Bioenergetics of the aging heart and skeletal muscles: Modern concepts and controversies

Ageing Research Reviews

Volumn 28, Issue , 2016, Pages 1-14

  Tepp, Kersti ^a   Timohhina, Natalja ^a   Puurand, Marju ^a   Klepinin, Aleksandr ^a   Chekulayev, Vladimir ^a   Shevchuk, Igor ^a   Kaambre, Tuuli ^a,b  

^a NATIONAL INSTITUTE OF CHEMICAL PHYSICS AND BIOPHYSICS   (Estonia)

^b TALLINN UNIVERSITY   (Estonia)

Author keywords

Creatine kinase; Energy metabolism; Energy transfer; Heart; Mitochondria; Skeletal muscle

Indexed keywords

AGING; BIOENERGY; ENERGY METABOLISM; ENERGY YIELD; HEART; HUMAN; HUMAN TISSUE; MITOCHONDRION; ORGAN CULTURE; OXIDATION; SKELETAL MUSCLE; CARDIAC MUSCLE; METABOLISM; PHYSIOLOGY;

REACTIVE OXYGEN METABOLITE;

AGING; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MUSCLE, SKELETAL; MYOCARDIUM; REACTIVE OXYGEN SPECIES;

EID: 84962792158     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2016.04.001     Document Type: Review

References (193)

1. Abel E.D. Glucose transport in the heart. Front. Biosci. 2004, 9:201-215.
2. Acin-Perez R., Enriquez J.A. The function of the respiratory supercomplexes: the plasticity model. Biochim. Biophys. Acta 2014, 1837:444-450.
3. Akki A., Su J., Yano T., Gupta A., Wang Y., Leppo M.K., Chacko V.P., Steenbergen C., Weiss R.G. Creatine kinase overexpression improves ATP kinetics and contractile function in postischemic myocardium. Am. J. Physiol. Heart Circ. Physiol. 2012, 303:H844-852.
4. Aliev M.K., Saks V.A. Mathematical modeling of intracellular transport processes and the creatine kinase systems: a probability approach. Mol. Cell. Biochem. 1994, 133-134:333-346.
5. Ames B.N., Shigenaga M.K., Hagen T.M. Mitochondrial decay in aging. Biochim. Biophys. Acta 1995, 1271:165-170.
6. Anmann T., Varikmaa M., Timohhina N., Tepp K., Shevchuk I., Chekulayev V., Saks V., Kaambre T. Formation of highly organized intracellular structure and energy metabolism in cardiac muscle cells during postnatal development of rat heart. Biochim. Biophys. Acta 2014, 1837:1350-1361.
7. Anversa P., Leri A., Kajstura J. Cardiac regeneration. J. Am. Coll. Cardiol. 2006, 47:1769-1776.
8. Atamna H., Walter P.B., Ames B.N. The role of heme and iron-sulfur clusters in mitochondrial biogenesis, maintenance, and decay with age. Arch. Biochem. Biophys. 2002, 397:345-353.
9. Bak M.I., Wei J.Y., Ingwall J.S. Interaction of hypoxia and aging in the heart: analysis of high energy phosphate content. J. Mol. Cell. Cardiol. 1998, 30:661-672.
10. Barazzoni R., Short K.R., Nair K.S. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J. Biol. Chem. 2000, 275:3343-3347.
11. Barja G. Free radicals and aging. Trends Neurosci. 2004, 27:595-600.
12. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 1998, 78:547-581.
13. Belsky D.W., Caspi A., Houts R., Cohen H.J., Corcoran D.L., Danese A., Harrington H., Israel S., Levine M.E., Schaefer J.D., Sugden K., Williams B., Yashin A.I., Poulton R., Moffitt T.E. Quantification of biological aging in young adults. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E4104-4110.
14. Beltrami A.P., Urbanek K., Kajstura J., Yan S.M., Finato N., Bussani R., Nadal-Ginard B., Silvestri F., Leri A., Beltrami C.A., Anversa P. Evidence that human cardiac myocytes divide after myocardial infarction. N. Engl. J. Med. 2001, 344:1750-1757.
15. Beltran Valls M.R., Wilkinson D.J., Narici M.V., Smith K., Phillips B.E., Caporossi D., Atherton P.J. Protein carbonylation and heat shock proteins in human skeletal muscle: relationships to age and sarcopenia. J. Gerontol. A. Biol. Sci. Med. Sci. 2015, 70:174-181.
16. Beraud N., Pelloux S., Usson Y., Kuznetsov A.V., Ronot X., Tourneur Y., Saks V. Mitochondrial dynamics in heart cells: very low amplitude high frequency fluctuations in adult cardiomyocytes and flow motion in non beating Hl-1 cells. J. Bioenerg. Biomembr. 2009, 41:195-214.
17. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., Zupicich J., Alkass K., Buchholz B.A., Druid H., Jovinge S., Frisen J. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
18. Bhandari P., Song M., Chen Y., Burelle Y., Dorn G.W. Mitochondrial contagion induced by Parkin deficiency in Drosophila hearts and its containment by suppressing mitofusin. Circ. Res. 2014, 114:257-265.
19. Bing R.J., Siegel A., Ungar I., Gilbert M. Metabolism of the human heart. II. Studies on fat: ketone and amino acid metabolism. Am. J. Med. 1954, 16:504-515.
20. Blagosklonny M.V. Validation of anti-aging drugs by treating age-related diseases. Aging (Albany, NY) 2009, 1:281-288.
21. Bodyak N., Kang P.M., Hiromura M., Sulijoadikusumo I., Horikoshi N., Khrapko K., Usheva A. Gene expression profiling of the aging mouse cardiac myocytes. Nucleic Acids Res. 2002, 30:3788-3794.
22. Bokov A., Chaudhuri A., Richardson A. The role of oxidative damage and stress in aging. Mech. Ageing Dev. 2004, 125:811-826.
23. Bottinger L., Horvath S.E., Kleinschroth T., Hunte C., Daum G., Pfanner N., Becker T. Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J. Mol. Biol. 2012, 423:677-686.
24. Callahan D.M., Bedrin N.G., Subramanian M., Berking J., Ades P.A., Toth M.J., Miller M.S. Age-related structural alterations in human skeletal muscle fibers and mitochondria are sex specific: relationship to single-fiber function. J. Appl. Physiol. 2014, 116:1582-1592.
25. Candow D.G., Chilibeck P.D., Forbes S.C. Creatine supplementation and aging musculoskeletal health. Endocrine 2014, 45:354-361.
26. Carmeli E., Coleman R., Reznick A.Z. The biochemistry of aging muscle. Exp. Gerontol. 2002, 37:477-489.
27. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria-central role of complex III. J. Biol. Chem. 2003, 278:36027-36031.
28. Chen X., Wilson R.M., Kubo H., Berretta R.M., Harris D.M., Zhang X., Jaleel N., MacDonnell S.M., Bearzi C., Tillmanns J., Trofimova I., Hosoda T., Mosna F., Cribbs L., Leri A., Kajstura J., Anversa P., Houser S.R. Adolescent feline heart contains a population of small, proliferative ventricular myocytes with immature physiological properties. Circ. Res. 2007, 100:536-544.
29. Chen Y., Liu Y., Dorn G.W. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 2011, 109:1327-1331.
30. Combaret L., Dardevet D., Bechet D., Taillandier D., Mosoni L., Attaix D. Skeletal muscle proteolysis in aging. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12:37-41.
31. Davydov V.V., Shvets V.N. Different changes in the cytosole creatine kinase isoenzymes from heart of adult and old rats during stress. Exp. Gerontol. 1999, 34:885-888.
32. Davydov V.V., Shvets V.N. Differential changes in the properties of mitochondrial isoenzyme creatine kinase from heart of adult and old rats during stress. Exp. Gerontol. 1999, 34:375-378.
33. Doran P., O'Connell K., Gannon J., Kavanagh M., Ohlendieck K. Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 2008, 8:364-377.
34. Dorn G.W., Vega R.B., Kelly D.P. Mitochondrial biogenesis and dynamics in the developing and diseased heart. Genes Dev. 2015, 29:1981-1991.
35. Druzhyna N.M., Wilson G.L., LeDoux S.P. Mitochondrial DNA repair in aging and disease. Mech. Ageing Dev. 2008, 129:383-390.
36. Duicu O.M., Mirica S.N., Gheorgheosu D.E., Privistirescu A.I., Fira-Mladinescu O., Muntean D.M. Ageing-induced decrease in cardiac mitochondrial function in healthy rats. Can. J. Physiol. Pharmacol. 2013, 91:593-600.
37. Dutta D., Calvani R., Bernabei R., Leeuwenburgh C., Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ. Res. 2012, 110:1125-1138.
38. Dyck J.R., Lopaschuk G.D. AMPK alterations in cardiac physiology and pathology: enemy or ally. J. Physiol. 2006, 574:95-112.
39. Dzeja P.P., Terzic A. Phosphotransfer networks and cellular energetics. J. Exp. Biol. 2003, 206:2039-2047.
40. Dzeja P.P., Vitkevicius K.T., Redfield M.M., Burnett J.C., Terzic A. Adenylate kinase-catalyzed phosphotransfer in the myocardium: increased contribution in heart failure. Circ. Res. 1999, 84:1137-1143.
41. Dzeja P.P., Terzic A., Wieringa B. Phosphotransfer dynamics in skeletal muscle from creatine kinase gene-deleted mice. Mol. Cell. Biochem. 2004, 256-257:13-27.
42. Dzeja, P.P., Chung, S., Terzic, A., 2007. Integration of Adenylate Kinase and Glycolytic and Glycogenolytic Circuits in Cellular Energetics, in: Prof. Valdur, S. (Ed.), Molecular System Bioenergetics, pp. 265-301.
43. Dzeja P.P., Hoyer K., Tian R., Zhang S., Nemutlu E., Spindler M., Ingwall J.S. Rearrangement of energetic and substrate utilization networks compensate for chronic myocardial creatine kinase deficiency. J. Physiol. 2011, 589:5193-5211.
44. Esterhammer R., Klug G., Wolf C., Mayr A., Reinstadler S., Feistritzer H.J., Metzler B., Schocke M.F. Cardiac high-energy phosphate metabolism alters with age as studied in 196 healthy males with the help of 31-phosphorus 2-dimensional chemical shift imaging. PLoS One 2014, 9:e97368.
45. Fry M., Green D.E. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 1981, 256:1874-1880.
46. Gibson M.C., Schultz E. Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 1983, 6:574-580.
47. Gnaiger E. Capacity of oxidative phosphorylation in human skeletal muscle New perspectives of mitochondrial physiology. Int. J. Biochem. Cell B 2009, 41:1837-1845.
48. Goldsmith T.C. Modern evolutionary mechanics theories and resolving the programmed/non-programmed aging controversy. Biochemistry (Mosc) 2014, 79:1049-1055.
49. Gomez L.A., Hagen T.M. Age-related decline in mitochondrial bioenergetics: does supercomplex destabilization determine lower oxidative capacity and higher superoxide production?. Semin. Cell Dev. Biol. 2012, 23:758-767.
50. Gomez L.A., Monette J.S., Chavez J.D., Maier C.S., Hagen T.M. Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch. Biochem. Biophys. 2009, 490:30-35.
51. Gonzalez-Granillo M., Grichine A., Guzun R., Usson Y., Tepp K., Chekulayev V., Shevchuk I., Karu-Varikmaa M., Kuznetsov A.V., Grimm M., Saks V., Kaambre T. Studies of the role of tubulin beta II isotype in regulation of mitochondrial respiration in intracellular energetic units in cardiac cells. J. Mol. Cell. Cardiol. 2012, 52:437-447.
52. Goodpaster B.H., Park S.W., Harris T.B., Kritchevsky S.B., Nevitt M., Schwartz A.V., Simonsick E.M., Tylavsky F.A., Visser M., Newman A.B. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J. Gerontol. A. Biol. Sci. Med. Sci. 2006, 61:1059-1064.
53. Gray R.P. Cardiology in the ageing heart: models. Drug Discovery Today 2005, 2:233-237.
54. Gupta A., Akki A., Wang Y., Leppo M.K., Chacko V.P., Foster D.B., Caceres V., Shi S., Kirk J.A., Su J., Lai S., Paolocci N., Steenbergen C., Gerstenblith G., Weiss R.G. Creatine kinase-mediated improvement of function in failing mouse hearts provides causal evidence the failing heart is energy starved. J. Clin. Invest. 2012, 122:291-302.
55. Gurland B.J., Wilder D.E., Lantigua R., Stern Y., Chen J., Killeffer E.H., Mayeux R. Rates of dementia in three ethnoracial groups. Int. J. Geriatr. Psychiatry 1999, 14:481-493.
56. Guzun R., Timohhina N., Tepp K., Monge C., Kaambre T., Sikk P., Kuznetsov A.V., Pison C., Saks V. Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties. Biochim. Biophys. Acta 2009, 1787:1089-1105.
57. Guzun R., Karu-Varikmaa M., Gonzalez-Granillo M., Kuznetsov A.V., Michel L., Cottet-Rousselle C., Saaremae M., Kaambre T., Metsis M., Grimm M., Auffray C., Saks V. Mitochondria-cytoskeleton interaction: distribution of beta-tubulins in cardiomyocytes and HL-1 cells. Biochim. Biophys. Acta 2011, 1807:458-469.
58. Guzun R., Kaambre T., Bagur R., Grichine A., Usson Y., Varikmaa M., Anmann T., Tepp K., Timohhina N., Shevchuk I., Chekulayev V., Boucher F., Dos Santos P., Schlattner U., Wallimann T., Kuznetsov A.V., Dzeja P., Aliev M., Saks V. Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation. Acta Physiol. 2015, 213:84-106.
59. Hall D., Minton A.P. Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim. Biophys. Acta 2003, 1649:127-139.
60. Hardie D.G. AMP-activated protein kinase: the guardian of cardiac energy status. J. Clin. Invest. 2004, 114:465-468.
61. Harper S. Economic and social implications of aging societies. Science 2014, 346:587-591.
62. Harvey A., Montezano A.C., Touyz R.M. Vascular biology of ageing-implications in hypertension. J. Mol. Cell. Cardiol. 2015, 83:112-121.
63. Hollingsworth K.G., Blamire A.M., Keavney B.D., Macgowan G.A. Left ventricular torsion, energetics, and diastolic function in normal human aging. Am. J. Physiol. Heart Circ. Physiol. 2012, 302:H885-892.
64. Hollingsworth K.G., Macgowan G.A., Morris L., Bates M.G., Taylor R., Jones D.E., Newton J.L., Blamire A.M. Cardiac torsion-strain relationships in fatigued primary biliary cirrhosis patients show accelerated aging: a pilot cross-sectional study. J. Appl. Physiol. 2012, 112:2043-2048.
65. Howlett S.E. Age-associated changes in excitation-contraction coupling are more prominent in ventricular myocytes from male rats than in myocytes from female rats. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H659-H670.
66. Huang C., Yitzhaki S., Perry C.N., Liu W., Giricz Z., Mentzer R.M., Gottlieb R.A. Autophagy induced by ischemic preconditioning is essential for cardioprotection. J. Cardiovasc. Transl. Res. 2010, 3:365-373.
67. Hutter E., Skovbro M., Lener B., Prats C., Rabol R., Dela F., Jansen-Durr P. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 2007, 6:245-256.
68. Ieda M. Heart development and regeneration via cellular interactionand reprogramming. Keio J. Med. 2013, 62:99-106.
69. Jiang C.H., Tsien J.Z., Schultz P.G., Hu Y. The effects of aging on gene expression in the hypothalamus and cortex of mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1930-1934.
70. Jimenez R.E., Kubli D.A., Gustafsson A.B. Autophagy and mitophagy in the myocardium: therapeutic potential and concerns. Br. J. Pharmacol. 2014, 171:1907-1916.
71. Johnson M.L., Robinson M.M., Nair K.S. Skeletal muscle aging and the mitochondrion. Trends Endocrinol. Metab. (TEM) 2013, 24:247-256.
72. Kaczor J.J., Ziolkowski W., Antosiewicz J., Hac S., Tarnopolsky M.A., Popinigis J. The effect of aging on anaerobic and aerobic enzyme activities in human skeletal muscle. J. Gerontol. A. Biol. Sci. Med. Sci. 2006, 61:339-344.
73. Kadi F., Charifi N., Denis C., Lexell J. Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 2004, 29:120-127.
74. Kaeberlein M., McVey M., Guarente L. Using yeast to discover the fountain of youth. Sci. Aging Knowl. Environ. (SAGE KE) 2001, 2001:pe1.
75. Kajstura J., Gurusamy N., Ogorek B., Goichberg P., Clavo-Rondon C., Hosoda T., D'Amario D., Bardelli S., Beltrami A.P., Cesselli D., Bussani R., del Monte F., Quaini F., Rota M., Beltrami C.A., Buchholz B.A., Leri A., Anversa P. Myocyte turnover in the aging human heart. Circ. Res. 2010, 107:1374-1386.
76. Kates A.M., Herrero P., Dence C., Soto P., Srinivasan M., Delano D.G., Ehsani A., Gropler R.J. Impact of aging on substrate metabolism by the human heart. J. Am. Coll. Cardiol. 2003, 41:293-299.
77. Kayo T., Allison D.B., Weindruch R., Prolla T.A. Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5093-5098.
78. Kimura W., Xiao F., Canseco D.C., Muralidhar S., Thet S., Zhang H.M., Abderrahman Y., Chen R., Garcia J.A., Shelton J.M., Richardson J.A., Ashour A.M., Asaithamby A., Liang H., Xing C., Lu Z., Zhang C.C., Sadek H.A. Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart. Nature 2015, 523:226-230.
79. Kuznetsov A.V., Veksler V., Gellerich F.N., Saks V., Margreiter R., Kunz W.S. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat. Protoc. 2008, 3:965-976.
80. Lakatta E.G., Sollott S.J. Perspectives on mammalian cardiovascular aging: humans to molecules. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 132:699-721.
81. Lakatta E.G. So! What's aging? Is cardiovascular aging a disease. J. Mol. Cell. Cardiol. 2015, 83:1-13.
82. Lapuente-Brun E., Moreno-Loshuertos R., Acin-Perez R., Latorre-Pellicer A., Colas C., Balsa E., Perales-Clemente E., Quiros P.M., Calvo E., Rodriguez-Hernandez M.A., Navas P., Cruz R., Carracedo A., Lopez-Otin C., Perez-Martos A., Fernandez-Silva P., Fernandez-Vizarra E., Enriquez J.A. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 2013, 340:1567-1570.
83. Larsson L. Morphological and functional characteristics of the ageing skeletal muscle in man: a cross-sectional study. Acta Physiol. Scand. Suppl. 1978, 457:1-36.
84. LeMoine C.M., McClelland G.B., Lyons C.N., Mathieu-Costello O., Moyes C.D. Control of mitochondrial gene expression in the aging rat myocardium. Biochem. Cell Biol. 2006, 84:191-198.
85. Lee C.K., Klopp R.G., Weindruch R., Prolla T.A. Gene expression profile of aging and its retardation by caloric restriction. Science 1999, 285:1390-1393.
86. Lenaz G., Bovina C., Castelluccio C., Fato R., Formiggini G., Genova M.L., Marchetti M., Pich M.M., Pallotti F., Parenti Castelli G., Biagini G. Mitochondrial complex I defects in aging. Mol. Cell. Biochem. 1997, 174:329-333.
87. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 2001, 52:159-164.
88. Leri A., Malhotra A., Liew C.C., Kajstura J., Anversa P. Telomerase activity in rat cardiac myocytes is age and gender dependent. J. Mol. Cell Cardiol. 2000, 32:385-390.
89. Levi S., Rovida E. The role of iron in mitochondrial function. Biochim. Biophys. Acta 2009, 1790:629-636.
90. Lieber S.C., Aubry N., Pain J., Diaz G., Kim S.J., Vatner S.F. Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H645-H651.
91. Loeb L.A., Wallace D.C., Martin G.M. The mitochondrial theory of aging and its relationship to reactive oxygen species damage and somatic mtDNA mutations. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18769-18770.
92. Lombardi A., Silvestri E., Cioffi F., Senese R., Lanni A., Goglia F., de Lange P., Moreno M. Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D- and Blue native-pAGE approach. J. Proteomics 2009, 72:708-721.
93. Lopaschuk G.D., Kelly D.P. Signalling in cardiac metabolism. Cardiovasc. Res. 2008, 79:205-207.
94. Lopaschuk G.D., Belke D.D., Gamble J., Itoi T., Schonekess B.O. Regulation of fatty acid oxidation in the mammalian heart in health and disease. Biochim. Biophys. Acta 1994, 1213:263-276.
95. Lopaschuk G.D., Ussher J.R., Folmes C.D., Jaswal J.S., Stanley W.C. Myocardial fatty acid metabolism in health and disease. Physiol. Rev. 2010, 90:207-258.
96. Lourenco Dos Santos S., Baraibar M.A., Lundberg S., Eeg-Olofsson O., Larsson L., Friguet B. Oxidative proteome alterations during skeletal muscle ageing. Redox Biol. 2015, 5:267-274.
97. Mahishale V. Ageing world: health care challenges. J. Sci. Soc. 2015, 42:138-143.
98. Marx J.O., Kraemer W.J., Nindl B.C., Larsson L. Effects of aging on human skeletal muscle myosin heavy-chain mRNA content and protein isoform expression. J. Gerontol. A. Biol. Sci. Med. Sci. 2002, 57:B232-238.
99. Marzetti E., Lawler J.M., Hiona A., Manini T., Seo A.Y., Leeuwenburgh C. Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction. in skeletal muscle. Free Radic. Biol. Med. 2008, 44:160-168.
100. Marzetti E., Wohlgemuth S.E., Lees H.A., Chung H.Y., Giovannini S., Leeuwenburgh C. Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech. Ageing Dev. 2008, 129:542-549.
101. McKenzie M., Lazarou M., Thorburn D.R., Ryan M.T. Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J. Mol. Biol. 2006, 361:462-469.
102. McMillin J.B., Taffet G.E., Taegtmeyer H., Hudson E.K., Tate C.A. Mitochondrial metabolism and substrate competition in the aging Fischer rat heart. Cardiovasc. Res. 1993, 27:2222-2228.
103. Mellor K.M., Curl C.L., Chandramouli C., Pedrazzini T., Wendt I.R., Delbridge L.M.D. Ageing-related cardiomyocyte functional decline is sex and angiotensin II dependent. Age 2014, 36:1155-1167.
104. Miljkovic N., Lim J.-Y., Miljkovic I., Frontera W.R. Aging of skeletal muscle fibers. Ann. Rehabil. Med. 2015, 39:155-162.
105. Miller M.S., Bedrin N.G., Callahan D.M., Previs M.J., Jennings M.E., 2nd Ades P.A., Maughan D.W., Palmer B.M., Toth M.J. Age-related slowing of myosin actin cross-bridge kinetics is sex specific and predicts decrements in whole skeletal muscle performance in humans. J. Appl. Physiol. 2013, 115:1004-1014.
106. Milner D.J., Mavroidis M., Weisleder N., Capetanaki Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J. Cell Biol. 2000, 150:1283-1298.
107. Moreno-Lastres D., Fontanesi F., Garcia-Consuegra I., Martin M.A., Arenas J., Barrientos A., Ugalde C. Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab. 2012, 15:324-335.
108. Narici M.V., Maffulli N. Sarcopenia: characteristics, mechanisms and functional significance. Br. Med. Bull. 2010, 95:139-159.
109. Navarro A., Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol. 2007, 292:C670-686.
110. Nemutlu E., Zhang S., Gupta A., Juranic N.O., Macura S.I., Terzic A., Jahangir A., Dzeja P. Dynamic phosphometabolomic profiling of human tissues and transgenic models by 18O-assisted (3)(1)P NMR and mass spectrometry. Physiol. Genomics 2012, 44:386-402.
111. Nemutlu E., Gupta A., Zhang S., Viqar M., Holmuhamedov E., Terzic A., Jahangir A., Dzeja P. Decline of phosphotransfer and substrate supply metabolic circuits hinders ATP cycling in aging myocardium. PLoS One 2015, 10:e0136556.
112. Neubauer S., Horn M., Cramer M., Harre K., Newell J.B., Peters W., Pabst T., Ertl G., Hahn D., Ingwall J.S., Kochsiek K. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 1997, 96:2190-2196.
113. Neubauer S. The failing heart-an engine out of fuel. N. Engl. J. Med. 2007, 356:1140-1151.
114. Nuss J.E., Amaning J.K., Bailey C.E., DeFord J.H., Dimayuga V.L., Rabek J.P., Papaconstantinou J. Oxidative modification and aggregation of creatine kinase from aged mouse skeletal muscle. Aging (Milano) 2009, 1:557-572.
115. Olivetti G., Melissari M., Capasso J.M., Anversa P. Cardiomyopathy of the aging human heart: myocyte loss and reactive cellular hypertrophy. Circ. Res. 1991, 68:1560-1568.
116. Olivetti G., Giordano G., Corradi D., Melissari M., Lagrasta C., Gambert S.R., Anversa P. Gender differences and aging: effects on the human heart. J. Am. Coll. Cardiol. 1995, 26:1068-1079.
117. Orogo A.M., Gonzalez E.R., Kubli D.A., Baptista I.L., Ong S.B., Prolla T.A., Sussman M.A., Murphy A.N., Gustafsson A.B. Accumulation of mitochondrial DNA mutations disrupts cardiac progenitor cell function and reduces survival. J. Biol. Chem. 2015, 290:22061-22075.
118. Panov A., Dikalov S., Shalbuyeva N., Hemendinger R., Greenamyre J.T., Rosenfeld J. Species- and tissue-specific relationships between mitochondrial permeability transition and generation of ROS in brain and liver mitochondria of rats and mice. Am. J. Physiol. Cell Physiol. 2007, 292:C708-718.
119. Papp Z., Czuriga D., Balogh L., Balogh A., Borbely B. How cardiomyocytes make the heart old. Curr. Pharm. Biotechnol. 2012, 13:2515-2521.
120. Paradies G., Ruggiero F.M. Age-related changes in the activity of the pyruvate carrier and in the lipid composition in rat-heart mitochondria. Biochim. Biophys. Acta 1990, 1016:207-212.
121. Paradies G., Paradies V., Ruggiero F.M., Petrosillo G. Changes in the mitochondrial permeability transition pore in aging and age-associated diseases. Mech. Ageing Dev. 2013, 134:1-9.
122. Paradies G., Paradies V., De Benedictis V., Ruggiero F.M., Petrosillo G. Functional role of cardiolipin in mitochondrial bioenergetics. Biochim. Biophys. Acta (BBA) 2014, 1837:408-417.
123. Pastoris O., Boschi F., Verri M., Baiardi P., Felzani G., Vecchiet J., Dossena M., Catapano M. The effects of aging on enzyme activities and metabolite concentrations in skeletal muscle from sedentary male and female subjects. Exp. Gerontol. 2000, 35:95-104.
124. Peterson C.M., Johannsen D.L., Ravussin E. Skeletal muscle mitochondria and aging: a review. J. Aging Res. 2012, 2012:194821.
125. Picard M., Ritchie D., Wright K.J., Romestaing C., Thomas M.M., Rowan S.L., Taivassalo T., Hepple R.T. Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 2010, 9:1032-1046.
126. Picard M., Taivassalo T., Ritchie D., Wright K.J., Thomas M.M., Romestaing C., Hepple R.T. Mitochondrial structure and function are disrupted by standard isolation methods. PLoS One 2011, 6:e18317.
127. Picard M., Wright K.J., Ritchie D., Thomas M.M., Hepple R.T. Mitochondrial function in permeabilized cardiomyocytes is largely preserved in the senescent rat myocardium. PLoS One 2012, 7:e43003.
128. Porras C.A., Bai Y. Respiratory supercomplexes: plasticity and implications. Front. Biosci. 2015, 20:621-634.
129. Rasmussen U.F., Krustrup P., Kjaer M., Rasmussen H.N. Experimental evidence against the mitochondrial theory of aging: a study of isolated human skeletal muscle mitochondria. Exp. Gerontol. 2003, 38:877-886.
130. Reeg S., Grune T. Protein oxidation in aging: does it play a role in aging progression?. Antioxid. Redox Signaling 2015, 23:239-255.
131. Rosca M., Minkler P., Hoppel C.L. Cardiac mitochondria in heart failure: normal cardiolipin profile and increased threonine phosphorylation of complex IV. Biochim. Biophys. Acta 2011, 1807:1373-1382.
132. Sabbah H.N., Chandler M.P., Mishima T., Suzuki G., Chaudhry P., Nass O., Biesiadecki B.J., Blackburn B., Wolff A., Stanley W.C. Ranolazine, a partial fatty acid oxidation (pFOX) inhibitor, improves left ventricular function in dogs with chronic heart failure. J. Card. Fail. 2002, 8:416-422.
133. Saks V.A., Aliev M.K. Is there the creatine kinase equilibrium in working heart cells?. Biochem. Biophys. Res. Commun. 1996, 227:360-367.
134. Saks V.A., Kaambre T., Sikk P., Eimre M., Orlova E., Paju K., Piirsoo A., Appaix F., Kay L., Regitz-Zagrosek V., Fleck E., Seppet E. Intracellular energetic units in red muscle cells. Biochem. J. 2001, 356:643-657.
135. Saks V., Kuznetsov A., Andrienko T., Usson Y., Appaix F., Guerrero K., Kaambre T., Sikk P., Lemba M., Vendelin M. Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells. Biophys. J. 2003, 84:3436-3456.
136. Saks V., Beraud N., Wallimann T. Metabolic compartmentation-a system level property of muscle cells: real problems of diffusion in living cells. Int. J. Mol. Sci. 2008, 9:751-767.
137. Saks V., Kaambre T., Guzun R., Anmann T., Sikk P., Schlattner U., Wallimann T., Aliev M., Vendelin M. The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations the Impact of the mitochondrial outer membrane and modelling approaches. Subcell. Biochem. 2008, 27-65.
138. Saks V., Guzun R., Timohhina N., Tepp K., Varikmaa M., Monge C., Beraud N., Kaambre T., Kuznetsov A., Kadaja L., Eimre M., Seppet E. Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial Interactosome. Biochim. Biophys. Acta 2010, 1797:678-697.
139. Saks V., Kuznetsov A.V., Gonzalez-Granillo M., Tepp K., Timohhina N., Karu-Varikmaa M., Kaambre T., Dos Santos P., Boucher F., Guzun R. Intracellular energetic units regulate metabolism in cardiac cells. J. Mol. Cell. Cardiol. 2012, 52:419-436.
140. Saks V., Schlattner U., Tokarska-Schlattner M., Wallimann T., Bagur R., Zorman S., Pelosse M., Santos P., Boucher F., Kaambre T., Guzun R. Systems level regulation of cardiac energy fluxes via metabolic cycles: role of creatine, phosphotransfer pathways, and AMPK signaling. Systems Biology of Metabolic and Signaling Networks 2014, 261-320. Springer, Berlin, Heidelberg. M.A. Aon, V. Saks, U. Schlattner (Eds.).
141. Sample J., Cleland J.G.F., Seymour A.-M.L. Metabolic remodeling in the aging heart. J. Mol. Cell. Cardiol. 2006, 40:56-63.
142. Sanz A., Stefanatos R.K. The mitochondrial free radical theory of aging: a critical view. Curr. Aging Sci. 2008, 1:10-21.
143. Schlattner U., Gehring F., Vernoux N., Tokarska-Schlattner M., Neumann D., Marcillat O., Vial C., Wallimann T. C-terminal lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. J. Biol. Chem. 2004, 279:24334-24342.
144. Schuenke M.D., Brooks N.E., Hikida R.S. Interactions of aging, overload, and creatine supplementation in rat plantaris muscle. J. Aging Res. 2011, 2011:393416.
145. Schultz E., Lipton B.H. Skeletal muscle satellite cells: changes in proliferation potential as a function of age. Mech. Ageing Dev. 1982, 20:377-383.
146. Selivanov V.A., Krause S., Roca J., Cascante M. Modeling of spatial metabolite distributions in the cardiac sarcomere. Biophys. J. 2007, 92:3492-3500.
147. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., Wu T.D., Guerquin-Kern J.L., Lechene C.P., Lee R.T. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493:433-436.
148. Seppet E.K., Eimre M., Anmann T., Seppet E., Piirsoo A., Peet N., Paju K., Guzun R., Beraud N., Pelloux S., Tourneur Y., Kuznetsov A.V., Kaambre T., Sikk P., Saks V.A. Structure-function relationships in the regulation of energy transfer between mitochondria and ATPases in cardiac cells. Exp Clin Cardiol 2006, 11:189-194.
149. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10771-10778.
150. Shih H., Lee B., Lee R.J., Boyle A.J. The aging heart and post-infarction left ventricular remodeling. J. Am. Coll. Cardiol. 2011, 57:9-17.
151. Short K.R., Bigelow M.L., Kahl J., Singh R., Coenen-Schimke J., Raghavakaimal S., Nair K.S. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5618-5623.
152. Sohal R.S., Ku H.H., Agarwal S., Forster M.J., Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech. Ageing Dev. 1994, 74:121-133.
153. Sohal R.S. Oxidative stress hypothesis of aging. Free Radic. Biol. Med. 2002, 33:573-574.
154. Song M., Dorn G.W. Mitoconfusion: noncanonical functioning of dynamism factors in static mitochondria of the heart. Cell Metab. 2015, 21:195-205.
155. Stanley W.C., Recchia F.A., Lopaschuk G.D. Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev. 2005, 85:1093-1129.
156. Strehler B.L. Genetic instability as the primary cause of human aging. Exp. Gerontol. 1986, 21:283-319.
157. Sung M.M.Y., Soltys C.L.M., Masson G., Boisvenue J.J., Dyck J.R.B. Improved cardiac metabolism and activation of the RISK pathway contributes to improved post-ischemic recovery in calorie restricted mice. J. Mol. Med. (JMM) 2011, 89:291-302.
158. Taneike M., Yamaguchi O., Nakai A., Hikoso S., Takeda T., Mizote I., Oka T., Tamai T., Oyabu J., Murakawa T., Nishida K., Shimizu T., Hori M., Komuro I., Takuji Shirasawa T.S., Mizushima N., Otsu K. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy 2010, 6:600-606.
159. Tatarkova Z., Kuka S., Racay P., Lehotsky J., Dobrota D., Mistuna D., Kaplan P. Effects of aging on activities of mitochondrial electron transport chain complexes and oxidative damage in rat heart. Physiol. Res./Academia Scientiarum Bohemoslovaca 2011, 60:281-289.
160. Tepp K., Shevchuk I., Chekulayev V., Timohhina N., Kuznetsov A.V., Guzun R., Saks V., Kaambre T. High efficiency of energy flux controls within mitochondrial interactosome in cardiac intracellular energetic units. Biochim. Biophys. Acta 2011, 1807:1549-1561.
161. Tepp K., Mado K., Varikmaa M., Klepinin A., Timohhina N., Shevchuk I., Chekulayev V., Kuznetsov A.V., Guzun R., Kaambre T. The role of tubulin in the mitochondrial metabolism and arrangement in muscle cells. J. Bioenerg. Biomembr. 2014, 46:421-434.
162. Terman A., Kurz T., Navratil M., Arriaga E.A., Brunk U.T. Mitochondrial turnover and aging of long-lived postmitotic cells: the mitochondrial-lysosomal axis theory of aging. Antioxid. Redox Signal. 2010, 12:503-535.
163. Timohhina N., Guzun R., Tepp K., Monge C., Varikmaa M., Vija H., Sikk P., Kaambre T., Sackett D., Saks V. Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for mitochondrial interactosome. J. Bioenerg. Biomembr. 2009, 41:259-275.
164. Troen B.R. The Biology of Aging 2003, 70:3-22. The Mount Sinai Journal of Medicine, New York.
165. Undrovinas A.I., Belardinelli L., Undrovinas N.A., Sabbah H.N. Ranolazine improves abnormal repolarization and contraction in left ventricular myocytes of dogs with heart failure by inhibiting late sodium current. J. Cardiovasc. Electrophysiol. 2006, 17(Suppl. 1):S169-S177.
166. Varikmaa M., Bagur R., Kaambre T., Grichine A., Timohhina N., Tepp K., Shevchuk I., Chekulayev V., Metsis M., Boucher F., Saks V., Kuznetsov A.V., Guzun R. Role of mitochondria-cytoskeleton interactions in respiration regulation and mitochondrial organization in striated muscles. Biochim. Biophys. Acta (BBA) 2014, 1837:232-245.
167. Vartak R., Porras C.A., Bai Y. Respiratory supercomplexes: structure, function and assembly. Protein Cell 2013, 4:582-590.
168. Vendelin M., Birkedal R. Anisotropic diffusion of fluorescently labeled ATP in rat cardiomyocytes determined by raster image correlation spectroscopy. Am. J. Physiol. Cell Physiol. 2008, 295:C1302-1315.
169. Vendelin M., Kongas O., Saks V. Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer. Am. J. Physiol. Cell Physiol. 2000, 278:C747-764.
170. Vendelin M., Eimre M., Seppet E., Peet N., Andrienko T., Lemba M., Engelbrecht J., Seppet E.K., Saks V.A. Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol. Cell. Biochem. 2004, 256-257:229-241.
171. Vendelin M., Beraud N., Guerrero K., Andrienko T., Kuznetsov A.V., Olivares J., Kay L., Saks V.A. Mitochondrial regular arrangement in muscle cells: a crystal-like pattern. Am. J. Physiol. Cell Physiol. 2005, 288:C757-767.
172. Vendelin, M., Saks, V., Engelbrecht, J., 2007. Principles of Mathematical Modeling and in Silico Studies of Integrated Cellular Energetics, in: Prof. Valdur, S. (Ed.), Molecular System Bioenergetics, pp. 407-433.
173. Ventura-Clapier R., Garnier A., Veksler V. Energy metabolism in heart failure. J. Physiol. 2004, 555:1-13.
174. Ventura-Clapier R., Garnier A., Veksler V., Joubert F. Bioenergetics of the failing heart. Biochim. Biophys. Acta (BBA) 2011, 1813:1360-1372.
175. Wai T., Garcia-Prieto J., Baker M.J., Merkwirth C., Benit P., Rustin P., Ruperez F.J., Barbas C., Ibanez B., Langer T. Imbalanced OPA1 processing and mitochondrial fragmentation cause heart failure in mice. Science 2015, 350:aad0116.
176. Wang M., Shah A.M. Age-associated pro-inflammatory remodeling and functional phenotype in the heart and large arteries. J. Mol. Cell. Cardiol. 2015, 83:101-111.
177. Wang X., Guo Z., Ding Z., Khaidakov M., Lin J., Xu Z., Sharma S.G., Jiwani S., Mehta J.L. Endothelin-1 upregulation mediates aging-related cardiac fibrosis. J. Mol. Cell. Cardiol. 2015.
178. Weber T.A., Reichert A.S. Impaired quality control of mitochondria: aging from a new perspective. Exp. Gerontol. 2010, 45:503-511.
179. Wei Y.H., Wu S.B., Ma Y.S., Lee H.C. Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med. J. 2009, 32:113-132.
180. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 2010, 11:872-884.
181. Williamson J.R., Ford C., Illingworth J., Safer B. Coordination of citric acid cycle activity with electron transport flux. Circ. Res. 1976, 38:I39-51.
182. Wittig I., Carrozzo R., Santorelli F.M., Schagger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 2006, 1757:1066-1072.
183. Yaffe M.P., Harata D., Verde F., Eddison M., Toda T., Nurse P. Microtubules mediate mitochondrial distribution in fission yeast. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11664-11668.
184. Yan L., Ge H., Li H., Lieber S.C., Natividad F., Resuello R.R., Kim S.J., Akeju S., Sun A., Loo K., Peppas A.P., Rossi F., Lewandowski E.D., Thomas A.P., Vatner S.F., Vatner D.E. Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts. J. Mol. Cell. Cardiol. 2004, 37:921-929.
185. Yaniv Y., Juhaszova M., Sollott S.J. Age-related changes of myocardial ATP supply and demand mechanisms. Trends Endocrinol. Metab. 2013, 24:495-505.
186. Yechiel E., Henis Y.I., Barenholz Y. Aging of rat heart fibroblasts: relationship between lipid composition, membrane organization and biological properties. Biochim. Biophys. Acta 1986, 859:95-104.
187. Zainal T.A., Oberley T.D., Allison D.B., Szweda L.I., Weindruch R. Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J. 2000, 14:1825-1836.
188. Zhang C., Liu V.W., Addessi C.L., Sheffield D.A., Linnane A.W., Nagley P. Differential occurrence of mutations in mitochondrial DNA of human skeletal muscle during aging. Hum. Mutat. 1998, 11:360-371.
189. Zhang M., Mileykovskaya E., Dowhan W. Gluing the respiratory chain together: cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 2002, 277:43553-43556.
190. Zhang Y., Ikeno Y., Qi W., Chaudhuri A., Li Y., Bokov A., Thorpe S.R., Baynes J.W., Epstein C., Richardson A., Van Remmen H. Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity. J. Gerontol. A. Biol. Sci. Med. Sci. 2009, 64:1212-1220.
191. Zhao L., Zou X., Feng Z., Luo C., Liu J., Li H., Chang L., Wang H., Li Y., Long J., Gao F., Liu J. Evidence for association of mitochondrial metabolism alteration with lipid accumulation in aging rats. Exp. Gerontol. 2014, 56:3-12.
192. van Berlo J.H., Molkentin J.D. An emerging consensus on cardiac regeneration. Nat. Med. 2014, 20:1386-1393.
193. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.