The effects of aging, physical training, and a single bout of exercise on mitochondrial protein expression in human skeletal muscle

Experimental Gerontology

Volumn 47, Issue 6, 2012, Pages 417-424

  Bori, Zoltan ^a   Zhao, Zhongfu ^a,b   Koltai, Erika ^a   Fatouros, Ioannis G ^c   Jamurtas, Athanasios Z ^d   Douroudos, Ioannis I ^c   Terzis, Gerasimos ^e   Chatzinikolaou, Athanasios ^c   Sovatzidis, Apostolos ^c   Draganidis, Dimitrios ^c   Boldogh, Istvan ^f   Radak, Zsolt ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b CHANGZHI MEDICAL COLLEGE   (China)

^c DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^d UNIVERSITY OF THESSALY   (Greece)

^e UNIVERSITY OF ATHENS   (Greece)

^f UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Aging; Exercise; Fusion and fission; Mitochondrial biogenesis; Skeletal muscle

Indexed keywords

ANTIINFLAMMATORY AGENT; CELL NUCLEUS DNA; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOCHROME C OXIDASE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; NEBIVOLOL; NUCLEAR RESPIRATORY FACTOR 1; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROBUCOL; TRANSCRIPTION FACTOR;

ADULT; AEROBIC CAPACITY; AGING; ARTICLE; BIOGENESIS; CONTROLLED STUDY; EXERCISE; FUSION GENE; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITTING; SKELETAL MUSCLE; TRAINING; TREADMILL EXERCISE;

ADULT; AGED; AGING; EXERCISE; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; YOUNG ADULT;

EID: 84861183528     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.03.004     Document Type: Article

References (56)

1. Abbott P.V. Analysis of a referral-based endodontic practice: Part 1. Demographic data and reasons for referral. J. Endod. 1994, 20:93-96.
2. ACSM Guidelines for Exercise Testing and Prescription 2005, Lippincott Williams & Wilkins, Philadelphia.
3. Arany Z. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr. Opin. Genet. Dev. 2008, 18:426-434.
4. Bell E.L., Emerling B.M., Ricoult S.J., Guarente L. SirT3 suppresses hypoxia inducible factor 1alpha and tumor growth by inhibiting mitochondrial ROS production. Oncogene 2011, 30:2986-2996.
5. Benard G., Karbowski M. Mitochondrial fusion and division: regulation and role in cell viability. Semin. Cell Dev. Biol. 2009, 20:365-374.
6. Bergström J. Muscle electrolytes in man. Scand. J. Clin. Lab. Invest. 1962, 14:1-110.
7. Bratic I., Trifunovic A. Mitochondrial energy metabolism and ageing. Biochim. Biophys. Acta 2010, 1797:961-967.
8. Cam H., Balciunaite E., Blais A., Spektor A., Scarpulla R.C., Young R., Kluger Y., Dynlacht B.D. A common set of gene regulatory networks links metabolism and growth inhibition. Mol. Cell 2004, 16:399-411.
9. Cartoni R., Leger B., Hock M.B., Praz M., Crettenand A., Pich S., Ziltener J.L., Luthi F., Deriaz O., Zorzano A., Gobelet C., Kralli A., Russell A.P. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J. Physiol. 2005, 567:349-358.
10. Chen H., Chomyn A., Chan D.C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 2005, 280:26185-26192.
11. Chen H.W., Rainey R.N., Balatoni C.E., Dawson D.W., Troke J.J., Wasiak S., Hong J.S., McBride H.M., Koehler C.M., Teitell M.A., French S.W. Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol. Cell. Biol. 2006, 26:8475-8487.
12. Chow L.S., Greenlund L.J., Asmann Y.W., Short K.R., McCrady S.K., Levine J.A., Nair K.S. Impact of endurance training on murine spontaneous activity, muscle mitochondrial DNA abundance, gene transcripts, and function. J. Appl. Physiol. 2007, 102:1078-1089.
13. Craig C.L., Marshall A.L., Sjostrom M., Bauman A.E., Booth M.L., Ainsworth B.E., Pratt M., Ekelund U., Yngve A., Sallis J.F., Oja P. International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc. 2003, 35:1381-1395.
14. Davies K.J., Quintanilha A.T., Brooks G.A., Packer L. Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 1982, 107:1198-1205.
15. di Prampero P.E. Factors limiting maximal performance in humans. Eur. J. Appl. Physiol. 2003, 90:420-429.
16. Ding H., Jiang N., Liu H., Liu X., Liu D., Zhao F., Wen L., Liu S., Ji L.L., Zhang Y. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim. Biophys. Acta 2010, 1800:250-256.
17. Fatouros I.G., Jamurtas A.Z., Villiotou V., Pouliopoulou S., Fotinakis P., Taxildaris K., Deliconstantinos G. Oxidative stress responses in older men during endurance training and detraining. Med. Sci. Sports Exerc. 2004, 36:2065-2072.
18. 2max: associations with carotid IMT and arterial stiffness. Med. Sci. Sports Exerc. 2003, 35:1670-1678.
19. Hayakawa H., Sekiguchi M. Human polynucleotide phosphorylase protein in response to oxidative stress. Biochemistry 2006, 45:6749-6755.
20. Holloszy J.O. Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J. Physiol. Pharmacol. 2008, 59(Suppl. 7):5-18.
21. Kelly D.P. Cell biology: ageing theories unified. Nature 2011, 470:342-343.
22. Kong X., Wang R., Xue Y., Liu X., Zhang H., Chen Y., Fang F., Chang Y. Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 2010, 5:e11707.
23. Koopman W.J., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecchi F., Smeitink J.A., Willems P.H. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid. Redox Signal. 2010, 12:1431-1470.
24. Lee S., Jeong S.Y., Lim W.C., Kim S., Park Y.Y., Sun X., Youle R.J., Cho H. Mitochondrial fission and fusion mediators, hFis1 and OPA1, modulate cellular senescence. J. Biol. Chem. 2007, 282:22977-22983.
25. 2max: what do we know, and what do we still need to know?. J. Physiol. 2008, 586:25-34.
26. Lezza A.M., Pesce V., Cormio A., Fracasso F., Vecchiet J., Felzani G., Cantatore P., Gadaleta M.N. Increased expression of mitochondrial transcription factor A and nuclear respiratory factor-1 in skeletal muscle from aged human subjects. FEBS Lett. 2001, 501:74-78.
27. Ljubicic V., Joseph A.M., Saleem A., Uguccioni G., Collu-Marchese M., Lai R.Y., Nguyen L.M., Hood D.A. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. Biochim. Biophys. Acta 2010, 1800:223-234.
28. Michailidis Y., Jamurtas A.Z., Nikolaidis M.G., Fatouros I.G., Koutedakis Y., Papassotiriou I., Kouretas D. Sampling time is crucial for measurement of aerobic exercise-induced oxidative stress. Med. Sci. Sports Exerc. 2007, 39:1107-1113.
29. Morss G.M., Jordan A.N., Skinner J.S., Dunn A.L., Church T.S., Earnest C.P., Kampert J.B., Jurca R., Blair S.N. Dose response to exercise in women aged 45-75yr (DREW): design and rationale. Med. Sci. Sports Exerc. 2004, 36:336-344.
30. Norrbom J., Wallman S.E., Gustafsson T., Rundqvist H., Jansson E., Sundberg C.J. Training response of mitochondrial transcription factors in human skeletal muscle. Acta Physiol (Oxf.) 2010, 198:71-79.
31. Otera H., Mihara K. Molecular mechanisms and physiologic functions of mitochondrial dynamics. J. Biochem. 2011, 149:241-251.
32. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
33. Qiu X., Brown K., Hirschey M.D., Verdin E., Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 2010, 12:662-667.
34. Radak Z., Sasvari M., Nyakas C., Taylor A.W., Ohno H., Nakamoto H., Goto S. Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch. Biochem. Biophys. 2000, 383:114-118.
35. Radak Z., Atalay M., Jakus J., Boldogh I., Davies K., Goto S. Exercise improves import of 8-oxoguanine DNA glycosylase into the mitochondrial matrix of skeletal muscle and enhances the relative activity. Free Radic. Biol. Med. 2009, 46:238-243.
36. Radak Z., Hart N., Sarga L., Koltai E., Atalay M., Ohno H., Boldogh I. Exercise plays a preventive role against Alzheimer's disease. J. Alzheimers Dis. 2010, 20:777-783.
37. Radak Z., Bori Z., Koltai E., Fatouros I.G., Jamurtas A.Z., Douroudos I.I., Terzis G., Nikolaidis M.G., Chatzinikolaou A., Sovatzidis A., Kumagai S., Naito H., Boldogh I. Age-dependent changes in 8-oxoguanine-DNA glycosylase activity are modulated by adaptive responses to physical exercise in human skeletal muscle. Free Radic. Biol. Med. 2011, 51:417-423.
38. Radak Z., Bori Z., Koltai E., Fatouros I., Jamurtas A., Douroudos I., Terzis G., Nikolaidis M., Chatzinikolaou A., Sovatzidis A., Kumagai S., Naito H., Boldogh I. Age-dependent changes in 8-oxoguanine-DNA-glycosylase activity is modulated by adaptive responses to physical exercise in human skeletal muscle. Free Radic. Biol. Med. 2011, 51:417-423.
39. Romanello V., Guadagnin E., Gomes L., Roder I., Sandri C., Petersen Y., Milan G., Masiero E., Del Piccolo P., Foretz M., Scorrano L., Rudolf R., Sandri M. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 2010, 29:1774-1785.
40. Rooyackers O.E., Adey D.B., Ades P.A., Nair K.S. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:15364-15369.
41. Rose G., Dato S., Altomare K., Bellizzi D., Garasto S., Greco V., Passarino G., Feraco E., Mari V., Barbi C., BonaFe M., Franceschi C., Tan Q., Boiko S., Yashin A.I., De Benedictis G. Variability of the SIRT3 gene, human silent information regulator Sir2 homologue, and survivorship in the elderly. Exp. Gerontol. 2003, 38:1065-1070.
42. Safdar A., Bourgeois J.M., Ogborn D.I., Little J.P., Hettinga B.P., Akhtar M., Thompson J.E., Melov S., Mocellin N.J., Kujoth G.C., Prolla T.A., Tarnopolsky M.A. Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4135-4140.
43. Sahin E., Colla S., Liesa M., Moslehi J., Muller F.L., Guo M., Cooper M., Kotton D., Fabian A.J., Walkey C., Maser R.S., Tonon G., Foerster F., Xiong R., Wang Y.A., Shukla S.A., Jaskelioff M., Martin E.S., Heffernan T.P., Protopopov A., Ivanova E., Mahoney J.E., Kost-Alimova M., Perry S.R., Bronson R., Liao R., Mulligan R., Shirihai O.S., Chin L., DePinho R.A. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 2011, 470:359-365.
44. Sarkar D., Lebedeva I.V., Emdad L., Kang D.C., Baldwin A.S., Fisher P.B. Human polynucleotide phosphorylase (hPNPaseold-35): a potential link between aging and inflammation. Cancer Res. 2004, 64:7473-7478.
45. Sarkar D., Park E.S., Emdad L., Randolph A., Valerie K., Fisher P.B. Defining the domains of human polynucleotide phosphorylase (hPNPaseOLD-35) mediating cellular senescence. Mol. Cell. Biol. 2005, 25:7333-7343.
46. Sastre J., Pallardo F.V., Vina J. The role of mitochondrial oxidative stress in aging. Free Radic. Biol. Med. 2003, 35:1-8.
47. Sawada S.S., Muto T., Tanaka H., Lee I.M., Paffenbarger R.S., Shindo M., Blair S.N. Cardiorespiratory fitness and cancer mortality in Japanese men: a prospective study. Med. Sci. Sports Exerc. 2003, 35:1546-1550.
48. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
49. Sriwijitkamol A., Coletta D.K., Wajcberg E., Balbontin G.B., Reyna S.M., Barrientes J., Eagan P.A., Jenkinson C.P., Cersosimo E., DeFronzo R.A., Sakamoto K., Musi N. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 2007, 56:836-848.
50. Terzis G., Georgiadis G., Stratakos G., Vogiatzis I., Kavouras S., Manta P., Mascher H., Blomstrand E. Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects. Eur. J. Appl. Physiol. 2008, 102:145-152.
51. Terzis G., Stratakos G., Manta P., Georgiadis G. Throwing performance after resistance training and detraining. J. Strength Cond. Res. 2008, 22:1198-1204.
52. Timmons J.A., Knudsen S., Rankinen T., Koch L.G., Sarzynski M., Jensen T., Keller P., Scheele C., Vollaard N.B., Nielsen S., Akerstrom T., MacDougald O.A., Jansson E., Greenhaff P.L., Tarnopolsky M.A., van Loon L.J., Pedersen B.K., Sundberg C.J., Wahlestedt C., Britton S.L., Bouchard C. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J. Appl. Physiol. 2010, 108:1487-1496.
53. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E., Shirihai O.S. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
54. Voorrips L.E., Ravelli A.C., Dongelmans P.C., Deurenberg P., Van Staveren W.A. A physical activity questionnaire for the elderly. Med. Sci. Sports Exerc. 1991, 23:974-979.
55. Wang G., Chen H.W., Oktay Y., Zhang J., Allen E.L., Smith G.M., Fan K.C., Hong J.S., French S.W., McCaffery J.M., Lightowlers R.N., Morse H.C., Koehler C.M., Teitell M.A. PNPASE regulates RNA import into mitochondria. Cell 2010, 142:456-467.
56. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 2010, 11:872-884.