Regulation of skeletal muscle oxidative capacity and muscle mass by SIRT3

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lin, Ligen ^a   Chen, Keyun ^a   Khalek, Waed Abdel ^b   Ward, Jack Lee ^a   Yang, Henry ^a   Chabi, Beatrice ^b   Wrutniak Cabello, Chantal ^b   Tong, Qiang ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Macau University of Science and Technology   (Macao)

^c University of Montpellier   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MUSCLE PROTEIN; MUSCLE PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; SIRTUIN 3; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIMETRY; CONTROLLED STUDY; ENERGY CONSUMPTION; ENERGY EXPENDITURE; ENZYME ACTIVATION; EXERCISE; FEMALE; GENE; LIPID OXIDATION; LUNG GAS EXCHANGE; MALE; MITOCHONDRIAL RESPIRATION; MOTOR COORDINATION; MOUSE; MURF 1 GENE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE METABOLISM; MUSCLE STRENGTH; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RUNNING; SKELETAL MUSCLE; TISSUE SPECIFICITY; TREADMILL; UPREGULATION;

ANIMALS; CITRATE (SI)-SYNTHASE; CREATINE KINASE, MM FORM; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; LIPID METABOLISM; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIA, MUSCLE; MUSCLE STRENGTH; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PHYSICAL EXERTION; SIRTUIN 3; UP-REGULATION;

EID: 84898645256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085636     Document Type: Article

References (71)

1. Fernandes G, Yunis EJ, Good RA (1976) Suppression of adenocarcinoma by the immunological consequences of calorie restriction. Nature 263: 504-507
2. Hansen BC, Bodkin NL (1993) Primary prevention of diabetes mellitus by prevention of obesity in monkeys. Diabetes 42: 1809-1814 (Pubitemid 23346418)
3. Hepple RT, Baker DJ, Kaczor JJ, Krause DJ (2005) Long-term caloric restriction abrogates the age-related decline in skeletal muscle aerobic function. FASEB J 19: 1320-1322 (Pubitemid 41113736)
4. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, et al. (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4: e76
5. McKiernan SH, Colman RJ, Lopez M, Beasley TM, Aiken JM, et al. (2011) Caloric restriction delays aging-induced cellular phenotypes in rhesus monkey skeletal muscle. Exp Gerontol 46: 23-29
6. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, et al. (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27: 8807-8814
7. Shi T, Wang F, Stieren E, Tong Q (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280: 13560-13567 (Pubitemid 40517248)
8. Palacios OM. Carmona JJ, Michan S, Chen KY, Manabe Y, et al. (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1a in skeletal muscle. Aging 1: 771-781
9. Hallows WC, Yu W, Smith BC, Devries MK, Ellinger JJ, et al. (2011) Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol Cell 41: 139-149
10. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464: 121-125
11. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, et al. (2010) SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab 12: 654-661
12. Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci U S A 103: 10224-10229 (Pubitemid 44051148)
13. Hallows WC, Lee S, Denu JM (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci U S A 103: 10230-10235 (Pubitemid 44051149)
14. Ahn BH, Kim HS, Song S, Lee IH, Liu J, et al. (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A 105: 14447-14452
15. Cimen H, Han MJ, Yang Y, Tong Q, Koc H, et al. (2010) Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 49: 304-311
16. Law IK, Liu L, Xu A, Lam KS, Vanhoutte PM, et al. (2009) Identification and characterization of proteins interacting with SIRT1 and SIRT3: implications in the anti-aging and metabolic effects of sirtuins. Proteomics 9: 2444-2456
17. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667
18. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, et al. (2010) Sirt3- mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40: 893-904
19. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, et al. (2011) Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12: 534-541
20. Someya S, Yu W, Hallows WC, Xu J, Vann JM, et al. (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143: 802-812
21. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, et al. (2009) Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J Clin Invest 119: 2758-2771
22. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, et al. (2010) Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging (Albany NY) 2: 914-923
23. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, et al. (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17: 41-52
24. Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, et al. (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci U S A 108: 14608-14613
25. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, et al. (2011) SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 44: 177-190
26. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, et al. (2008) Endurance exercise as a countermeasure for aging. Diabetes 57: 2933-2942
27. Joseph AM, Adhihetty PJ, Buford TW, Wohlgemuth SE, Lees HA, et al. (2012) The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high- and low-functioning elderly individuals. Aging Cell 11: 801-809
28. Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1: 15-25 (Pubitemid 43960587)
29. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS (2002) AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277: 23977-23980 (Pubitemid 34951907)
30. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, et al. (2007) Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56: 2062-2069 (Pubitemid 47195818)
31. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, et al. (2008) AMPK and PPARdelta agonists are exercise mimetics. Cell 134: 405-415
32. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460 (Pubitemid 40269760)
33. Furuyama T, Yamashita H, Kitayama K, Higami Y, Shimokawa I, et al. (2002) Effects of aging and caloric restriction on the gene expression of Foxo1, 3, and 4 (FKHR, FKHRL1, and AFX) in the rat skeletal muscles. Microsc Res Tech 59: 331-334 (Pubitemid 35332954)
34. Kamei Y, Mizukami J, Miura S, Suzuki M, Takahashi N, et al. (2003) A forkhead transcription factor FKHR up-regulates lipoprotein lipase expression in skeletal muscle. FEBS Lett 536: 232-236 (Pubitemid 36206437)
35. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51 (Pubitemid 38076464)
36. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, et al. (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, downregulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123 (Pubitemid 39287713)
37. Waddell DS, Baehr LM, van den Brandt J, Johnsen SA, Reichardt HM, et al. (2008) The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 295: E785-797
38. Rabinowitz JD, White E (2010) Autophagy and metabolism. Science 330: 1344-1348
39. Demontis F, Perrimon N (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143: 813-825
40. Cooper HM, Huang JY, Verdin E, Spelbrink JN (2009) A new splice variant of the mouse SIRT3 gene encodes the mitochondrial precursor protein. PLoS One 4: e4986
41. Jin L, Galonek H, Israelian K, Choy W, Morrison M, et al. (2009) Biochemical characterization, localization, and tissue distribution of the longer form of mouse SIRT3. Protein Sci 18: 514-525
42. Bao J, Lu Z, Joseph JJ, Carabenciov D, Dimond CC, et al. (2010) Characterization of the murine SIRT3 mitochondrial localization sequence and comparison of mitochondrial enrichment and deacetylase activity of long and short SIRT3 isoforms. J Cell Biochem 110: 238-247
43. Yang Y, Hubbard BP, Sinclair DA, Tong Q (2010) Characterization of murine SIRT3 transcript variants and corresponding protein products. J Cell Biochem 111: 1051-1058
44. Yang Y, Chen KY, Tong Q (2011) Murine Sirt3 protein isoforms have variable half-lives. Gene 488: 46-51
45. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, et al. (2012) A PGC- 1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151: 1319-1331
46. Cox GA, Cole NM, Matsumura K, Phelps SF, Hauschka SD, et al. (1993) Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature 364: 725-729 (Pubitemid 23273127)
47. Kregel (2006) Resource Book for the Design of Animal Exercise Protocols
48. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, et al. (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2: e294
49. Ogilvie RW, Feeback DL (1990) A metachromatic dye-ATPase method for the simultaneous identification of skeletal muscle fiber types I, IIA, IIB and IIC. Stain Technol 65: 231-241 (Pubitemid 20253944)
50. Schiaffino S, Gorza L, Pitton G, Saggin L, Ausoni S, et al. (1988) Embryonic and neonatal myosin heavy chain in denervated and paralyzed rat skeletal muscle. Dev Biol 127: 1-11
51. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, et al. (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10: 197-205
52. Lanza IR, Nair KS (2009) Functional assessment of isolated mitochondria in vitro. Methods Enzymol 457: 349-372
53. Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, et al. (2010) Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochim Biophys Acta 1797: 968-980
54. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
55. Gnaiger E (2001) Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 128: 277-297 (Pubitemid 33054060)
56. Donoviel DB, Shield MA, Buskin JN, Haugen HS, Clegg CH, et al. (1996) Analysis of muscle creatine kinase gene regulatory elements in skeletal and cardiac muscles of transgenic mice. Mol Cell Biol 16: 1649-1658 (Pubitemid 26095637)
57. Johnson JE, Wold BJ, Hauschka SD (1989) Muscle creatine kinase sequence elements regulating skeletal and cardiac muscle expression in transgenic mice. Mol Cell Biol 9: 3393-3399 (Pubitemid 19189628)
58. Tschop MH, Speakman JR, Arch JR, Auwerx J, Bruning JC, et al. (2012) A guide to analysis of mouse energy metabolism. Nat Methods 9: 57-63
59. Arany Z, Lebrasseur N, Morris C, Smith E, Yang W, et al. (2007) The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5: 35-46 (Pubitemid 44939399)
60. Schiaffino S (2010) Fibre types in skeletal muscle: a personal account. Acta Physiol (Oxf) 199: 451-463
61. Dyck DJ, Peters SJ, Glatz J, Gorski J, Keizer H, et al. (1997) Functional differences in lipid metabolism in resting skeletal muscle of various fiber types. Am J Physiol 272: E340-351
62. Zong H, Ren JM, Young LH, Pypaert M, Mu J, et al. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99: 15983-15987 (Pubitemid 35462735)
63. Pillai VB, Sundaresan NR, Kim G, Gupta M, Rajamohan SB, et al. (2010) Exogenous NAD blocks cardiac hypertrophic response via activation of the SIRT3-LKB1-AMP-activated kinase pathway. J Biol Chem 285: 3133-3144
64. Paul PK, Gupta SK, Bhatnagar S, Panguluri SK, Darnay BG, et al. (2010) Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J Cell Biol 191: 1395-1411
65. Nystrom GJ, Lang CH (2008) Sepsis and AMPK Activation by AICAR Differentially Regulate FoxO-1, -3 and -4 mRNA in Striated Muscle. Int J Clin Exp Med 1: 50-63
66. Nakashima K, Yakabe Y (2007) AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71: 1650-1656 (Pubitemid 47358716)
67. Krawiec BJ, Nystrom GJ, Frost RA, Jefferson LS, Lang CH (2007) AMPactivated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells. Am J Physiol Endocrinol Metab 292: E1555-1567 (Pubitemid 47084689)
68. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, et al. (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29: 1774-1785
69. Dixit M, Bess E, Fisslthaler B, Hartel FV, Noll T, et al. (2008) Shear stressinduced activation of the AMP-activated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells. Cardiovasc Res 77: 160-168 (Pubitemid 351195147)
70. Chen BL, Ma YD, Meng RS, Xiong ZJ, Wang HN, et al. (2010) Activation of AMPK inhibits cardiomyocyte hypertrophy by modulating of the FOXO1/ MuRF1 signaling pathway in vitro. Acta Pharmacol Sin 31: 798-804
71. Srere PA (1969) [1] Citrate synthase: [EC 4.1.3.7. Citrate oxaloacetate-lyase (CoA-acetylating)]. In: John ML, editor. Methods in Enzymology: Academic Press. 3-11