Skip to main content
SpringerLink
Log in

Muscle Biopsy To Investigate Mitochondrial Turnover

  • Chapter
Cellular Physiology and Metabolism of Physical Exercise

  • 2244 Accesses

Abstract

Skeletal muscle biopsy is a long-established diagnostic used primarily as a diagnostic tool for neuromuscular disorders characterized by reduced muscle function and strength. For anatomical and functional characteristics, leg muscles and especially the vastus lateralis have been most commonly investigated. Percutaneous needles, which overcame the more invasive open biopsies, were introduced more than 50 years ago, with the original instruments named after Bergstrom [1], in honor of his pioneering work in their development (Fig. 8.1). When adequate suction is applied and a sufficient amount of muscle tissue is recovered, muscle biopsy allows for multiple measurements as well as the assessment of different anatomical or physiological parameters. Fiber and cell isolation, incubation, or culture are also possible and enable additional ex vivo studies. Muscular dystrophies, mitochondrial myopathies, and conditions often characterized by impaired muscle strength and function were early and obvious targets for diagnostic and research applications of muscle biopsy. Needle biopsy has been further extensively applied in the study of exercise physiology and pathophysiology, with the goal of investigating the regulation of mitochondrial function and substrate oxidation. In recent years, studies in the fields of obesity and diabetes have also focused on muscle mitochondrial function, and muscle biopsies have become increasingly common in human metabolic assessments.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bergstrom J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35:609–616

    Article  PubMed  CAS  Google Scholar 

  2. Saunders PU, Pyne DB, Telford RD, Hawley JA (2004) Factors affecting running economy in trained distance runners. Sports Med 34:465–485

    Article  PubMed  Google Scholar 

  3. Tessari P, Inchiostro S, Biolo G, Vincenti E, Sabadin L (1991) Effects of acute systemic hyperinsulinemia on forearm muscle proteolysis in healthy man. J Clin Invest 88:27–33

    Article  PubMed  CAS  Google Scholar 

  4. Nair KS, Ford GC, Ekberg K, Fernqvist-Forbes E, Wahren J (1995) Protein dynamics in whole body and in splanchnic and leg tissues in type I diabetic patients. J Clin Invest 95:2926–2937

    Article  PubMed  CAS  Google Scholar 

  5. Stephens FB, Constantin-Teodosiu D, Greenhaff PL (2007) New insights concerning the role of carnitine in the regulation of fuel metabolism in skeletal muscle. J Physiol 581:431–444

    Article  PubMed  Google Scholar 

  6. Kim YI, Lee FN, Choi WS, Lee S, Youn JH (2006) Insulin regulation of skeletal muscle PDK4 mRNA expression is impaired in acute insulin-resistant states. Diabetes 55:2311–2337

    Article  PubMed  CAS  Google Scholar 

  7. Winder WW, Hardie DG (1999) AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Physiol 277:E1–E10

    PubMed  CAS  Google Scholar 

  8. Long YC, Zierath JR (2006) AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116:1776–1783

    Article  PubMed  CAS  Google Scholar 

  9. Cantó C, Auwerx J (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 20:98–105

    Article  PubMed  Google Scholar 

  10. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127:1109–1122

    Article  PubMed  CAS  Google Scholar 

  11. Cantó C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Exercise Cell Metab 11:213–219

    Article  Google Scholar 

  12. Holloszy JO (2008) Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharmacol 59 Suppl 7:5–18

    PubMed  Google Scholar 

  13. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, McConnell JP, Nair KS (2008) Endurance exercise as a countermeasure for aging. Diabetes 57:2933–2942

    Article  PubMed  CAS  Google Scholar 

  14. Wojtaszewski JF, MacDonald C, Nielsen JN (2003) Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab 284:E813–E822

    PubMed  CAS  Google Scholar 

  15. Adhihetty PJ, Irrcher I, Joseph AM, Ljubicic V, Hood DA (2003) Plasticity of skeletal muscle mitochondria in response to contractile activity. Exp Physiol 88:99–107

    Article  PubMed  CAS  Google Scholar 

  16. Finck BN, Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116:615–622

    Article  PubMed  CAS  Google Scholar 

  17. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204

    Article  PubMed  CAS  Google Scholar 

  18. Fontana L, Meyer TE, Klein S, Holloszy JO (2004) Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans. Proc Natl Acad Sci U S A 101:6659–6663

    Article  PubMed  CAS  Google Scholar 

  19. Barazzoni R, Zanetti M, Bosutti A, Biolo G, Vitali-Serdoz L, Stebel M, Guarnieri G (2005) Moderate caloric restriction, but not physiological hyperleptinemia per se, enhances mitochondrial oxidative capacity in rat liver and skeletal muscle—tissue-specific impact on tissue triglyceride content and AKT activation. Endocrinology 146:2098–2106

    Article  PubMed  CAS  Google Scholar 

  20. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314–317

    Article  PubMed  CAS  Google Scholar 

  21. Zangarelli A, Chanseaume E, Morio B, Brugère C, Mosoni L, Rousset P, Giraudet C, Patrac V, Gachon P, Boirie Y, Walrand S (2006) Synergistic effects of caloric restriction with maintained protein intake on skeletal muscle performance in 21-month-old rats: a mitochondria-mediated pathway. FASEB J 20:2439–2450

    Article  PubMed  CAS  Google Scholar 

  22. Harman D (1981) The aging process. Proc Natl Acad Sci 78:7124–7128

    Article  PubMed  CAS  Google Scholar 

  23. Sinclair DA (2005) Toward a unified theory of caloric restriction and longevity regulation. Mech Ageing Dev 126:987–1002

    Article  PubMed  CAS  Google Scholar 

  24. Rachek LI, Musiyenko SI, LeDoux SP, Wilson GL (2007) Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 148:293–299

    Article  PubMed  CAS  Google Scholar 

  25. Pimenta AS, Gaidhu MP, Habib S, So M, Fediuc S, Mirpourian M, Musheev M, Curi R, Ceddia RB (2008) Prolonged exposure to palmitate impairs fatty acid oxidation despite activation of AMP-activated protein kinase in skeletal muscle cells. J Cell Physiol 217:478–485

    Article  PubMed  CAS  Google Scholar 

  26. Hirabara SM, Curi R, Maechler P (2010) Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells. J Cell Physiol 222:187–194

    Article  PubMed  CAS  Google Scholar 

  27. Yuzefovych L, Wilson G, Rachek L (2010) Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: role of oxidative stress. Am J Physiol Endocrinol Metab 299:E1096–E105

    Article  PubMed  CAS  Google Scholar 

  28. Brandt JM, Djouadi F, Kelly DP (1998) Fatty acids activate transcription of the muscle carnitine palmitoyltransferase I gene in cardiac myocytes via the peroxisome proliferator-activated receptor alpha. J Biol Chem 273:23786–23792

    Article  PubMed  CAS  Google Scholar 

  29. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Barletta A, Liverini G (2003) Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br J Nutr 90:953–960

    Article  PubMed  CAS  Google Scholar 

  30. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926–1933

    Article  PubMed  CAS  Google Scholar 

  31. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092

    Article  PubMed  CAS  Google Scholar 

  32. Garcia-Roves P, Huss JM, Han DH, Hancock CR, Iglesias-Gutierrez E, Chen M, Holloszy JO (2007) Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci U S A 104:10709–10713

    Article  PubMed  CAS  Google Scholar 

  33. Bigrigg JK, Heigenhauser GJ, Inglis JG, LeBlanc PJ, Peters SJ (2009) Carbohydrate refeeding after a high-fat diet rapidly reverses the adaptive increase in human skeletal muscle PDH kinase activity. Am J Physiol Regul Integr Comp Physiol 297:R885–R891

    Article  PubMed  CAS  Google Scholar 

  34. Medikayala S, Piteo B, Zhao X, Edwards JG (2011) Chronically elevated glucose compromises myocardial mitochondrial DNA integrity by alteration of mitochondrial topoisomerase function. Am J Physiol Cell Physiol 300:C338–C348

    Article  PubMed  CAS  Google Scholar 

  35. Aas V, Hessvik NP, Wettergreen M, Hvammen AW, Hallén S, Thoresen GH, Rustan AC (2011) Chronic hyperglycemia reduces substrate oxidation and impairs metabolic switching of human myotubes. Biochim Biophys Acta 1812:94–105

    PubMed  CAS  Google Scholar 

  36. Liu HY, Cao SY, Hong T, Han J, Liu Z, Cao W (2009) Insulin is a stronger inducer of insulin resistance than hyperglycemia in mice with type 1 diabetes mellitus (T1DM). J Biol Chem 284:27090–27100

    Article  PubMed  CAS  Google Scholar 

  37. Ragheb R, Shanab GM, Medhat AM, Seoudi DM, Adeli K, Fantus IG (2009) Free fatty acid-induced muscle insulin resistance and glucose uptake dysfunction: evidence for PKC activation and oxidative stress-activated signaling pathways. Biochem Biophys Res Commun 389:211–216

    Article  PubMed  CAS  Google Scholar 

  38. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H, Rieusset J (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of dietinduced insulin-resistant mice. J Clin Invest 118:789–800

    PubMed  CAS  Google Scholar 

  39. Anderson EJ, Lustig ME, Boyle KE, (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119:573–581

    Article  PubMed  CAS  Google Scholar 

  40. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787–790

    Article  PubMed  CAS  Google Scholar 

  41. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116:1793–1801

    Article  PubMed  CAS  Google Scholar 

  42. Supinski GS, Callahan LA (2007) Free radical-mediated skeletal muscle dysfunction in inflammatory conditions. J Appl Physiol 102:2056–2063

    Article  PubMed  CAS  Google Scholar 

  43. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, Stump CS (2008) Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab 294:E345–E351

    Article  PubMed  CAS  Google Scholar 

  44. Green CJ, Macrae K, Fogarty S, Hardie DG, Sakamoto K, Hundal HS (2011) Counter modulation of fatty acid-induced proinflammatory NFkB signalling in rat skeletal muscle cells by AMPK. Biochem J 435:463–474

    Article  PubMed  CAS  Google Scholar 

  45. Kim JK, Kim J, Fillmore JJ, Chen Y, Moore I, Lee J, Yuan M, Li ZW, Karin M, Perret P, Shoelson SE, Shulman GI (2001) Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 108:437–446

    PubMed  CAS  Google Scholar 

  46. Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116:2791–2798

    PubMed  CAS  Google Scholar 

  47. Spriet LL, Heigenhauser GJ (2002) Regulation of pyruvate dehydrogenase (PDH) activity in human skeletal muscle during exercise. Exerc Sport Sci Rev 30:91–95

    Article  PubMed  Google Scholar 

  48. Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546:851–858.

    Article  PubMed  CAS  Google Scholar 

  49. Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M (2009) Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol 106:929–934

    Article  PubMed  CAS  Google Scholar 

  50. Little JP, Safdar A, Cermak N, Tarnopolsky MA, Gibala MJ (2010) Acute endurance exercise increases the nuclear abundance of PGC-1alpha in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 298:R912–R917

    Article  PubMed  CAS  Google Scholar 

  51. Schrauwen P, Hesselink MK (2004) Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53:1412–1417

    Article  PubMed  CAS  Google Scholar 

  52. Summers SA (2010) Sphingolipids and insulin resistance: the five Ws. Curr Opin Lipidol 21:128–135

    Article  PubMed  CAS  Google Scholar 

  53. Muoio DM (2010) Intramuscular triacylglycerol and insulin resistance: guilty as charged or wrongly accused? Biochim Biophys Acta 1801:281–288

    PubMed  CAS  Google Scholar 

  54. Morino K, Petersen KF, Shulman GI (2006) Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55 Suppl 2:S9–S15

    Article  PubMed  CAS  Google Scholar 

  55. Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944–2950

    Article  PubMed  CAS  Google Scholar 

  56. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE (2005) Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54:8–14

    Article  PubMed  CAS  Google Scholar 

  57. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, Neschen S, White MF, Bilz S, Sono S, Pypaert M, Shulman GI (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115:3587–3593

    Article  PubMed  CAS  Google Scholar 

  58. Mogensen M, Sahlin K, Fernström M, Glintborg D, Vind BF, Beck-Nielsen H, Højlund K (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56:1592–1599

    Article  PubMed  CAS  Google Scholar 

  59. Heilbronn LK, Gan SK, Turner N, Campbell LV, Chisholm DJ (2007) Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects. J Clin Endocrinol Metab 92:1467–1473

    Article  PubMed  CAS  Google Scholar 

  60. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R, Dela F (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50:790–796

    Article  PubMed  CAS  Google Scholar 

  61. Ritov VB, Menshikova EV, Azuma K, Wood R, Toledo FG, Goodpaster BH, Ruderman NB, Kelley DE (2010) Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Am J Physiol Endocrinol Metab 298:E49–E58

    Article  PubMed  CAS  Google Scholar 

  62. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273

    Article  PubMed  CAS  Google Scholar 

  63. Richardson DK, Kashyap S, Bajaj M, Cusi K, Mandarino SJ, Finlayson J, DeFronzo RA, Jenkinson CP, Mandarino LJ (2005) Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J Biol Chem 280:10290–10297

    Article  PubMed  CAS  Google Scholar 

  64. Bajaj M, Medina-Navarro R, Suraamornkul S, Meyer C, DeFronzo RA, Mandarino LJ (2007) Paradoxical changes in muscle gene expression in insulin-resistant subjects after sustained reduction in plasma free fatty acid concentration. Diabetes 56:743–752

    Article  PubMed  CAS  Google Scholar 

  65. Chavez AO, Kamath S, Jani R, Sharma LK, Monroy A, Abdul-Ghani MA, Centonze VE, Sathyanarayana P, Coletta DK, Jenkinson CP, Bai Y, Folli F, DeFronzo RA, Tripathy D (2010) Effect of short-term free fatty acids elevation on mitochondrial function in skeletal muscle of healthy individuals. J Clin Endocrinol Metab 95:422–429

    Article  PubMed  CAS  Google Scholar 

  66. Rabøl R, Højberg PM, Almdal T, Boushel R, Haugaard SB, Madsbad S, Dela F (2009) Effect 8 Muscle Biopsy To Investigate Mitochondrial Turnover 83 of hyperglycemia on mitochondrial respiration in type 2 diabetes. J Clin Endocrinol Metab 94:1372–1378

    Article  PubMed  Google Scholar 

  67. Toledo FG, Menshikova EV, Azuma K, Radiková Z, Kelley CA, Ritov VB, Kelley DE (2008) Mitochondrial capacity in skeletal muscle is not stimulated by weight loss despite increases in insulin action and decreases in intramyocellular lipid content. Diabetes 57:987–994

    Article  PubMed  CAS  Google Scholar 

  68. Phielix E, Meex R, Moonen-Kornips E, Hesselink MK, Schrauwen P (2010) Exercise training increases mitochondrial content and ex vivo mitochondrial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia 53:1714–1721

    Article  PubMed  CAS  Google Scholar 

  69. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, Dyck DJ (2006) Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 291:E99–E107

    Article  PubMed  CAS  Google Scholar 

  70. Bordenave S, Metz L, Flavier S, Lambert K, Ghanassia E, Dupuy AM, Michel F, Puech-Cathala AM, Raynaud E, Brun JF, Mercier J (2008) Training-induced improvement in lipid oxidation in type 2 diabetes mellitus is related to alterations in muscle mitochondrial activity. Effect of endurance training in type 2 diabetes. Diabetes Metab 34:162–168

    Article  PubMed  CAS  Google Scholar 

  71. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS (2003) Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52:1888–1896

    Article  PubMed  CAS  Google Scholar 

  72. Sartorio A, Fontana P, Trecate L, Lafortuna CL (2003) Short-term changes of fatigability and muscle performance in severe obese patients after an integrated body mass reduction program. Diabetes Nutr Metab 16:88–93

    PubMed  CAS  Google Scholar 

  73. Sartorio A, Narici MV, Fumagalli E, Faglia G, Lafortuna CL (2001) Aerobic and anaerobic performance before and after a short-term body mass reduction program in obese subjects. Diabetes Nutr Metab 14:51–57

    PubMed  CAS  Google Scholar 

  74. Stump CS, Short KR, Bigelow ML, Schimke JM, Nair KS (2003) Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci U S A 100:7996–8001

    Article  PubMed  CAS  Google Scholar 

  75. Asmann YW, Stump CS, Short KR, Coenen-Schimke JM, Guo Z, Bigelow ML, Nair KS (2006) Skeletal muscle mitochondrial functions, mitochondrial DNA copy numbers, and gene transcript profiles in type 2 diabetic and nondiabetic subjects at equal levels of low or high insulin and euglycemia. Diabetes 55:3309–3319

    Article  PubMed  CAS  Google Scholar 

  76. Hoeks J, van Herpen NA, Mensink M, Moonen-Kornips E, van Beurden D, Hesselink MK, Schrauwen P (2010) Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 59:2117–2125

    Article  PubMed  CAS  Google Scholar 

  77. Østergård T, Andersen JL, Nyholm B, Lund S, Nair KS, Saltin B, Schmitz O (2006) Impact of exercise training on insulin sensitivity, physical fitness, and muscle oxidative capacity in firstdegree relatives of type 2 diabetic patients. Am J Physiol Endocrinol Metab 290:E998–E1005

    Article  PubMed  Google Scholar 

  78. Nair KS, Bigelow ML, Asmann YW, Chow LS, Coenen-Schimke JM, Klaus KA, Guo ZK, Sreekumar R, Irving BA (2008) Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57:1166–1175

    Article  PubMed  CAS  Google Scholar 

  79. Choi CS, Befroy DE, Codella R, Kim S, Reznick RM, Hwang YJ, Liu ZX, Lee HY, Distefano A, Samuel VT, Zhang D, Cline GW, Handschin C, Lin J, Petersen KF, Spiegelman BM, Shulman GI (2008) Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci U S A 105:19926–19931

    Article  PubMed  CAS  Google Scholar 

  80. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114:1752–1761

    PubMed  CAS  Google Scholar 

  81. Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R, Simsolo RB (1995) The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J Clin Invest 95:2111–2119

    Article  PubMed  CAS  Google Scholar 

  82. Melov S, Shoffner JM, Kaufman A, Wallace DC (1995) Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acids Res 23:4122–4126 84 R. Barazzoni

    Article  PubMed  CAS  Google Scholar 

  83. 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

    Article  PubMed  CAS  Google Scholar 

  84. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS (2005) Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci U S A 102:5618–5623

    Article  PubMed  CAS  Google Scholar 

  85. Kouidi E, Albani M, Natsis K, Megalopoulos A, Gigis P, Guiba-Tziampiri O, Tourkantonis A, Deligiannis A (1998) The effects of exercise training on muscle atrophy in haemodialysis patients. Nephrol Dial Transplant 13:685–699

    Article  PubMed  CAS  Google Scholar 

  86. Gosker HR, Schrauwen P, Broekhuizen R, Hesselink MK, Moonen-Kornips E, Ward KA, Franssen FM, Wouters EF, Schols AM (2006) Exercise training restores uncoupling protein-3 content in limb muscles of patients with chronic obstructive pulmonary disease. Am J Physiol Endocrinol Metab 290:E976–E981

    Article  PubMed  CAS  Google Scholar 

  87. Tyni-Lenné R, Gordon A, Jansson E, Bermann G, Sylvén C (1997) Skeletal muscle endurance training improves peripheral oxidative capacity, exercise tolerance, and health-related quality of life in women with chronic congestive heart failure secondary to either ischemic cardiomyopathy or idiopathic dilated cardiomyopathy. Am J Cardiol 80:1025–1029

    Article  PubMed  Google Scholar 

  88. Gielen S, Adams V, Linke A, Erbs S, Möbius-Winkler S, Schubert A, Schuler G, Hambrecht R (2005) Exercise training in chronic heart failure: correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur J Cardiovasc Prev Rehabil 12:393–400

    Article  PubMed  Google Scholar 

  89. Fredriksson K, Tjäder I, Keller P, Petrovic N, Ahlman B, Schéele C, Wernerman J, Timmons JA, Rooyackers O (2008) Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS One 3:e3686

    Article  PubMed  Google Scholar 

  90. Adey D, Kumar R, McCarthy JT, Nair KS (2000) Reduced synthesis of muscle proteins in chronic renal failure. Am J Physiol Endocrinol Metab 278:E219–E225

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical, Surgical and Health Sciences, University of Trieste, Trieste, Italy

    Rocco Barazzoni

Authors
  1. Rocco Barazzoni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rocco Barazzoni .

Editor information

Editors and Affiliations

  1. Department of Sport Sciences, Nutrition and Health, University of Milan, Milan, Italy

    Livio Luzi

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Italia

About this chapter

Cite this chapter

Barazzoni, R. (2012). Muscle Biopsy To Investigate Mitochondrial Turnover. In: Luzi, L. (eds) Cellular Physiology and Metabolism of Physical Exercise. Springer, Milano. https://doi.org/10.1007/978-88-470-2418-2_8

Download citation

Publish with us

Policies and ethics

Search

Navigation