Autophagy is not required to sustain exercise and PRKAA1/AMPK activity but is important to prevent mitochondrial damage during physical activity

Autophagy

Volumn 10, Issue 11, 2014, Pages 1883-1894

  Lo Verso, Francesca ^a,b   Carnio, Silvia ^a   Vainshtein, Anna ^c   Sandri, Marco ^a,b,d,e  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c YORK UNIVERSITY   (Canada)

^d CNR   (Italy)

^e TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

Author keywords

AMPK; Autophagy; Exercise; Metabolism; Mitochondria; Skeletal muscle

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENYLATE KINASE; AUTOPHAGY PROTEIN 7; PROTEIN; PROTEIN KINASE AMP ACTIVATED ALPHA 1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; AMPK ALPHA1 SUBUNIT, MOUSE; ANTIOXIDANT; ATG7 PROTEIN, MOUSE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ECCENTRIC MUSCLE CONTRACTION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SUBUNIT; EXERCISE; FEMALE; MALE; MITOCHONDRION; MOUSE; MUSCLE CONTRACTION; MUSCLE INJURY; NONHUMAN; OXIDATIVE STRESS; PHYSICAL ACTIVITY; PHYSICAL PERFORMANCE; SEX DIFFERENCE; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; ANIMAL; CHEMISTRY; GENETICS; HOMEOSTASIS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; AUTOPHAGY; FEMALE; GLUCOSE; HOMEOSTASIS; MALE; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MUSCLE CONTRACTION; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL;

EID: 84919765112     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.32154     Document Type: Article

References (36)

1. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147:728-41; PMID:22078875; http://dx.doi.org/10.1016/j.cell.2011.10.026
2. Zoncu R, Bar-Peled L, Efeyan A., Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(C)-ATPase. Science 2011; 334:678-83; PMID:22053050; http://dx.doi.org/10.1126/science.1207056
3. Liu K, Czaja MJ. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 2013; 20:3-11; PMID:22595754; http://dx.doi.org/10.1038/cdd.2012.63
4. Nascimbeni AC, Fanin M, Masiero E., Angelini C, Sandri M. Impaired autophagy contributes to muscle atrophy in glycogen storage disease type II patients. Autophagy 2012; 8:1697-700; PMID:22940840; http://dx.doi.org/10.4161/auto.21691
5. Nascimbeni AC, Fanin M, Masiero E., Angelini C, Sandri M. The role of autophagy in the pathogenesis of glycogen storage disease type II (GSDII). Cell Death Differ 2012; 19:1698-708; PMID:22595755; http://dx.doi.org/10.1038/cdd.2012.52
6. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
7. Rubinsztein DC., Mariño G, Kroemer G. Autophagy and aging. Cell 2011; 146:682-95; PMID:21884931; http://dx.doi.org/10.1016/j.cell.2011.07.030
8. Mizushima N, Yamamoto A, Matsui M., Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
9. 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 2009; 10:507-15; PMID:19945408; http://dx.doi.org/10.1016/j.cmet.2009.10.008
10. De Palma C., Morisi F, Cheli S., Pambianco S, Cappello V, Vezzoli M., Rovere-Querini P, Moggio M, Ripolone M., Francolini M, et al. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis 2012; 3:e418; PMID:23152054; http://dx.doi.org/10.1038/cddis.2012.159
11. Grumati P, Coletto L, Sabatelli P., Cescon M, Angelin A, Bertaggia E., Blaauw B, Urciuolo A, Tiepolo T., Merlini L, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010; 16:1313-20; PMID:21037586; http://dx.doi.org/10.1038/nm.2247
12. Melov S, Tarnopolsky MA, Beckman K, Felkey K., Hubbard A. Resistance exercise reverses aging in human skeletal muscle. PLoS One 2007; 2:e465; PMID:17520024; http://dx.doi.org/10.1371/journal.pone.0000465
13. Fontana L, Klein S, Holloszy JO. Effects of long-term calorie restriction and endurance exercise on glucose tolerance, insulin action, and adipokine production. Age (Dordr) 2010; 32:97-108; PMID:19904628; http://dx.doi.org/10.1007/s11357-009-9118-z
14. Sandri M, Barberi L, Bijlsma AY, Blaauw B., Dyar KA, Milan G, Mammucari C, Meskers CG, Pallafacchina G., Paoli A, et al. Signalling pathways regulating muscle mass in ageing skeletal muscle: the role of the IGF1-Akt-mTOR-FoxO pathway. Biogerontology 2013; 14:303-23; PMID:23686362; http://dx.doi.org/10.1007/s10522-013-9432-9
15. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B., Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 2013; 280:4294-314; PMID:23517348; http://dx.doi.org/10.1111/febs.12253
16. Coen PM, Jubrias SA, Distefano G, Amati F., Mackey DC, Glynn NW, Manini TM, Wohlgemuth SE, Leeuwenburgh C., Cummings SR, et al. Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol A Biol Sci Med Sci 2013; 68:447-55; PMID:23051977; http://dx.doi.org/10.1093/gerona/gls196
17. Toledo FG, Goodpaster BH. The role of weight loss and exercise in correcting skeletal muscle mitochondrial abnormalities in obesity, diabetes and aging. Mol Cell Endocrinol 2013; 379:30-4; PMID:23792186; http://dx.doi.org/10.1016/j.mce.2013.06.018
18. Safdar A, Bourgeois JM, Ogborn DI, Little JP, Hettinga BP, Akhtar M, Thompson JE, Melov S., Mocellin NJ, Kujoth GC, et al. Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc Natl Acad Sci U S A 2011; 108:4135-40; PMID:21368114; http://dx.doi.org/10.1073/pnas.1019581108
19. Grumati P, Coletto L, Schiavinato A., Castagnaro S, Bertaggia E, Sandri M., Bonaldo P. Physical exercise stimulates autophagy in normal skeletal muscles but is detrimental for collagen VI-deficient muscles. Autophagy 2011; 7:1415-23; PMID:22024752; http://dx.doi.org/10.4161/auto.7.12.17877
20. He C, Bassik MC, Moresi V, Sun K., Wei Y, Zou Z, An Z., Loh J, Fisher J, Sun Q., et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012; 481:511-5; PMID:22258505; http://dx.doi.org/10.1038/nature10758
21. Kim KH, Jeong YT, Oh H, Kim SH, Cho JM, Kim YN, Kim SS, Kim H, Hur KY, Kim HK, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 2013; 19:83-92; PMID:23202295; http://dx.doi.org/10.1038/nm.3014
22. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 2004; 279:22284-93; PMID:14985369; http://dx.doi.org/10.1074/jbc.M312847200
23. Hanson GT, Aggeler R, Oglesbee D., Cannon M, Capaldi RA, Tsien RY, Remington SJ. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 2004; 279:13044-53; PMID:14722062; http://dx.doi.org/10.1074/jbc.M312846200
24. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L., Lewis W, Harrison DG, Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010; 107:106-16; PMID:20448215; http://dx.doi.org/10.1161/CIRCRESAHA.109.214601
25. He C., Sumpter R Jr., Levine B. Exercise induces autophagy in peripheral tissues and in the brain. Autophagy 2012; 8:1548-51; PMID:22892563; http://dx.doi.org/10.4161/auto.21327
26. Masiero E, Sandri M. Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy 2010; 6:307-9; PMID:20104028; http://dx.doi.org/10.4161/auto.6.2.11137
27. Lira VA, Okutsu M, Zhang M., Greene NP, Laker RC, Breen DS, Hoehn KL, Yan Z. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J 2013; 27:4184-93; PMID:23825228; http://dx.doi.org/10.1096/fj.13-228486
28. Ristow M, Zarse K, Oberbach A., Klöting N, Birringer M., Kiehntopf M, Stumvoll M, Kahn CR, Blüher M. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 2009; 106:8665-70; PMID:19433800; http://dx.doi.org/10.1073/pnas.0903485106
29. Sandri M. FOXOphagy path to inducing stress resistance and cell survival. Nat Cell Biol 2012; 14:786-8; PMID:22854812; http://dx.doi.org/10.1038/ncb2550
30. van der Vos KE, Eliasson P, Proikas-Cezanne T, Vervoort SJ, van Boxtel R, Putker M, van Zutphen IJ, Mauthe M., Zellmer S, Pals C, et al. Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat Cell Biol 2012; 14:829-37; PMID:22820375; http://dx.doi.org/10.1038/ncb2536
31. Frezza C, Zheng L, Folger O., Rajagopalan KN, MacKenzie ED, Jerby L, Micaroni M., Chaneton B, Adam J, Hedley A., et al. Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature 2011; 477:225-8; PMID:21849978; http://dx.doi.org/10.1038/nature10363
32. Sciacovelli M, Guzzo G, Morello V., Frezza C, Zheng L, Nannini N., Calabrese F, Laudiero G, Esposito F., Landriscina M, et al. The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase. Cell Metab 2013; 17:988-99; PMID:23747254; http://dx.doi.org/10.1016/j.cmet.2013.04.019
33. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G., Frezza C, Bernard NJ, Kelly B, Foley NH, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 2013; 496:238-42; PMID:23535595; http://dx.doi.org/10.1038/nature11986
34. Sandri M, Sandri C, Gilbert A., Skurk C, Calabria E, Picard A., Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophyrelated ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117:399-412; PMID:15109499; http://dx.doi.org/10.1016/S0092-8674(04)00400-3
35. Romanello V, Guadagnin E, Gomes L., Roder I, Sandri C, Petersen Y., Milan G, Masiero E, Del Piccolo P., Foretz M, et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 2010; 29:1774-85; PMID:20400940; http://dx.doi.org/10.1038/emboj.2010.60
36. Vainshtein A, Kazak L, Hood DA Effects of endurance training on apoptotic susceptibility in striated muscle. J Appl Physiol (1985) 2011; 110:1638-45; PMID:21474699; http://dx.doi.org/10.1152/japplphysiol.00020.20111894