Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome

Amthor, 2009, Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity, Proceedings of the National Academy of Sciences of the United States of America, 106, 7479, 10.1073/pnas.0811129106

Andres-Mateos, 2013, Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy, EMBO Molecular Medicine, 5, 80, 10.1002/emmm.201201443

Arndt, 2010, Chaperone-assisted selective autophagy is essential for muscle maintenance, Current Biology, 20, 143, 10.1016/j.cub.2009.11.022

Baehr, 2011, Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids, Journal of Physiology, 589, 4759, 10.1113/jphysiol.2011.212845

Bdolah, 2007, Atrophy-related ubiquitin ligases atrogin-1 and MuRF-1 are associated with uterine smooth muscle involution in the postpartum period, American Journal of Physiology: Regulatory Integrative and Comparative Physiology, 292, R971

Bechet, 2005, Lysosomal proteolysis in skeletal muscle, International Journal of Biochemistry & Cell Biology, 37, 2098, 10.1016/j.biocel.2005.02.029

Bello, 2009, The E3 ubiquitin ligase specificity subunit ASB2beta is a novel regulator of muscle differentiation that targets filamin B to proteasomal degradation, Cell Death and Differentiation, 16, 921, 10.1038/cdd.2009.27

Bentzinger, 2013, Differential response of skeletal muscles to mTORC1 signaling during atrophy and hypertrophy, Skeletal Muscle, 3, 6, 10.1186/2044-5040-3-6

Blaauw, 2009, Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation, FASEB Journal, 23, 3896, 10.1096/fj.09-131870

Bodine, 2001, Identification of ubiquitin ligases required for skeletal muscle atrophy, Science, 294, 1704, 10.1126/science.1065874

Bonaldo, 2013, Cellular and molecular mechanisms of muscle atrophy, Disease Models & Mechanisms, 6, 25, 10.1242/dmm.010389

Bothe, 2000, Selective expression of Cre recombinase in skeletal muscle fibers, Genesis, 26, 165, 10.1002/(SICI)1526-968X(200002)26:2<165::AID-GENE22>3.0.CO;2-F

Brault, 2010, Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy, Journal of Biological Chemistry, 285, 19460, 10.1074/jbc.M110.113092

Brocca, 2012, The time course of the adaptations of human muscle proteome to bed rest and the underlying mechanisms, Journal of Physiology, 590, 5211, 10.1113/jphysiol.2012.240267

Brunet, 2001, Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a), Molecular and Cellular Biology, 21, 952, 10.1128/MCB.21.3.952-965.2001

Calnan, 2008, The FoxO code, Oncogene, 27, 2276, 10.1038/onc.2008.21

Caron, 2011, The proteasome inhibitor MG132 reduces immobilization-induced skeletal muscle atrophy in mice, BMC Musculoskeletal Disorders, 12, 185, 10.1186/1471-2474-12-185

Chang, 2012, Bcl-2-associated autophagy regulator Naf-1 required for maintenance of skeletal muscle, Human Molecular Genetics, 21, 2277, 10.1093/hmg/dds048

Clarke, 2007, The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle, Cell Metabolism, 6, 376, 10.1016/j.cmet.2007.09.009

Cohen, 2009, During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation, Journal of Cell Biology, 185, 1083, 10.1083/jcb.200901052

Cohen, 2012, Ubiquitylation by Trim32 causes coupled loss of desmin Z-bands, and thin filaments in muscle atrophy, Journal of Cell Biology, 198, 575, 10.1083/jcb.201110067

Combaret, 2005, USP19 is a ubiquitin-specific protease regulated in rat skeletal muscle during catabolic states, American Journal of Physiology: Endocrinology and Metabolism, 288, E693

Cong, 2011, Inhibition of atrogin-1/MAFbx expression by adenovirus-delivered small hairpin RNAs attenuates muscle atrophy in fasting mice, Human Gene Therapy, 22, 313, 10.1089/hum.2010.057

Csibi, 2010, The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse, PLoS ONE, 5, e8994, 10.1371/journal.pone.0008994

Cullup, 2013, Recessive mutations in EPG5 cause Vici syndrome, a multisystem disorder with defective autophagy, Nature Genetics, 45, 83, 10.1038/ng.2497

Derde, 2012, Early parenteral nutrition evokes a phenotype of autophagy deficiency in liver and skeletal muscle of critically ill rabbits, Endocrinology, 153, 2267, 10.1210/en.2011-2068

Deval, 2001, Identification of cathepsin L as a differentially expressed message associated with skeletal muscle wasting, Biochemical Journal, 360, 143, 10.1042/0264-6021:3600143

Enrico, 2007, Unexpected cardiotoxicity in haematological bortezomib treated patients, British Journal of Haematology, 138, 396, 10.1111/j.1365-2141.2007.06659.x

Fielitz, 2007, Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3, Journal of Clinical Investigation, 117, 2486, 10.1172/JCI32827

Geng, 2011, PGC-1alpha promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice, American Journal of Pathology, 178, 1738, 10.1016/j.ajpath.2011.01.005

Gomes, 2001, Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy, Proceedings of the National Academy of Sciences of United States of America, 98, 14440, 10.1073/pnas.251541198

Grumati, 2010, Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration, Nature Medicine, 16, 1313, 10.1038/nm.2247

Grumati, 2011, Physical exercise stimulates autophagy in normal skeletal muscles but is detrimental for collagen VI-deficient muscles, Autophagy, 7, 1415, 10.4161/auto.7.12.17877

Hanna, 2012, Microtubule-associated protein 1 Light Chain 3 (LC3) interacts with Bnip3 to selectively remove endoplasmic reticulum and mitochondria via autophagy, Journal of Biological Chemistry, 287, 19094, 10.1074/jbc.M111.322933

Hara, 2006, Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice, Nature, 441, 885, 10.1038/nature04724

He, 2012, Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis, Nature, 481, 511, 10.1038/nature10758

Hishiya, 2006, A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy, EMBO Journal, 25, 554, 10.1038/sj.emboj.7600945

Jackson, 2012, Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy, American Journal of Physiology: Cell Physiology, 303, C854, 10.1152/ajpcell.00207.2012

Jamart, 2012, Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise, European Journal of Applied Physiology, 112, 3173, 10.1007/s00421-011-2287-3

Jamart, 2012, Modulation of autophagy and ubiquitin-proteasome pathways during ultra-endurance running, Journal of Applied Physiology, 112, 1529, 10.1152/japplphysiol.00952.2011

Jamart, 2011, Prevention of muscle disuse atrophy by MG132 proteasome inhibitor, Muscle & Nerve, 43, 708, 10.1002/mus.21949

Kedar, 2004, Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I, Proceedings of the National Academy of Sciences of United States of America, 101, 18135, 10.1073/pnas.0404341102

Kim, 2013, Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine, Nature Medicine, 19, 83, 10.1038/nm.3014

Kirkin, 2009, A role for NBR1 in autophagosomal degradation of ubiquitinated substrates, Molecular Cell, 33, 505, 10.1016/j.molcel.2009.01.020

Kline, 2007, Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol, Journal of Applied Physiology, 102, 740, 10.1152/japplphysiol.00873.2006

Komatsu, 2007, Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice, Cell, 131, 1149, 10.1016/j.cell.2007.10.035

Kudryashova, 2012, Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H, Journal of Clinical Investigation, 122, 1764, 10.1172/JCI59581

Kumar, 2012, TWEAK and TRAF6 regulate skeletal muscle atrophy, Current Opinion in Clinical Nutrition and Metabolic Care, 15, 233, 10.1097/MCO.0b013e328351c3fc

Lee, 2012, Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway, Proceedings of the National Academy of Sciences of United States of America, 109, E2353, 10.1073/pnas.1206410109

Li, 2004, Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex, Journal of Clinical Investigation, 114, 1058, 10.1172/JCI200422220

Lokireddy, 2012, Identification of atrogin-1-targeted proteins during the myostatin-induced skeletal muscle wasting, American Journal of Physiology: Cell Physiology, 303, C512, 10.1152/ajpcell.00402.2011

Lokireddy, 2012, The ubiquitin ligase mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli, Cell Metabolism, 16, 613, 10.1016/j.cmet.2012.10.005

Luo, 2013, Chronic resistance training activates autophagy and reduces apoptosis of muscle cells by modulating IGF-1 and its receptors Akt/mTOR and Akt/FOXO3a signaling in aged rats, Experimental Gerontology, 48, 427, 10.1016/j.exger.2013.02.009

Mammucari, 2007, FoxO3 controls autophagy in skeletal muscle in vivo, Cell Metabolism, 6, 458, 10.1016/j.cmet.2007.11.001

Masiero, 2009, Autophagy is required to maintain muscle mass, Cell Metabolism, 10, 507, 10.1016/j.cmet.2009.10.008

McCarthy, 2011, Effective fiber hypertrophy in satellite cell-depleted skeletal muscle, Development, 138, 3657, 10.1242/dev.068858

Mieulet, 2007, S6 kinase inactivation impairs growth and translational target phosphorylation in muscle cells maintaining proper regulation of protein turnover, American Journal of Physiology: Cell Physiology, 293, C712, 10.1152/ajpcell.00499.2006

Minetti, 2011, Galphai2 signaling promotes skeletal muscle hypertrophy, myoblast differentiation, and muscle regeneration, Science Signaling, 4, ra80, 10.1126/scisignal.2002038

Mizushima, 2011, Autophagy: renovation of cells and tissues, Cell, 147, 728, 10.1016/j.cell.2011.10.026

Mizushima, 2004, In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker, Molecular Biology of the Cell, 15, 1101, 10.1091/mbc.E03-09-0704

Mofarrahi, 2012, Autophagy and skeletal muscles in sepsis, PLoS ONE, 7, e47265, 10.1371/journal.pone.0047265

Moresi, 2012, Histone deacetylases 1 and 2 regulate autophagy flux and skeletal muscle homeostasis in mice, Proceedings of the National Academy of Sciences of United States of America, 109, 1649, 10.1073/pnas.1121159109

Moresi, 2010, Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases, Cell, 143, 35, 10.1016/j.cell.2010.09.004

Nagpal, 2012, The ubiquitin ligase nedd4-1 participates in denervation-induced skeletal muscle atrophy in mice, PLoS ONE, 7, e46427, 10.1371/journal.pone.0046427

Narendra, 2011, Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control, Antioxidants & Redox Signaling, 14, 1929, 10.1089/ars.2010.3799

Nascimbeni, 2012, Impaired autophagy contributes to muscle atrophy in glycogen storage disease type II patients, Autophagy, 8, 1697, 10.4161/auto.21691

Nascimbeni, 2012, The role of autophagy in the pathogenesis of glycogen storage disease type II (GSDII), Cell Death and Differentiation, 19, 1698, 10.1038/cdd.2012.52

Nemazanyy, 2013, Defects of Vps15 in skeletal muscles lead to autophagic vacuolar myopathy and lysosomal disease, EMBO Molecular Medicine, 30

Novak, 2010, Nix is a selective autophagy receptor for mitochondrial clearance, EMBO Reports, 11, 45, 10.1038/embor.2009.256

O’Leary, 2012, Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals, American Journal of Physiology: Cell Physiology, 303, C447, 10.1152/ajpcell.00451.2011

O’Leary, 2013, Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle, American Journal of Physiology: Cell Physiology, 304, C422, 10.1152/ajpcell.00240.2012

Pankiv, 2007, p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy, Journal of Biological Chemistry, 282, 24131, 10.1074/jbc.M702824200

Paul, 2012, The E3 ubiquitin ligase TRAF6 intercedes in starvation-induced skeletal muscle atrophy through multiple mechanisms, Molecular and Cellular Biology, 32, 1248, 10.1128/MCB.06351-11

Paul, 2010, Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice, Journal of Cell Biology, 191, 1395, 10.1083/jcb.201006098

Penna, 2013, Autophagic degradation contributes to muscle wasting in cancer cachexia, American Journal of Pathology, 182, 1367, 10.1016/j.ajpath.2012.12.023

Piccirillo, 2012, The p97/VCP ATPase is critical in muscle atrophy and the accelerated degradation of muscle proteins, EMBO Journal, 31, 3334, 10.1038/emboj.2012.178

Polge, 2011, Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1, FASEB Journal, 25, 3790, 10.1096/fj.11-180968

Porporato, 2013, Acylated and unacylated ghrelin impair skeletal muscle atrophy in mice, Journal of Clinical Investigations, 123, 611

Puigserver, 2003, Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction, Nature, 423, 550, 10.1038/nature01667

Qiu, 2012, Hyperammonemia-mediated autophagy in skeletal muscle contributes to sarcopenia of cirrhosis, American Journal of Physiology: Endocrinology and Metabolism, 303, E983

Quy, 2013, Proteasome-dependent activation of mammalian target of rapamycin complex 1 (mTORC1) is essential for autophagy suppression and muscle remodeling following denervation, Journal of Biological Chemistry, 288, 1125, 10.1074/jbc.M112.399949

Raben, 2008, Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease, Human Molecular Genetics, 17, 3897, 10.1093/hmg/ddn292

Raffaello, 2010, JunB transcription factor maintains skeletal muscle mass and promotes hypertrophy, Journal of Cell Biology, 191, 101, 10.1083/jcb.201001136

Romanello, 2010, Mitochondrial fission and remodelling contributes to muscle atrophy, EMBO Journal, 29, 1774, 10.1038/emboj.2010.60

Romanello, 2010, Mitochondrial biogenesis and fragmentation as regulators of muscle protein degradation, Current Hypertension Reports, 12, 433, 10.1007/s11906-010-0157-8

Romanello, 2013, Mitochondrial biogenesis and fragmentation as regulators of protein degradation in striated muscles, Journal of Molecular and Cellular Cardiology, 55, 64, 10.1016/j.yjmcc.2012.08.001

Ruas, 2012, A PGC-1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy, Cell, 151, 1319, 10.1016/j.cell.2012.10.050

Sandri, 2010, Autophagy in skeletal muscle, FEBS Letters, 584, 1411, 10.1016/j.febslet.2010.01.056

Sandri, 2006, PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription, Proceedings of the National Academy of Sciences of United States of America, 103, 16260, 10.1073/pnas.0607795103

Sarraf, 2013, Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization, Nature, 496, 372, 10.1038/nature12043

Settembre, 2011, TFEB links autophagy to lysosomal biogenesis, Science, 332, 1429, 10.1126/science.1204592

Settembre, 2012, A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB, EMBO Journal, 31, 1095, 10.1038/emboj.2012.32

Shi, 2011, The SCF-Fbxo40 complex induces IRS1 ubiquitination in skeletal muscle, limiting IGF1 signaling, Developmental Cell, 21, 835, 10.1016/j.devcel.2011.09.011

Smuder, 2011, Exercise protects against doxorubicin-induced oxidative stress and proteolysis in skeletal muscle, Journal of Applied Physiology, 110, 935, 10.1152/japplphysiol.00677.2010

Sundaram, 2009, USP19-deubiquitinating enzyme regulates levels of major myofibrillar proteins in L6 muscle cells, American Journal of Physiology: Endocrinology and Metabolism, 297, E1283

Supinski, 2009, Effect of proteasome inhibitors on endotoxin-induced diaphragm dysfunction, American Journal of Physiology: Lung Cell Molecular Physiology, 296, L994

Tassa, 2003, III phosphoinositide 3-kinase–Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes, Biochemical Journal, 376, 577, 10.1042/bj20030826

Tian, 2010, C. elegans screen identifies autophagy genes specific to multicellular organisms, Cell, 141, 1042, 10.1016/j.cell.2010.04.034

Tintignac, 2005, Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase, Journal of Biological Chemistry, 280, 2847, 10.1074/jbc.M411346200

Wenz, 2009, Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging, Proceedings of the National Academy of Sciences of United States of America, 106, 20405, 10.1073/pnas.0911570106

White, 2010, Dynamics of muscle fibre growth during postnatal mouse development, BMC Developmental Biology, 10, 21, 10.1186/1471-213X-10-21

Wohlgemuth, 2010, Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise, Experimental Gerontology, 45, 138, 10.1016/j.exger.2009.11.002

Wu, 1999, Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1, Cell, 98, 115, 10.1016/S0092-8674(00)80611-X

Youle, 2011, Mechanisms of mitophagy, Nature Reviews Molecular Cell Biology, 12, 9, 10.1038/nrm3028

Zhao, 2013, Mice deficient in Epg5 exhibit selective neuronal vulnerability to degeneration, Journal of Cell Biology, 200, 731, 10.1083/jcb.201211014

Zhao, 2007, FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells, Cell Metabolism, 6, 472, 10.1016/j.cmet.2007.11.004

Ziviani, 2010, Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin, Proceedings of the National Academy of Sciences of United States of America, 107, 5018, 10.1073/pnas.0913485107

Zoncu, 2011, mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase, Science, 334, 678, 10.1126/science.1207056