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Dietary stimulators of the PGC-1 superfamily and mitochondrial biosynthesis in skeletal muscle. A mini-review

  • Mini Review
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Abstract

Mitochondrial dysfunction has been linked to many diseases including metabolic diseases such as diabetes. Peroxisome proliferator-activated receptor gamma co-activator 1 (PGC-1) is a superfamily of transcriptional co-activators which are important precursors to mitochondrial biosynthesis found in most cells including skeletal muscle. The PGC-1 superfamily consists of three variants all of which are directly involved in controlling metabolic gene expression including those regulating fatty acid oxidation and mitochondrial proteins. In contrast to previous reviews on PGC-1, this mini-review summarizes the current knowledge of many known dietary stimulators of PGC-1 and the subsequent mitochondrial biosynthesis with associated metabolic benefit in skeletal muscle.

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Abbreviations

AC:

Adenylate cyclase

AICAR:

5-Aminoimidazole-4-carboxamide-1-β-d-ribofuranoside

AMPK:

5′ Adenosine monophosphate-activated protein kinase

ATF:

Activating transcription factor

CAMK:

Calcium/calmodulin-dependent protein kinase

CREB:

cAMP-related element binding protein

DHA:

Docosahexaenoic acid

EPA:

Eicosapentaenoic acid

ERR:

Estrogen related receptor

FOXO:

Forkhead box proteins

GCN5:

General control nonderepressible 5

GPCR:

G-Protein coupled receptors

HIF:

Hypoxia-inducible factor

MAPK:

p38 Mitogen-activated protein kinase

MEF:

2-myocyte enhancing factor

MyoD:

Myogenic regulatory factor D

NO:

Nitric oxide

NRF:

1/2 Nuclear respiratory factors 1 and 2

PGC-1α:

Peroxisome proliferator-activated receptor γ co-activator-1

PGC-1:

PGC superfamily

PDE:

Phosphodiesterase

PKA:

Protein kinase A

PPAR:

Peroxisome proliferator-activated receptor

PUFA:

Poly-unsaturated fatty acids

RXR:

Retinoid X receptor

SIRT:

Sirtuin

SRC3:

Steroid receptor coactivator 3

TFAM:

Mitochondrial transcription factor A

TFBs:

Transcription specificity factors TFB1M and TFB2M

TTA:

Tetradecylthioacetic acid

TZD:

Thiozolidinediones

VEGF:

Vascular endothelial growth factor

References

  1. Abd TT, Jacobson TA (2011) Statin-induced myopathy: a review and update. Expert Opin Drug Saf 10:373–387

    CAS  PubMed  Google Scholar 

  2. Alaynick WA (2008) Nuclear receptors, mitochondria and lipid metabolism. Mitochondrion 8:329–337

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Amat R, Planavila A, Chen SL et al (2009) SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma co-activator-1 alpha (PGC-1 alpha) gene in skeletal muscle through the PGC-1 alpha autoregulatory loop and interaction with MyoD. J Biol Chem 284:21872–21880

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Arany Z, Foo SY, Ma YH et al (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1 alpha. Nature 451:1008–1012

    CAS  PubMed  Google Scholar 

  5. Barroso E, Rodriguez-Calvo R, Serrano-Marco L et al (2011) The PPAR beta/delta activator GW501516 prevents the down-regulation of AMPK caused by a high-fat diet in liver and amplifies the PGC-1 alpha-lipin 1-PPAR alpha pathway leading to increased fatty acid oxidation. Endocr 152:1848–59

    CAS  Google Scholar 

  6. Baur JA, Pearson KJ, Price NL et al (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342

    CAS  PubMed  Google Scholar 

  7. Bouitbir J, Charles AL, Echaniz-Laguna A et al (2012) Opposite effects of statins on mitochondria of cardiac and skeletal muscles: a omitohormesis’ mechanism involving reactive oxygen species and PGC-1. Eur Heart J 33:1397–1407

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Brenmoehl J, Hoeflich A (2013) Dual control of mitochondrial biogenesis by sirtuin 1 and sirtuin 3. Mitochondrion 6:755–761

    Google Scholar 

  9. Bruckbauer A, Zemel MB (2011) Effects of dairy consumption on SIRT1 and mitochondrial biogenesis in adipocytes and muscle cells. Nutr Metab 8:91

    CAS  Google Scholar 

  10. Bruckbauer A, Zemel MB, Thorpe T et al (2012) Synergistic effects of leucine and resveratrol on insulin sensitivity and fat metabolism in adipocytes and mice. Nutr Metab 9:77

    CAS  Google Scholar 

  11. Canto C, Jiang LQ, Deshmukh AS et al (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11:213–219

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Caton PW, Holness MJ, Bishop-Bailey D et al (2011) PPAR alpha-LXR as a novel metabolostatic signalling axis in skeletal muscle that acts to optimize substrate selection in response to nutrient status. Biochem J 437:521–530

    CAS  PubMed  Google Scholar 

  13. Choi JH, Banks AS, Kamenecka TM et al (2011) Antidiabetic actions of a non-agonist PPAR gamma ligand blocking Cdk5-mediated phosphorylation. Nature 477:477–481

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Chowdhury SKR, Dobrowsky RT, Femyhough P (2011) Nutrient excess and altered mitochondrial proteome and function contribute to neurodegeneration in diabetes. Mitochondrion 11:845–854

    CAS  PubMed  Google Scholar 

  15. Coletta DK, Sriwijitkamol A, Wajcberg E et al (2009) Pioglitazone stimulates AMP-activated protein kinase signalling and increases the expression of genes involved in adiponectin signalling, mitochondrial function and fat oxidation in human skeletal muscle in vivo: a randomised trial. Diabetologia 52:723–732

    CAS  PubMed  Google Scholar 

  16. Coll T, Alvarez-Guardia D, Barroso E et al (2010) Activation of peroxisome proliferator-activated receptor-delta by GW501516 prevents fatty acid-induced nuclear factor-kappa B activation and insulin resistance in skeletal muscle cells. Endocr 151:1560–1569

    CAS  Google Scholar 

  17. Conn CA, Vaughan RA, Sherman WS (2013) Nutritional genetics and energy metabolism in human obesity. Curr Nutr Rep 2:142–150

    CAS  Google Scholar 

  18. Costford SR, Bajpeyi S, Pasarica M et al (2010) Skeletal muscle NAMPT is induced by exercise in humans. Am J Physiol-Endocr Metab 298:E117–E126

    CAS  Google Scholar 

  19. da Costa Santos VB, Ruiz RJ, Vettorato ED et al (2011) Effects of chronic caffeine intake and low-intensity exercise on skeletal muscle of Wistar rats. Exp Physiol 96:1228–1238

    PubMed  Google Scholar 

  20. Delacruz MJ, Alemany J, Roncero I et al (1988) Change induced by caffeine, theophylline and theobromine on calcium-uptake, respiration and ATP levels in rat-liver mitochondria. Compar Biochem Physiol 91:443–447

    CAS  Google Scholar 

  21. Deng YT, Chang TW, Lee MS, Lin JK (2012) Suppression of free fatty acid-induced insulin resistance by phytopolyphenols in C2C12 mouse skeletal muscle cells. J Ag Food Chem 60:1059–1066

    CAS  Google Scholar 

  22. Denu JM (2012) Fortifying the link between SIRT1, resveratrol, and mitochondrial function. Cell Metabolism 15:566–567

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Dulloo AG (2011) The search for compounds that stimulate thermogenesis in obesity management: from pharmaceuticals to functional food ingredients. Obesity Rev 12:866–883

    CAS  Google Scholar 

  24. Dulloo AG, Duret C, Rohrer D et al (1999) Efficacy of a green tea extract rich in catechin polyphenols and caffeine in increasing 24-h energy expenditure and fat oxidation in humans. Am J Clin Nutr 70:1040–1045

    CAS  PubMed  Google Scholar 

  25. Dyson PA (2010) The therapeutics of lifestyle management on obesity. Diabetes Obes Metab 12:941–946

    CAS  PubMed  Google Scholar 

  26. Evans MJ, Scarpulla RC (1990) NRF-1: a transactivator of nuclear-encoded respiratory genes in animal cells. Genes Dev 4:1023–1034

    CAS  PubMed  Google Scholar 

  27. Flachs P, Horakova O, Brauner P et al (2005) Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 48:2365–2375

    CAS  PubMed  Google Scholar 

  28. Frier BC, Hancock CR, Little JP et al (2011) Reductions in RIP140 are not required for exercise- and AICAR-mediated increases in skeletal muscle mitochondrial content. J Appl Physiol 111:688–695

    CAS  PubMed  Google Scholar 

  29. Frier BC, Jacobs RL, Wright DC (2011) Interactions between the consumption of a high-fat diet and fasting in the regulation of fatty acid oxidation enzyme gene expression: an evaluation of potential mechanisms. Am J Physiol-Regul Integr Compar Physiol 300:R212–R221

    CAS  Google Scholar 

  30. Frier BC, Wan Z, Williams DB et al (2012) Epinephrine and AICAR-induced PGC-1 alpha mRNA expression is intact in skeletal muscle from rats fed a high-fat diet. Am J Physiol-Cell Physiol 302:C1772–1779

    CAS  PubMed  Google Scholar 

  31. Fu WJJ, Haynes TE, Kohli R et al (2005) l-Arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 135:714–721

    CAS  PubMed  Google Scholar 

  32. Gacias M, Perez-Marti A, Pujol-Vidal M et al (2012) PGC-1 beta regulates mouse carnitine-acylcarnitine translocase through estrogen-related receptor alpha. Biochem Biophys Res Com 423:838–843

    CAS  PubMed  Google Scholar 

  33. Gao ZG, Yin J, Zhang J et al (2009) Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58:1509–1517

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  35. Gleyzer N, Vercauteren K, Scarpulla RC (2005) Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol Cell Biol 25:1354–1366

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Gokcel A, Gumurdulu Y, Karakose H et al (2002) Evaluation of the safety and efficacy of sibutramine, orlistat and metformin in the treatment of obesity. Diabetes Obes Metab 4:49–55

    CAS  PubMed  Google Scholar 

  37. Goncalves DA, Lira EC, Baviera AM et al (2009) Mechanisms involved in 3′,5′-cyclic adenosine monophosphate-mediated inhibition of the ubiquitin-proteasome system in skeletal muscle. Endocrinology 150:5395–5404

    CAS  PubMed  Google Scholar 

  38. Gordon JW, Rungi AA, Inagaki H et al (2001) Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J Appl Physiol 90:389–396

    CAS  PubMed  Google Scholar 

  39. Handschin C, Rhee J, Lin JD et al (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1 alpha expression in muscle. Proc Natl Acad Sci 100:7111–7116

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Hernandez-Alvarez MI, Thabit H, Burns N et al (2010) Subjects with early-onset type 2 diabetes show defective activation of the skeletal muscle PGC-1 alpha/mitofusin-2 regulatory pathway in response to physical activity. Diabetes Care 33:645–651

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Herzig S, Long FX, Jhala US et al (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413:652–652

    CAS  Google Scholar 

  42. Hodgson AB, Randell RK, Jeukendrup AE (2013) The effect of green tea extract on fat oxidation at rest and during exercise: evidence of efficacy and proposed mechanisms. Advances in Nutr 4:129–140

    CAS  Google Scholar 

  43. Holloszy JO (2008) Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharm 59:5–18

    Google Scholar 

  44. Hondares E, Pineda-Torra I, Iglesias R et al (2007) PPAR delta, but not PPAR alpha, activates PGC-l alpha gene transcription in muscle. Biochem Biophys Res Com 354:1021–1027

    CAS  PubMed  Google Scholar 

  45. Jager S, Handschin C, Pierre J et al (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1 alpha. Proc Natl Acad Sci 104:12017–12022

    PubMed Central  PubMed  Google Scholar 

  46. Jorgensen SB, Richter EA, Wojtaszewski JFP (2006) Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol-London 574:17–31

    PubMed Central  PubMed  Google Scholar 

  47. Jorgensen SB, Treebak JT, Viollet B et al (2007) Role of AMPK alpha 2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle. Am J Physiol-Endocr Metab 292:E331–E339

    Google Scholar 

  48. Jove M, Salla J, Planavila A et al (2004) Impaired expression of NADH dehydrogenase subunit 1 and PPAR gamma coactivator-1 in skeletal muscle of ZDF rats: restoration by troglitazone. J Lipid Res 45:113–123

    CAS  PubMed  Google Scholar 

  49. Kleiner S, Nguyen-Tran V, Bare O et al (2009) PPAR delta agonism activates fatty acid oxidation via PGC-1 alpha but does not increase mitochondrial gene expression and function. J Bio Chem 284:18624–18633

    CAS  Google Scholar 

  50. Knutti D, Kaul A, Kralli A (2000) A tissue-specific coactivator of steroid receptors, identified in a functional genetic screen. Mol Cell Biol 20:2411–2422

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Knutti D, KresslerD KA (2001) Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a repressor. Proc Natl Acad Sci 98:9713–9718

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Kusuhara K, Madsen K, Jensen L et al (2007) Calcium signalling in the regulation of PGC-1 alpha, PDK4 and HKII mRNA expression. Biol Chem 388:481–488

    CAS  PubMed  Google Scholar 

  53. Lagouge M, Argmann C, Gerhart-Hines Z et al (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1 alpha. Cell 127:1109–1122

    CAS  PubMed  Google Scholar 

  54. Lanza IR, Blachnio-Zabielska A, Zabielski P et al (2013) Influence of fish oil on skeletal muscle mitochondrial energetics and lipid metabolites during high-fat diet. FASEB J 27:E1391–1403

    Google Scholar 

  55. Lawrence JC, Salsgiver WJ (1984) Evidence that levels of malate-dehydrogenase and fumerase are increased by cAMP in rat myotubes. Am J Physiol 247:C33–C38

    CAS  PubMed  Google Scholar 

  56. Leick L, Fentz J, Bienso RS et al (2010) PGC-1 alpha is required for AICAR-induced expression of GLUT4 and mitochondrial proteins in mouse skeletal muscle. Am J Physiol-Endocr Metab 299:E456–E465

    CAS  Google Scholar 

  57. Lira VA, Brown DL, Lira AK et al (2010) Nitric oxide and AMPK cooperatively regulate PGC-1 alpha in skeletal muscle cells. J Physiol-London 588:3551–3566

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Long YC, Glund S, Garcia-Roves PM et al (2007) Calcineurin regulates skeletal muscle metabolism via coordinated changes in gene expression. J Biol Chem 282:1607–1614

    CAS  PubMed  Google Scholar 

  59. Lorente-Cebrian S, Perez-Matute P, Martinez JA et al (2006) Effects of eicosapentaenoic acid (EPA) on adiponectin gene expression and secretion in primary cultured rat adipocytes. J Physiol Biochem 62:61–69

    CAS  PubMed  Google Scholar 

  60. McCarty MF (2005) Up-regulation of PPAR-gamma coactivator-1 alpha as a strategy for preventing and reversing insulin resistance and obesity. Med Hypothesis 64:399–407

    CAS  Google Scholar 

  61. McConell GK, Ng GPY, Phillips M et al (2010) Central role of nitric oxide synthase in AICAR and caffeine-induced mitochondrial biogenesis in L6 myocytes. J Appl Physiol 108:589–595

    CAS  PubMed  Google Scholar 

  62. Mecleiros DM (2008) Assessing mitochondria biogenesis. Methods 46:288–294

    Google Scholar 

  63. Mensink M, Hesselink MKC, Russell AP et al (2007) Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1 alpha and PPAR beta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int J Obesity 31:1302–1310

    CAS  Google Scholar 

  64. Menzies KJ, Singh K, Saleem A, Hood DA (2013) Sirtuin 1-mediated effects of exercise and resveratrol on mitochondrial biogenesis. J Biol Chem 288:6968–6979

    CAS  PubMed  Google Scholar 

  65. Miura S, Kawanaka K, Kai Y et al (2007) An increase in murine skeletal muscle peroxisome proliferator-activated receptor-gamma coactivator-1 alpha (PGC-1 alpha) mRNA in response to exercise is mediated by beta-adrenergic receptor activation. Endocr 148:3414–3418

    Google Scholar 

  66. Mootha VK, Handschin C, Arlow D et al (2004) Err alpha and Gabpa/b specify PGC-1 alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci 101:6570–6575

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Morino K, Petersen KF, Dufour S et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Nishikawa S, Hosokawa M, Miyashita K (2012) Fucoxanthin promotes translocation and induction of glucose transporter 4 in skeletal muscles of diabetic/obese KK-A(y) mice. Phytomedicine 19:389–394

    CAS  PubMed  Google Scholar 

  70. O’Hagan KA, Cocchiglia S, Zhdanov AV et al (2009) PGC-1 alpha is coupled to HIF-1 alpha-dependent gene expression by increasing mitochondrial oxygen consumption in skeletal muscle cells. Proc Natl Acad Sci 106:2188–2193

    PubMed Central  PubMed  Google Scholar 

  71. Ojuka EO (2004) Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc of the Nutr Soc 63:275–278

    CAS  Google Scholar 

  72. Ojuka EO, Jones TE, Han DH et al (2003) Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle. FASEB J 17:675–681

    CAS  PubMed  Google Scholar 

  73. Ojuka EO, Jones TE, Han DH et al (2002) Intermittent increases in cytosolic Ca2+ stimulate mitochondrial biogenesis in muscle cells. Endocr Metab 283:E1040–E1045

    CAS  Google Scholar 

  74. Pagel-Langenickel I, Bao JJ, Joseph JJ et al (2008) PGC-1 alpha integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J Biol Chem 283:22464–22472

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Palacios OM, Carmona JJ, Michan S et al (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1 alpha in skeletal muscle. Aging-Us 1:771–783

    CAS  Google Scholar 

  76. Patti ME, Butte AJ, Crunkhorn S et al (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci 100:8466–8471

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Petrovic V, Korac A, Buzadzic B et al (2008) Nitric oxide regulates mitochondrial re-modelling in interscapular brown adipose tissue: ultrastructural and morphometric-stereologic studies. J Microscopy 232:542–548

    CAS  Google Scholar 

  78. Price NL, Gomes AP, Ling AJY et al (2012) SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab 15:675–690

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Prior SL, Clark AR, Jones DA et al (2012) Association of the PGC-1 alpha rs8192678 variant with microalbuminuria in subjects with type 2 diabetes mellitus. Dis Markers 32:363–369

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Puigserver P, Rhee J, Donovan J et al (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1 alpha interaction. Nature 423:550–555

    CAS  PubMed  Google Scholar 

  81. Puigserver P, Rhee J, Lin JD et al (2001) Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPAR gamma coactivator-1. Mol Cell 8:971–982

    CAS  PubMed  Google Scholar 

  82. Rangwala SM, Wang XM, Calvo JA et al (2010) Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285:22619–22629

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Reginato MJ, Lazar MA (1999) Mechanisms by which thiazolidinediones enhance insulin action. Trends in Endocrinol Metab 10:9–13

    CAS  Google Scholar 

  84. Rhee J, Ge HF, Yang WL et al (2006) Partnership of PGC-1 alpha and HNF4 alpha in the regulation of lipoprotein metabolism. J Biol Chem 281:14683–14690

    CAS  PubMed  Google Scholar 

  85. Rohas LM, St-Pierre J, Uldry M et al (2007) A fundamental system of cellular energy homeostasis regulated by PGC-1 alpha. Proc Natl Acad Sci 104:7933–7938

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Rowe GC, Jang C, Patten IS et al (2011) PGC-1 beta regulates angiogenesis in skeletal muscle. American J Physiol-Endocr Metab 301:E155–E163

    CAS  Google Scholar 

  87. Ryder JW, Bassel-Duby R, Olson EN et al (2003) Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278:44298–44304

    CAS  PubMed  Google Scholar 

  88. Sae-tan S, Grove KA, Kennett MJ et al (2011) (−)-Epigallocatechin-3-gallate increases the expression of genes related to fat oxidation in the skeletal muscle of high fat-fed mice. Food & Function 2:111–116

    CAS  Google Scholar 

  89. Scarpulla RC (2002) Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286:81–89

    CAS  PubMed  Google Scholar 

  90. Scarpulla RC (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochem Et Biophys Acta-Mol Cell Res 1813:1269–1278

    CAS  Google Scholar 

  91. Schaeffer PJ, Wende AR, Magee CJ et al (2004) Calcineurin and calcium/calmodulin-dependent protein kinase activate distinct metabolic gene regulatory programs in cardiac muscle. J Biol Chem 279:39593–39603

    CAS  PubMed  Google Scholar 

  92. Schreiber SN, Emter R, Hock MB et al (2004) The estrogen-related receptor alpha (ERR alpha) functions in PPAR gamma coactivator 1 alpha (PGC-1 alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci 101:6472–6477

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Seifarth C, Schehler B, Schneider HJ (2013) Effectiveness of metformin on weight loss in non-diabetic individuals with obesity. Exper Clin Endocrinol Diabetes 121:27–31

    CAS  Google Scholar 

  94. Semple RK, Crowley VC, Sewter CP et al (2004) Expression of the thermogenic nuclear hormone receptor coactivator PGC-1 alpha is reduced in the adipose tissue of morbidly obese subjects. Int J Obes 28:176–179

    CAS  Google Scholar 

  95. Shao D, Liu Y, Liu X et al (2010) PGC-1 beta-regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERR alpha. Mitochondrion 10:516–527

    CAS  PubMed  Google Scholar 

  96. Staels B, Dallongeville J, Auwerx J et al (1998) Mechanism of action of fibrates on lipid and lipoprotein metabolism. Circulation 98:2088–2093

    CAS  PubMed  Google Scholar 

  97. Summermatter S, Handschin C (2012) PGC-1 alpha and exercise in the control of body weight. Int J of Obesity 36:1428–1425

    CAS  Google Scholar 

  98. Sun X, Zemel MB (2007) Leucine and calcium regulate fat metabolism and energy partitioning in murine adipocytes and muscle cells. Lipids 42:297–305

    CAS  PubMed  Google Scholar 

  99. Sun X, Zemel MB (2009) Leucine modulation of mitochondrial mass and oxygen consumption in skeletal muscle cells and adipocytes. Nutr Metab 6:26

    Google Scholar 

  100. Sutherland LN, Bomhof MR, Capozzi LC et al (2009) Exercise and adrenaline increase PGC-1 alpha mRNA expression in rat adipose tissue. J Physiol-London 587:1607–1617

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Suwa M, Egashira T, Nakano H et al (2006) Metformin increases the PGC-1 alpha protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo. J Appl Physiol 101:1685–1692

    CAS  PubMed  Google Scholar 

  102. Tadaishi M, Miura S, Kai Y et al (2011) Skeletal muscle-specific expression of PGC-1 alpha-b, an exercise-responsive isoform, increases exercise capacity and peak oxygen uptake. Plos One 6:13

    Google Scholar 

  103. Tadaishi M, Miura S, Kai Y et al (2011) Effect of exercise intensity and AICAR on isoform-specific expressions of murine skeletal muscle PGC-1 alpha mRNA: a role of beta(2)-adrenergic receptor activation. Endocr and Metab 300:E341–E349

    CAS  Google Scholar 

  104. Timmers S, Konings E, Bilet L et al (2011) Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 14:612–622

    CAS  PubMed  Google Scholar 

  105. Ueda M, Nishiumi S, Nagayasu H et al (2008) Epigallocatechin gallate promotes GLUT4 translocation in skeletal muscle. Bioch Biophys Res Com 377:286–290

    CAS  Google Scholar 

  106. Uguccioni G, D’Souza D, Hood DA (2010) Regulation of PPARγ coactivator-1α function and expression in muscle: effect of exercise. PPAR Res doi: 10.1155/2010/937123

  107. Vaughan RA, Garcia-Smith R, Bisoffi M et al (2013) Ubiquinol rescues simvastatin-suppression of mitochondrial content, function and metabolism: implications for statin-induced rhabdomyolysis. Eur J Pharm 711:1–9

    CAS  Google Scholar 

  108. Vaughan RA, Garcia-Smith R, Gannon NP et al (2013) Leucine treatment enhances oxidative capacity through complete carbohydrate oxidation and increased mitochondrial density in skeletal muscle cells. Amino Acids 4:901–911

    Google Scholar 

  109. Vaughan RA, Garcia-Smith R, Bisoffi M et al (2012) Conjugated linoleic acid or omega 3 fatty acids increase mitochondrial biosynthesis and metabolism in skeletal muscle cells. Lipids Health Dis 11:142

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Vaughan RA, Garcia-Smith R, Bisoffi M et al (2012) Effects of caffeine on metabolism and mitochondria biogenesis in rhabdomyosarcoma cells compared with 2,4-dinitrophenol. Nutr Metab Insights 5:59

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Vaughan RA, Garcia-Smith R, Bisoffi M et al (2012) Treatment of human muscle cells with popular dietary supplements increase mitochondrial function and metabolic rate. Nutr Metab 9:101

    CAS  Google Scholar 

  112. Vega RB, Huss JM, Kelly DP (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20:1868–1876

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Viollet B, Guigas B, Sanz Garcia N et al (2012) Cellular and molecular mechanisms of metformin: an overview. Clin Science 122:253–270

    CAS  Google Scholar 

  114. Virbasius JV, Scarpulla RC (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors—a potential regulatory link between nuclear and mitochondrial gene expression in organelle biosynthesis. Proc Natl Acad Sci 91:1309–1313

    CAS  PubMed Central  PubMed  Google Scholar 

  115. Wagner AE, Ernst IMA, Birringer M et al (2012) A combination of lipoic acid plus coenzyme Q10 induces PGC1 alpha, a master switch of energy metabolism, improves stress response, and increases cellular glutathione levels in cultured C2C12 skeletal muscle cells. Oxidative Med Cell Longevity 9

  116. Wang Y, Beydoun MA, Liang L et al (2008) Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity 16:2323–2330

    PubMed  Google Scholar 

  117. Wang YX, Zhang CL, Yu RT et al (2004) Regulation of muscle fiber type and running endurance by PPAR delta. Plos Biol 2:e294

    PubMed Central  PubMed  Google Scholar 

  118. Wenz T, Diaz F, Spiegelman BM et al (2008) Activation of the PPAR/PGC-1 alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Cell Metab 8:249–256

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Winder WW, Holmes BF, Rubink DS et al (2000) Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88:2219–2226

    CAS  PubMed  Google Scholar 

  120. Wright DC, Geiger PC, Han DH et al (2007) Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1 alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282:18793–18799

    CAS  PubMed  Google Scholar 

  121. Wright DC, Han D-H, Garcia-Roves PM et al (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1 alpha expression. J Biol Chem 282:194–199

    CAS  PubMed  Google Scholar 

  122. Wu H, Kanatous SB, Thurmond FA et al (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349–352

    CAS  PubMed  Google Scholar 

  123. Wu ZD, Puigserver P, Andersson U et al (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124

    CAS  PubMed  Google Scholar 

  124. Yang XL, Enerback S, Smith U (2003) Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 11:1182–1191

    CAS  PubMed  Google Scholar 

  125. Yoon JC, Puigserver P, Chen GX et al (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413:131–138

    CAS  PubMed  Google Scholar 

  126. Zheng J, Chen LL, Zhang HH et al (2012) Resveratrol improves insulin resistance of catch-up growth by increasing mitochondrial complexes and antioxidant function in skeletal muscle. Metab-Clin Exp 61:954–965

    CAS  PubMed  Google Scholar 

  127. Zong HH, Ren JM, Young LH et al (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci 99:15983–15987

    CAS  PubMed Central  PubMed  Google Scholar 

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No funding was received for this work. The authors of this work declare no conflict of interest.

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Authors and Affiliations

  1. Department of Health, Exercise and Sports Science, University of New Mexico, 1 University Blvd, Albuquerque, NM, 87131, USA

    Roger A. Vaughan & Christine M. Mermier

  2. Department of Biochemistry and Molecular Biology, University of New Mexico Health Sciences Center, Albuquerque, NM, 87131, USA

    Roger A. Vaughan, Marco Bisoffi & Kristina A. Trujillo

  3. Department of Individual, Family, and Community Education: Nutrition, University of New Mexico, Albuquerque, NM, 87131, USA

    Roger A. Vaughan & Carole A. Conn

  4. Cancer Center, University of New Mexico, Albuquerque, NM, 87131, USA

    Marco Bisoffi & Kristina A. Trujillo

  5. Biological Sciences, Chapman University, Orange, CA, 92866, USA

    Marco Bisoffi

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  1. Roger A. Vaughan
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  2. Christine M. Mermier
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  3. Marco Bisoffi
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  4. Kristina A. Trujillo
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  5. Carole A. Conn
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Correspondence to Roger A. Vaughan.

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Vaughan, R.A., Mermier, C.M., Bisoffi, M. et al. Dietary stimulators of the PGC-1 superfamily and mitochondrial biosynthesis in skeletal muscle. A mini-review. J Physiol Biochem 70, 271–284 (2014). https://doi.org/10.1007/s13105-013-0301-4

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  • DOI: https://doi.org/10.1007/s13105-013-0301-4

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