A role for peroxisome proliferator-activated receptor γ coactivator 1 (PGC-1) in the regulation of cardiac mitochondrial phospholipid biosynthesis

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2250-2259

  Lai, Ling ^a   Wang, Miao ^a   Martin, Ola J ^a   Leone, Teresa C ^a   Vega, Rick B ^a   Han, Xianlin ^a   Kelly, Daniel P ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COACTIVATORS; GENETIC DEFECTS; MITOCHONDRIAL METABOLISM; MOUSE HEART; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; TRANSCRIPTIONAL REGULATOR;

BIOCHEMISTRY; CYTOLOGY; DEFECTS; MAMMALS; METABOLISM; PHOSPHOLIPIDS; PHYSIOLOGY;

BIOSYNTHESIS;

CARDIOLIPIN; CDP DIACYLGLYCEROL SYNTHASE 1; CHECKPOINT KINASE 2; ENZYME; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARTH SYNDROME; CDS1 GENE; CELL SIZE; CONTROLLED STUDY; ENZYME REGULATION; FEMALE; GENE; GENE ACTIVATION; GENE CONTROL; GENE OVEREXPRESSION; HEART; LIPIDOMICS; MALE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL VOLUME DENSITY; MOUSE; NEWBORN; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PHOSPHOLIPID SYNTHESIS REGULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION;

CARDIAC METABOLISM; CARDIOLIPIN; GENE REGULATION; HEART; LIPIDOMICS; MITOCHONDRIA; PHOSPHOLIPIDS; POLYUNSATURATED FATTY ACIDS; TRANSCRIPTIONAL COREGULATORS;

ANIMALS; BARTH SYNDROME; CELL LINE; DIACYLGLYCEROL CHOLINEPHOSPHOTRANSFERASE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; RECEPTORS, ESTROGEN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84893109080     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.523654     Document Type: Article

References (46)

1. Zambrano, F., Fleischer, S., and Fleischer, B. (1975) Lipid composition of the Golgi apparatus of rat kidney and liver in comparison with other subcellular organelles. Biochim. Biophys. Acta 380, 357-369
2. Bissler, J. J., Tsoras, M., Göring, H. H., Hug, P., Chuck, G., Tombragel, E., McGraw, C., Schlotman, J., Ralston, M. A., and Hug, G. (2002) Infantile dilated X-linked cardiomyopathy, G4.5 mutations, altered lipids, and ultrastructural malformations of mitochondria in heart, liver, and skeletal muscle. Lab. Invest. 82, 335-344
3. Hallman, M. (1971) Changes in mitochondrial respiratory chain proteins during perinatal development. Evidence of the importance of environmental oxygen tension. Biochim. Biophys. Acta 253, 360-372
4. Smolich, J. J., Walker, A. M., Campbell, G. R., and Adamson, T. M. (1989) Left and right ventricular myocardial morphometry in fetal, neonatal, and adult sheep. Am. J. Physiol. 257, H1-H9
5. Marin-Garcia, J., Ananthakrishnan, R., and Goldenthal, M. J. (2000) Heart mitochondrial DNA and enzyme changes during early human development. Mol. Cell. Biochem. 210, 47-52
6. Scarpulla, R. C., Vega, R. B., and Kelly, D. P. (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 23, 459-466
7. Lin, J., Handschin, C., and Spiegelman, B. M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370
8. Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., and Kelly, D. P. (2000) Peroxisome proliferator-activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106, 847-856
9. Lai, L., Leone, T. C., Zechner, C., Schaeffer, P. J., Kelly, S. M., Flanagan, D. P., Medeiros, D. M., Kovacs, A., and Kelly, D. P. (2008) Transcriptional coactivators PGC-1α; and PGC-lβ control overlapping programs required for perinatal maturation of the heart. Genes Dev. 22, 1948-1961
10. 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
11. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C. Y., Mootha, V. K., Jäger, 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
12. 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, M., Storlien, L., Strömstedt, 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
13. Sonoda, J., Mehl, I. R., Chong, L. W., Nofsinger, R. R., and Evans, R. M. (2007) PGC-1β controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc. Natl. Acad. Sci. U.S.A. 104, 5223-5228
14. Soriano, F. X., Liesa, M., Bach, D., Chan, D. C., Palacín, M., and Zorzano, A. (2006) Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-γ coactivator-1α, estrogenrelated receptor-α, and mitofusin 2. Diabetes 55, 1783-1791
15. Sihag, S., Cresci, S., Li, A. Y., Sucharov, C. C., and Lehman, J. J. (2009) PGC-1α and ERRα target gene downregulation is a signature of the failing human heart. J. Mol. Cell. Cardiol. 46, 201-212
16. 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
17. Christie, W. W., and Han, X. (2010) Lipid Analysis: Isolation, Separation, Identification and Lipidomic Analysis, 4th Ed., pp. 55-66. The Oily Press, Bridgewater, UK
18. Han, X., Yang, K., and Gross, R. W. (2008) Microfluidics-based electrospray ionization enhances the intrasource separation of lipid classes and extends identification of individual molecular species through multi-dimensional mass spectrometry: development of an automated highthroughput platform for shotgun lipidomics. Rapid Commun. Mass Spectrom. 22, 2115-2124
19. Yang, K., Cheng, H., Gross, R. W., and Han, X. (2009) Automated lipid identification and quantification by multidimensional mass spectrometry-based shotgun lipidomics. Anal. Chem. 81, 4356-4368
20. Han, X., Yang, K., Yang, J., Cheng, H., and Gross, R. W. (2006) Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples. J. Lipid Res. 47, 864-879
21. Yang, K., and Han, X. (2011) Accurate quantification of lipid species by electrospray ionization mass spectrometry-Meet a key challenge in lipidomics. Metabolites 1, 21-40
22. Wang, M., Fang, H., and Han, X. (2012) Shotgun lipidomics analysis of 4-hydroxyalkenal species directly from lipid extracts after one-step in situ derivatization. Anal. Chem. 84, 4580-4586
23. Koo, S. H., Satoh, H., Herzig, S., Lee, C. H., Hedrick, S., Kulkarni, R., Evans, R. M., Olefsky, J., and Montminy, M. (2004) PGC-1 promotes insulin resistance in liver through PPAR-α-dependent induction of TRB-3. Nat. Med. 10, 530-534
24. 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
25. Huss, J. M., Torra, I. P., Staels, B., Giguère, V., and Kelly, D. P. (2004) Estrogen-related receptor α directs peroxisome proliferator-activated receptor α signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24, 9079-9091
26. 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
27. Huss, J. M., Kopp, R. P., and Kelly, D. P. (2002) Peroxisome proliferatoractivated receptor coactivator-1α (PGC-1α) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-α and-γ. Identification of novel leucine-rich interaction motif within PGC-1α. J. Biol. Chem. 277, 40265-40274
28. Lin, J., Puigserver, P., Donovan, J., Tarr, P., and Spiegelman, B. M. (2002) Peroxisome proliferator-activated receptor γ coactivator 1β (PGC-1β), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648
29. Wende, A. R., Huss, J. M., Schaeffer, P. J., Giguère, V., and Kelly, D. P. (2005) PGC-1α coactivates PDK4 gene expression via the orphan nuclear receptor ERRα: a mechanism for transcriptional control of muscle glucose metabolism. Mol. Cell. Biol. 25, 10684-10694
30. Yang, J., Williams, R. S., and Kelly, D. P. (2009) Bcl3 interacts cooperatively with peroxisome proliferator-activated receptor γ (PPARγ) coactivator 1α to coactivate nuclear receptors estrogen-related receptor α and PPARα. Mol. Cell. Biol. 29, 4091-4102
31. Schlame, M., Rua, D., and Greenberg, M. L. (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39, 257-288
32. van Werkhoven, M. A., Thorburn, D. R., Gedeon, A. K., and Pitt, J. J. (2006) Monolysocardiolipin in cultured fibroblasts is a sensitive and specific marker for Barth syndrome. J. Lipid Res. 47, 2346-2351
33. Houtkooper, R. H., Rodenburg, R. J., Thiels, C., van Lenthe, H., Stet, F., Poll-The, B. T., Stone, J. E., Steward, C. G., Wanders, R. J., Smeitink, J., Kulik, W., and Vaz, F. M. (2009) Cardiolipin and monolysocardiolipin analysis in fibroblasts, lymphocytes, and tissues using high-performance liquid chromatography-mass spectrometry as a diagnostic test for Barth syndrome. Anal. Biochem. 387, 230-237
34. Han, X., Yang, K., and Gross, R. W. (2012) Multi-dimensional mass spectrometry-based shotgun lipidomics and novel strategies for lipidomic analyses. Mass Spectrom. Rev. 31, 134-178
35. Sun, D., and Gilboe, D. D. (1994) Effect of the platelet-activating factor antagonist BN 50739 and its diluents on mitochondrial respiration and membrane lipids during and following cerebral ischemia. J. Neurochem. 62, 1929-1938
36. Lu, Z., Xu, X., Hu, X., Fassett, J., Zhu, G., Tao, Y., Li, J., Huang, Y., Zhang, P., Zhao, B., and Chen, Y. (2010) PGC-1α regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid. Redox Signal. 13, 1011-1022
37. Dufour, C. R., Wilson, B. J., Huss, J. M., Kelly, D. P., Alaynick, W. A., Downes, M., Evans, R. M., Blanchette, M., and Giguère, V. (2007) Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRα and γ. Cell Metab. 5, 345-356
38. Huss, J. M., and Kelly, D. P. (2004) Nuclear receptor signaling and cardiac energetics. Circ. Res. 95, 568-578
39. Finck, B. N., and Kelly, D. P. (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116, 615-622
40. Tamura, Y., Harada, Y., Nishikawa, S., Yamano, K., Kamiya, M., Shiota, T., Kuroda, T., Kuge, O., Sesaki, H., Imai, K., Tomii, K., and Endo, T. (2013) Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab. 17, 709-718
41. Ovide-Bordeaux, S., Bescond-Jacquet, A., and Grynberg, A. (2005) Cardiac mitochondrial alterations induced by insulin deficiency and hyperinsulinaemia in rats: targeting membrane homeostasis with trimetazidine. Clin. Exp. Pharmacol. Physiol. 32, 1061-1070
42. Infante, J. P., and Huszagh, V. A. (1997) On the molecular etiology of decreased arachidonic (20:4n-6), docosapentaenoic (22:5n-6), and docosahexaenoic (22:6n-3) acids in Zellweger syndrome and other peroxisomal disorders. Mol. Cell. Biochem. 168, 101-115
43. Infante, J. P., and Huszagh, V. A. (2001) Impaired arachidonic (20:4n-6) and docosahexaenoic (22:6n-3) acid synthesis by phenylalanine metabolites as etiological factors in the neuropathology of phenylketonuria. Mol. Genet. Metab. 72, 185-198
44. Harding, C. O., Gillingham, M. B., van Calcar, S. C., Wolff, J. A., Verhoeve, J. N., and Mills, M. D. (1999) Docosahexaenoic acid and retinal function in children with long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency. J. Inherit. Metab. Dis. 22, 276-280
45. Gillingham, M., Van Calcar, S., Ney, D., Wolff, J., and Harding, C. (1999) Dietary management of long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency (LCHADD).Acase report and survey. J. Inherit. Metab. Dis. 22, 123-131
46. Sparagna, G. C., Chicco, A. J., Murphy, R. C., Bristow, M. R., Johnson, C. A., Rees, M. L., Maxey, M. L., McCune, S. A., and Moore, R. L. (2007) Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J. Lipid Res. 48, 1559-1570