Mitochondrial function in permeabilized cardiomyocytes is largely preserved in the senescent rat myocardium

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

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

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CITRATE SYNTHASE; COPPER ZINC SUPEROXIDE DISMUTASE; ELECTRON TRANSPORT CHAIN PROTEIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; SAPONIN; UNCLASSIFIED DRUG;

ADULT ANIMAL; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; HEART MITOCHONDRION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; RAT; RESPIRATORY CHAIN; SENSITIZATION; STRUCTURE ANALYSIS;

AGE FACTORS; AGING; ANIMALS; APOPTOSIS; BODY WEIGHT; CALCIUM; CITRATE (SI)-SYNTHASE; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FIBROSIS; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, CARDIAC; ORGAN SIZE; RATS; SAPONINS;

EID: 84864994781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043003     Document Type: Article

References (57)

1. Wallace DC, ((2005)) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:: 359--407.
2. Bratic I, Trifunovic A, ((2010)) Mitochondrial energy metabolism and ageing. Biochim Biophys Acta 1797:: 961--967.
3. Sahin E, Depinho RA, ((2010)) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464:: 520--528.
4. Wanagat J, Wolff MR, Aiken JM, ((2002)) Age-associated changes in function, structure and mitochondrial genetic and enzymatic abnormalities in the Fischer 344 x Brown Norway F(1) hybrid rat heart. J Mol Cell Cardiol 34:: 17--28.
5. Kakarla SK, Rice KM, Katta A, Paturi S, Wu M, et al. ((2010)) Possible molecular mechanisms underlying age-related cardiomyocyte apoptosis in the F344XBN rat heart. J Gerontol A Biol Sci Med Sci 65:: 147--155.
6. Boyle AJ, Shih H, Hwang J, Ye J, Lee B, et al. ((2011)) Cardiomyopathy of aging in the mammalian heart is characterized by myocardial hypertrophy, fibrosis and a predisposition towards cardiomyocyte apoptosis and autophagy. Exp Gerontol 46:: 549--559.
7. Hacker TA, McKiernan SH, Douglas PS, Wanagat J, Aiken JM, ((2006)) Age-related changes in cardiac structure and function in Fischer 344 x Brown Norway hybrid rats. Am J Physiol Heart Circ Physiol 290:: H304--311.
8. Anversa P, Palackal T, Sonnenblick EH, Olivetti G, Meggs LG, et al. ((1990)) Myocyte cell loss and myocyte cellular hyperplasia in the hypertrophied aging rat heart. Circ Res 67:: 871--885.
9. Kwak HB, Song W, Lawler JM, ((2006)) Exercise training attenuates age-induced elevation in Bax/Bcl-2 ratio, apoptosis, and remodeling in the rat heart. FASEB J 20:: 791--793.
10. Olivetti G, Melissari M, Capasso JM, Anversa P, ((1991)) Cardiomyopathy of the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circ Res 68:: 1560--1568.
11. Hagen TM, Moreau R, Suh JH, Visioli F, ((2002)) Mitochondrial decay in the aging rat heart: evidence for improvement by dietary supplementation with acetyl-L-carnitine and/or lipoic acid. Ann N Y Acad Sci 959:: 491--507.
12. Kajstura J, Cheng W, Sarangarajan R, Li P, Li B, et al. ((1996)) Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am J Physiol 271:: H1215--1228.
13. Lakatta EG, Levy D, ((2003)) Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part II: the aging heart in health: links to heart disease. Circulation 107:: 346--354.
14. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP, ((1989)) Left ventricular mass and incidence of coronary heart disease in an elderly cohort. The Framingham Heart Study. Ann Intern Med 110:: 101--107.
15. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP, ((1990)) Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 322:: 1561--1566.
16. Hofer T, Servais S, Seo AY, Marzetti E, Hiona A, et al. ((2009)) Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech Ageing Dev 130:: 297--307.
17. Ljubicic V, Menzies KJ, Hood DA, ((2010)) Mitochondrial dysfunction is associated with a pro-apoptotic cellular environment in senescent cardiac muscle. Mech Ageing Dev 131:: 79--88.
18. Petrosillo G, Moro N, Paradies V, Ruggiero FM, Paradies G, ((2010)) Increased susceptibility to Ca(2+)-induced permeability transition and to cytochrome c release in rat heart mitochondria with aging: effect of melatonin. J Pineal Res 48:: 340--346.
19. Phaneuf S, Leeuwenburgh C, ((2002)) Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age. Am J Physiol Regul Integr Comp Physiol 282:: R423--430.
20. Corsetti G, Pasini E, D'Antona G, Nisoli E, Flati V, et al. ((2008)) Morphometric changes induced by amino acid supplementation in skeletal and cardiac muscles of old mice. Am J Cardiol 101:: 26E--34E.
21. Frolkis VV, Frolkis RA, Mkhitarian LS, Shevchuk VG, Fraifeld VE, et al. ((1988)) Contractile function and Ca2+ transport system of myocardium in ageing. Gerontology 34:: 64--74.
22. Picard M, Taivassalo T, Gouspillou G, Hepple RT, ((2011)) Mitochondria: Isolation, Structure and Function. J Physiol 589:: 4413--4421.
23. Lemieux H, Vazquez EJ, Fujioka H, Hoppel CL, ((2010)) Decrease in Mitochondrial Function in Rat Cardiac Permeabilized Fibers Correlates With the Aging Phenotype. J Gerontol A Biol Sci Med Sci. DOI: 0.1093/gerona/glq11411.
24. Picard M, Ritchie D, Wright KJ, Romestaing C, Melissa MT, et al. ((2010)) Mitochondrial Functional Impairment with Aging is Exaggerated in Isolated Mitochondria compared to Permeabilized Myofibers. Aging Cell 9:: 1032--1046.
25. Betik AC, Thomas MM, Wright KJ, Riel CD, Hepple RT, ((2009)) Exercise training from late middle age until senescence does not attenuate the declines in skeletal muscle aerobic function. Am J Physiol Regul Integr Comp Physiol 297:: R744--755.
26. Bancroft JD, Stevens A (1982) Theory and practice of histological techniques. New York: Churchill Livingstone.
27. Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA, ((1987)) Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892:: 191--196.
28. Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, et al. ((1998)) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184:: 81--100.
29. Picard M, Csukly K, Robillard ME, Godin R, Ascah A, et al. ((2008)) Resistance to Ca2+-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. Am J Physiol Regul Integr Comp Physiol 295:: R659--668.
30. 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--851.
31. Tweedie C, Romestaing C, Burelle Y, Safdar A, Tarnopolsky MA, et al. ((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.
32. Kajstura J, Gurusamy N, Ogorek B, Goichberg P, Clavo-Rondon C, et al. ((2010)) Myocyte turnover in the aging human heart. Circ Res 107:: 1374--1386.
33. Niemann B, Chen Y, Issa H, Silber RE, Rohrbach S, ((2010)) Caloric restriction delays cardiac ageing in rats: role of mitochondria. Cardiovasc Res 88:: 267--276.
34. Shinmura K, Tamaki K, Sano M, Murata M, Yamakawa H, et al. ((2011)) Impact of long-term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging. J Mol Cell Cardiol 50:: 117--127.
35. Lipman RD, Chrisp CE, Hazzard DG, Bronson RT, ((1996)) Pathologic characterization of brown Norway, brown Norway x Fischer 344, and Fischer 344 x brown Norway rats with relation to age. J Gerontol A Biol Sci Med Sci 51:: B54--59.
36. Miro O, Casademont J, Casals E, Perea M, Urbano-Marquez A, et al. ((2000)) Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain enzyme defects. Cardiovasc Res 47:: 624--631.
37. Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C, ((2005)) Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19:: 419--421.
38. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, et al. ((2006)) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:: 397--408.
39. Gredilla R, Sanz A, Lopez-Torres M, Barja G, ((2001)) Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 15:: 1589--1591.
40. Hansford RG, Hogue BA, Mildaziene V, ((1997)) Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age. J Bioenerg Biomembr 29:: 89--95.
41. Mansouri A, Muller FL, Liu Y, Ng R, Faulkner J, et al. ((2006)) Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127:: 298--306.
42. Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, et al. ((2009)) Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 119:: 2789--2797.
43. Dai DF, Chen T, Wanagat J, Laflamme M, Marcinek DJ, et al. ((2010)) Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 9:: 536--544.
44. Hua Y, Zhang Y, Ceylan-Isik AF, Wold LE, Nunn JM, et al. ((2011)) Chronic Akt activation accentuates aging-induced cardiac hypertrophy and myocardial contractile dysfunction: role of autophagy. Basic Res Cardiol 106:: 1173--1191.
45. Zhang D, Ezekiel UR, Chang SW, Zassenhaus HP, ((2005)) Gene expression profile in dilated cardiomyopathy caused by elevated frequencies of mitochondrial DNA mutations in the mouse heart. Cardiovasc Pathol 14:: 61--69.
46. Lesnefsky EJ, Gudz TI, Moghaddas S, Migita CT, Ikeda-Saito M, et al. ((2001)) Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 33:: 37--47.
47. Manzelmann MS, Harmon HJ, ((1987)) Lack of age-dependent changes in rat heart mitochondria. Mech Ageing Dev 39:: 281--288.
48. Hood DA, ((2001)) Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90:: 1137--1157.
49. Fannin SW, Lesnefsky EJ, Slabe TJ, Hassan MO, Hoppel CL, ((1999)) Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch Biochem Biophys 372:: 399--407.
50. Picard M, Taivassalo T, Ritchie D, Wright KJ, Thomas MT, et al. ((2011)) Mitochondrial Structure and Function are Disrupted by Standard Isolation Methods PLoS One. 6:: e18317.
51. Ong SB, Hausenloy DJ, ((2010)) Mitochondrial morphology and cardiovascular disease. Cardiovasc Res 88:: 16--29.
52. Skulachev VP, ((2001)) Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem Sci 26:: 23--29.
53. Lesnefsky EJ, Hoppel CL, ((2006)) Oxidative phosphorylation and aging. Ageing Res Rev 5:: 402--433.
54. Picard M, ((2011)) Pathways to aging: the mitochondrion at the intersection of biological and psychosocial sciences. J Aging Res 2011:: 814096.
55. Wohlgemuth SE, Julian D, Akin DE, Fried J, Toscano K, et al. ((2007)) Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res 10:: 281--292.
56. Seo AY, Joseph AM, Dutta D, Hwang JCY, Aris JP, et al. ((2010)) New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J Cell Sci 123:: 2532--2542.
57. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, et al. ((2008)) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:: 433--446.