Dual modulation of both lipid oxidation and synthesis by peroxisome proliferator-activated receptor-γ coactivator-1α and -1β in cultured myotubes

FASEB Journal

Volumn 24, Issue 4, 2010, Pages 1003-1014

  Espinoza, Daniel O ^a,b   Boros, Laszlo G ^c,d   Crunkhorn, Sarah ^a,b   Gami, Hiral ^a,b   Patti, Mary Elizabeth ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SIDMAP LLC   (United States)

Author keywords

Fatty acid metabolism; Lipid metabolism; Metabolomics

Indexed keywords

CARBON 13; CARBON 14; COMPLEMENTARY DNA; FATTY ACID; GLUCOSE; LIPID; MESSENGER RNA; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; RNA; PALMITIC ACID DERIVATIVE; PPARGC1A PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ARTICLE; FATTY ACID METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN METABOLISM; ISOTOPE LABELING; LIPID METABOLISM; LIPID OXIDATION; MYOTUBE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; SKELETAL MUSCLE;

ANIMALS; CELL LINE; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION REGULATION; MICE; MUSCLE FIBERS, SKELETAL; OBESITY; OXIDATION-REDUCTION; PALMITATES; TRANS-ACTIVATORS;

EID: 77951633406     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-133728     Document Type: Article

References (57)

1. 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. Mol. Cell. Biol. 20, 1868-1876
2. Rhee, J., Inoue, Y., Yoon, J. C., Puigserver, P., Fan, M., Gonzalez, F. J., and Spiegelman, B. M. (2003) Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis. Proc. Natl. Acad. Sci. U. S. A. 100, 4012-4017
3. Scarpulla, R. C. (2002) Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286, 81-89
4. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., St. Pierre, J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N., Willy, P. J., Schulman, I. G., Heyman, R. A., Lander, E. S., and Spiegelman, B. M. (2004) Errα and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U. S. A. 101, 6570-6575
5. Lin, J., Yang, R., Tarr, P. T., Wu, P. H., Handschin, C., Li, S., Yang, W., Pei, L., Uldry, M., Tontonoz, P., Newgard, C. B., and Spiegelman, B. M. (2005) Hyperlipidemic effects of dietary saturated fats mediated through PGC-1β coactivation of SREBP. Cell 120, 261-273
6. Lin, J., Wu, H., Tarr, P. T., Zhang, C. Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N., Lowell, B. B., Bassel-Duby, R., and Spiegelman, B. M. (2002) Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418, 797-801
7. Arany, Z., Lebrasseur, N., Morris, C., Smith, E., Yang, W., Ma, Y., Chin, S., and Spiegelman, B. M. (2007) The transcriptional coactivator PGC-1β drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab. 5, 35-46
8. Puigserver, P., Rhee, J., Donovan, J., Walkey, C. J., Yoon, J. C., Oriente, F., Kitamura, Y., Altomonte, J., Dong, H., Accili, D., and Spiegelman, B. M. (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423, 550-555
9. Handschin, C., Rhee, J., Lin, J., Tarr, P. T., and Spiegelman, B. M. (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor γ coactivator 1α expression in muscle. Proc. Natl. Acad. Sci. U. S. A. 100, 7111-7116
10. Kamei, Y., Ohizumi, H., Fujitani, Y., Nemoto, T., Tanaka, T., Takahashi, N., Kawada, T., Miyoshi, M., Ezaki, O., and Kakizuka, A. (2003) PPARγ coactivator 1β/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc. Natl. Acad. Sci. U. S. A. 100, 12378-12383
11. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124
12. Wende, A. R., Schaeffer, P. J., Parker, G. J., Zechner, C., Han, D. H., Chen, M. M., Hancock, C. R., Lehman, J. J., Huss, J. M., McClain, D. A., Holloszy, J. O., and Kelly, D. P. (2007) A role for the transcriptional coactivator PGC-1α in muscle refueling. J. Biol. Chem. 282, 36642-36651
13. Michael, L. F., Wu, Z., Cheatham, R. B., Puigserver, P., Adelmant, G., Lehman, J. J., Kelly, D. P., and Spiegelman, B. M. (2001) Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. U. S. A. 98, 3820-3825
14. Benton, C. R., Nickerson, J. G., Lally, J., Han, X. X., Holloway, G. P., Glatz, J. F., Luiken, J. J., Graham, T. E., Heikkila, J. J., and Bonen, A. (2008) Modest PGC-1α overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J. Biol. Chem. 283, 4228-4240
15. Arany, Z., He, H., Lin, J., Hoyer, K., Handschin, C., Toka, O., Ahmad, F., Matsui, T., Chin, S., Wu, P. H., Rybkin, I., Shelton, J. M., Manieri, M., Cinti, S., Schoen, F. J., Bassel-Duby, R., Rosenzweig, A., Ingwall, J. S., and Spiegelman, B. M. (2005) Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle. Cell Metab. 1, 259-271
16. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St. Pierre, J., Zhang, C. Y., Mootha, V. K., Jager, S., Vianna, C. R., Reznick, R. M., Cui, L., Manieri, M., Donovan, M. X., Wu, Z., Cooper, M. P., Fan, M. C., Rohas, L. M., Zavacki, A. M., Cinti, S., Shulman, G. I., Lowell, B. B., Krainc, D., and Spiegelman, B. M. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119, 121-135
17. Leone, T. C., Lehman, J. J., Finck, B. N., Schaeffer, P. J., Wende, A. R., Boudina, S., Courtois, M., Wozniak, D. F., Sambandam, N., Bernal-Mizrachi, C., Chen, Z., Holloszy, J. O., Medeiros, D. M., Schmidt, R. E., Saffitz, J. E., Abel, E. D., Semenkovich, C. F., and Kelly, D. P. (2005) PGC-1α deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101
18. Handschin, C., Chin, S., Li, P., Liu, F., Maratos-Flier, E., Lebrasseur, N. K., Yan, Z., and Spiegelman, B. M. (2007) Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals. J. Biol. Chem. 282, 30014-30021
19. Handschin, C., Choi, C. S., Chin, S., Kim, S., Kawamori, D., Kurpad, A. J., Neubauer, N., Hu, J., Mootha, V. K., Kim, Y. B., Kulkarni, R. N., Shulman, G. I., and Spiegelman, B. M. (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1α knockout mice reveals skeletal muscle-pancreatic β cell crosstalk. J. Clin. Invest. 117, 3463-3474
20. Lelliott, C. J., Medina-Gomez, G., Petrovic, N., Kis, A., Feldmann, H. M., Bjursell, M., Parker, N., Curtis, K., Campbell, M., Hu, P., Zhang, D., Litwin, S. E., Zaha, V. G., Fountain, K. T., Boudina, S., Jimenez-Linan, M., Blount, M., Lopez, M., Meirhaeghe, A., Bohlooly, Y., Storlien, L., Stromstedt, M., Snaith, M., Oresic, M., Abel, E. D., Cannon, B., and Vidal-Puig, A. (2006) Ablation of PGC-1β results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 4, e369
21. Vianna, C. R., Huntgeburth, M., Coppari, R., Choi, C. S., Lin, J., Krauss, S., Barbatelli, G., Tzameli, I., Kim, Y. B., Cinti, S., Shulman, G. I., Spiegelman, B. M., and Lowell, B. B. (2006) Hypomorphic mutation of PGC-1β causes mitochondrial dysfunction and liver insulin resistance. Cell Metab. 4, 453-464
22. Sonoda, J., Mehl, I., Chong, L.-W., Nofsinger, R., and Evans, R. PGC-1β controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc. Natl. Acad. Sci. U. S. A. 104, 5223-5228
23. Patti, M. E., Butte, A. J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., Landaker, E. J., Goldfine, A. B., Mun, E., DeFronzo, R., Finlayson, J., Kahn, C. R., and Mandarino, L. J. (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. U. S. A. 100, 8466-8471
24. Mootha, V. K., Lindgren, C. M., Eriksson, K. F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E., Houstis, N., Daly, M. J., Patterson, N., Mesirov, J. P., Golub, T. R., Tamayo, P., Spiegelman, B., Lander, E. S., Hirschhorn, J. N., Altshuler, D., and Groop, L. C. (2003) PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273
25. Larrouy, D., Vidal, H., Andreelli, F., Laville, M., and Langin, D. (1999) Cloning and mRNA tissue distribution of human PPARγ coactivator-1. Int. J. Obes. Relat. Metab. Disord. 23, 1327-1332
26. Hammarstedt, A., Jansson, P. A., Wesslau, C., Yang, X., and Smith, U. (2003) Reduced expression of PGC-1 and insulin-signaling molecules in adipose tissue is associated with insulin resistance. Biochem. Biophys. Res. Commun. 301, 578-582
27. Semple, R. K., Crowley, V. C., Sewter, C. P., Laudes, M., Christodoulides, C., Considine, R. V., Vidal-Puig, A., and O'Rahilly, S. (2004) Expression of the thermogenic nuclear hormone receptor coactivator PGC-1α is reduced in the adipose tissue of morbidly obese subjects. Int. J. Obes. Relat. Metab. Disord. 28, 176-179
28. Crunkhorn, S., Dearie, F., Mantzoros, C., Gami, H., da Silva, W. S., Espinoza, D., Faucette, R., Barry, K., Bianco, A. C., and Patti, M. E. (2007) Peroxisome proliferator activator receptor γ coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 282, 15439-15450
29. Koves, T. R., Li, P., An, J., Akimoto, T., Slentz, D., Ilkayeva, O., Dohm, G. L., Yan, Z., Newgard, C. B., and Muoio, D. M. (2005) Peroxisome proliferator-activated receptor- co-activator 1α-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J. Biol. Chem. 280, 33588-33598
30. Sparks, L. M., Xie, H., Koza, R. A., Mynatt, R., Hulver, M. W., Bray, G. A., and Smith, S. R. (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54, 1926-1933
31. Richardson, D. K., Kashyap, S., Bajaj, M., Cusi, K., Mandarino, S. J., Finlayson, J., DeFronzo, R. A., Jenkinson, C. P., and Mandarino, L. J. (2004) Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases expression of extracellular matrix genes in human skeletal muscle. J. Biol. Chem. 280, 10290-10297
32. Kelley, D. E., He, J., Menshikova, E. V., and Ritov, V. B. (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950
33. Petersen, K. F., Dufour, S., Befroy, D., Garcia, R., and Shulman, G. I. (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350, 664-671
34. Tortorella, L. L., and Pilch, P. F. (2002) C2C12 myocytes lack an insulin-responsive vesicular compartment despite dexamethasone-induced GLUT4 expression. Am. J. Physiol. Endocrinol. Metab. 283, E514-E524
35. Folli, F., Saad, M. J. A., Backer, J. M., and Kahn, C. R. (1993) Regulation of phosphatidylinositol 3-kinase activity in liver and muscle of animal models of insulin-resistant and insulin-deficient diabetes mellitus. J. Clin. Invest. 92, 1787-1794 (Pubitemid 23304544)
36. Babson, A. L., Shapiro, P. O., and Phillips, G. E. (1962) A new assay for cholesterol and cholesterol esters in serum which is not affected by bilirubin. Clin. Chim. Acta 7, 800-804
37. Bodennec, J., Koul, O., Aguado, I., Brichon, G., Zwingelstein, G., and Portoukalian, J. (2000) A procedure for fractionation of sphingolipid classes by solid-phase extraction on aminopropyl cartridges. J. Lipid Res. 41, 1524-1531
38. Storey, J. D. (2002) A direct approach to false discovery rates. J. R. Stat. Soc. B 64, 479-498
39. Holland, W. L., Brozinick, J. T., Wang, L. P., Hawkins, E. D., Sargent, K. M., Liu, Y., Narra, K., Hoehn, K. L., Knotts, T. A., Siesky, A., Nelson, D. H., Karathanasis, S. K., Fontenot, G. K., Birnbaum, M. J., and Summers, S. A. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab. 5, 167-179
40. Adams, J. M., Pratipanawatr, T., Berria, R., Wang, E., DeFronzo, R. A., Sullards, M. C., and Mandarino, L. J. (2004) Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 53, 25-31
41. Pewzner-Jung, Y., Ben Dor, S., and Futerman, A. H. (2006) When do Lasses (longevity assurance genes) become CerS (ceramide synthases)? Insights into the regulation of ceramide synthesis. J. Biol. Chem. 281, 25001-25005
42. Simoneau, J. A., and Kelley, D. E. (1997) Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 83, 166-171
43. Kelley, D. E., and Mandarino, L. J. (2000) Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49, 677-683 (Pubitemid 30339979)
44. Dufour, C. R., Wilson, B. J., Huss, J. M., Kelly, D. P., Alaynick, W. A., Downes, M., Evans, R. M., Blanchette, M., and Giguere, V. (2007) Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRα and γ. Cell Metab. 5, 345-356
45. Schreiber, S. N., Knutti, D., Brogli, K., Uhlmann, T., and Kralli, A. (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
46. Montell, E., Turini, M., Marotta, M., Roberts, M., Noe, V., Ciudad, C. J., Mace, K., and Gomez-Foix, A. M. (2001) DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells. Am. J. Physiol. Endocrinol. Metab. 280, E229-E237
47. Itani, S. I., Ruderman, N. B., Schmieder, F., and Boden, G. (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IκB-α. Diabetes 51, 2005-2011 (Pubitemid 34729001)
48. Savage, D. B., Petersen, K. F., and Shulman, G. I. (2007) Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol. Rev. 87, 507-520
49. Jakobsson, A., Westerberg, R., and Jacobsson, A. (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45, 237-249
50. Haus, J. M., Kashyap, S. R., Kasumov, T., Zhang, R., Kelly, K. R., DeFronzo, R. A., and Kirwan, J. P. (2009) Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 58, 337-343
51. Yang, G., Badeanlou, L., Bielawski, J., Roberts, A. J., Hannun, Y. A., and Samad, F. (2009) Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am. J. Physiol. Endocrinol. Metab. 297, E211-E224
52. Crowder, C. M. (2009) Cell biology. Ceramides - friend or foe in hypoxia? Science 324, 343-344
53. Calvo, J. A., Daniels, T. G., Wang, X., Paul, A., Lin, J., Spiegelman, B. M., Stevenson, S. C., and Rangwala, S. M. (2008) Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 104, 1304-1312
54. Russell, A. P., Hesselink, M. K., Lo, S. K., and Schrauwen, P. (2005) Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 19, 986-988
55. Goodpaster, B. H., He, J., Watkins, S., and Kelley, D. E. (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 86, 5755-5561
56. Jacob, S., Machann, J., Rett, K., Brechtel, K., Volk, A., Renn, W., Maerker, E., Matthaei, S., Schick, F., Claussen, C. D., and Haring, H. U. (1999) Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 48, 1113-1119
57. Simoneau, J. A., and Kelley, D. E. (1997) Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 83, 166-171