Effect of chronic contractile activity on SS and IMF mitochondrial apoptotic susceptibility in skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 292, Issue 3, 2007, Pages

  Adhihetty, Peter J ^a   Ljubicic, Vladimir ^a   Hood, David A ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

Apoptosis; Exercise; Mitochondrial permeability transaction pore; Reactive oxygen species; Respiration

Indexed keywords

APOPTOSIS INDUCING FACTOR; CALPAIN; CASPASE; CYTOCHROME C; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BIOGENESIS; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL RESPIRATION; ELECTRIC STIMULATION; MALE; MITOCHONDRIA, MUSCLE; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SARCOLEMMA;

EID: 33947186240     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00311.2006     Document Type: Article

References (51)

1. Adhihetty PJ, Irrcher I, Joseph AM, Ljubicic V, Hood DA. Plasticity of skeletal muscle mitochondria in response to contractile activity. Exp Physiol 88: 99-107, 2003.
2. Adhihetty PJ, Hood DA. Mechanisms of apoptosis in skeletal muscle. Basic Appl Myol 13: 171-179, 2003.
3. Adhihetty PJ, Ljubicic V, Menzies KJ, Hood DA. Differential susceptibility of SS and IMF mitochondria to apoptotic stimuli. Am J Physiol Cell Physiol 289: C994-C1001, 2005.
4. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol Cell Physiol 273: C579-C587, 1997.
5. Allen DL, Roy RR, Edgerton VR. Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22: 1350-1360, 1999.
6. Arthur GD, Booker TS, Belcastro AN. Exercise promotes a subcellular redistribution of calcium-stimulated protease activity in striated muscle. Can J Physiol Pharmacol 77: 42-47, 1999.
7. Bartoli M, Richard I. Calpains in muscle wasting. Int J Biochem Cell Biol 37: 2115-2133, 2005.
8. Bauer MF, Gempel K, Reichert AS, Rappold GA, Lichtner P, Gerbitz KD, Neupert W, Brunner M, Hofmann S. Genetic and structural characterization of the human mitochondrial inner membrane translocase. J Mol Biol 289: 69-82, 1999.
9. Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2: 469-475, 2000.
10. Belcastro AN. Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol 74: 1381-1386, 1993.
11. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29: 222-230, 2000.
12. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389, 1993.
13. Das DK, Maulik N. Preconditioning potentiates redox signaling and converts death signal into survival signal. Arch Biochem Biophys 420: 305-311, 2003.
14. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N, Prevost MC, Leber B, Andrews D, Penninger J, Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 14: 729-739, 2000.
15. Dirks AJ, Leeuwenburgh C. 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, 2004.
16. Dirks AJ, Leeuwenburgh C. The role of apoptosis in age-related skeletal muscle atrophy. Sports Med 35: 473-483, 2005.
17. Ekhterae D, Lin Z, Lundberg MS, Crow MT, Brosius FC 3rd, Nunez G. ARC inhibits cytochrome c release from mitochondria and protects against hypoxia-induced apoptosis in heart-derived H9c2 cells. Circ Res 85: e70-e77, 1999.
18. Hood DA. Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90: 1137-1157, 2001.
19. Hoppeler H. Exercise-induced ultrastructural changes in skeletal muscle. Int J Sports Med 7: 187-204, 1986.
20. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflügers Arch 403: 369-376, 1985.
21. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287: C834-C843, 2004.
22. Ji LL. Exercise-induced modulation of antioxidant defense. Ann NY Acad Sci 959: 82-92, 2002.
23. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zuniga-Pflucker JC, Kroemer G, Penninger JM. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410: 549-554, 2001.
24. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257, 1972.
25. Koseki T, Inohara N, Chen S, Nunez G. ARC, an inhibitor of apoptosis expressed in skeletal muscle and heart that interacts selectively with caspases. Proc Natl Acad Sci USA 95: 5156-5160, 1998.
26. Krieger DA, Tate CA, Millin-Wood J, Booth FW. Populations of rat skeletal muscle mitochondria after exercise and immobilization. J Appl Physiol 48: 23-28, 1980.
27. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
28. Ljubicic V, Adhihetty PJ, Hood DA. Role of UCP3 in state 4 respiration during contractile activity-induced mitochondrial biogenesis. J Appl Physiol 97: 976-983, 2004.
29. Ljubicic V, Adhihetty PJ, Hood DA. Application of animal models: chronic electrical stimulation-induced contractile activity. Can J Appl Physiol 30: 625-643, 2005.
30. Locke M, Noble EG. Stress proteins: the exercise response. Can J Appl Physiol 20: 155-167, 1995.
31. Martin TP. Predictable adaptations by skeletal muscle mitochondria to different exercise training workloads. Comp Biochem Physiol B 88: 273-276, 1987.
32. Nomura K, Imai H, Koumura T, Kobayashi T, Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem J 351: 183-193, 2000.
33. Ornatsky OI, Connor MK, Hood DA. Expression of stress proteins and mitochondrial chaperonins in chronically stimulated skeletal muscle. Biochem J 311: 119-123, 1995.
34. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E. Oxidative stress and cell signalling. Curr Med Chem 11: 1163-1182, 2004.
35. Polster BM, Basanez G, Etxebarria A, Hardwick JM, Nicholls DG. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280: 6447-6454, 2005.
36. Primeau AJ, Adhihetty PJ, Hood DA. Apoptosis in heart and skeletal muscle. Can J Appl Physiol 27: 349-395, 2002.
37. Putman CT, Dusterhoft S, Pette D. Changes in satellite cell content and myosin isoforms in low-frequency-stimulated fast muscle of hypothyroid rat. J Appl Physiol 86: 40-51, 1999.
38. Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C, Kroemer G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3: 839-843, 2001.
39. Riley DA, Slocum GR, Bain JL, Sedlak FR, Sowa TE, Mellender JW. Rat hindlimb unloading: soleus histochemistry, ultrastructure, and electromyography. J Appl Physiol 69: 58-66, 1990.
40. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB, Korsmeyer SJ. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 92: 7834-7838, 1995.
41. Servais S, Couturier K, Koubi H, Rouanet JL, Desplanches D, Sornay-Mayet MH, Sempore B, Lavoie JM, Favier R. Effect of voluntary exercise on H2O2 release by subsarcolemmal and intermyofibrillar mitochondria. Free Radic Biol Med 35: 24-32, 2003.
42. Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. FASEB J 18: 1150-1152, 2004.
43. Siu PM, Pistilli EE, Alway SE. Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats. Am J Physiol Regul Integr Comp Physiol 289: R1015-R1026, 2005.
44. Stevens RJ, Nishio ML, Hood DA. Effect of hypothyroidism on the expression of cytochrome c and cytochrome c oxidase in heart and muscle during development. Mol Cell Biochem 143: 119-127, 1995.
45. Sultan KR, Dittrich BT, Pette D. Calpain activity in fast, slow, transforming, and regenerating skeletal muscles of rat. Am J Physiol Cell Physiol 279: C639-C647, 2000.
46. Sultan KR, Dittrich BT, Leisner E, Paul N, Pette D. Fiber type-specific expression of major proteolytic systems in fast- to slow-transforming rabbit muscle. Am J Physiol Cell Physiol 280: C239-C247, 2001.
47. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Brenner C, Larochette N, Prevost MC, Alzari PM, Kroemer G. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J Exp Med 189: 381-394, 1999.
48. Takahashi M, Hood DA. Chronic stimulation-induced changes in mitochondria and performance in rat skeletal muscle. J Appl Physiol 74: 934-941, 1993.
49. Takahashi M, Hood DA. Protein import into subsarcolemmal and intermyofibrillar skeletal muscle mitochondria. Differential import regulation in distinct subcellular regions. J Biol Chem 271: 27285-27291, 1996.
50. Takahashi M, Chesley A, Freyssenet D, Hood DA. Contractile activity-induced adaptations in the mitochondrial protein import system. Am J Physiol Cell Physiol 274: C1380-C1387, 1998.
51. Vahsen N, Cande C, Briere JJ, Benit P, Joza N, Larochette N, Mastroberardino PG, Pequignot MO, Casares N, Lazar V, Feraud O, Debili N, Wissing S, Engelhardt S, Madeo F, Piacentini M, Penninger JM, Schagger H, Rustin P, Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J 23: 4679-4689, 2004.