Sod2 overexpression preserves myoblast mitochondrial mass and function, but not muscle mass with aging

Aging Cell

Volumn 8, Issue 3, 2009, Pages 296-310

  Lee, Sukkyoo ^a   Van Remmen, Holly ^b,c   Csete, Marie ^a,d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^d California Institute for Regenerative Medicine   (United States)

Author keywords

Hydrogen peroxide; ; Mitochondria; Muscle aging; Myoblast; PI3 kinase Akt signaling; Superoxide

Indexed keywords

HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; MITOGENIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE; THREONINE;

AGED; AGING; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HETEROZYGOTE; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE MASS; MUSCLE MITOCHONDRION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; HETEROZYGOTE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TRANS-ACTIVATORS;

MUS;

EID: 66149171510     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00477.x     Document Type: Article

References (63)

1. Asikainen TM, Huang TT, Taskinen E, Levonen AL, Carlson E, Lapatto R, Epstein CJ, Raivio KO (2002) Increased sensitivity of homozygous Sod2 mutant mice to oxygen toxicity. Free Radic. Biol. Med. 32, 175-186.
2. Bakker WJ, Harris IS, Mak TW (2007) FOXO3a is activated in response to hypoxic stress and inhibits HIF1-induced apoptosis via regulation of CITED2. Mol. Cell 28, 941-953.
3. Bigot A, Jacquemin V, Debacq-Chainiaux F, Butler-Browne GS, Toussaint O, Furling D, Mouly V (2008) Replicative aging down-regulates the myogenic regulatory factors in human myoblasts. Biol. Cell 100, 189-199.
4. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014-1019.
5. Brack AS, Rando TA (2007) Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 3, 226-237.
6. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt F, Greenberg ME (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015.
7. Burgering BM, Kops GJ (2002) Cell cycle and death control: Long live Forkheads. Trends Biochem. Sci. 27, 352-360.
8. Chabi B, Ljubicic V, Menzies KJ, Huang JH, Saleem A, Hood DA (2008) Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7, 2-12.
9. Chen Z, Siu B, Ho YS, Vincent R, Chua CC, Hamdy RC, Chua BH (1998) Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J. Mol. Cell. Cardiol. 30, 2281-2289.
10. Close GL, Kayani AC, Ashton T, McArdle A, Jackson MJ (2007) Release of superoxide from skeletal muscle of adult and old mice: An experimental test of the reductive hotspot hypothesis. Aging Cell 6, 189-195.
11. Collins CA, Zammit PS, Ruiz AP, Morgan JE, Partridge TA (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885-894.
12. Csete M, Walikonis J, Slawny N, Wei Y, Korsnes S, Doyle JC, Wold B (2001) Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J. Cell. Physiol. 189, 189-196.
13. Diel P, Baadners D, Schlupmann K, Velders M, Schwarz JP (2008) C2C12 myoblastoma cell differentiation and proliferation is stimulated by androgens and associated with a modulation of myostatin and Pax7 expression. J. Mol. Endocrinol. 40, 231-241.
14. Fridovich I (2004) Mitochondria: Are they the seat of senescence? Aging Cell 3, 13-16.
15. Friedman JS, Lopez MF, Fleming MD, Rivera A, Martin FM, Welsh ML, Boyd A, Doctrow SR, Burakoff SJ (2004) SOD2-deficiency anemia: Protein oxidation and altered protein expression reveal targets of damage, stress response, and antioxidant responsiveness. Blood 104, 2565-2573.
16. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc. Natl. Acad. Sci. USA 98, 14440-14445.
17. Heron-Milhavet L, Franckhauser C, Rana V, Berthenet C, Fisher D, Hemmings BA, Fernandez A, Lamb NJC (2006) Only Akt1 is required for proliferation, while Akt2 promotes cell cycle exit through p21 binding. Mol. Cell. Biol. 26, 8267-8280.
18. Huang TT, Carlson EJ, Kozy HM, Mantha S, Goodman SI, Ursell PC, Epstein CJ (2001) Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice. Free Radic. Biol. Med. 31, 1101-1110.
19. Husom AD, Peters EA, Kolling EA, Fugere NA, Thompson LV, Ferrington DA (2004) Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 421, 67-76.
20. Jiang BH, Aoki M, Zheng JZ, Li Z, Vogt PK (1999) Myogenic signaling of phosphatidylinositol 3-kinase requires the serine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. USA 96, 2077-2081.
21. +/-) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc. Natl. Acad. Sci. USA 98, 2278-2283.
22. Kushnareva Y, Murphy AN, Andreyev A (2002) Complex I-mediated reactive oxygen species generation: Modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 368, 545-553.
23. Kuzman JA, O'Connell TD, Gerdes AM (2007) Rapamycin prevents thyroid hormone-induced cardiac hypertrophy. Endocrinology 148, 3477-3484.
24. Lebovitz RM, Zhang H, Vogel H, Cartwright J Jr, Dionne L, Lu N, Huang S, Matzuk MM (1996) Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. USA 93, 9782-9787.
25. Lee S, Shin HS, Shireman PK, Vasilaki A, Van Remmen H, Csete ME (2006) Glutathione-peroxidase-1 null muscle progenitor cells are globally defective. Free Radic. Biol. Med. 41, 1174-1184.
26. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP (2006) Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 576, 923-933.
27. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106, 847-856.
28. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, Wallace DC, Epstein CJ (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376-381.
29. -/+) mice. Free Radic. Biol. Med. 36, 542-554.
30. Lin J, Puigserver P, Donovan J, Tarr P, Spiegelman BM (2002) Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1beta), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648.
31. Mansouri A, Muller FL, Liu Y, Ng R, Faulkner J, Hamilton M, Richardson A, Huang T-T, Epstein CJ, Van Remmen H (2006) Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limg skeletal muscle during aging. Mech. Ageing Dev. 127, 198-306.
32. Mauro A (1961) Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495.
33. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, Zastawny TH, Dizdaroglu M, Goodman SI, Huang TT, Miziorko H, Epstein CJ, Wallace DC (1999) Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. USA 96, 846-851.
34. Mieulet V, Roceri M, Espeillac C, Sotiropoulos A, Ohanna M, Oorschot V, Klumperman J, Sandri M, Pende M (2007) S6 kinase inactivation impairs growth and translational target phosphorylation in muscle cells maintaining proper regulation of protein turnover. Am. J. Physiol. Cell Physiol. 293, C712-C722.
35. Miller FJ, Rosenfeldt FL, Zhang C, Linnane AW, Nagley P (2003) Precise determination of mitochondrial DNA copy number in human skeletal and cardiac muscle by a PCR-based assay: Lack of change of copy number with age. Nucleic Acids Res. 31, e61.
36. Mukhopadhyay P, Rajesh M, Yoshihiro K, Hasko G, Pacher P (2007) Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem. Biophys. Res. Commun. 358, 203-208.
37. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, Sonenberg N, Kelly PA, Sotiropoulos A, Pende M (2005) Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat. Cell Biol. 7, 286-294.
38. Peskin AV, Winterbourn CC (2000) A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1). Clin. Chim. Acta 293, 157-166.
39. Powell CS, Jackson RM (2003) Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: Modulation of enzyme activities by MnSOD. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L189-L198.
40. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839.
41. Rando TA, Blau HM (1994) Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125, 1275-1287.
42. Richler C, Yaffe D (1970) The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev. Biol. 23, 1-22.
43. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3, 1009-1013.
44. Rosen H, Rakita RM, Waltersdorph AM, Klebanoff SJ (1987) Myeloperoxidase-mediated damage to the succinate oxidase system of Escherichia coli. Evidence for selective inactivation of the dehydrogenase component. J. Biol. Chem. 262, 15004-15010.
45. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412.
46. Schafer FQ, Buettner GW (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212.
47. Serra C, Palacios D, Mozzetta C, Forcales SV, Morantte I, Ripani M, Jones DR, Du K, Jhala US, Simone C, Puri PL (2007) Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/ PI3K/AKT pathways during muscle differentiation. Mol. Cell 28, 200-213.
48. Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: Defining the myogenic potency of aging skeletal muscle. Dev. Biol. 294, 50-66.
49. Shen X, Zheng S, Metreveli NS, Epstein PH (2006) Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 55, 798-805.
50. Silva JP, Shabalina IG, Dufour E, Petrovic N, Backlund EC, Hultenby K, Wibom R, Nedergaard J, Cannon B, Larsson NG (2005) SOD2 overexpression: enhanced mitochondrial tolerance but absence of effect on UCP activity. EMBO J. 24, 4061-4070.
51. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395-403.
52. Strassburger M, Bloch W, Sulyok S, Schuller J, Keist AF, Schmidt A, Wenk J, Peters T, Wlaschek M, Lenart J, Krieg T, Hafner M, Kumin A, Werner S, Muller W, Scharffetter-Kochanek K (2005) Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic. Biol. Med. 38, 1458-1470.
53. Suzuki K, Murtuza B, Sammut IA, Latif N, Jayakumar J, Smolenski RT, Kaneda Y, Sawa Y, Matsuda H, Yacoub MH (2002) Heat shock protein 72 enhances manganese superoxide dismutase activity during myocardial ischemia-reperfusion injury, associated with mitochondrial protection and apoptosis reduction. Circulation 106, 1270-1276.
54. Takaishi H, Konishi H, Matsuzaki H, Ono Y, Shirai Y, Saito N, Kitamura T, Ogawa W, Kasuga M, Kikkawa U, Nishizuka Y (1999) Regulation of nuclear translocation of forkhead transcription factor AFX by protein kinase B. Proc. Natl. Acad. Sci. USA 96, 11836-11841.
55. Tamir Y, Bengal E (2000) Phosphoinositide 3-kinase induces the transcriptional activity for MEF2 proteins during muscle differentiation. J. Biol. Chem. 275, 34424-34432.
56. Vaillant F, Nagley P (1995) Human cell mutants with very low mitochondrial DNA copy number (rho d). Hum. Mol. Genet. 4, 903-914.
57. Van Remmen H, Salvador C, Yang H, Huang TT, Epstein CJ, Richardson A (1999) Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch. Biochem. Biophys. 363, 91-97.
58. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, Epstein CJ, Huang TT, Richardson A (2001) Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. 281, H1422-H1432.
59. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, Alderson NL, Baynes JW, Epstein CJ, Huang TT, Nelson J, Strong R, Richardson A (2003) Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16, 29-37.
60. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ (2007) Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am. J. Physiol. Endocrinol. Metab. 292, E151-E157.
61. Wilson EM, Rotwein P (2007) Selective control of skeletal muscle differentiation by Akt1. J. Biol. Chem. 282, 5106-5110.
62. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124.
63. Yablonka-Reuveni Z, Nameroff M (1990) Temporal differences in desmin expression between myoblasts from embryonic and adult chicken skeletal muscle. Differentiation 45, 21-28.