Mitochondrial theory of skeletal muscle ageing –new facts, new doubts

1. Altun M., Besche H.C., Overkleeft H.S., Piccirillo R., Edelmann M.J., Kessler B.M., Goldberg A.L., Ulfhake B.: Muscle wasting in aged, sarcopenic rats is associated with enhanced activity of the ubiquitin proteasome pathway. J Biol Chem 2010, 285, 39597–39608.10.1074/jbc.M110.129718300094120940294Search in Google Scholar

2. Amara C.E., Shankland E.G., Jubrias S.A., Marcinek D.J., Kushmerick M.J., Conley K.E.: Mild mitochondrial uncoupling impacts cellular aging in human muscles in vivo. Proc Natl Acad Sci USA 2007, 104, 1057–1062.10.1073/pnas.0610131104176633617215370Search in Google Scholar

3. Barazzoni R., Short K.R., Nair K.S.: Effects of aging on mitochondria DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J Biol Chem 2000, 275, 3343–3347.10.1074/jbc.275.5.334310652323Search in Google Scholar

4. Barrciro E., Cornell C., Lavina B., Ramirez-Sarmiento A., Orozco-Levi M., Gea J.: Aging sex differences and oxidative stress in human respiratory and limb muscles. Free Radic Biol Med 2006, 41, 797–809.10.1016/j.freeradbiomed.2006.05.02716895800Search in Google Scholar

5. Barrientos A., Casademont J., Cardellach F.: Qualitative and quantitative changes in skeletal muscle mtDNA and expression of mitochondrial-encoded genes in the human aging process. Biochem Mol Med 1997, 62, 165–171.10.1006/bmme.1997.26479441868Search in Google Scholar

6. Bevilacqua L., Ramsey J.J., Hagopian K., Weindruch R., Harper M.E.: Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab 2005, 289, E429–E438.10.1152/ajpendo.00435.200415886224Search in Google Scholar

7. Bjelakovic G., Nikolova D., Gluud L.I., Simonetti R.G., Gluud C.: Mortality in randomized trials of antioxidant supplements for primary and secondary prevention, systematic review and meta-analysis. J Am Med Assoc 2007, 297, 842–857.10.1001/jama.297.8.84217327526Search in Google Scholar

8. Bua E., Johnson J., Herbst A., Delong B., McKenzie D., Salamat S., Aiken J.M.: Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am J Hum Genet 2006, 79, 469–480.10.1086/507132155955016909385Search in Google Scholar

9. Capel F., Rimbert V., Lioger D., Diot A., Rousset P., Mirand P.P., Boirie Y., Morio B., Mosoni L.: Due to reverse electron transfer, mitochondrial H₂O₂ release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mech Ageing Dev 2005, 126, 505–511.10.1016/j.mad.2004.11.00115722109Search in Google Scholar

10. Cipolat S., Rudka T., Hartmann D., Costa V., Serneels L., Craessaerts K., Metzger K., Frezza C., Annaert W., D'Adamio L., Derks C., Dejaegere T., Pellegrini L., D'Hooge R., Scorrano L., De Strooper B.: Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodelling. Cell 2006, 126, 1, 163–175.10.1016/j.cell.2006.06.02116839884Search in Google Scholar

11. Conley K.E., Marcinek D.J., Villarin J.: Mitochondrial dysfunction and age. Curr Opin Nutr Metab Care 2007, 10, 688–692.10.1097/MCO.0b013e3282f0dbfb18089948Search in Google Scholar

12. Crane J.D., Devries M.C., Safdar A., Hamadeh M.J., Tarnopolsky M.A.: The effect of aging on human skeletal muscle mitochondrial and intramyocellular lipid ultrastructure. J Gerontol A Biol Sci Med Sci 2010, 65, 119–128.10.1093/gerona/glp17919959566Search in Google Scholar

13. Cuervo A.M., Bergamini E., Brunk U.T., Droge W., Ffrench M., Terman A.: Autophagy and aging, the importance of maintaining “clean cells”. Autophagy 2005, 1, 131–140.10.4161/auto.1.3.201716874025Search in Google Scholar

14. Chabi B., Ljubicic V., Menzies K.J., Huang J.H., Saleem A., Hood D.A.: Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2008, 7, 2–12.10.1111/j.1474-9726.2007.00347.x18028258Search in Google Scholar

15. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., McCaffery J.M., Chan D.C.: Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141, 280–289.10.1016/j.cell.2010.02.026287681920403324Search in Google Scholar

16. Diaz F., Bayona-Bafaluy M.P., Rana M., Mora M., Hao H., Moraes C.T.: Human mitochondrial DNA with large deletions repopulates organelles faster than full-length genomes under relaxed copy number control. Nucleic Acids Res 2002, 30, 4626–4633.10.1093/nar/gkf60213582212409452Search in Google Scholar

17. Drew B., Phaneuf S., Dirks A., Selman C., Gredilla R., Lezza A,. Barja G., Leeuwenburgh C.: Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am J Physiol 2003, 284, 474–480.10.1152/ajpregu.00455.200212388443Search in Google Scholar

18. Figueiredo P.A., Powers S.K., Ferreira R.M., Amado F., Appell H.J., Duarte J.A.: Impact of lifelong sedentary behaviour on mitochondrial function of mice skeletal muscle. J Gerontol A Biol Sci Med Sci 2009, 64, 927–939.10.1093/gerona/glp066298145219465709Search in Google Scholar

19. Fink S.L., Cookson B.T.: Apoptosis, pyroptosis, and necrosis: Mechanistic Description of Dead and Dying Eukaryotic Cells. Infect Immun 2005, 73, 1907–1916.10.1128/IAI.73.4.1907-1916.2005108741315784530Search in Google Scholar

20. Gelfi C., Vigano A., Ripamonti M., Pontoglio A., Begum S., Pellegrino M.A., Grassi B., Bottinelli R., Wait R., Cerretelli P.: The human muscle proteome in aging. J Proteome Res 2006, 5, 1344–1353.10.1021/pr050414x16739986Search in Google Scholar

21. Giorgi C., Marchi S., Simoes I.C.M., Ren Z., Morciano G., Perrone M., Patalas-Krawczyk P., Borchard S., Jędrak P., Pierzynowska K., Szymański J., Wang D.Q., Portincasa P., Węgrzyn G., Zischka H., Dobrzyn P., Bonora M., Duszynski J., Rimessi A., Karkucińska-Wieckowska A., Dobrzyn A., Szabadkai G., Zavan B., Oliveira P.J., Sardao V.A., Pinton P., Wieckowski M.R.: Mitochondria and reactive oxygen species in aging and age-related diseases. Int Rev Cell Mol Biol 2018, 340, 209–344.10.1016/bs.ircmb.2018.05.006812733230072092Search in Google Scholar

22. Hayashi J.I., Hashizume O., Ishikawa K., Shimizu A.: Mutations in mitochondrial DNA regulate mitochondrial diseases and metastasis but do not regulate aging. Curr Opin Genet Dev 2016, 38, 63–67.10.1016/j.gde.2016.03.00427078865Search in Google Scholar

23. Hepple R.T., Baker D.J., Kaczor J.J., Krause D.J.: Long-term caloric restriction abrogates the age-related decline in skeletal muscle aerobic function. FASEB J 2005, 19, 1320–1322.10.1096/fj.04-3535fje15955841Search in Google Scholar

24. Holloszy J.O.: Skeletal muscle “mitochondrial deficiency” does not mediate insulin resistance. Am J Clin Nutr 2009, 89, 463–466.10.3945/ajcn.2008.26717C19056574Search in Google Scholar

25. Jackson J.R., Ryan M.J., Always S.E.: Long-term supplementation with resveratrol alleviates oxidative stress but does not attenuate sarcopenia in aged mice. J Gerontol A Biol Sci Med Sci 2011, 66, 751–764.10.1093/gerona/glr047314334621454355Search in Google Scholar

26. Jo E.K., Kim J.K., Shin D.M., Sasakawa C.: Molecular mechanisms regulating NLRP3 inflammasome activation. Cell Mol Immunol 2016, 13, 148–159.10.1038/cmi.2015.95478663426549800Search in Google Scholar

27. Johannsen D.L., Conley K.E., Bajpeyi S., Punyanitya M., Gallagher D., Zhang Z., Covington J., Smith S.R., Ravussin E.: Ectopic lipid accumulation and reduced glucose tolerance in elderly adults are accompanied by altered skeletal muscle mitochondrial activity. J Clin Endocrinol Metab 2012, 97, 242–250.10.1210/jc.2011-1798325194022049170Search in Google Scholar

28. Johannsen D.L., DeLany J.P., Frisard M.I., Welsch M.A., Rowley C.K., Fang X., Jazwinski S.M., Ravussin E.: Physical activity in aging: comparison among young, aged, and nonagenarian individuals. J Appl Physiol 2008, 105, 495–501.10.1152/japplphysiol.90450.2008251994318556430Search in Google Scholar

29. Khrapko K.: The timing of mitochondrial DNA mutations in aging. Nat Genet 2011, 43, 726–727.10.1038/ng.895367097021792237Search in Google Scholar

30. Khrapko K., Vijg J.: Mitochondrial DNA mutations and aging: devils in the details? Trends Genet 2009, 25, 91–98.10.1016/j.tig.2008.11.007281109219110336Search in Google Scholar

31. Kirkwood T.B.L.: A systematic look at an old problem. Nature 2008, 451, 644–647.10.1038/451644a18256658Search in Google Scholar

32. Kowald A., Kirkwood T.B.L.: Evolution of the mitochondrial fusion-fission cycle and its role in aging. Proc Natl Acad Sci USA 2011, 108, 10237–10242.10.1073/pnas.1101604108312181021646529Search in Google Scholar

33. Krishnan K.J., Reeve A.K., Samuels D.C., Chinnery P.F., Blackwood J.K., Taylor R.W., Wanrooij S., Spelbrink J.N, Lightowlers R.N., Turnbull D.M.: What causes mitochondrial DNA deletions in human cells? Nat Genet 2008, 40, 275–279.10.1038/ng.f.9418305478Search in Google Scholar

34. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., Van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., Prolla T.A.: Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005, 309, 481–484.10.1126/science.111212516020738Search in Google Scholar

35. Kushnareva Y., Murphy A.N., Andreyev A.: Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J 2002, 368, 545–553.10.1042/bj20021121122299912180906Search in Google Scholar

36. Lam J., McKeague M., Dietary modulation of mitochondrial DNA damage: implications in aging and associated diseases. J Nutr Biochem 2018, 63, 1–10.10.1016/j.jnutbio.2018.07.00330071405Search in Google Scholar

37. Lanza I.R., Larsen R.G., Kent-Braun J.A.: Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J Physiol 2007, 583, 1093–1105.10.1113/jphysiol.2007.138362227719417673506Search in Google Scholar

38. Lanza I.R., Short D.K., Short K.R., Raghavakaimal S., Basu R., Joyner M.J.: Endurance exercise as a countermeasure for aging. Diabetes 2008, 57, 2933–2942.10.2337/db08-0349257038918716044Search in Google Scholar

39. Larsson N.G.: Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem 2010, 79, 683–706.10.1146/annurev-biochem-060408-09370120350166Search in Google Scholar

40. Lee H.Y., Choi C.S., Birkenfeld A.L., Alves T.C., Jonayvaz F.R., Jurczak M.J., Zhang D., Woo D.K., Shadel G.S., Ladiges W., Rabinovitch P.S.., Santos J.H., Petersen K.F., Samuel V.T., Shulman G.I.: Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metab 2010, 12, 668–674.10.1016/j.cmet.2010.11.004301334921109199Search in Google Scholar

41. Leeuwenburgh C., Gurley C.M., Strotman B.A., Dupont-Versteegden E.E.: Age-related differences in apoptosis with disuse atrophy in soleus muscle. Am J Physiol 2005, 288, R1288–R1296.10.1152/ajpregu.00576.200415650125Search in Google Scholar

42. Lodi R., Tonon C., Valentino M.L., Iotti S., Clementi V., Malucelli E., Barboni P., Longanesi L., Schimpf S., Wissinger B., Baruzzi A., Barbiroli B., Carelli V.: Deficit of in vivo mitochondrial ATP production in OPA1-related dominant optic atrophy. Ann Neurol 2004, 56, 719–723.10.1002/ana.2027815505825Search in Google Scholar

43. Low P.: The role of ubiquitin-proteasome system in ageing. Gen Comp Endocrinol 2011, 172, 39–43.10.1016/j.ygcen.2011.02.00521324320Search in Google Scholar

44. Marcinek D.J., Schenkman K.A., Ciesielski W.A., Lee D., Conley K.E.: Reduced mitochondrial coupling in vivo alters cellular energetics in aged mouse skeletal muscle. J Physiol 2005, 569, 467–473.10.1113/jphysiol.2005.097782146424716254011Search in Google Scholar

45. Marzetti E., Hwang J.C., Lees H.A., Wohlgemuth S.E., Dupont-Versteegden E.E., Carter C.S., Bernabei R., Leeuwenburgh C.: Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy. Biochim Biophys Acta 2010, 1800, 235–244.10.1016/j.bbagen.2009.05.007282651419450666Search in Google Scholar

46. Melov S., Tarnopolsky M.A,. Beckman K., Felkey K., Hubbard A.: Resistance exercise reverses aging in human skeletal muscle. PLoS ONE 2007, 2, e465.10.1371/journal.pone.0000465186618117520024Search in Google Scholar

47. Miller B.F., Robinson M.M., Bruss M.D., Hellerstein M., Hamilton K.L.: A comprehensive assessment of mitochondrial protein synthesis and cellular proliferation with age and caloric restriction. Aging Cell 2012, 11, 150–161.10.1111/j.1474-9726.2011.00769.x325737122081942Search in Google Scholar

48. Molnar R.I., Bartelmes G., Dinkelacker I., Witte H, Sommer R.J.: Mutation rates and intraspecific divergence of the mitochondrial genome of pristionchus pacificus. Mol Biol Evol 2011, 28, 2317–2326.10.1093/molbev/msr05721368317Search in Google Scholar

49. Murase T., Haramizu S., Ota N., Hase T.: Suppression of the aging-associated decline in physical performance by a combination of resveratrol intake and habitual exercise in senescence-accelerated mice. Biogerontology 2009, 10, 423–434.10.1007/s10522-008-9177-z18830683Search in Google Scholar

50. Nakamura S., Takamura T., Matsuzawa-Nagata N., Takayama H., Misu H., Noda H., Nabemoto S., Kurita S., Ota T., Ando H., Miyamoto K., Kaneko S.: Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J Biol Chem 2009, 284, 14809–14818.10.1074/jbc.M901488200268566219332540Search in Google Scholar

51. O’Connell K., Ohlendieck K.: Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 2009, 9, 5509–5524.10.1002/pmic.20090047219834913Search in Google Scholar

52. Okamoto K., Kondo-Okamoto N., Ohsumi Y.: Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009, 17, 87–97.10.1016/j.devcel.2009.06.01319619494Search in Google Scholar

53. Park S.Y., Kim H.Y., Lee J.H., Yoon K.H., Chang M.S., Park S.K.: The age-dependent induction of apoptosis-inducing factor (AIF) in the human semitendinosus skeletal muscle. Cell Mol Biol Lett 2010, 15, 1–2.10.2478/s11658-009-0030-4627559819685011Search in Google Scholar

54. Payne B.A., Wilson I.J., Yu-Wai-Man P., Coxhead J., Deehan D., Horvath R., Taylor R.W., Samuels D.C., Santibanez-Koref M., Chinnery P.F.: Universal heteroplasmy of human mitochondrial DNA. Hum Mol Genet 2013, 22, 384–390.10.1093/hmg/dds435352616523077218Search in Google Scholar

55. Petersen K.F., Befroy D., Dufour S.: Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003, 300, 5622, 1140–1142.10.1126/science.1082889300442912750520Search in Google Scholar

56. Peterson C.M., Johannsen D.L., Ravussin E.: Skeletal muscle mitochondria and aging: A review. J Aging Res 2012, 2012: 194821, doi: 10.1155/2012/194821.10.1155/2012/194821340865122888430Search in Google Scholar

57. Ren J., Li Q., Wu S., Li S.Y., Babcock S.A.: Cardiac overexpression of antioxidant catalase attenuates aging-induced cardiomyocyte relaxation dysfunction. Mech Ageing Dev 2007, 128, 276–285.10.1016/j.mad.2006.12.007184733117250874Search in Google Scholar

58. Reznick R.M., Zong H., Li J.: Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 2007, 5, 151–156.10.1016/j.cmet.2007.01.008188596417276357Search in Google Scholar

59. Romanello V., Guadagnin E., Gomes L.: Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 2010, 29, 1774–1785.10.1038/emboj.2010.60287696520400940Search in Google Scholar

60. Ross J.M., Stewart J.B., Hagstrom E., Brene S., Mouries A., Coppotelli G., Freyer C., Lagouge M., Hoffer B.J., Olson L., Larsson N.G.: Germline mitochondrial DNA mutations aggravate ageing and can impair brain development. Nature 2013, 501, 412–415.10.1038/nature12474382042023965628Search in Google Scholar

61. Safdar S., Hamadeh M.J., Kaczor J.J., Raha S., Debeer J., Tarnopolsky M.A.: Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLoS ONE 2010, 5, e10778.10.1371/journal.pone.0010778287539220520725Search in Google Scholar

62. Scheckhuber C.Q., Wanger R.A., Mignat C.A., Osiewacz H.D.: Unopposed mitochondrial fission leads to severe lifespan shortening. Cell Cycle 2011, 10, 3105–3110.10.4161/cc.10.18.1719621912203Search in Google Scholar

63. Schunk K., Pitton M., Duber C., Kersjes W., Schadmand-Fischer S., Thelen M.: Dynamic phosphorus-31 magnetic resonance spectroscopy of the quadriceps muscle: effects of age and sex on spectroscopic results. Invest Radiol 1999, 34, 116–125.10.1097/00004424-199902000-000049951791Search in Google Scholar

64. Seirafi M., Kozlov G., Gehring K.: Parkin structure and function. FEBS J 2015, 282, 2076–2088.10.1111/febs.13249467269125712550Search in Google Scholar

65. Short K.R., Vittone J.L., Bigelow M.L., Proctor D.N., Nair K.S.: Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol 2004, 286, 92–101.10.1152/ajpendo.00366.200314506079Search in Google Scholar

66. Shulman G.I.: Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metab 2010, 12, 668–674.10.1016/j.cmet.2010.11.004301334921109199Search in Google Scholar

67. Song S., Pursell Z.F., Copeland W.C., Longley M.J., Kunkel T.A., Mathews C.K.: DNA precursor asymmetries in mammalian tissue mitochondria and possible contribution to mutagenesis through reduced replication fidelity. Proc Natl Acad Sci USA 2005, 102, 4990–4995.10.1073/pnas.050025310255599615784738Search in Google Scholar

68. Speakman J.R., Mitchell S.E.: Caloric restriction. Mol Aspects Med 2011, 32, 159–221.10.1016/j.mam.2011.07.00121840335Search in Google Scholar

69. Stumpf J.D., Saneto R.P., Copeland W.C.: Clinical and molecular features of POLG-related mitochondrial disease. Cold Spring Harb Perspect Biol 2013, 5, a011395.10.1101/cshperspect.a011395368390223545419Search in Google Scholar

70. Taylor E.B., Rutter J.: Mitochondrial quality control by the ubiquitin-proteasome system. Biochem Soc Trans 2011, 39, 1509–1513.10.1042/BST039150921936843Search in Google Scholar

71. Twig G., Hyde B., Shirihai O.S.: Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 2008, 1777, 1092–1097.10.1016/j.bbabio.2008.05.001380901718519024Search in Google Scholar

72. Um J.H., Park S.J., Kang H., Yang S., Foretz M., McBurney M.W., Kim M.K., Viollet B., Chung J.H.: AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 2010, 59, 554–563.10.2337/db09-0482282864719934007Search in Google Scholar

73. Wenz T., Rossi S.G., Rotundo R.L., Spiegelman B.M., Moraes C.T.: Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci U S A. 2009, 106, 20405–20410.Search in Google Scholar

74. Whitman S.A., Wacker M.J., Richmond S.R., Godard M.P.: Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch 2005, 450, 437–446.10.1007/s00424-005-1473-815952031Search in Google Scholar

75. Wohlgemuth S.E., Seo A.Y., Marzetti E., Lees H.A., Leeuwenburgh C.: Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 2010, 45, 138–148.10.1016/j.exger.2009.11.002282994219903516Search in Google Scholar

76. Wolff J.N., Camus M.F., Dowling D.K., Rogell B.: Mitochondrial genome variation affects the mutation rate of the nuclear genome in Drosophila melanogaster. BioRXiV 2017, doi: 10.1101/122234.10.1101/122234Open DOISearch in Google Scholar

77. 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, 1825–1836.10.1096/fj.99-0881com10973932Search in Google Scholar

78. Zarse K., Schmeisser S., Groth M., Priebe S., Beuster G., Kuhlow D., Guthke R., Platzer M., Kahn C.R., Ristow M.: Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab 2012, 15, 451–465.10.1016/j.cmet.2012.02.013484485322482728Search in Google Scholar