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Increased superoxide in vivo accelerates age‐associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration

dc.contributor.authorJang, Youngmok C.
dc.contributor.authorLustgarten, Michael S.
dc.contributor.authorLiu, Yuhong
dc.contributor.authorMuller, Florian L.
dc.contributor.authorBhattacharya, Arunabh
dc.contributor.authorLiang, Hanyu
dc.contributor.authorSalmon, Adam B.
dc.contributor.authorBrooks, Susan V.
dc.contributor.authorLarkin, Lisa
dc.contributor.authorHayworth, Christopher R.
dc.contributor.authorRichardson, Arlan
dc.contributor.authorVan Remmen, Holly
dc.date.accessioned2020-04-02T18:39:58Z
dc.date.available2020-04-02T18:39:58Z
dc.date.issued2010-05
dc.identifier.citationJang, Youngmok C.; Lustgarten, Michael S.; Liu, Yuhong; Muller, Florian L.; Bhattacharya, Arunabh; Liang, Hanyu; Salmon, Adam B.; Brooks, Susan V.; Larkin, Lisa; Hayworth, Christopher R.; Richardson, Arlan; Van Remmen, Holly (2010). "Increased superoxide in vivo accelerates age‐associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration." The FASEB Journal 24(5): 1376-1390.
dc.identifier.issn0892-6638
dc.identifier.issn1530-6860
dc.identifier.urihttps://hdl.handle.net/2027.42/154668
dc.publisherFederation of American Societies for Experimental Biology
dc.publisherWiley Periodicals, Inc.
dc.subject.othersarcopenia
dc.subject.otherapoptosis
dc.subject.otheroxidative stress
dc.titleIncreased superoxide in vivo accelerates age‐associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelBiology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/154668/1/fsb2fj09146308.pdf
dc.identifier.doi10.1096/fj.09-146308
dc.identifier.sourceThe FASEB Journal
dc.identifier.citedreferenceAnderson, R., and Prolla, T. ( 2009 ) PGC‐1α in aging and anti‐aging interventions. Biochim. Biophys. Acta. 1790, 1059 – 1066
dc.identifier.citedreferenceShefner, J. M., Reaume, A. G., Flood, D. G., Scott, R. W., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Upton‐Rice, M., and Brown, R. H., Jr. ( 1999 ) Mice lacking cytosolic copper/zinc superoxide dismutase display a distinctive motor axonopathy. Neurology 53, 1239 – 1246
dc.identifier.citedreferenceFlood, D. G., Reaume, A. G., Gruner, J. A., Hoffman, E. K., Hirsch, J. D., Lin, Y. G., Dorfman, K. S., and Scott, R. W. ( 1999 ) Hindlimb motor neurons require Cu/Zn superoxide dismutase for maintenance of neuromuscular junctions. Am. J. Pathol. 155, 663 – 672
dc.identifier.citedreferenceFeng, G., Mellor, R. H., Bernstein, M., Keller‐Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., and Sanes, J. R. ( 2000 ) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41 – 51
dc.identifier.citedreferenceKostrominova, T. Y., Pasyk, K. A., Van Remmen, H., Richardson, A. G., and Faulkner, J. A. ( 2006 ) Adaptive changes in structure of skeletal muscles from adult Sod1 homozygous knockout mice. Cell Tissue Res. 327, 595 – 605
dc.identifier.citedreferenceChen, F., Qian, L., Yang, Z. H., Huang, Y., Ngo, S. T., Ruan, N. J., Wang, J., Schneider, C., Noakes, P. G., Ding, Y. Q., Mei, L., and Luo, Z. G. ( 2007 ) Rapsyn interaction with calpain stabilizes AChR clusters at the neuromuscular junction. Neuron 55, 247 – 260
dc.identifier.citedreferenceDobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Bonconpagni, S., Belia, S., Wannenes, F., Nicoletti, C., Del Prete, Z., Rosenthal, N., Molinaro, M., Protasi, F., Fano, G., Sandri, M., and Musaro, A. ( 2008 ) Skeletal muscle is a primary target of SOD1G93A‐mediated toxicity. Cell Metab. 8, 425 – 436
dc.identifier.citedreferenceLee, H. C., and Wei, Y. H. ( 2005 ) Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int. J. Biochem. Cell Biol. 37, 822 – 834
dc.identifier.citedreferenceSt‐Pierre, J., Drori, S., Uldry, M., Silvaggi, J. M., Rhee, J., Jager, S., Handschin, C., Zheng, K., Lin, J., Yang, W., Simon, D. K., Bachoo, R., and Spiegelman, B. M. ( 2006 ) Suppression of reactive oxygen species and neurodegeneration by the PGC‐1 transcriptional coactivators. Cell 127, 397 – 408
dc.identifier.citedreferenceTerman, A., and Brunk, U. T. ( 2006 ) Oxidative stress, accumulation of biological ‘garbage’, and aging. Antioxid. Redox Signal. 8, 197 – 204
dc.identifier.citedreferenceTerman, A., Gustafsson, B., and Brunk, U. T. ( 2006 ) The lysosomal‐mitochondrial axis theory of postmitotic aging and cell death. Chem. Biol. Interact. 163, 29 – 37
dc.identifier.citedreferenceLyons, C. N., Mathieu‐Costello, O., and Moyes, C. D. ( 2006 ) Regulation of skeletal muscle mitochondrial content during aging. J. Gerontol. A Biol. Sci. Med. Sci. 61, 3 – 13
dc.identifier.citedreferenceWenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M., and Moraes, C. T. ( 2009 ) Increased muscle PGC‐1α expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. U. S. A. 106, 20405 – 20410
dc.identifier.citedreferencePotthoff, M. J., Olson, E. N., and Bassel‐Duby, R. ( 2007 ) Skeletal muscle remodeling. Curr. Opin. Rheumatol. 19, 542 – 549
dc.identifier.citedreferenceCohen, T. J., Barrientos, T., Hartman, Z. C., Garvey, S. M., Cox, G. A., and Yao, T. P. ( 2009 ) The deacetylase HDAC4 controls myocyte enhancing factor‐2‐dependent structural gene expression in response to neural activity. FASEB J. 23, 99 – 106
dc.identifier.citedreferenceSiu, P. M., Pistilli, E. E., and Alway, S. E. ( 2005 ) Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1015 – R1026
dc.identifier.citedreferenceAdhihetty, P. J., O’Leary, M. F., Chabi, B., Wicks, K. L., and Hood, D. A. ( 2007 ) Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J. Appl. Physiol. 102, 1143 – 1151
dc.identifier.citedreferenceBruusgaard, J. C., Liestol, K., and Gundersen, K. ( 2006 ) Distribution of myonuclei and microtubules in live muscle fibers of young, middle‐aged, and old mice. J. Appl. Physiol. 100, 2024 – 2030
dc.identifier.citedreferenceBrack, A. S., Bildsoe, H., and Hughes, S. M. ( 2005 ) Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age‐related muscle atrophy. J. Cell Sci. 118, 4813 – 4821
dc.identifier.citedreferenceScherz‐Shouval, R., and Elazar, Z. ( 2007 ) ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 17, 422 – 427
dc.identifier.citedreferenceLi, Y. P., Chen, Y., Li, A. S., and Reid, M. B. ( 2003 ) Hydrogen peroxide stimulates ubiquitin‐conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am. J. Physiol. Cell Physiol. 285, C806 – C812
dc.identifier.citedreferenceGiniatullin, A. R., Darios, F., Shakirzyanova, A., Davletov, B., and Giniatullin, R. ( 2006 ) SNAP25 is a pre‐synaptic target for the depressant action of reactive oxygen species on transmitter release. J. Neurochem. 98, 1789 – 1797
dc.identifier.citedreferenceBrookes, P. S., Yoon, Y., Robotham, J. L., Anders, M. W., and Sheu, S. S. ( 2004 ) Calcium, ATP, and ROS: a mitochondrial love‐hate triangle. Am. J. Physiol. Cell Physiol. 287, C817 – C833
dc.identifier.citedreferenceGiorgi, C., Romagnoli, A., Pinton, P., and Rizzuto, R. ( 2008 ) Ca 2+ signaling, mitochondria and cell death. Curr. Mol. Med. 8, 119 – 130
dc.identifier.citedreferenceCsukly, K., Ascah, A., Matas, J., Gardiner, P. F., Fontaine, E., and Burelle, Y. ( 2006 ) Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J. Physiol. 574, 319 – 327
dc.identifier.citedreferenceGrady, R. M., Starr, D. A., Ackerman, G. L., Sanes, J. R., and Han, M. ( 2005 ) Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl. Acad. Sci. U. S. A. 102, 4359 – 4364
dc.identifier.citedreferenceConboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., and Rando, T. A. ( 2005 ) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760 – 764
dc.identifier.citedreferenceBrack, A. S., Conboy, M. J., Roy, S., Lee, M., Kuo, C. J., Keller, C., and Rando, T. A. ( 2007 ) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807 – 810
dc.identifier.citedreferenceJejurikar, S. S., Marcelo, C. L., and Kuzon, W. M., Jr. ( 2002 ) Skeletal muscle denervation increases satellite cell susceptibility to apoptosis. Plast. Reconstr. Surg. 110, 160 – 168
dc.identifier.citedreferenceBruusgaard, J. C., and Gundersen, K. ( 2008 ) In vivo time‐lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J. Clin. Invest. 118, 1450 – 1457
dc.identifier.citedreferenceMansouri, A., Muller, F. L., Liu, Y., Ng, R., Faulkner, J., Hamilton, M., Richardson, A., Huang, T. T., Epstein, C. J., and Van Remmen, H. ( 2006 ) Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind‐limb skeletal muscle during aging. Mech. Ageing Dev. 127, 298 – 306
dc.identifier.citedreferenceMoylan, J. S., and Reid, M. B. ( 2007 ) Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35, 411 – 429
dc.identifier.citedreferenceChoksi, K. B., Nuss, J. E., Deford, J. H., and Papaconstantinou, J. ( 2008 ) Age‐related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes. Free Radic. Biol. Med. 45, 826 – 838
dc.identifier.citedreferenceFigueiredo, P. A., Powers, S. K., Ferreira, R. M., Appell, H. J., and Duarte, J. A. ( 2009 ) Aging impairs skeletal muscle mitochondrial bioenergetic function. J. Gerontol. A Biol. Sci. Med. Sci. 64, 21 – 33
dc.identifier.citedreferenceLexell, J., Taylor, C. C., and Sjostrom, M. ( 1988 ) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15‐ to 83‐year‐old men. J. Neurol. Sci. 84, 275 – 294
dc.identifier.citedreferenceDupont‐Versteegden, E. E. ( 2005 ) Apoptosis in muscle atrophy: relevance to sarcopenia. Exp. Gerontol. 40, 473 – 481
dc.identifier.citedreferenceDirks, 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
dc.identifier.citedreferenceBrooks, S. V., and Faulkner, J. A. ( 1994 ) Skeletal muscle weakness in old age: underlying mechanisms. Med. Sci. Sports. Exerc. 26, 432 – 439
dc.identifier.citedreferenceCederna, P. S., Asato, H., Gu, X., van der Meulen, J., Kuzon, W. M., Jr., Carlson, B. M., and Faulkner, J. A. ( 2001 ) Motor unit properties of nerve‐intact extensor digitorum longus muscle grafts in young and old rats. J. Gerontol. A Biol. Sci. Med. Sci. 56, B254 – B258
dc.identifier.citedreferenceBalice‐Gordon, R. J. ( 1997 ) Age‐related changes in neuromuscular innervation. Muscle Nerve Suppl. 5, S83 – S87
dc.identifier.citedreferenceLysakowski, A., Figueras, H., Price, S. D., and Peng, Y. Y. ( 1999 ) Dense‐cored vesicles, smooth endoplasmic reticulum, and mitochondria are closely associated with non‐specialized parts of plasma membrane of nerve terminals: implications for exocytosis and calcium buffering by intraterminal organelles. J. Comp. Neurol. 403, 378 – 390
dc.identifier.citedreferenceDupuis, L., Gonzalez de Aguilar, J. L., Echaniz‐Laguna, A., Eschbach, J., Rene, F., Oudart, H., Halter, B., Huze, C., Schaeffer, L., Bouillaud, F., and Loeffler, J. P. ( 2009 ) Muscle mitochondrial uncoupling dismantles neuromuscular junction and triggers distal degeneration of motor neurons. PLoS One 4, e5390
dc.identifier.citedreferenceMuller, F. L., Song, W., Jang, Y., Liu, Y., Sabia, M., Richardson, A., and Van Remmen, H. ( 2007 ) Denervation‐induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am. J. Physiol. 293, R1159 – R1168
dc.identifier.citedreferenceElchuri, S., Oberley, T. D., Qi, W., Eisenstein, R. S., Jackson Roberts, L., Van Remmen, H., Epstein, C. J., and Huang, T. T. ( 2005 ) CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24, 367 – 380
dc.identifier.citedreferenceMuller, F., Song, W., Liu, Y. H., Qi, W. B., Strong, R., Roberts, L. J., Chaudhuri, A., Faulkner, J., Huang, T. T., Epstein, C., Richardson, A., and Van Remmen, H. ( 2005 ) Absence of Cu, Zn‐Sod causes severe oxidative stress and acceleration of age‐dependent skeletal muscle atrophy. Free Rad. Biol. Med. 39, S127 – S127
dc.identifier.citedreferenceBhattacharya, A., Muller, F. L., Liu, Y., Sabia, M., Liang, H., Song, W., Jang, Y. C., Ran, Q., and Van Remmen, H. ( 2009 ) Denervation induces cytosolic phospholipase A2‐mediated fatty acid hydroperoxide generation by muscle mitochondria. J. Biol. Chem. 284, 46 – 55
dc.identifier.citedreferenceMuller, F. L., Liu, Y., and Van Remmen, H. ( 2004 ) Complex III Releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 279, 49064 – 49073
dc.identifier.citedreferencePagliari, L. J., Kuwana, T., Bonzon, C., Newmeyer, D. D., Tu, S., Beere, H. M., and Green, D. R. ( 2005 ) The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc. Natl. Acad. Sci. U. S. A. 102, 17975 – 17980
dc.identifier.citedreferenceNewmeyer, D. D., Farschon, D. M., and Reed, J. C. ( 1994 ) Cell‐free apoptosis in Xenopus egg extracts: inhibition by Bcl‐2 and requirement for an organelle fraction enriched in mitochondria. Cell 79, 353 – 364
dc.identifier.citedreferenceSaelim, N., Holstein, D., Chocron, E. S., Camacho, P., and Lechleiter, J. D. ( 2007 ) Inhibition of apoptotic potency by ligand stimulated thyroid hormone receptors located in mitochondria. Apoptosis 12, 1781 – 1794
dc.identifier.citedreferenceWada, K. I., Katsuta, S., and Soya, H. ( 2003 ) Natural occurrence of myofiber cytoplasmic enlargement accompanied by decrease in myonuclear number. Jpn. J. Physiol. 53, 145 – 150
dc.identifier.citedreferenceWada, K. I., Takahashi, H., Katsuta, S., and Soya, H. ( 2002 ) No decrease in myonuclear number after long‐term denervation in mature mice. Am. J. Physiol. Cell Physiol. 283, C484 – C488
dc.identifier.citedreferenceSchaefer, A. M., Sanes, J. R., and Lichtman, J. W. ( 2005 ) A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J. Comp. Neurol. 490, 209 – 219
dc.identifier.citedreferenceBurkholder, T. J., Fingado, B., Baron, S., and Lieber, R. L. ( 1994 ) Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J. Morphol. 221, 177 – 190
dc.identifier.citedreferenceOkado‐Matsumoto, A., and Fridovich, I. ( 2001 ) Subcellular distribution of superoxide dismutases (SOD) in rat liver Cu, Zn‐SOD in mitochondria. J. Biol. Chem. 276, 38388 – 38393
dc.identifier.citedreferencePowers, S. K., and Jackson, M. J. ( 2008 ) Exercise‐induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243 – 1276
dc.identifier.citedreferenceKagan, V. E., Borisenko, G. G., Tyurina, Y. Y., Tyurin, V. A., Jiang, J., Potapovich, A. I., Kini, V., Amoscato, A. A., and Fujii, Y. ( 2004 ) Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 37, 1963 – 1985
dc.identifier.citedreferenceAllen, D. L., Roy, R. R., and Edgerton, V. R. ( 1999 ) Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22, 1350 – 1360
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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