Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 4, 2012, Pages

  O'Leary, Michael F N ^a   Vainshtein, Anna ^a   Carter, Heather N ^a   Zhang, Yuan ^a   Hood, David A ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

Mitochondria; Mitophagy; Muscle atrophy; Reactive oxygen species

Indexed keywords

BECLIN 1; CASPASE 3; CYTOCHROME C; PROTEIN BAK; PROTEIN BAX; PROTEIN BID; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA FRAGMENTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; MITOCHONDRIAL RESPIRATION; MITOPHAGY; MUSCLE ATROPHY; MUSCLE DENERVATION; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WILD TYPE;

ANIMALS; APOPTOSIS; AUTOPHAGY; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MUSCLE DENERVATION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MUSCULAR DISORDERS, ATROPHIC;

EID: 84865109297     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00451.2011     Document Type: Article

References (43)

1. Adhihetty PJ, O'Leary MF, Chabi B, Wicks KL, Hood DA. Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J Appl Physiol 102: 1143-1151, 2007.
2. Adhihetty PJ, O'Leary MF, Hood DA. Mitochondria in skeletal muscle: adaptable rheostats of apoptotic susceptibility. Exerc Sport Sci Rev 36: 116-121, 2008.
3. Babij P, Booth FW. Clenbuterol prevents or inhibits loss of specific mRNAs in atrophying rat skeletal muscle. Am J Physiol Cell Physiol 254: C657-C660, 1988.
4. Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature 466: 68-76, 2010.
5. Bertaggia E, Coletto L, Sandri M. Post-translational modifications control FoxO3 activity during denervation. Am J Physiol Cell Physiol 302: C587-C596, 2012.
6. Clavel S, Siffroi-Fernandez S, Coldefy AS, Boulukos K, Pisani DF, Derijard B. Regulation of the intracellular localization of Foxo3a by stress-activated protein kinase signaling pathways in skeletal muscle cells. Mol Cell Biol 30: 470-480, 2010.
7. Dejean LM, Martinez-Caballero S, Kinnally KW. Is MAC the knife that cuts cytochrome c from mitochondria during apoptosis? Cell Death Differ 13: 1387-1395, 2006.
8. Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C, Boncompagni S, Belia S, Wannenes F, Nicoletti C, Del PZ, Rosenthal N, Molinaro M, Protasi F, Fano G, Sandri M, Musaro A. Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab 8: 425-436, 2008.
9. Eisenberg HA, Hood DA. Blood flow, mitochondria, and performance in skeletal muscle after denervation and reinnervation. J Appl Physiol 76: 859-866, 1994.
10. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 Plays an Essential Role in Mediating Starvation-Induced Autophagy in Cardiac Myocytes. Circ Res 107: 1470-1482, 2010.
11. Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab 34: 465-472, 2009.
12. Kamada Y, Sekito T, Ohsumi Y. Autophagy in yeast: a TOR-mediated response to nutrient starvation. Curr Top Microbiol Immunol 279: 73-84, 2004.
13. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169: 425-434, 2005.
14. Lai RY, Ljubicic V, D'souza D, Hood DA. Effect of chronic contractile activity on mRNA stability in skeletal muscle. Am J Physiol Cell Physiol 299: C155-C163, 2010.
15. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del PP, Burden SJ, Di LR, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471, 2007.
16. Marzetti E, Privitera G, Simili V, Wohlgemuth SE, Aulisa L, Pahor M, Leeuwenburgh C. Multiple pathways to the same end: mechanisms of myonuclear apoptosis in sarcopenia of aging. Scientific World Journal 10: 340-349, 2010.
17. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. Autophagy is required to maintain muscle mass. Cell Metab 10: 507-515, 2009.
18. McClung JM, Judge AR, Powers SK, Yan Z. p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting. Am J Physiol Cell Physiol 298: C542-C549, 2010.
19. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22: 132-139, 2010.
20. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075, 2008.
21. Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421-429, 2002.
22. Morimoto N, Nagai M, Ohta Y, Miyazaki K, Kurata T, Morimoto M, Murakami T, Takehisa Y, Ikeda Y, Kamiya T, Abe K. Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res 1167: 112-117, 2007.
23. O'Leary MF, Hood DA. Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle. J Appl Physiol 105: 114-120, 2008.
24. O'Leary MF, Hood DA. Denervation-induced oxidative stress and autophagy signaling in muscle. Autophagy 5: 230-231, 2009.
25. Onodera J, Ohsumi Y. Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J Biol Chem 280: 31582-31586, 2005.
26. Plant PJ, Bain JR, Correa JE, Woo M, Batt J. Absence of caspase-3 protects against denervation-induced skeletal muscle atrophy. J Appl Physiol 107: 224-234, 2009.
27. Raben N, Roberts A, Plotz PH. Role of autophagy in the pathogenesis of Pompe disease. Acta Myol 26: 45-48, 2007.
28. Repnik U, Turk B. Lysosomal-mitochondrial cross-talk during cell death. Mitochondrion 10: 662-669, 2010.
29. Sakamoto K, Hirshman MF, Aschenbach WG, Goodyear LJ. Contraction regulation of Akt in rat skeletal muscle. J Biol Chem 277: 11910-11917, 2002.
30. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H, Candau R. AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 113: 695-710, 2012.
31. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36: 30-38, 2011.
32. Schiaffino S, Hanzlikova V. Studies on the effect of denervation in developing muscle. II The lysosomal system J Ultrastruct Res 39: 1-14, 1972.
33. Singh K, Hood DA. Effect of denervation-induced muscle disuse on mitochondrial protein import. Am J Physiol Cell Physiol 300: C138-C145, 2011.
34. Sinha S, Levine B. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 27, Suppl 1: S137-S148, 2008.
35. Siu PM, Alway SE. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 565: 309-323, 2005.
36. Siu PM, Alway SE. Deficiency of the Bax gene attenuates denervationinduced apoptosis. Apoptosis 11: 967-981, 2006.
37. Tanida I, Wakabayashi M, Kanematsu T, Minematsu-Ikeguchi N, Sou YS, Hirata M, Ueno T, Kominami E. Lysosomal turnover of GABARAP-phospholipid conjugate is activated during differentiation of C2C12 cells to myotubes without inactivation of the mTor kinase-signaling pathway. Autophagy 2: 264-271, 2006.
38. Vainshtein A, Kazak L, Hood DA. Effects of endurance training on apoptotic susceptibility in striated muscle. J Appl Physiol 110: 1638-1645, 2011.
39. Wagatsuma A, Osawa T. Time course of changes in angiogenesis-related factors in denervated muscle. Acta Physiol (Oxf) 187: 503-509, 2006.
40. Wicks KL, Hood DA. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am J Physiol Cell Physiol 260: C841-C850, 1991.
41. Xilouri M, Stefanis L. Autophagic pathways in Parkinson disease and related disorders. Expert Rev Mol Med 13: e8, 2011.
42. Yen WL, Klionsky DJ. How to live long and prosper: autophagy, mitochondria, and aging. Physiology (Bethesda) 23: 248-262, 2008.
43. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472-483, 2007.