Weissman, L., de Souza-Pinto, N. C., Stevnsner, T. and Bohr, V. A. (2007) DNA repair, mitochondria, and neurodegeneration. Neuroscience 145, 1318-1329.
33. Chabi, B., Ljubicic, V., Menzies, K. J., Huang, J. H., Saleem, A., and Hood, D. A. (2008) Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7, 2-12.
34. Muller-Hocker, J., Schneiderbanger, K., Stefani, F. H., and Kadenbach, B. (1992) Progressive loss of cytochrome c oxidase in the human ex-traocular muscles in ageing-a cytochemical-immunohistochemical study. Mutat. Res. 275, 115-124.
35. Aspnes, L. E., Lee, C. M., Weindruch, R., Chung, S. S., Roecker, E. B., and Aiken, J. M. (1997) Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle. FASEB J. 11, 573-581.
36. Lee, C. M., Lopez, M. E., Weindruch, R., and Aiken, J. M. (1998) Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radic. Biol. Med. 25, 964-972.
37. Bua, E. A., McKiernan, S. H., Wanagat, J., McKenzie, D., and Aiken, J. M. (2002) Mitochondrial abnormalities are more frequent in muscles under-going sarcopenia. J. Appl. Physiol. 92, 2617-2624.
38. Lee, C. M., Aspnes, L. E., Chung, S. S., Weindruch, R., and Aiken, J. M. (1998) Influences of caloric restriction on age-associated skeletal muscle fiber characteristics and mitochondrial changes in rats and mice. Ann. NY Acad. Sci. 854, 182-191.
39. Bua, E., McKiernan, S. H., and Aiken, J. M. (2004) Calorie restriction limits the generation but not the progression of mitochondrial abnormalities in aging skeletal muscle. FASEB J. 18, 582-584.
40. Bevilacqua, L., Ramsey, J. J., Hagopian, K., Weindruch, R., and Harper, M. E. (2004) Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am. J. Physiol. Endocrinol. Metab. 286, E852-E861.
41. Lal, S. B., Ramsey, J. J., Monemdjou, S., Weindruch, R., and Harper, M. E. (2001) Effects of caloric restriction on skeletal muscle mitochondrial proton leak in aging rats. J. Gerontol. A Biol. Sci. Med. Sci. 56, B116-B122.
42. Lambert, A. J. and Merry, B. J. (2004) Effect of caloric restriction on mitochondrial reactive oxygen species production and bioenergetics: reversal by insulin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R71-R79.
43. Sreekumar, R., Unnikrishnan, J., Fu, A., Nygren, J., Short, K. R., Schimke, J., Barazzoni, R., and Nair, K. S. (2002) Effects of caloric restriction on mitochondrial function and gene transcripts in rat muscle. Am. J. Physiol. Endocrinol. Metab. 283, E38-E43. (Pubitemid 34686665)
44. Faulks, S. C., Turner, N., Else, P. L., and Hulbert, A. J. (2006) Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J. Gerontol. A Biol. Sci. Med. Sci. 61, 781-794.
45. Cefalu, W. T., Wang, Z. Q., Bell Farrow, A. D., Terry, J. G., Sonntag, W., Waite, M., and Parks, J. (2000) Chronic caloric restriction alters muscle membrane fatty acid content. Exp. Gerontol. 35, 331-341.
46. Lass, A., Sohal, B. H., Weindruch, R., Forster, M. J., and Sohal, R. S. (1998) Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria. Free Radic. Biol. Med. 25, 1089-1097.
47. Civitarese, A. E., Carling, S., Heilbronn, L. K., Hulver, M. H., Ukropcova, B., Deutsch, W. A., Smith, S. R., and Ravussin, E. (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med. 4, e76.
48. Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., Moncada, S., and Carruba, M. O. (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314-317.
49. Poulos, T. L., Li, H., and Raman, C. S. (1999) Heme-mediated oxygen activation in biology: cytochrome c oxidase and nitric oxide synthase. Curr. Opin. Chem. Biol. 3, 131-137.
50. Ponka, P. (1999) Cell biology of heme. Am. J. Med. Sci. 318, 241-256.
51. Castellani, R. J., Moreira, P. I., Liu, G., Dobson, J., Perry, G., Smith, M. A., and Zhu, X. (2007) Iron: the Redox-active center of oxidative stress in Alzheimer disease. Neurochem. Res. 32, 1640-1645.
52. Yantiri, F. and Andersen, J. K. (1999) The role of iron in Parkinson disease and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. IUBMB Life 48, 139-141.
53. Altun, M., Edstrom, E., Spooner, E., Flores-Moralez, A., Bergman, E., Tollet-Egnell, P., Norstedt, G., Kessler, B. M., and Ulfhake, B. (2007) Iron load and redox stress in skeletal muscle of aged rats. Muscle Nerve 36, 223-233.
54. Xu, J., Knutson, M. D., Carter, C. S., and Leeuwenburgh, C. (2008) Iron accumulation with age, oxidative stress and functional decline. PLoS ONE 3, e2865.
55. Jung, S. H., DeRuisseau, L. R., Kavazis, A. N., and Deruisseau, K. C. (2008) Plantaris muscle of aged rats demonstrates iron accumulation and altered expression of iron regulation proteins. Exp. Physiol. 93, 407-414.
56. Seo, A. Y., Xu, J., Servais, S., Hofer, T., Marzetti, E., Wohlgemuth, S. E., Knutson, M. D., Chung, H. Y., and Leeuwenburgh, C. (2008) Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7, 706-716.
57. Bian, K., Gao, Z., Weisbrodt, N., and Murad, F. (2003) The nature of heme/iron-induced protein tyrosine nitration. Proc. Natl. Acad. Sci. USA 100, 5712-5717.
58. Chua, A. C., Graham, R. M., Trinder, D., and Olynyk, J. K. (2007) The regulation of cellular iron metabolism. Crit. Rev. Clin. Lab. Sci. 44, 413-459.
59. Kondo, H., Miura, M., Kodama, J., Ahmed, S. M., and Itokawa, Y. (1992) Role of iron in oxidative stress in skeletal muscle atrophied by immobilization. Pflugers Arch. 421, 295-297.
60. Tsujimoto, Y. and Shimizu, S. (2007) Role of the mitochondrial membrane permeability transition in cell death. Apoptosis. 12, 835-840.
61. Cook, C. I. and Yu, B. P. (1998) Iron accumulation in aging: modulation by dietary restriction. Mech. Ageing Dev. 102, 1-13.
62. Sohal, R. S., Wennberg-Kirch, E., Jaiswal, K., Kwong, L. K., and Forster, M. J. (1999) Effect of age and caloric restriction on bleomycin-chelatable and nonheme iron in different tissues of C57BL/6 mice. Free Radic. Biol. Med. 27, 287-293.
63. Borten, O., Liberman, A., Tuchweber, B., Chevalier, S., Ferland, G., and Schipper, H. M. (2004) Effects of dietary restriction and metal supplementation on the accumulation of iron-laden glial inclusions in the aging rat hippocampus. Biogerontology 5, 81-88.
64. Dirks, A. J. and Leeuwenburgh, C. (2005) The role of apoptosis in agerelated skeletal muscle atrophy. Sports Med. 35, 473-483. (Pubitemid 41002968)
65. Marzetti, E. and Leeuwenburgh, C. (2006) Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp. Gerontol. 41, 1234-1238.
66. Marzetti, E., Lawler, J. M., Hiona, A., Manini, T., Seo, A. Y., and Leeuwenburgh, C. (2008) Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic. Biol. Med. 44, 160-168.
67. Pistilli, E. E., Jackson, J. R., and Alway, S. E. (2006) Death receptorassociated pro-apoptotic signaling in aged skeletal muscle. Apoptos is 11, 2115-2126.
68. Danial, N. N. and Korsmeyer, S. J. (2004) Cell death: critical control points. Cell 116, 205-219.
69. van, G. M., Festjens, N., van, L. G., Saelens, X., and Vandenabeele, P. (2003) Mitochondrial intermembrane proteins in cell death. Biochem. Biophys. Res. Commun. 304, 487-497.
70. Dirks, A. J. and Leeuwenburgh, C. (2004) Aging and lifelong calorie restriction result in adaptations of skeletal muscle apoptosis repressor, apoptosis-inducing factor, X-linked inhibitor of apoptosis, caspase-3, and caspase-12. Free Radic. Biol. Med. 36, 27-39.
71. Marzetti, E., Carter, C. S., Wohlgemuth, S. E., Lees, H. A., Giovannini, S., Anderson, B., Quinn, L. S., and Leeuwenburgh, C. (2009) Changes in IL-15 expression and death-receptor apoptotic signalling in rat gastrocnemius muscle with aging and life-long calorie restriction. Mech. Ageing Dev. In press, doi: 10.1016/J.mad.2008.12.008.
72. Kiffin, R., Bandyopadhyay, U., and Cuervo, A. M. (2006) Oxidative stress and autophagy. Antioxid. Redox Signal. 8, 152-162.
73. Xie, Z. and Klionsky, D. J. (2007) Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109.
74. Meijer, A. J. and Codogno, P. (2004) Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36, 2445-2462.
75. Wang, C. W. and Klionsky, D. J. (2003) The molecular mechanism of autophagy. Mol. Med. 9, 65-76.
76. Melendez, A., Talloczy, Z., Seaman, M., Eskelinen, E. L., Hall, D. H., and Levine, B. (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391.
77. Toth, M. L., Sigmond, T., Borsos, E., Barna, J., Erdelyi, P., Takacs-Vellai, K., Orosz, L., Kovacs, A. L., Csikos, G., Sass, M., and Vellai, T. (2008) Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy 4, 330-338.
78. Simonsen, A., Cumming, R. C., Brech, A., Isakson, P., Schubert, D. R., and Finley, K. D. (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4, 176-184.
79. Terman, A. (1995) The effect of age on formation and elimination of autophagic vacuoles in mouse hepatocytes. Gerontology 41 (Suppl 2), 319-326.
80. Cuervo, A. M., Bergamini, E., Brunk, U. T., Droge, W., Ffrench, M., and Terman, A. (2005) Autophagy and aging: the importance of maintaining "clean" cells. Autophagy 1, 131-140.
81. Cuervo, A. M. and Dice, J. F. (2000) Age-related decline in chaperonemediated autophagy. J. Biol. Chem. 275, 31505-31513.
82. Donati, A., Cavallini, G., Paradiso, C., Vittorini, S., Pollera, M., Gori, Z., and Bergamini, E. (2001) Age-related changes in the regulation of autophagic proteolysis in rat isolated hepatocytes. J. Gerontol. A Biol. Sci. Med. Sci. 56, B288-B293.
83. Terman, A. and Brunk, U. T. (2006) Oxidative stress, accumulation of biological 'garbage', and aging. Antioxid. Redox Signal. 8, 197-204.
84. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111.
85. Wohlgemuth, S. E., Julian, D., Akin, D. E., Fried, J., Toscano, K., Leeuwenburgh, C., and Dunn, W. A., Jr. (2007) Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res. 10, 281-292.
86. Saftig, P., Tanaka, Y., Lullmann-Rauch, R., and von, F. K. (2001) Disease model: LAMP-2 enlightens Danon disease. Trends Mol. Med. 7, 37-39.
87. Fukuda, T., Ewan, L., Bauer, M., Mattaliano, R. J., Zaal, K., Ralston, E., Plotz, P. H., and Raben, N. (2006) Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann. Neurol. 59, 700-708.
88. Yorimitsu, T. and Klionsky, D. J. (2005) Autophagy: molecular machinery for self-eating. Cell Death Differ. 12 (Suppl 2), 1542-1552.
89. Yang, Y. P., Liang, Z. Q., Gu, Z. L., and Qin, Z. H. (2005) Molecular mechanism and regulation of autophagy. Acta Pharmacol. Sin. 26, 1421-1434.
90. Del Roso, A., Vittorini, S., Cavallini, G., Donati, A., Gori, Z., Masini, M., Pollera, M., and Bergamini, E. (2003) Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Exp. Gerontol. 38, 519-527.
91. Bergamini, E., Cavallini, G., Donati, A., and Gori, Z. (2003) The antiageing effects of caloric restriction may involve stimulation of macroautophagy and lysosomal degradation, and can be intensified pharmacologically. Biomed. Pharmacother. 57, 203-208.
92. Corradetti, M. N. and Guan, K. L. (2006) Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 25, 6347-6360.
93. Blommaart, E. F., Luiken, J. J., Blommaart, P. J., van Woerkom, G. M., and Meijer, A. J. (1995) Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J. Biol. Chem. 270, 2320-2326.
94. Tassa, A., Roux, M. P., Attaix, D., and Bechet, D. M. (2003) Class III phosphoinositide 3-kinase-Beclin1 complex mediates the amino aciddependent regulation of autophagy in C2C12 myotubes. Biochem. J. 376, 577-586.
95. Vellai, T., Takacs-Vellai, K., Zhang, Y., Kovacs, A. L., Orosz, L., and Muller, F. (2003) Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 426, 620.
96. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H., and Goldberg, A. L. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412.
97. Sandri, M., Lin, J., Handschin, C., Yang, W., Arany, Z. P., Lecker, S. H., Goldberg, A. L., and Spiegelman, B. M. (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.
98. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del, P. P., Burden, S. J., Di, L. R., Sandri, C., Zhao, J., Goldberg, A. L., Schiaffino, S., and Sandri, M. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6, 458-471.
99. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., and Goldberg, L, A. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483.
100. Willcox, B. J., Donlon, T. A., He, Q., Chen, R., Grove, J. S., Yano, K., Masaki, K. H., Willcox, D. C., Rodriguez, B., and Curb, J. D. (2008) FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. USA 105, 13987-13992.
101. Colman, R. J., Beasley, T. M., Allison, D. B. and Weindruch, R. (2008) Attenuation of sarcopenia by dietary restriction in rhesus monkeys. J. Gerontol. A Biol. Sci. Med. Sci. 63, 556-559.
102. Dirks, A. J. and Leeuwenburgh, C. (2006) Caloric restriction in humans: potential pitfalls and health concerns. Mech. Ageing Dev. 127, 1-7.