Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles

Aging Cell

Volumn 10, Issue 6, 2011, Pages 1047-1055

  Picard, Martin ^a   Ritchie, Darmyn ^b   Thomas, Melissa M ^b   Wright, Kathryn J ^b   Hepple, Russell T ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Aging; Sarcopenia; Skeletal muscle

Indexed keywords

CALCIUM; CATALASE; CITRATE SYNTHASE; CYTOCHROME C OXIDASE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL ENZYME; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON TRANSPORT; ENZYME ACTIVITY; EXTENSOR DIGITORUM LONGUS MUSCLE; GASTROCNEMIUS MUSCLE; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MUSCLE ATROPHY; MUSCLE CELL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SOLEUS MUSCLE;

AGING; ANIMALS; CALCIUM; CITRATE (SI)-SYNTHASE; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION; HYDROGEN PEROXIDE; MALE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCULAR ATROPHY; ORGAN SPECIFICITY; PERMEABILITY; RATS; SAPONINS;

RATTUS;

EID: 81155138284     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00745.x     Document Type: Article

References (45)

1. Abruzzo PM, di Tullio S, Marchionni C, Belia S, Fano G, Zampieri S, Carraro U, Kern H, Sgarbi G, Lenaz G, Marini M (2010) Oxidative stress in the denervated muscle. Free Radic. Res. 44, 563-576.
2. Anderson EJ, Neufer PD (2006) Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. Am. J. Physiol. Cell Physiol. 290, C844-C851.
3. Armstrong RB, Phelps RO (1984) Muscle fiber type composition of the rat hindlimb. Am. J. Anat. 171, 259-272.
4. Baker DJ, Hepple RT (2006) Elevated caspase and AIF signaling correlates with the progression of sarcopenia during aging in male F344BN rats. Exp. Gerontol. 41, 1149-1156.
5. Baker DJ, Betik AC, Krause DJ, Hepple RT (2006) No decline in skeletal muscle oxidative capacity with aging in long-term caloric restricted rats: effects are independent of mtDNA integrity. J. Gerontol. A Biol. Sci. Med. Sci. 61A, 675-684.
6. Boffoli D, Scacco SC, Vergari R, Solarino G, Santacroce G, Papa S (1994) Decline with age of the respiratory chain activity in human skeletal muscle. Biochim. Biophys. Acta 1226, 73-82.
7. Bua E, Johnson J, Herbst A, Delong B, McKenzie D, Salamat S, Aiken JM (2006) Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum.Genet. 79, 469-480.
8. Capel F, Rimbert V, Lioger D, Diot A, Rousset P, Mirand PP, Boirie Y, Morio B, Mosoni L (2005) Due to reverse electron transfer, mitochondrial H2O2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mech. Ageing Dev. 126, 505-511.
9. 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.
10. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764.
11. Cooper JM, Mann VM, Schapira AH (1992) Analyses of mitochondrial respiratory chain function and mitochondrial DNA deletion in human skeletal muscle: effect of ageing. J. Neurol. Sci. 113, 91-98.
12. Cruz-Jentoft AJ, Landi F, Topinkova E, Michel JP (2010) Understanding sarcopenia as a geriatric syndrome. Curr. Opin. Clin. Nutr. Metab. Care. 13, 1-7.
13. Delp MD, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J. Appl. Physiol. 80, 261-270.
14. Desai VG, Weindruch R, Hart RW, Feuers RJ (1996) Influences of age and dietary restriction on gastrocnemius electron transport system activities in mice. Arch. Biochem. Biophys. 333, 145-151.
15. Dirks A, Leeuwenburgh C (2002) Apoptosis in skeletal muscle with aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R519-R527.
16. Figueiredo PA, Powers SK, Ferreira RM, Amado F, Appell HJ, Duarte JA (2009) Impact of lifelong sedentary behavior on mitochondrial function of mice skeletal muscle. J. Gerontol. A Biol. Sci. Med. Sci. 64, 927-939.
17. Gouspillou G, Bourdel-Marchasson I, Rouland R, Calmettes G, Franconi JM, Deschodt-Arsac V, Diolez P (2010) Alteration of mitochondrial oxidative phosphorylation in aged skeletal muscle involves modification of adenine nucleotide translocator. Biochim. Biophys. Acta 1797, 143-151.
18. Hagen JL, Krause DJ, Baker DJ, Fu MH, Tarnopolsky MA, Hepple RT (2004) Skeletal muscle aging in F344BN F1-hybrid rats: I. Mitochondrial dysfunction contributes to the age-associated reduction in VO2max. J. Gerontol. A Biol. Sci. Med. Sci. 59, 1099-1110.
19. Hepple RT (2011) Alterations in mitochondria and their impact in aging skeletal muscle. In Sarcopenia - Age-related Muscle Wasting and Weakness: Mechanisms and Treatments (G Lynch, ed.). New York: Springer, pp. 135-158.
20. 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.
21. Hiona A, Leeuwenburgh C (2008) The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp. Gerontol. 43, 24-33.
22. Hiona A, Sanz A, Kujoth GC, Pamplona R, Seo AY, Hofer T, Someya S, Miyakawa T, Nakayama C, Samhan-Arias AK, Servais S, Barger JL, Portero-Otin M, Tanokura M, Prolla TA, Leeuwenburgh C (2010) Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PLoS ONE 5, e11468.
23. Hutter E, Skovbro M, Lener B, Prats C, Rabol R, Dela F, Jansen-Durr P (2007) Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 6, 245-256.
24. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309, 481-484.
25. Lanza IR, Sreekumaran Nair K (2010) Regulation of skeletal muscle mitochondrial function: genes to proteins. Acta Physiol. (Oxf) 199(4), 529-547.
26. Ljubicic V, Hood DA (2009) Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell 8, 394-404.
27. Marzetti E, Wohlgemuth SE, Lees HA, Chung HY, Giovannini S, Leeuwenburgh C (2008) Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech. Ageing Dev. 129, 542-549.
28. Marzetti E, Hwang JC, Lees HA, Wohlgemuth SE, Dupont-Versteegden EE, Carter CS, Bernabei R, Leeuwenburgh C (2010) Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy. Biochim. Biophys. Acta 1800, 235-244.
29. Mathieu-Costello O, Ju Y, Trejo-Morales M, Cui L (2005) Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats. J. Appl. Physiol. 99, 281-289.
30. McClung JM, Whidden MA, Kavazis AN, Falk DJ, Deruisseau KC, Powers SK (2008) Redox regulation of diaphragm proteolysis during mechanical ventilation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1608-R1617.
31. Muller FL, Song W, Jang YC, Liu Y, Sabia M, Richardson A, Van Remmen H (2007) Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1159-1168.
32. Navarro A, Boveris A (2007) The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol. 292, C670-C686.
33. Picard M, Ritchie D, Wright KJ, Romestaing C, Thomas MM, Rowan SL, Taivassalo T, Hepple RT (2010) Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 9, 1032-1046.
34. Picard M, Taivassalo T, Ritchie D, Wright KJ, Thomas MM, Romestaing C, Hepple RT (2011) Mitochondrial structure and function are disrupted by standard isolation methods. PLoS ONE 6, e18317.
35. Rice KM, Blough ER (2006) Sarcopenia-related apoptosis is regulated differently in fast- and slow-twitch muscles of the aging F344/NxBN rat model. Mech. Ageing Dev. 127, 670-679.
36. Rooyackers OE, Adey DB, Ades PA, Nair KS (1996) Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. U S A 93, 15364-15369.
37. Rowan SL, Purves-Smith FM, Solbak NM, Hepple RT (2011) Accumulation of severely atrophic myofibers marks the acceleration of sarcopenia in slow and fast twitch muscles. Exp. Gerontol. 46, 660-669.
38. Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol. Cell. Biochem. 184, 81-100.
39. Seo AY, Xu J, Servais S, Hofer T, Marzetti E, Wohlgemuth SE, Knutson MD, Chung HY, Leeuwenburgh C (2008) Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7, 706-716.
40. Siu PM, Pistilli EE, Butler DC, Alway SE (2005) Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am. J. Physiol. Cell Physiol. 288, C338-C349.
41. Tong JF, Yan X, Zhu MJ, Du M (2009) AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes. J. Cell. Biochem. 108, 458-468.
42. Treberg JR, Quinlan CL, Brand MD (2010). Hydrogen peroxide efflux from muscle mitochondria underestimates matrix superoxide production - a correction using glutathione depletion. FEBS J 277(13), 2766-2778.
43. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly Y, Gidlof S, Oldfors A, Wibom R, Tornell J, Jacobs HT, Larsson NG (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423.
44. Tweedie C, Romestaing C, Burelle Y, Safdar A, Tarnopolsky MA, Seadon S, Britton SL, Koch LG, Hepple RT (2011) Lower oxidative DNA damage despite greater ROS production in muscles from rats selectively bred for high running capacity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R544-553.
45. Wanagat J, Cao Z, Pathare P, Aiken JM (2001) Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J. 15, 322-332.