Publication Cover
Archives of Physiology and Biochemistry
The Journal of Metabolic Diseases
Volume 124, 2018 - Issue 3
457
Views
7
CrossRef citations to date
0
Altmetric
Original Article

Understanding mitochondrial biogenesis through energy sensing pathways and its translation in cardio-metabolic health

&
Pages 194-206 | Received 22 Jan 2017, Accepted 10 Oct 2017, Published online: 26 Oct 2017

References

  • Adhihetty, P.J., et al., 2009. The role of PGC-1α on mitochondrial function and apoptotic susceptibility in muscle. American journal of physiology-cell physiology, 297, C217–C225.
  • Alaynick, W.A., 2008. Nuclear receptors, mitochondria and lipid metabolism. Mitochondrion, 8, 329–337.
  • Amat, R., et al., 2009. SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-γ co-activator-1α (PGC-1α) gene in skeletal muscle through the PGC-1α autoregulatory loop and interaction with MyoD. Journal of biological chemistry, 284, 21872–21880.
  • American Diabetes Association. 1999. Diabetes mellitus: a major risk factor for cardiovascular disease. A joint editorial statement by the American diabetes association; the national heart, lung, and blood institute; the juvenile diabetes foundation international; the national institute of diabetes and digestive and kidney diseases; and the American heart association. Circulation, 100, 1132–1133.
  • Aquilano, K., et al., 2010. Peroxisome Proliferator-activated receptor γ Co-activator 1α (PGC-1α) and Sirtuin 1 (SIRT1) reside in mitochondria possible direct function in mitochondrial biogenesis. Journal of biological chemistry, 285, 21590–21599.
  • Banks, A.S., et al., 2008. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell metabolism, 8, 333–341.
  • Baar, K., et al., 2002. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. The FASEB journal, 16, 1879–1886.
  • Boily, G., et al., 2008. SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS One, 3, 1759.
  • Bordone, L., et al., 2005. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic β cells. PLoS biology, 4, e31.
  • Boudina, S. and Graham, T.E., 2014. Mitochondrial function/dysfunction in white adipose tissue. Experimental physiology, 99, 1168–1178.
  • Boutant, M. and Cantó, C., 2014. SIRT1 metabolic actions: integrating recent advances from mouse models. Molecular metabolism, 3, 5–18.
  • Brenmoehl, J. and Hoeflich, A., 2013. Dual control of mitochondrial biogenesis by sirtuin 1 and sirtuin 3. Mitochondrion, 13, 755–761.
  • Brunet, A., et al., 2004. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science, 303, 2011–2015.
  • Burris, T.P., et al., 2013. Nuclear receptors and their selective pharmacologic modulators. Pharmacological reviews, 65, 710–778.
  • Calvo, J.A., et al., 2008. Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake. Journal of applied physiology, 104, 1304–1312.
  • Cantó, C. and Auwerx, J., 2009. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Current opinion in lipidology, 20, 98–105.
  • Chang, L.T., et al., 2006. Downregulation of peroxisme proliferator activated receptor gamma co-activator 1alpha in diabetic rats. International heart journal, 47, 901–910.
  • Chinsomboon, J., et al., 2009. The transcriptional coactivator PGC-1α mediates exercise-induced angiogenesis in skeletal muscle. Proceedings of the national academy of sciences, 106, 21401–21406.
  • Civitarese, A.E., et al., 2007. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS medicine, 4, e76.
  • Contreras, A.V., Torres, N., and Tovar, A.R., 2013. PPAR-α as a key nutritional and environmental sensor for metabolic adaptation. Advances in nutrition: An international review journal, 4, 439–452.
  • Coste, A., et al., 2008. The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1α. Proceedings of the national academy of sciences, 105, 17187–17192.
  • Cuala, J.M., Osuji, I.M., and Lopez-Zuirta, C., 2017. Investigating methylated arginine residue in PGC-1α. The FASEB journal, 31, Ib141.
  • De Matteis, R., et al., 2013. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutrition, metabolism and cardiovascular diseases, 23, 582–590.
  • Dominy, J.E., et al., 2010. Nutrient-dependent regulation of PGC-1α's acetylation state and metabolic function through the enzymatic activities of Sirt1/GCN5. Biochimica et biophysica acta (BBA)-proteins and proteomics, 1804, 1676–1683.
  • Duchen, M.R., 2004. Roles of mitochondria in health and disease. Diabetes, 53, S96–S102.
  • Evans, M.J. and Scarpulla, R., 1989. Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. Journal of biological chemistry, 264, 14361–14368.
  • Fan, W. and Evans, R., 2015. PPARs and ERRs: molecular mediators of mitochondrial metabolism. Current opinion in cell biology, 33, 49–54.
  • Feige, J.N., et al., 2008. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell metabolism, 8, 347–358.
  • Fernandez-Marcos, P.J. and Auwerx, J., 2011. Regulation of PGC-1α, a nodal regulator of mitochondrial biogenesis. The American journal of clinical nutrition, 93, 884S–890S.
  • Ferré, P., 2004. The biology of peroxisome proliferator-activated receptors relationship with lipid metabolism and insulin sensitivity. Diabetes, 53, S43–S50.
  • Finck, B.N. and Kelly, D.P., 2006. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. Journal of clinical investigation, 116, 615–622.
  • Finck, B.N. and Kelly, D.P., 2007. Peroxisome proliferator–activated receptor γ coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease. Circulation, 115, 2540–2548.
  • Finkel, T., Deng, C.X., and Mostoslavsky, R., 2009. Recent progress in the biology and physiology of sirtuins. Nature, 460, 587–591.
  • Finley, L.W. and Haigis, M.C., 2009. The coordination of nuclear and mitochondrial communication during aging and calorie restriction. Ageing research reviews, 8, 173–188.
  • Ford, R.J., Desjardins, E.M., and Steinberg, G.R., 2017. Are SIRT1 activators another indirect method to increase AMPK for beneficial effects on aging and the metabolic syndrome? EBioMedicine, 19, 16–17.
  • Freyssenet, D., Berthon, P., and Denis, C., 1996. Mitochondrial biogenesis in skeletal muscle in response to endurance exercises. Archives of physiology and biochemistry, 104, 129–141.
  • Garesse, R. and Vallejo, C.G., 2001. Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene, 263, 1–16.
  • Garnier, A., et al., 2003. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. The journal of physiology, 551, 491–501.
  • Gil, A., et al., 2011. Is adipose tissue metabolically different at different sites? International journal of pediatric obesity, 6, 13–20.
  • Greer, E.L., et al., 2007. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. Journal of biological chemistry, 282, 30107–30119.
  • Haigis, M.C. and Sinclair, D.A., 2010. Mammalian sirtuins: biological insights and disease relevance. Annual review of pathology: mechanisms of disease, 5, 253–295.
  • Handschin, C., et al., 2007. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals. Journal of biological chemistry, 282, 30014–30021.
  • Handschin, C., et al., 2003. An autoregulatory loop controls peroxisome proliferator-activated receptor γ coactivator 1α expression in muscle. Proceedings of the national academy of sciences, 100, 7111–7116.
  • Handschin, C. and Spiegelman, B.M., 2008. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature, 454, 463–469.
  • Hashidume, T., et al., 2011. Consumption of soy protein isolate reduces hepatic SREBP-1c and lipogenic gene expression in wild-type mice, but not in FXR-deficient mice. Bioscience, biotechnology, and biochemistry, 75, 1702–1707.
  • Heilbronn, L.K., et al., 2006. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA, 295, 1539–1548.
  • Hesselink, M.K., Schrauwen-Hinderling, V., and Schrauwen, P., 2016. Skeletal muscle mitochondria as a target to prevent or treat type 2 diabetes mellitus. Nature reviews endocrinology, 12, 633–645.
  • Hirschey, M.D., et al., 2011. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Molecular cell, 44, 177–190.
  • Hock, M.B. and Kralli, A., 2009. Transcriptional control of mitochondrial biogenesis and function. Annual review of physiology, 71, 177–203.
  • Jäger, S., et al., 2007. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proceedings of the national academy of sciences, 104, 12017–12022.
  • Jing, E., et al., 2011. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proceedings of the national academy of sciences, 108, 14608–14613.
  • Jornayvaz, F.R. and Shulman, G.I., 2010. Regulation of mitochondrial biogenesis. Essays in biochemistry, 47, 69–84.
  • Joseph, A.M., et al., 2011. Mitochondrial dysregulation in the pathogenesis of diabetes: potential for mitochondrial biogenesis-mediated interventions. Experimental diabetes research, 2012, 1–16.
  • Kahn, B.B., et al., 2005. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell metabolism, 1, 15–25.
  • Kelly, D.P. and Scarpulla, R.C., 2004. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes and development, 18, 357–368.
  • Kleiner, S., et al., 2012. Development of insulin resistance in mice lacking PGC-1α in adipose tissues. Proceedings of the national academy of sciences, 109, 9635–9640.
  • Knutti, D. and Kralli, A., 2001. PGC-1, a versatile coactivator. Trends in endocrinology and metabolism: Tem, 12, 360–365.
  • Koves, T.R., et al., 2013. PPARγ coactivator-1α contributes to exercise-induced regulation of intramuscular lipid droplet programming in mice and humans. Journal of lipid research, 54, 522–534.
  • Kressler, D., et al., 2002. The PGC-1-related protein PERC is a selective coactivator of estrogen receptor α. Journal of biological chemistry, 277, 13918–13925.
  • Lagouge, M., et al., 2006. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell, 127, 1109–1122.
  • Leick, L., et al., 2008. PGC-1α is not mandatory for exercise-and training-induced adaptive gene responses in mouse skeletal muscle. American journal of physiology-endocrinology and metabolism, 294, E463–E474.
  • Lerin, C., et al., 2006. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1α. Cell metabolism, 3, 429–438.
  • Li, J., et al., 2010. Comparison of effects of simvastatin versus atorvastatin on oxidative stress in patients with coronary heart disease. Clinical cardiology, 33, 222–227.
  • Li, X., 2013. SIRT1 and energy metabolism. Acta biochimica et biophysica sinica, 45, 51–60.
  • Li, J., et al., 2017. Dissecting the role of AMP-activated protein kinase in human diseases. Acta pharmaceutica sinica B, 7, 249–259.
  • Liang, H. and Ward, W.F., 2006. PGC-1alpha: a key regulator of energy metabolism. Advances in physiology education, 30, 145–151.
  • Lin, J., et al., 2002. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature, 41, 797–801.
  • Lin, J., et al., 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell, 119, 121–135.
  • Lin, H.V. and Accili, D., 2011. Hormonal regulation of hepatic glucose production in health and disease. Cell metabolism, 14, 9–19.
  • Lin, J., Handschin, C., and Spiegelman, B.M., 2005. Metabolic control through the PGC-1 family of transcription coactivators. Cell metabolism, 1, 361–370.
  • Little, J.P., et al., 2010. Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. American journal of physiology-regulatory, integrative and comparative physiology, 298, R912–R917.
  • Little, J.P., et al., 2011. Skeletal muscle and beyond: the role of exercise as a mediator of systemic mitochondrial biogenesis. Applied physiology, nutrition, and metabolism, 36, 598–607.
  • López-Lluch, G., et al., 2008. Mitochondrial biogenesis and healthy aging. Experimental gerontology, 43, 813–819.
  • Lustig, Y., et al., 2011. Separation of the gluconeogenic and mitochondrial functions of PGC-1α through S6 kinase. Genes and development, 25, 1232–1244.
  • Marín-García, J., et al., 2009. Regional distribution of mitochondrial dysfunction and apoptotic remodeling in pacing-induced heart failure. Journal of cardiac failure, 15, 700–708.
  • Mathai, A.S., et al., 2008. Rapid exercise-induced changes in PGC-1α mRNA and protein in human skeletal muscle. Journal of applied physiology, 105, 1098–1105.
  • Matsushima, S. and Sadoshima, J., 2015. The role of sirtuins in cardiac disease. American journal of physiology. heart and circulatory physiology, 309, H1375–H1389.
  • Meex, R.C., et al., 2010. Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes, 59, 572–579.
  • Menshikova, E.V., et al., 2005. Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. American journal of physiology-endocrinology and metabolism, 288, E818–E825.
  • Miura, S., et al., 2008. Isoform-specific increases in murine skeletal muscle peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) mRNA in response to β2-adrenergic receptor activation and exercise. Endocrinology, 149, 4527–4533.
  • Montagner, A., et al., 2016. Liver PPARα is crucial for whole-body fatty acid homeostasis and is protective against NAFLD. Gut, 65, 1202–1214.
  • Montgomery, M.K. and Turner, N., 2015. Mitochondrial dysfunction and insulin resistance: an update. Endocrine connections, 4, R1–R15.
  • Mootha, V.K., et al., 2003. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature genetics, 34, 267–273.
  • Nirwane, A. and Majumdar, A., 2016a. Resveratrol and pterostilbene ameliorate the metabolic derangements associated with smokeless tobacco in estrogen deficient female rats. Journal of functional foods, 23, 261–277.
  • Nirwane, A. and Majumdar, A., 2016b. Resveratrol and pterostilbene attenuated smokeless tobacco induced cardiovascular aberrations in estrogen deficient female rats. Toxicology research, 5, 1604–1618.
  • Nisoli, E., et al., 2007. Defective mitochondrial biogenesis a hallmark of the high cardiovascular risk in the metabolic syndrome? Circulation research, 100, 795–806.
  • Oberkofler, H., et al., 2002. Peroxisome proliferator-activated receptor (PPAR) γ coactivator-1 recruitment regulates PPAR subtype specificity. Journal of biological chemistry, 277, 16750–16757.
  • Ongwijitwat, S., et al., 2006. Nuclear respiratory factor 2 senses changing cellular energy demands and its silencing down-regulates cytochrome oxidase and other target gene mRNAs. Gene, 374, 39–49.
  • Pardo, R., et al., 2011. Rosiglitazone-induced mitochondrial biogenesis in white adipose tissue is independent of peroxisome proliferator-activated receptor γ coactivator-1α. PLoS one, 6, e26989.
  • Patti, M.E., et al., 2003. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proceedings of the national academy of sciences, 100, 8466–8471.
  • Pearson, K.J., et al., 2008. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell metabolism, 8, 157–168.
  • Pfluger, P.T., et al., 2008. Sirt1 protects against high-fat diet-induced metabolic damage. Proceedings of the national academy of sciences, 105, 9793–9798.
  • Phielix, E., et al., 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.
  • Picard, M. and Burelle, Y., 2012. Mitochondria: starving to reach quorum?: insight into the physiological purpose of mitochondrial fusion Bioessays: News and reviews in molecular, cellular and developmental biology, 34, 272–274.
  • Pilegaard, H., Saltin, B., and Neufer, P.D., 2003. Exercise induces transient transcriptional activation of the PGC‐1α gene in human skeletal muscle. The journal of physiology, 546, 851–858.
  • Puigserver, P., et al., 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 92, 829–839.
  • Puigserver, P., et al., 2001. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARγ coactivator-1. Molecular cell, 8, 971–982.
  • Puigserver, P. and Spiegelman, B.M., 2003. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocrine reviews, 24, 78–90.
  • Reznick, R.M., et al., 2007. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell metabolism, 5, 151–156.
  • Rhee, J., et al., 2003. Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis. Proceedings of the national academy of sciences, 100, 4012–4017.
  • Rimbaud, S., Garnier, A., and Ventura-Clapier, R., 2009. Mitochondrial biogenesis in cardiac pathophysiology. Pharmacological reports, 61, 131–138.
  • Rodgers, J.T., et al., 2005. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature, 434, 113–118.
  • Rodgers, J.T., et al., 2008. Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways. FEBS letters, 582, 46–53.
  • Rowe, G.C., et al., 2012. PGC-1α is dispensable for exercise-induced mitochondrial biogenesis in skeletal muscle. PLoS one, 7, 41817.
  • Ruderman, N. and Prentki, M., 2004. AMP kinase and malonyl-CoA: targets for therapy of the metabolic syndrome. Nature reviews. drug discovery, 3, 340–351.
  • Ruderman, N.B., et al., 2010. AMPK and SIRT1: a long-standing partnership? American journal of physiology-endocrinology and metabolism, 298, E751–E760.
  • Safdar, A., et al., 2011. Exercise increases mitochondrial PGC-1α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. Journal of biological chemistry, 286, 10605–10617.
  • Scarpulla, R.C., 2002. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochimica et biophysica acta (BBA)-gene structure and expression, 1576, 1–14.
  • Scarpulla, R.C., 2011. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochimica et biophysica acta (BBA)-molecular cell research, 1813, 1269–1278.
  • Scarpulla, R.C., 2012. Nucleus-encoded regulators of mitochondrial function: Integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochimica et biophysica acta (BBA)-gene regulatory mechanisms, 1819, 1088–1097.
  • Sebastiani, M., et al., 2007. Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. Journal of the American College of Cardiology, 50, 1362–1369.
  • Sinclair, D.A. and Guarente, L., 2006. Unlocking the secrets of longevity genes. Scientific american, 294, 48–57.
  • Sonoda, J., Pei, L., and Evans, R.M., 2008. Nuclear receptors: decoding metabolic disease. FEBS letters, 582, 2–9.
  • Staels, B., et al., 1998. Mechanism of action of fibrates on lipid and lipoprotein metabolism. Circulation, 98, 2088–2093.
  • Sun, C.K., et al., 2007. Losartan preserves integrity of cardiac gap junctions and PGC-1. ALPHA. gene expression and prevents cellular apoptosis in remote area of left ventricular myocardium following acute myocardial infarction. International heart journal, 48, 533–546.
  • Sutherland, L.N., et al., 2008. Time course of high-fat diet-induced reductions in adipose tissue mitochondrial proteins: potential mechanisms and the relationship to glucose intolerance. American journal of physiology-endocrinology and metabolism, 295, E1076–E1083.
  • Sutherland, L.N., et al., 2009. Exercise and adrenaline increase PGC‐1α mRNA expression in rat adipose tissue. The journal of physiology, 587, 1607–1617.
  • Taylor, R.W. and Turnbull, D.M., 2005. Mitochondrial DNA mutations in human disease. Nature reviews. Genetics, 6, 389–402.
  • Terada, S., et al., 2002. Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochemical and biophysical research communications, 296, 350–354.
  • Teyssier, C., et al., 2005. Activation of nuclear receptor coactivator PGC-1α by arginine methylation. Genes and development, 19, 1466–1473.
  • Tiraby, C., et al., 2003. Acquirement of brown fat cell features by human white adipocytes. Journal of biological chemistry, 278, 33370–33376.
  • Tyagi, S., et al., 2011. The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. Journal of advanced pharmaceutical technology and research, 2, 236–240.
  • Vásquez‐Trincado, C., et al., 2016. Mitochondrial dynamics, mitophagy and cardiovascular disease. The journal of physiology, 594, 509–525.
  • Vega, R.B., Huss, J.M., and Kelly, D.P., 2000. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Molecular and cellular biology, 20, 1868–1876.
  • Virbasius, C.A., Virbasius, J.V., and Scarpulla, R.C., 1993. NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes and development, 7, 2431–2445.
  • Walther, D.M. and Rapaport, D., 2009. Biogenesis of mitochondrial outer membrane proteins. Biochimica et biophysica acta (BBA)-molecular cell research, 1793, 42–51.
  • Wang, K. and Wan, Y.J.Y., 2008. Nuclear receptors and inflammatory diseases. Experimental biology and medicine, 233, 496–506.
  • Wang, Y., et al., 2012. SIRT1 in metabolic syndrome: where to target matters. Pharmacology and therapeutics, 136, 305–318.
  • Wang, L., et al., 2013. Erythropoietin contributes to slow oxidative muscle fiber specification via PGC-1α and AMPK activation. The international journal of biochemistry & cell biology, 45, 1155–1164.
  • Watson, P.A., et al., 2007. Restoration of CREB function is linked to completion and stabilization of adaptive cardiac hypertrophy in response to exercise. American journal of physiology-heart and circulatory physiology, 293, H246–H259.
  • Wilson, D.M., III., and Brooks, P.J., 2010. The mitochondrial genome: dynamics, mechanisms of repair, and a target in disease and therapy. Environmental and molecular mutagenesis, 51, 349–351.
  • Witt, H., et al., 2008. Sex-specific pathways in early cardiac response to pressure overload in mice. Journal of molecular medicine, 86, 1013–1024.
  • Wright, D.C., et al., 2007. Calcium induces increases in peroxisome proliferator-activated receptor γ coactivator-1α and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. Journal of biological chemistry, 282, 18793–18799.
  • Wu, Z., et al., 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell, 98, 115–124.
  • Wu, H., et al., 2016. PGC-1α, glucose metabolism and type 2 diabetes mellitus. The journal of endocrinology, 229, R99–115.
  • Yoboue, E.D. and Devin, A., 2012. Reactive oxygen species-mediated control of mitochondrial biogenesis. International journal of cell biology, 2012, 1–9.
  • Yoshino, J. and Imai, S.I., 2011. Mitochondrial SIRT3: a new potential therapeutic target for metabolic syndrome. Molecular cell, 44, 170–171.
  • Yu, X. and Long, Y.C., 2015. Autophagy modulates amino acid signaling network in myotubes: differential effects on mTORC1 pathway and the integrated stress response. The FASEB journal, 29, 394–407.
  • Zechner, C., et al., 2010. Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell metabolism, 12, 633–642.
  • Zhang, H.H., et al., 2015. SIRT1 overexpression in skeletal muscle in vivo induces increased insulin sensitivity and enhanced complex I but not complex II–V functions in individual subsarcolemmal and intermyofibrillar mitochondria. Journal of physiology and biochemistry, 71, 177–190.
  • Zhang, Y., et al., 2004. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes and development, 18, 157–169.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.