Supplementation with α-Lipoic Acid, CoQ10, and Vitamin E Augments Running Performance and Mitochondrial Function in Female Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Abadi, Arkan ^a   Crane, Justin D ^a   Ogborn, Daniel ^a   Hettinga, Bart ^a   Akhtar, Mahmood ^a   Stokl, Andrew ^a   MacNeil, Lauren ^a   Safdar, Adeel ^a   Tarnopolsky, Mark ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANION CHANNEL; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LACTATE DEHYDROGENASE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROSTAGLANDIN SYNTHASE; STRESS ACTIVATED PROTEIN KINASE 1; THIOCTIC ACID; TUBULIN; UBIDECARENONE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3; VOLTAGE DEPENDENT ANION CHANNEL IV; VOLTAGE DEPENDENT ANION CHANNEL V;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING RATE; CELL FUNCTION; CONTROLLED STUDY; COPPER ZINC SUPEROXIDE DISMUTASE GENE; CYCLOOXYGENASE GENE; DIET SUPPLEMENTATION; ENDURANCE TRAINING; ENZYME ACTIVATION; FEMALE; GENE; MALE; MANGANESE SUPEROXIDE DISMUTASE GENE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRION; MOTOR PERFORMANCE; MOUSE; MUSCLE FUNCTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUADRICEPS FEMORIS MUSCLE; RUNNING; SEX DIFFERENCE; TASK PERFORMANCE; TREADMILL EXERCISE; UPREGULATION; VITAMIN SUPPLEMENTATION; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; DIETARY SUPPLEMENTS; FEMALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; PHYSICAL EXERTION; THIOCTIC ACID; UBIQUINONE; VITAMIN E;

MUS;

EID: 84875670281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060722     Document Type: Article

References (64)

1. Survey NHANE (2011) Antioxidant Supplements for Health: An Introduction. National Center for Complementary and Alternative Medicine, National Institutes of Health http://nccam.nih.gov/health/antioxidants/introduction.htm. NCCAM Pub No.: D450 NCCAM Pub No.: D450.
2. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C (2008) Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database Syst Rev: CD007176.
3. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C, (2007) Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297: 842-857.
4. Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, et al. (2009) Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 301: 39-51.
5. Radak Z, Sasvari M, Nyakas C, Taylor AW, Ohno H, et al. (2000) Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys 383: 114-118.
6. Powers SK, Duarte J, Kavazis AN, Talbert EE, (2010) Reactive oxygen species are signalling molecules for skeletal muscle adaptation. Exp Physiol 95: 1-9.
7. Zanuso S, Jimenez A, Pugliese G, Corigliano G, Balducci S, (2010) Exercise for the management of type 2 diabetes: a review of the evidence. Acta Diabetol 47: 15-22.
8. Powers SK, Jackson MJ, (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276.
9. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, et al. (2008) Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87: 142-149.
10. Strobel NA, Peake JM, Matsumoto A, Marsh SA, Coombes JS, et al. (2011) Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med Sci Sports Exerc 43: 1017-1024.
11. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH, (2011) Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 301: E779-784.
12. Yfanti C, Nielsen AR, Akerstrom T, Nielsen S, Rose AJ, et al. (2011) Effect of antioxidant supplementation on insulin sensitivity in response to endurance exercise training. Am J Physiol Endocrinol Metab 300: E761-770.
13. Bailey DM, Williams C, Betts JA, Thompson D, Hurst TL, (2011) Oxidative stress, inflammation and recovery of muscle function after damaging exercise: effect of 6-week mixed antioxidant supplementation. Eur J Appl Physiol 111: 925-936.
14. Theodorou AA, Nikolaidis MG, Paschalis V, Koutsias S, Panayiotou G, et al. (2011) No effect of antioxidant supplementation on muscle performance and blood redox status adaptations to eccentric training. Am J Clin Nutr 93: 1373-1383.
15. Bhagavan HN, Chopra RK, (2006) Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res 40: 445-453.
16. Burton GW, Cheeseman KH, Doba T, Ingold KU, Slater TF, (1983) Vitamin E as an antioxidant in vitro and in vivo. Ciba Found Symp 101: 4-18.
17. Burton GW, Joyce A, Ingold KU, (1982) First proof that vitamin E is major lipid-soluble, chain-breaking antioxidant in human blood plasma. Lancet 2: 327.
18. Azzi A, Ricciarelli R, Zingg JM, (2002) Non-antioxidant molecular functions of alpha-tocopherol (vitamin E). FEBS Lett 519: 8-10.
19. Azzi A, Gysin R, Kempna P, Munteanu A, Negis Y, et al. (2004) Vitamin E mediates cell signaling and regulation of gene expression. Ann N Y Acad Sci 1031: 86-95.
20. Reed LJ, (1957) The chemistry and function of lipoic acid. Adv Enzymol Relat Subj Biochem 18: 319-347.
21. Gunsalus IC (1953) The chemistry and function of the pyruvate oxidation factor (lipoic acid). J Cell Physiol Suppl 41: 113-136.
22. Packer L, Witt EH, Tritschler HJ, (1995) alpha-Lipoic acid as a biological antioxidant. Free Radic Biol Med 19: 227-250.
23. Shay KP, Moreau RF, Smith EJ, Smith AR, Hagen TM, (2009) Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 1790: 1149-1160.
24. Wang Y, Li X, Guo Y, Chan L, Guan X, (2010) alpha-Lipoic acid increases energy expenditure by enhancing adenosine monophosphate-activated protein kinase-peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling in the skeletal muscle of aged mice. Metabolism 59: 967-976.
25. Lee WJ, Song KH, Koh EH, Won JC, Kim HS, et al. (2005) Alpha-lipoic acid increases insulin sensitivity by activating AMPK in skeletal muscle. Biochem Biophys Res Commun 332: 885-891.
26. Zong H, Ren JM, Young LH, Pypaert M, Mu J, et al. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99: 15983-15987.
27. Jensen TE, Wojtaszewski JF, Richter EA, (2009) AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient? Acta Physiol (Oxf) 196: 155-174.
28. Wadley GD, McConell GK, (2010) High-dose antioxidant vitamin C supplementation does not prevent acute exercise-induced increases in markers of skeletal muscle mitochondrial biogenesis in rats. J Appl Physiol 108: 1719-1726.
29. Hartmann A, Niess AM, Grunert-Fuchs M, Poch B, Speit G, (1995) Vitamin E prevents exercise-induced DNA damage. Mutat Res 346: 195-202.
30. Meydani M, Evans WJ, Handelman G, Biddle L, Fielding RA, et al. (1993) Protective effect of vitamin E on exercise-induced oxidative damage in young and older adults. Am J Physiol 264: R992-998.
31. Nieman DC, Henson DA, McAnulty SR, McAnulty LS, Morrow JD, et al. (2004) Vitamin E and immunity after the Kona Triathlon World Championship. Med Sci Sports Exerc 36: 1328-1335.
32. Tarnopolsky MA, (2008) The mitochondrial cocktail: rationale for combined nutraceutical therapy in mitochondrial cytopathies. Adv Drug Deliv Rev 60: 1561-1567.
33. Rodriguez MC, MacDonald JR, Mahoney DJ, Parise G, Beal MF, et al. (2007) Beneficial effects of creatine, CoQ10, and lipoic acid in mitochondrial disorders. Muscle Nerve 35: 235-242.
34. Liu J, Ames BN, (2005) Reducing mitochondrial decay with mitochondrial nutrients to delay and treat cognitive dysfunction, Alzheimer's disease, and Parkinson's disease. Nutr Neurosci 8: 67-89.
35. Booth FW, Laye MJ, Spangenburg EE, (2010) Gold standards for scientists who are conducting animal-based exercise studies. J Appl Physiol 108: 219-221.
36. Knab AM, Bowen RS, Moore-Harrison T, Hamilton AT, Turner MJ, et al. (2009) Repeatability of exercise behaviors in mice. Physiol Behav 98: 433-440.
37. Li L, Muhlfeld C, Niemann B, Pan R, Li R, et al. (2011) Mitochondrial biogenesis and PGC-1alpha deacetylation by chronic treadmill exercise: differential response in cardiac and skeletal muscle. Basic Res Cardiol.
38. Hardie DG, (2011) Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism. Proc Nutr Soc 70: 92-99.
39. Kramer HF, Goodyear LJ, (2007) Exercise, MAPK, and NF-kappaB signaling in skeletal muscle. J Appl Physiol 103: 388-395.
40. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, et al. (2005) Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593.
41. Puigserver P, Rhee J, Lin J, Wu Z, Yoon JC, et al. (2001) Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol Cell 8: 971-982.
42. Scarpulla RC, (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14.
43. O'Neill HM, Maarbjerg SJ, Crane JD, Jeppesen J, Jorgensen SB, et al. (2011) AMP-activated protein kinase (AMPK) beta1beta2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc Natl Acad Sci U S A 108: 16092-16097.
44. Steinberg GR, O'Neill HM, Dzamko NL, Galic S, Naim T, et al. (2010) Whole body deletion of AMP-activated protein kinase {beta}2 reduces muscle AMPK activity and exercise capacity. J Biol Chem 285: 37198-37209.
45. Garcia-Roves PM, Osler ME, Holmstrom MH, Zierath JR, (2008) Gain-of-function R225Q mutation in AMP-activated protein kinase gamma3 subunit increases mitochondrial biogenesis in glycolytic skeletal muscle. J Biol Chem 283: 35724-35734.
46. Jager S, Handschin C, St-Pierre J, Spiegelman BM, (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 104: 12017-12022.
47. Shen QW, Zhu MJ, Tong J, Ren J, Du M, (2007) Ca2+/calmodulin-dependent protein kinase kinase is involved in AMP-activated protein kinase activation by alpha-lipoic acid in C2C12 myotubes. Am J Physiol Cell Physiol 293: C1395-1403.
48. Ying Z, Kampfrath T, Sun Q, Parthasarathy S, Rajagopalan S, (2011) Evidence that alpha-lipoic acid inhibits NF-kappaB activation independent of its antioxidant function. Inflamm Res 60: 219-225.
49. Kwong LK, Kamzalov S, Rebrin I, Bayne AC, Jana CK, et al. (2002) Effects of coenzyme Q(10) administration on its tissue concentrations, mitochondrial oxidant generation, and oxidative stress in the rat. Free Radic Biol Med 33: 627-638.
50. Sun M, Qian F, Shen W, Tian C, Hao J, et al. (2011) Mitochondrial nutrients stimulate performance and mitochondrial biogenesis in exhaustively exercised rats. Scand J Med Sci Sports.
51. Matsuzawa A, Ichijo H, (2008) Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys Acta 1780: 1325-1336.
52. Espinosa A, Leiva A, Pena M, Muller M, Debandi A, et al. (2006) Myotube depolarization generates reactive oxygen species through NAD(P)H oxidase; ROS-elicited Ca2+ stimulates ERK, CREB, early genes. J Cell Physiol 209: 379-388.
53. Osorio-Fuentealba C, Valdes JA, Riquelme D, Hidalgo J, Hidalgo C, et al. (2009) Hypoxia stimulates via separate pathways ERK phosphorylation and NF-kappaB activation in skeletal muscle cells in primary culture. J Appl Physiol 106: 1301-1310.
54. Ji LL, Gomez-Cabrera MC, Vina J, (2007) Role of nuclear factor kappaB and mitogen-activated protein kinase signaling in exercise-induced antioxidant enzyme adaptation. Appl Physiol Nutr Metab 32: 930-935.
55. Vinayagamoorthi R, Bobby Z, Sridhar MG, (2008) Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 197: 287-296.
56. Comitato R, Nesaretnam K, Leoni G, Ambra R, Canali R, et al. (2009) A novel mechanism of natural vitamin E tocotrienol activity: involvement of ERbeta signal transduction. Am J Physiol Endocrinol Metab 297: E427-437.
57. Pedram A, Razandi M, Wallace DC, Levin ER, (2006) Functional estrogen receptors in the mitochondria of breast cancer cells. Mol Biol Cell 17: 2125-2137.
58. Papa L, Germain D, (2011) Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J Cell Sci 124: 1396-1402.
59. Ryan MJ, Dudash HJ, Docherty M, Geronilla KB, Baker BA, et al. (2010) Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp Gerontol 45: 882-895.
60. Kamzalov S, Sumien N, Forster MJ, Sohal RS, (2003) Coenzyme Q intake elevates the mitochondrial and tissue levels of Coenzyme Q and alpha-tocopherol in young mice. J Nutr 133: 3175-3180.
61. Chae CH, Shin CH, Kim HT, (2008) The combination of alpha-lipoic acid supplementation and aerobic exercise inhibits lipid peroxidation in rat skeletal muscles. Nutr Res 28: 399-405.
62. Kagan V, Serbinova E, Packer L, (1990) Antioxidant effects of ubiquinones in microsomes and mitochondria are mediated by tocopherol recycling. Biochem Biophys Res Commun 169: 851-857.
63. Schneider D, Elstner EF, (2000) Coenzyme Q10, vitamin E, and dihydrothioctic acid cooperatively prevent diene conjugation in isolated low-density lipoprotein. Antioxid Redox Signal 2: 327-333.
64. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsoe R, et al. (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796.