111
Views
276
CrossRef citations to date
0
Altmetric
Gene Expression

PGC-1α Coactivates PDK4 Gene Expression via the Orphan Nuclear Receptor ERRα: a Mechanism for Transcriptional Control of Muscle Glucose Metabolism

, , , &
Pages 10684-10694 | Received 18 May 2005, Accepted 21 Sep 2005, Published online: 27 Mar 2023

REFERENCES

  • Arany, Z., H. He, J. Lin, K. Hoyer, C. Handschin, O. Toka, F. Ahmad, T. Matsui, S. Chin, P.-H. Wu, I. I. Rybkin, J. M. Shelton, M. Manieri, S. Cinti, F. J. Schoen, R. Bassel-Duby, A. Rosenzweig, J. S. Ingwall, and B. M. Spiegelman. 2005. Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle. Cell Metab. 1:259–271.
  • Baar, K., A. R. Wende, T. E. Jones, M. Marison, L. A. Nolte, M. Chen, D. P. Kelly, and J. O. Holloszy. 2002. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1α. FASEB J. 16:1879–1886.
  • Brandt, J., F. Djouadi, and D. P. Kelly. 1998. Fatty acids activate transcription of the muscle carnitine palmitoyltransferase I gene in cardiac myocytes via the peroxisome proliferator-activated receptor α. J. Biol. Chem. 273:23786–23792.
  • Carter, M. E., T. Gulick, B. D. Raisher, T. Caira, J. A. Ladias, D. D. Moore, and D. P. Kelly. 1993. Hepatocyte nuclear factor-4 activates medium chain acyl-CoA dehydrogenase gene transcription by interacting with a complex regulatory element. J. Biol. Chem. 268:13805–13810.
  • Caruso, M., C. Miele, P. Formisano, G. Condorelli, G. Bifulco, A. Oliva, R. Auricchio, G. Riccardi, B. Capaaldo, and F. Beguinot. 1997. In skeletal muscle, glucose storage and oxidation are differentially impaired by the IR1152 mutant receptor. J. Biol. Chem. 272:7290–7297.
  • Disch, D. L., T. A. Rader, S. Cresci, T. C. Leone, P. M. Barger, R. Vega, P. A. Wood, and D. P. Kelly. 1996. Transcriptional control of a nuclear gene encoding a mitochondrial fatty acid oxidation enzyme in transgenic mice: role for nuclear receptors in cardiac and brown adipose expression. Mol. Cell. Biol. 16:4043–4051.
  • Finck, B. N., C. Bernal-Mizrachi, D. H. Han, T. Coleman, N. Sambandam, L. L. LaRiviere, J. O. Holloszy, C. F. Semenkovich, and D. P. Kelly. 2005. A potential link between muscle peroxisome proliferator-activated receptor α signaling and obesity-related diabetes. Cell Metab. 1:133–144.
  • Finck, B. N., J. J. Lehman, T. C. Leone, M. J. Welch, M. J. Bennett, A. Kovacs, X. Han, R. W. Gross, R. Kozak, G. D. Lopaschuk, and D. P. Kelly. 2002. The cardiac phenotype induced by PPARα overexpression mimics that caused by diabetes mellitus. J. Clin. Investig. 109:121–130.
  • Furuyama, T., K. Kitayama, H. Yamashita, and N. Mori. 2003. Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem. J. 375:365–371.
  • Giguère, V., N. Yang, P. Segui, and R. M. Evans. 1988. Identification of a new class of steroid hormone receptors. Nature 331:91–94.
  • Gorman, C. 1985. High efficiency gene transfer into mammalian cells, p. 143–190. In D. M. Glover (ed.), DNA cloning, a practical approach. IRL Press, Oxford, United Kingdom.
  • Goto, M., S. Terada, M. Kato, M. Katoh, T. Yokozeki, I. Tabata, and T. Shimokawa. 2000. cDNA cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochem. Biophys. Res. Commun. 274:350–354.
  • Harris, R. A., M. M. Bowker-Kinley, B. Huang, and P. Wu. 2002. Regulation of the activity of the pyruvate dehydrogenase complex. Adv. Enzyme Regul. 42:249–259.
  • Herzig, S., F. Long, U. S. Jhala, S. Hedrick, R. Quinn, A. Bauer, D. Rudolph, G. Schutz, C. Yoon, P. Puigserver, B. Spiegelman, and M. Montminy. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413:179–183.
  • Hildebrandt, A. L., H. Pilegaard, and P. D. Neufer. 2003. Differential transcriptional activation of select metabolic genes in response to variations in exercise intensity and duration. Am. J. Physiol. Endocrinol. Metab. 285:E1021–E1027.
  • Holness, M. J., and M. C. Sugden. 2003. Regulation of pyruvate dehydrogenase complex activity by reversible phosphorylation. Biochem. Soc. Trans. 31:1143–1151.
  • Huang, B., P. Wu, M. M. Bowker-Kinley, and H. A. Harris. 2002. Regulation of pyruvate dehydrogenase kinase expression by peroxisome proliferator-activated receptor-α ligands, glucocorticoids, and insulin. Diabetes 51:276–283.
  • Huss, J. M., R. P. Kopp, and D. P. Kelly. 2002. PGC-1α coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and -γ. J. Biol. Chem. 277:40265–40274.
  • Huss, J. M., F. H. Levy, and D. P. Kelly. 2001. Hypoxia inhibits the PPARα/RXR gene regulatory pathway in cardiac myocytes. J. Biol. Chem. 276:27605–27612.
  • Huss, J. M., I. Pinéda Torra, B. Staels, V. Giguère, and D. P. Kelly. 2004. ERRα directs PPARα signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24:9079–9091.
  • Im, H., J. A. Grass, K. D. Johnson, M. E. Boyer, J. Wu, and E. H. Bresnick. 2004. Measurement of protein-DNA interactions in vivo by chromatin immunoprecipitation. Methods Mol. Biol. 284:129–146.
  • Itoh, Y., T. Esaki, K. Shimoji, M. Cook, J. Law, E. Kaufman, and L. Sokoloff. 2003. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose oxidation by brain in vivo. Proc. Natl. Acad. Sci. USA 100:4879–4884.
  • Johnston, S. D., Z. Liu, F. Zuo, T. L. Eisenbraun, S. R. Wiley, R. J. Krauss, and J. E. Mertz. 1997. Estrogen-related receptor α1 functionally binds as a monomer to extended half-site sequences including ones contained within estrogen-response elements. Mol. Endocrinol. 11:342–352.
  • Kelly, D. P., J. J. Kim, J. J. Billadello, B. E. Hainline, T. W. Chu, and A. W. Strauss. 1987. Nucleotide sequence of medium-chain acyl-CoA dehydrogenase mRNA and its expression in enzyme-deficient human tissue. Proc. Natl. Acad. Sci. USA 84:4068–4072.
  • Kelly, D. P., and R. C. Scarpulla. 2004. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18:357–368.
  • Kwon, H. S., B. Huang, G. Unterman, and R. A. Harris. 2004. Protein kinase B-α inhibits human pyruvate dehydrogenase kinase-4 gene induction by dexamethasone through inactivation of FOXO transcription factors. Diabetes 53:899–910.
  • Laganiere, J., G. B. Tremblay, C. R. Dufour, S. Giroux, F. Rousseau, and V. Giguère. 2004. A polymorphic autoregulatory hormone response element in the human estrogen-related receptor α (ERRα) promoter dictates peroxisome proliferator-activated receptor γ coactivator-1α control of ERRα expression. J. Biol. Chem. 279:18504–18510.
  • Lehman, J. J., P. M. Barger, A. Kovacs, J. E. Saffitz, D. Medeiros, and D. P. Kelly. 2000. PPARγ coactivator-1 (PGC-1) promotes cardiac mitochondrial biogenesis. J. Clin. Investig. 106:847–856.
  • Leone, T. C., J. J. Lehman, B. N. Finck, P. J. Schaeffer, A. R. Wende, S. Boudina, M. Courtois, D. F. Wozniak, N. Sambandam, C. Bernal-Mizrachi, Z. Chen, J. O. Holloszy, D. M. Medeiros, R. E. Schmidt, J. E. Saffitz, E. D. Abel, C. F. Semenkovich, and D. P. Kelly. 2005. PGC-1α deficient mice exhibit multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control, and hepatic steatosis. PLoS Biol. 3:672–687.
  • Lin, J., H. Wu, P. T. Tarr, C. Y. Zhang, Z. Wu, O. Boss, L. F. Michael, P. Puigserver, E. Isotanni, E. N. Olson, B. B. Lowell, R. Bassel-Duby, and B. M. Spiegelman. 2002. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibers. Nature 418:797–801.
  • Lin, J., P.-H. Wu, P. T. Tarr, K. S. Lindenberg, J. St.-Pierre, C.-Y. Zhang, V. K. Mootha, S. Jãger, C. R. Vianna, R. M. Reznick, L. Cui, M. Manieri, M. X. Donovan, Z. Wu, M. P. Cooper, M. C. Fan, L. M. Rohas, A. M. Zavacki, S. Cinti, G. I. Shulman, B. B. Lowell, D. Krainc, and B. M. Spiegelman. 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119:121–135.
  • Luo, J., R. Sladek, J. Carrier, J. A. Bader, D. Richard, and V. Giguère. 2003. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol. Cell. Biol. 23:7947–7956.
  • Michael, L. F., Z. Wu, R. B. Cheatham, P. Puigserver, G. Adelmant, J. J. Lehman, D. P. Kelly, and B. M. Spiegelman. 2001. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. USA 98:3820–3825.
  • Miura, S., Y. Kai, M. Ono, and O. Ezaki. 2003. Overexpression of peroxisome proliferator-activated receptor γ coactivator-1α down-regulates GLUT4 mRNA in skeletal muscles. J. Biol. Chem. 278:31385–31390.
  • Mootha, V. K., C. Handschin, D. Arlow, X. Xie, J. St. Pierre, S. Sihag, W. Yang, D. Altshuler, P. Puigserver, N. Patterson, P. J. Willy, I. G. Schulman, R. A. Heyman, E. S. Lander, and B. M. Spiegelman. 2004. ERRα and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. USA 101:6570–6575.
  • Mootha, V. K., C. M. Lindgren, K.-F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstråle, E. Laurila, N. Houstis, M. J. Daly, N. Patterson, J. P. Mesirov, T. R. Golub, P. Tamayo, B. M. Spiegelman, E. S. Lander, J. N. Hirschhorn, D. Altshuler, and L. C. Groop. 2003. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:267–273.
  • Pilegaard, H., G. A. Ordway, B. Saltin, and P. D. Neufer. 2000. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am. J. Physiol. Endocrinol. Metab. 279:E806–E814.
  • Pilegaard, H., B. Saltin, and P. D. Neufer. 2003. Exercise induces transient transcriptional activation of the PGC-1α gene in human skeletal muscle. J. Physiol. 546:851–858.
  • Puigserver, P., J. Rhee, J. Donovan, C. J. Walkey, J. C. Yoon, F. Oriente, Y. Kitamura, J. Altomonte, H. Dong, D. Accili, and B. M. Spiegelman. 2003. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423:550–555.
  • Puigserver, P., and B. M. Spiegelman. 2003. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocrine Rev. 24:78–90.
  • Puigserver, P., Z. Wu, C. W. Park, R. Graves, M. Wright, and B. M. Spiegelman. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829–839.
  • Randle, P. J., C. N. Hales, and P. B. Garland. 1963. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet i:785–789.
  • Rowles, J., S. W. Scherer, T. Xi, M. Majer, D. C. Nickle, J. M. Rommens, K. M. Popov, R. A. Harris, N. L. Riebow, J. Xia, L. C. Tsui, C. Bogardus, and M. Prochazka. 1996. Cloning and characterization of PDK4 on 7q21.3 encoding a fourth pyruvate dehydrogenase kinase isoenzyme in human. J. Biol. Chem. 271:22376–22382.
  • Russell, L. K., C. M. Mansfield, J. J. Lehman, A. Kovacs, M. Courtois, J. E. Saffitz, D. M. Medeiros, M. L. Valencik, J. A. McDonald, and D. P. Kelly. 2004. Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor γ coactivator-1α promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ. Res. 94:525–533.
  • Schreiber, S. N., R. Emter, M. B. Hock, D. Knutti, J. Cardenas, M. Podvinec, E. J. Oakeley, and A. Kralli. 2004. The estrogen-related receptor alpha (ERRα) functions in PPARγ coactivator 1α (PGC-1α)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. USA 101:6472–6477.
  • Schreiber, S. N., D. Knutti, K. Brogli, T. Uhlmann, and A. Kralli. 2003. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor α (ERRα). J. Biol. Chem. 278:9013–9018.
  • Sladek, R. J., J.-A. Bader, and V. Giguère. 1997. The orphan nuclear receptor estrogen-related receptor α is a transcriptional regulator of the human medium-chain acyl coenzyme A dehydrogenase gene. Mol. Cell. Biol. 17:5400–5409.
  • Sugden, M. C., and M. J. Holness. 2003. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am. J. Phys. Endocrinol. Metab. 284:E855–E862.
  • Tang, E. D., G. Nuñez, G. Barr, and K.-L. Guan. 1999. Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274:16741–16746.
  • Trapp, T., and F. Holsboer. 1996. Nuclear orphan receptor as a repressor of glucocorticoid receptor transcriptional activity. J. Biol. Chem. 271:9879–9882.
  • Vega, R. B., J. M. Huss, and D. P. Kelly. 2000. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20:1868–1876.
  • Weinmann, A. S., and P. J. Farnham. 2002. Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods 26:37–47.
  • Willy, P. J., I. R. Murray, J. Qian, B. B. Busch, W. C. Stevens, R. Martin, R. Mohan, S. Zhou, P. Ordentlich, P. Wei, D. W. Sapp, R. A. Horlick, R. A. Heyman, and I. G. Schulman. 2004. Regulation of PPARγ coactivator 1α (PGC-1α) signaling by an estrogen-related receptor α (ERRα) ligand. Proc. Natl. Acad. Sci. USA 101:8912–8917.
  • Wu, P., K. Inskeep, M. M. Bowker-Kinley, K. M. Popov, and R. A. Harris. 1999. Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 48:1593–1599.
  • Wu, P., J. M. Peters, and R. A. Harris. 2001. Adaptive increase in pyruvate dehydrogenase kinase 4 during starvation is mediated by peroxisome proliferator-activated receptor α. Biochem. Biophys. Res. Commun. 287:391–396.
  • Wu, Z., P. Puigserver, U. Andersson, C. Zhang, G. Adelmant, V. Mootha, A. Troy, S. Cinti, B. Lowell, R. C. Scarpulla, and B. M. Spiegelman. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124.
  • Yoon, J. C., P. Puigserver, G. Chen, J. Donovan, Z. Wu, J. Rhee, G. Adelmant, J. Stafford, C. R. Kahn, D. K. Granner, C. B. Newgard, and B. M. Spiegelman. 2001. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413:131–138.

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.