Mitochondrial death effectors: Relevance to sarcopenia and disuse muscle atrophy

Biochimica et Biophysica Acta - General Subjects

Volumn 1800, Issue 3, 2010, Pages 235-244

  Marzetti, Emanuele ^a,b   Hwang, Judy C Y ^a   Lees, Hazel A ^a   Wohlgemuth, Stephanie E ^a   Dupont Versteegden, Esther E ^c   Carter, Christy S ^a   Bernabei, Roberto ^b   Leeuwenburgh, Christiaan ^a  

^a Institute on Aging   (United States)

^b CATHOLIC UNIVERSITY   (Italy)

^c Department of Rehabilitation Sciences   (United States)

Author keywords

Apoptosis; Apoptosis inducing factor; Caspases; Endonuclease G; Iron; Mitochondria; Muscle atrophy; Sarcopenia

Indexed keywords

IRON; MITOCHONDRIAL DNA; APOPTOSIS INDUCING FACTOR; CASPASE 12; CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 8; CASPASE 9; ENDONUCLEASE G; FAS ASSOCIATED DEATH DOMAIN PROTEIN; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR RECEPTOR;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; CELL ORGANELLE; DEGENERATIVE DISEASE; DISEASE COURSE; DISEASE EXACERBATION; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA FRAGMENTATION; ELECTRON TRANSPORT; GENE MUTATION; HOMEOSTASIS; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE DENERVATION; MUSCLE MASS; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; POLYNEUROPATHY; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW; RNA METABOLISM; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; TISSUE LEVEL; CELL LOSS; CONFERENCE PAPER; ENZYME ACTIVATION; MITOCHONDRION; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ADULT; AGED; AGING; ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; HEME; HUMANS; IRON; IRON-SULFUR PROTEINS; MUSCLE, SKELETAL; MUSCULAR DISORDERS, ATROPHIC; OXYGEN CONSUMPTION; SARCOPENIA; STEROIDS;

EID: 76749136290     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2009.05.007     Document Type: Review

References (143)

1. Rolland Y., Czerwinski S., Van Kan A.G., Morley J.E., Cesari M., Onder G., Woo J., Baumgartner R., Pillard F., Boirie Y., Chumlea W.M., and Vellas B. Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J. Nutr. Health Aging 12 (2008) 433-450
2. Roubenoff R. Sarcopenia: a major modifiable cause of frailty in the elderly. J. Nutr. Health Aging 4 (2000) 140-142
3. Rantanen T., Guralnik J.M., Foley D., Masaki K., Leveille S., Curb J.D., and White L. Midlife hand grip strength as a predictor of old age disability. JAMA 281 (1999) 558-560
4. Metter E.J., Talbot L.A., Schrager M., and Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J. Gerontol. A, Biol. Sci. Med. Sci. 57 (2002) B359-B365
5. Janssen I., Shepard D.S., Katzmarzyk P.T., and Roubenoff R. The healthcare costs of sarcopenia in the United States. J. Am. Geriatr. Soc. 52 (2004) 80-85
6. Edgerton V.R., Roy R.R., Allen D.L., and Monti R.J. Adaptations in skeletal muscle disuse or decreased-use atrophy. Am. J. Phys. Med. Rehabil. 81 (2002) S127-S147
7. Zarzhevsky N., Carmeli E., Fuchs D., Coleman R., Stein H., and Reznick A.Z. Recovery of muscles of old rats after hindlimb immobilisation by external fixation is impaired compared with those of young rats. Exp. Gerontol. 36 (2001) 125-140
8. Strasser H., Tiefenthaler M., Steinlechner M., Bartsch G., and Konwalinka G. Urinary incontinence in the elderly and age-dependent apoptosis of rhabdosphincter cells. Lancet 354 (1999) 918-919
9. Dirks A., and Leeuwenburgh C. Apoptosis in skeletal muscle with aging. Am. J. Physiol., Regul. Integr. Comp. Physiol 282 (2002) R519-R527
10. Dirks A.J., and 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 (2004) 27-39
11. Phillips T., and Leeuwenburgh C. Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J. 19 (2005) 668-670
12. Whitman S.A., Wacker M.J., Richmond S.R., and Godard M.P. Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch. 450 (2005) 437-446
13. Pistilli E.E., Jackson J.R., and Alway S.E. Death receptor-associated pro-apoptotic signaling in aged skeletal muscle. Apoptosis 11 (2006) 2115-2126
14. Marzetti E., Wohlgemuth S.E., Lees H.A., Chung H.Y., Giovannini S., and Leeuwenburgh C. Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech. Ageing Dev. 129 (2008) 542-549
15. Marzetti E., Groban L., Wohlgemuth S.E., Lees H.A., Lin M., obe H.J., Giovannini S., Leeuwenburgh C., and Carter C.S. 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 (2008) R558-R567
16. Marzetti E., Carter C.S., Wohlgemuth S.E., Lees H.A., Giovannini S., Anderson B., Quinn L.S., and Leeuwenburgh C. Changes in IL-15 expression and death-receptor apoptotic signaling in rat gastrocnemius muscle with aging and life-long calorie restriction. Mech. Ageing Dev. 130 (2009) 272-280
17. Jin H., Wu Z., Tian T., and Gu Y. Apoptosis in atrophic skeletal muscle induced by brachial plexus injury in rats. J. Trauma 50 (2001) 31-35
18. Alway S.E., Degens H., Krishnamurthy G., and Chaudhrai A. Denervation stimulates apoptosis but not Id2 expression in hindlimb muscles of aged rats. J. Gerontol. A, Biol. Sci. Med. Sci. 58 (2003) 687-697
19. Leeuwenburgh C., Gurley C.M., Strotman B.A., and Dupont-Versteegden E.E. Age-related differences in apoptosis with disuse atrophy in soleus muscle. Am. J. Physiol., Regul. Integr. Comp. Physiol. 288 (2005) R1288-R1296
20. Siu P.M., and Alway S.E. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J. Physiol. 565 (2005) 309-323
21. Siu P.M., and Alway S.E. Deficiency of the Bax gene attenuates denervation-induced apoptosis. Apoptosis 11 (2006) 967-981
22. Dupont-Versteegden E.E., Strotman B.A., Gurley C.M., Gaddy D., Knox M., Fluckey J.D., and Peterson C.A. Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am. J. Physiol., Regul. Integr. Comp. Physiol. 291 (2006) R1730-R1740
23. Adhihetty P.J., O'Leary M.F., Chabi B., Wicks K.L., and Hood D.A. Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J. Appl. Physiol. 102 (2007) 1143-1151
24. Ferreira R., Neuparth M.J., Vitorino R., Appell H.J., Amado F., and Duarte J.A. Evidences of apoptosis during the early phases of soleus muscle atrophy in hindlimb suspended mice. Physiol. Res. 57 (2008) 601-611
25. Dupont-Versteegden E.E. Apoptosis in muscle atrophy: relevance to sarcopenia. Exp. Gerontol. 40 (2005) 473-481
26. Adhihetty P.J., O'Leary M.F., and Hood D.A. Mitochondria in skeletal muscle: adaptable rheostats of apoptotic susceptibility. Exerc. Sport Sci. Rev. 36 (2008) 116-121
27. Palmer J.W., Tandler B., and Hoppel C.L. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J. Biol. Chem. 252 (1977) 8731-8739
28. Riva A., Tandler B., Lesnefsky E.J., Conti G., Loffredo F., Vazquez E., and Hoppel C.L. Structure of cristae in cardiac mitochondria of aged rat. Mech. Ageing Dev. 127 (2006) 917-921
29. Adhihetty P.J., Ljubicic V., Menzies K.J., and Hood D.A. Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am. J. Physiol., Cell Physiol. 289 (2005) C994-C1001
30. Chabi B., Ljubicic V., Menzies K.J., Huang J.H., Saleem A., and Hood D.A. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7 (2008) 2-12
31. Seo A.Y., Xu J., Servais S., Hofer T., Marzetti E., Wohlgemuth S.E., Knutson M.D., Chung H.Y., and Leeuwenburgh C. Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7 (2008) 706-716
32. Jezek P., and Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 37 (2005) 2478-2503
33. Ajioka R.S., Phillips J.D., and Kushner J.P. Biosynthesis of heme in mammals. Biochim. Biophys. Acta 1763 (2006) 723-736
34. Lill R., Diekert K., Kaut A., Lange H., Pelzer W., Prohl C., and Kispal G. The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol. Chem. 380 (1999) 1157-1166
35. Miller W.L. Mitochondrial specificity of the early steps in steroidogenesis. J. Steroid Biochem. Mol. Biol. 55 (1995) 607-616
36. McBride H.M., Neuspiel M., and Wasiak S. Mitochondria: more than just a powerhouse. Curr. Biol. 16 (2006) R551-R560
37. Jeong S.Y., and Seol D.W. The role of mitochondria in apoptosis. BMB Rep. 41 (2008) 11-22
38. Harman D. The biologic clock: the mitochondria?. J. Am. Geriatr. Soc. 20 (1972) 145-147
39. Miquel J., Economos A.C., Fleming J., and Johnson Jr. J.E. Mitochondrial role in cell aging. Exp. Gerontol. 15 (1980) 575-591
40. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11 (1956) 298-300
41. Yakes F.M., and Van H.B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 514-519
42. Wei Y.H., and Lee H.C. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp. Biol. Med. (Maywood) 227 (2002) 671-682
43. Piko L., Hougham A.J., and Bulpitt K.J. Studies of sequence heterogeneity of mitochondrial DNA from rat and mouse tissues: evidence for an increased frequency of deletions/additions with aging. Mech. Ageing Dev. 43 (1988) 279-293
44. Cortopassi G.A., and Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res. 18 (1990) 6927-6933
45. Yen T.C., Su J.H., King K.L., and Wei Y.H. Ageing-associated 5 kb deletion in human liver mitochondrial DNA. Biochem. Biophys. Res. Commun. 178 (1991) 124-131
46. Corral-Debrinski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., and Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 2 (1992) 324-329
47. Wanagat J., Cao Z., Pathare P., and Aiken J.M. Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J. 15 (2001) 322-332
48. Bua E., Johnson J., Herbst A., Delong B., McKenzie D., Salamat S., and Aiken J.M. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum. Genet. 79 (2006) 469-480
49. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., Van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., and Prolla T.A. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309 (2005) 481-484
50. Muller-Hocker J., Schneiderbanger K., Stefani F.H., and Kadenbach B. Progressive loss of cytochrome c oxidase in the human extraocular muscles in ageing-a cytochemical-immunohistochemical study. Mutat. Res. 275 (1992) 115-124
51. Aspnes L.E., Lee C.M., Weindruch R., Chung S.S., Roecker E.B., and Aiken J.M. Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle. FASEB J. 11 (1997) 573-581
52. Lee C.M., Lopez M.E., Weindruch R., and Aiken J.M. Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radic. Biol. Med. 25 (1998) 964-972
53. Cao Z., Wanagat J., McKiernan S.H., and Aiken J.M. Mitochondrial DNA deletion mutations are concomitant with ragged red regions of individual, aged muscle fibers: analysis by laser-capture microdissection. Nucleic Acids Res. 29 (2001) 4502-4508
54. Conley K.E., Marcinek D.J., and Villarin J. Mitochondrial dysfunction and age. Curr. Opin. Clin. Nutr. Metab. Care 10 (2007) 688-692
55. Zahn J.M., Sonu R., Vogel H., Crane E., Mazan-Mamczarz K., Rabkin R., Davis R.W., Becker K.G., Owen A.B., and Kim S.K. Transcriptional profiling of aging in human muscle reveals a common aging signature. PLoS Genet. 2 (2006) e115
56. Reznick R.M., Zong H., Li J., Morino K., Moore I.K., Yu H.J., Liu Z.X., Dong J., Mustard K.J., Hawley S.A., Befroy D., Pypaert M., Hardie D.G., Young L.H., and Shulman G.I. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 5 (2007) 151-156
57. R. Anderson and T. Prolla, PGC-1alpha in aging and anti-aging interventions, Biochim. Biophys. Acta (2009). doi:10.1016/j.bbagen.2009.04.005.
58. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., and Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 (1999) 115-124
59. Brunk U.T., and Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem. 269 (2002) 1996-2002
60. Levine B., and Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 (2004) 463-477
61. Dirks A.J., Hofer T., Marzetti E., Pahor M., and Leeuwenburgh C. Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle. Ageing Res. Rev. 5 (2006) 179-195
62. Gonzalvez F., and Gottlieb E. Cardiolipin: setting the beat of apoptosis. Apoptosis 12 (2007) 877-885
63. Paradies G., Petrosillo G., Pistolese M., and Ruggiero F.M. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286 (2002) 135-141
64. Petrosillo G., Ruggiero F.M., Di Venosa N., and Paradies G. Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J. 17 (2003) 714-716
65. Shidoji Y., Hayashi K., Komura S., Ohishi N., and Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem. Biophys. Res. Commun. 264 (1999) 343-347
66. Petrosillo G., Ruggiero F.M., and Paradies G. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J. 17 (2003) 2202-2208
67. O'Leary M.F., and Hood D.A. Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle. J. Appl. Physiol. 105 (2008) 114-120
68. Yajid F., Mercier J.G., Mercier B.M., Dubouchaud H., and Prefaut C. Effects of 4 wk of hindlimb suspension on skeletal muscle mitochondrial respiration in rats. J. Appl. Physiol. 84 (1998) 479-485
69. Oishi Y., Ogata T., Yamamoto K.I., Terada M., Ohira T., Ohira Y., Taniguchi K., and Roy R.R. Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiol. (Oxf) 192 (2008) 381-395
70. Lawler J.M., Song W., and Demaree S.R. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic. Biol. Med. 35 (2003) 9-16
71. Liu M.J., Li J.X., Lee K.M., Qin L., and Chan K.M. Oxidative stress after muscle damage from immobilization and remobilization occurs locally and systemically. Clin. Orthop. Relat. Res (2005) 246-250
72. Servais S., Letexier D., Favier R., Duchamp C., and Desplanches D. Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis?. Free Radic. Biol. Med. 42 (2007) 627-635
73. Siu P.M., Pistilli E.E., and Alway S.E. Age-dependent increase in oxidative stress in gastrocnemius muscle with unloading. J. Appl. Physiol. 105 (2008) 1695-1705
74. Hofer T., Marzetti E., Xu J., Seo A.Y., Gulec S., Knutson M.D., Leeuwenburgh C., and Dupont-Versteegden E.E. Increased iron content and RNA oxidative damage in skeletal muscle with aging and disuse atrophy. Exp. Gerontol. 43 (2008) 563-570
75. Powers S.K., Kavazis A.N., and McClung J.M. Oxidative stress and disuse muscle atrophy. J. Appl. Physiol. 102 (2007) 2389-2397
76. Chua A.C., Graham R.M., Trinder D., and Olynyk J.K. The regulation of cellular iron metabolism. Crit. Rev. Clin. Lab. Sci. 44 (2007) 413-459
77. S. Levi and E .Rovida, The role of iron in mitochondrial function, Biochim. Biophys. Acta (2008). doi:10.1016/j.bbagen.2008.09.008.
78. Atamna H., Walter P.B., and Ames B.N. The role of heme and iron-sulfur clusters in mitochondrial biogenesis, maintenance, and decay with age. Arch. Biochem. Biophys. 397 (2002) 345-353
79. Ames B.N., and Liu J. Delaying the mitochondrial decay of aging with acetylcarnitine. Ann. N.Y. Acad. Sci. 1033 (2004) 108-116
80. Vasquez-Vivar J., Kalyanaraman B., and Kennedy M.C. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J. Biol. Chem. 275 (2000) 14064-14069
81. Kondo H., Miura M., Kodama J., Ahmed S.M., and Itokawa Y. Role of iron in oxidative stress in skeletal muscle atrophied by immobilization. Pflugers Arch. 421 (1992) 295-297
82. Altun M., Edstrom E., Spooner E., Flores-Moralez A., Bergman E., Tollet-Egnell P., Norstedt G., Kessler B.M., and Ulfhake B. Iron load and redox stress in skeletal muscle of aged rats. Muscle Nerve 36 (2007) 223-233
83. Xu J., Knutson M.D., Carter C.S., and Leeuwenburgh C. Iron accumulation with age, oxidative stress and functional decline. PLoS ONE 3 (2008) e2865
84. Jung S.H., DeRuisseau L.R., Kavazis A.N., and Deruisseau K.C. Plantaris muscle of aged rats demonstrates iron accumulation and altered expression of iron regulation proteins. Exp. Physiol. 93 (2008) 407-414
85. Marzetti E., Lees H.A., Wohlgemuth S.E., and Leeuwenburgh C. Sarcopenia of aging: underlying cellular mechanisms and protection by calorie restriction. BioFactors 35 (2009) 28-35
86. Liang L.P., Jarrett S.G., and Patel M. Chelation of mitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury. J. Neurosci. 28 (2008) 11550-11556
87. Kakhlon O., Manning H., Breuer W., Melamed-Book N., Lu C., Cortopassi G., Munnich A., and Cabantchik Z.I. Cell functions impaired by frataxin deficiency are restored by drug-mediated iron relocation. Blood 112 (2008) 5219-5227
88. Whitnall M., Rahmanto Y.S., Sutak R., Xu X., Becker E.M., Mikhael M.R., Ponka P., and Richardson D.R. The MCK mouse heart model of Friedreich's ataxia: alterations in iron-regulated proteins and cardiac hypertrophy are limited by iron chelation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 9757-9762
89. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
90. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
91. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
92. Wang Z.B., Liu Y.Q., and Cui Y.F. Pathways to caspase activation. Cell Biol. Int. 29 (2005) 489-496
93. Nakagawa T., and Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150 (2000) 887-894
94. van Loo G., Saelens X., van Gurp M., MacFarlane M., Martin S.J., and Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9 (2002) 1031-1042
95. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schagger H., Rustin P., and Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23 (2004) 4679-4689
96. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S.A., Zamzami N., and Kroemer G. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 476 (2000) 118-123
97. Cande C., Vahsen N., Kouranti I., Schmitt E., Daugas E., Spahr C., Luban J., Kroemer R.T., Giordanetto F., Garrido C., Penninger J.M., and Kroemer G. AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis. Oncogene 23 (2004) 1514-1521
98. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y., Sasaki T., Elia A.J., Cheng H.Y., Ravagnan L., Ferri K.F., Zamzami N., Wakeham A., Hakem R., Yoshida H., Kong Y.Y., Mak T.W., Zuniga-Pflucker J.C., Kroemer G., and Penninger J.M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410 (2001) 549-554
99. Huang K.J., Ku C.C., and Lehman I.R. Endonuclease G: a role for the enzyme in recombination and cellular proliferation. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8995-9000
100. Li L.Y., Luo X., and Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412 (2001) 95-99
101. van Loo G., Schotte P., van Gurp M., Demol H., Hoorelbeke B., Gevaert K., Rodriguez I., Ruiz-Carrillo A., Vandekerckhove J., Declercq W., Beyaert R., and Vandenabeele P. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ. 8 (2001) 1136-1142
102. Chipuk J.E., Bouchier-Hayes L., and Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13 (2006) 1396-1402
103. Gogvadze V., Orrenius S., and Zhivotovsky B. Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim. Biophys. Acta 1757 (2006) 639-647
104. Chao D.T., and Korsmeyer S.J. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 16 (1998) 395-419
105. Antonsson B., Conti F., Ciavatta A., Montessuit S., Lewis S., Martinou I., Bernasconi L., Bernard A., Mermod J.J., Mazzei G., Maundrell K., Gambale F., Sadoul R., and Martinou J.C. Inhibition of Bax channel-forming activity by Bcl-2. Science 277 (1997) 370-372
106. van Delft M.F., and Huang D.C. How the Bcl-2 family of proteins interact to regulate apoptosis. Cell Res. 16 (2006) 203-213
107. Zhou L., and Chang D.C. Dynamics and structure of the Bax-Bak complex responsible for releasing mitochondrial proteins during apoptosis. J. Cell Sci. 121 (2008) 2186-2196
108. Kinnally K.W., and Antonsson B. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 12 (2007) 857-868
109. Chipuk J.E., and Green D.R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?. Trends Cell Biol. 18 (2008) 157-164
110. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
111. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 Pt. 2 (1999) 233-249
112. Crompton M., Virji S., and Ward J.M. Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem. 258 (1998) 729-735
113. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., and Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427 (2004) 461-465
114. Baines C.P., Kaiser R.A., Sheiko T., Craigen W.J., and Molkentin J.D. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 9 (2007) 550-555
115. Zamzami N., El Hamel C., Maisse C., Brenner C., Munoz-Pinedo C., Belzacq A.S., Costantini P., Vieira H., Loeffler M., Molle G., and Kroemer G. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 19 (2000) 6342-6350
116. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., and Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
117. Tsujimoto Y., and Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12 (2007) 835-840
118. Rajesh K.G., Sasaguri S., Suzuki R., and Maeda H. Antioxidant MCI-186 inhibits mitochondrial permeability transition pore and upregulates Bcl-2 expression. Am. J. Physiol., Heart Circ. Physiol. 285 (2003) H2171-H2178
119. Marriott H.M., Ali F., Read R.C., Mitchell T.J., Whyte M.K., and Dockrell D.H. Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J. 18 (2004) 1126-1128
120. Mishra O.P., Randis T., Ashraf Q.M., and Delivoria-Papadopoulos M. Hypoxia-induced Bax and Bcl-2 protein expression, caspase-9 activation, DNA fragmentation, and lipid peroxidation in mitochondria of the cerebral cortex of newborn piglets: the role of nitric oxide. Neuroscience 141 (2006) 1339-1349
121. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost M.C., Xie Z., Matsuyama S., Reed J.C., and Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281 (1998) 2027-2031
122. Zamzami N., Brenner C., Marzo I., Susin S.A., and Kroemer G. Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene 16 (1998) 2265-2282
123. Marzetti E., and Leeuwenburgh C. Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp. Gerontol. 41 (2006) 1234-1238
124. Marzetti E., Lawler J.M., Hiona A., Manini T., Seo A.Y., and Leeuwenburgh C. Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic. Biol. Med. 44 (2008) 160-168
125. Alway S.E., Degens H., Krishnamurthy G., and Smith C.A. Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am. J. Physiol., Cell Physiol. 283 (2002) C66-C76
126. Song W., Kwak H.B., and Lawler J.M. Exercise training attenuates age-induced changes in apoptotic signaling in rat skeletal muscle. Antioxid. Redox Signal. 8 (2006) 517-528
127. Pistilli E.E., Siu P.M., and Alway S.E. Molecular regulation of apoptosis in fast plantaris muscles of aged rats. J. Gerontol. A, Biol. Sci. Med. Sci. 61 (2006) 245-255
128. Siu P.M., Pistilli E.E., and Alway S.E. Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats. Am. J. Physiol., Regul. Integr. Comp. Physiol. 289 (2005) R1015-R1026
129. Baker D.J., and Hepple R.T. Elevated caspase and AIF gene expression correlate with progression of sarcopenia during aging in male F344BN rats. Exp. Gerontol. 41 (2006) 1149-1156
130. Rice K.M., and Blough E.R. Sarcopenia-related apoptosis is regulated differently in fast and slow-twitch muscles of the aging F344/N x BN rat model. Mech. Ageing Dev. 127 (2006) 670-679
131. Braga M., Sinha Hikim A.P., Datta S., Ferrini M.G., Brown D., Kovacheva E.L., Gonzalez-Cadavid N.F., and Sinha-Hikim I. Involvement of oxidative stress and caspase 2-mediated intrinsic pathway signaling in age-related increase in muscle cell apoptosis in mice. Apoptosis 13 (2008) 822-832
132. Rajah R., Lee K.W., and Cohen P. Insulin-like growth factor binding protein-3 mediates tumor necrosis factor-alpha-induced apoptosis: role of Bcl-2 phosphorylation. Cell Growth Differ. 13 (2002) 163-171
133. Tamilselvan J., Jayaraman G., Sivarajan K., and Panneerselvam C. Age-dependent upregulation of p53 and cytochrome c release and susceptibility to apoptosis in skeletal muscle fiber of aged rats: role of carnitine and lipoic acid. Free Radic. Biol. Med. 43 (2007) 1656-1669
134. Chung L., and Ng Y.C. Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. Biochim. Biophys. Acta 1762 (2006) 103-109
135. Allen D.L., Linderman J.K., Roy R.R., Bigbee A.J., Grindeland R.E., Mukku V., and Edgerton V.R. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am. J. Physiol. 273 (1997) C579-C587
136. Tews D.S., Behrhof W., and Schindler S. Expression patterns of initiator and effector caspases in denervated human skeletal muscle. Muscle Nerve 31 (2005) 175-181
137. Tews D.S., Behrhof W., and Schindler S. SMAC-expression in denervated human skeletal muscle as a potential inhibitor of coexpressed inhibitor-of-apoptosis proteins. Appl. Immunohistochem. Mol. Morphol. 16 (2008) 66-70
138. Tews D.S., and Goebel H.H. Apoptosis-related proteins in skeletal muscle fibers of spinal muscular atrophy. J. Neuropathol. Exp. Neurol. 56 (1997) 150-156
139. Tews D.S., and Goebel H.H. DNA fragmentation and BCL-2 expression in infantile spinal muscular atrophy. Neuromuscul. Disord. 6 (1996) 265-273
140. Csukly K., Ascah A., Matas J., Gardiner P.F., Fontaine E., and Burelle Y. Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J. Physiol. 574 (2006) 319-327
141. Vazeille E., Codran A., Claustre A., Averous J., Listrat A., Bechet D., Taillandier D., Dardevet D., Attaix D., and Combaret L. The ubiquitin-proteasome and the mitochondria-associated apoptotic pathways are sequentially downregulated during recovery after immobilization-induced muscle atrophy. Am. J. Physiol., Endocrinol. Metab. 295 (2008) E1181-E1190
142. Bruusgaard J.C., and Gundersen K. In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J. Clin. Invest. 118 (2008) 1450-1457
143. Allen D.L., Monke S.R., Talmadge R.J., Roy R.R., and Edgerton V.R. Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J. Appl. Physiol. 78 (1995) 1969-1976