Transcriptional coactivators PGC-lα and PGC-lβ control overlapping programs required for perinatal maturation of the heart

Genes and Development

Volumn 22, Issue 14, 2008, Pages 1948-1961

  Lai, Ling ^a   Leone, Teresa C ^a   Zechner, Christoph ^a   Schaeffer, Paul J ^a,b   Kelly, Sean M ^a   Flanagan, Daniel P ^a   Medeiros, Denis M ^c   Kovacs, Attila ^a   Kelly, Daniel P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MIAMI UNIVERSITY   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

Energy metabolism; Heart development; Mitochondria; Transcriptional regulation

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HEART BLOCK; HEART DEVELOPMENT; HEART FAILURE; HEART FUNCTION; HEART OUTPUT; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL DEVELOPMENT; PRIORITY JOURNAL;

ADIPOSE TISSUE, BROWN; ANIMALS; BLOTTING, SOUTHERN; FEMALE; GENE EXPRESSION PROFILING; HEART; INTEGRASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS;

MUS;

EID: 47549114849     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1661708     Document Type: Article

References (57)

1. Agah, R., Frenkel, P.A., French, B.A., Michael, L.H., Overbeek, P.A., and Schneider, M.D. 1997. Gene recombination in postmitotic cells. Targeted expression of cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest. 100: 169-179.
2. Alaynick, W.A., Kondo, R.P., Xie, W., He, W., Dufour, C.R., Downes, M., Jonker, J.W., Giles, W., Naviaux, R.K., Giguère, V., et al. 2007. ERRγ directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab. 6: 13-24.
3. Andersson, U. and Scarpulla, R.C. 2001. PGC-1-related coacti-vator, a novel, serum-inducible coactivator of nuclear respiratory factor-1-dependent transcription in mammalian cells. Mol. Cell. Biol. 21: 3738-3749.
4. Arany, Z., Novikov, M., Chin, S., Ma, Y., Rosenzweig, A., and Spiegelman, B.M. 2006. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPARγ coactivator 1α. Proc. Natl. Acad. Sci. 103: 10086-10091.
5. 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.
6. Bhattacharya, S.K., Thakar, J.H., Johnson, P.L., and Shanklin, D.R. 1991. Isolation of skeletal muscle mitochonria using an ionic medium containing ethylenediaminetetraacetic acid and nagarse. Anal. Biochem. 192: 344-349.
7. Bing, R.J. 1955. The metabolism of the heart. Harvey Lect. 50: 27-70.
8. Bligh, E.G. and Dyer, W.J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
9. Buroker, N.E., Ning, X.-H., and Portman, M. 2008. Cardiac PPARα protein expression is constant as alternate nuclear receptors and PGC-1 coordinately increase during the postnatal metabolic transition. PPAR Research 2008: 279531. doi: 10.1155/2008/279531.
10. Cresci, S., Wright, L.D., Spratt, J.A., Briggs, F.N., and Kelly, D.P. 1996. Activation of a novel metabolic gene regulatory pathway by chronic stimulation of skeletal muscle. Am. J. Physiol. 270: C1413-C1420.
11. 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 orphan nuclear receptors ERRα and γ. Cell Metabolism 5: 345-356.
12. 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.
13. Fisher, D.J., Heymann, M.A., and Rudolph, A.M. 1980. Myocardial oxygen and carbohydrate consumption in fetal lambs in utero and in adult sheep. Am. J. Phys. 238: H399-H405.
14. Fisher, D.J., Heymann, M.A., and Rudolph, A.M. 1981. Myocardial consumption of oxygen and carbohydrates in newborn sheep. Pediatr. Res. 15: 843-846.
15. Girard, J., Ferré, P., Pégorier, J.P., and Duée, P.H. 1992. Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiol. Rev. 72: 507-562.
16. Hallman, M. 1971. Changes in mitochondrial respiratory chain proteins during perinatal development. Evidence of the importance of environmental oxygen tension. Biochim. Bio-phys. Acta 253: 360-372.
17. Handschin, C. and Spiegelman, B.M. 2006. Peroxisome prolif-erator- activated receptor γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27: 728-735.
18. Herzig, S., Long, F., Jhala, U.S., Hedrick, S., Quinn, R., Bauer, A., Rudolph, D., Schutz, G., Yoon, C., Puigserver, P., et al. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183.
19. Huss, J.M., Kopp, R.P., and Kelly, D.P. 2002. PGC-1α coacti-vates the cardiac-enriched nuclear receptors estrogen-related receptor-α and -γ. J. Biol. Chem. 277: 40265-40274.
20. Huss, J.M., Pinéda Torra, I., Staels, B., Giguère, V., and Kelly, D.P. 2004. ERRα directs PPARa signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24: 9079-9091.
21. Itoi, T. and Lopaschuk, G.D. 1993. The contribution of glycolysis, glucose oxidation, lactate oxidation, and fatty acid oxidation to ATP production in isolated biventricular working hearts from 2-week-old rabbits. Pediatr. Res. 34: 735-741.
22. Kamei, Y., Ohizumi, H., Fujitani, Y., Nemoto, T., Tanaka, T., Takahashi, N., Kawada, T., Miyoshi, M., Ezaki, O., and Kakizuka, A. 2003. PPAR-γ coactivator 1β/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc. Natl. Acad. Sci. 100: 12378-12383.
23. Kelly, D.P. and Strauss, A.W. 1994. Inherited cardiomyopathies. N. Engl. J. Med. 330: 913-919.
24. Kelly, D.P., Gordon, J.I., Alpers, R., and Strauss, A.W. 1989. The tissue-specific expression and developmental regulation of the two nuclear genes encoding rat mitochondrial proteins: Medium-chain acyl-CoA dehydrogenase and mitochondrial malate dehydrogenase. J. Biol. Chem. 264: 18921-18925.
25. Koo, S.H., Satoh, H., Herzig, S., Lee, C.H., Hedrick, S., Kulkarni, R., Evans, R.M., Olefsky, J., andMontminy, M. 2004. PGC-1 promotes insulin resistance in liver through PPARα-depen-dent induction of TRB-3. Nat. Med. 10: 530-534.
26. Kressler, D., Schreiber, S.N., Knutti, D., and Kralli, A. 2002. The PGC-1-related protein PERC is a selective coactivator of estrogen receptor α. J. Biol. Chem. 277: 13918-13925.
27. Lehman, J.J. and Kelly, D.P. 2002. Transcriptional activation of energy metabolic switches in the developing and hypertro-phied heart. Clin. Exp. Pharmacol. Physiol. 29: 339-345.
28. Lehman, J.J., Barger, P.M., Kovacs, A., Saffitz, J.E., Medeiros, D., and Kelly, D.P. 2000. PPARγ coactivator-1 (PGC-1) promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106: 847-856.
29. Lelliott, C.J., Medina-Gomez, G., Petrovic, N., Kis, A., Feldmann, H.M., Bjursell, M., Parker, N., Curtis, K., Campbell, M., Hu, P., et al. 2006. Ablation of PGC-1β results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol. 4: 2042-2056.
30. 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, et al. 2005. PGC-1a deficient mice exhibit multi-system energy metabolic derangements: Muscle dysfunction, abnormal weight control, and hepatic steatosis. PLoS Biol. 3: 672-687.
31. Lin, J., Puigserver, P., Donovan, J., Tarr, P., and Spiegelman, B.M. 2002a. 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.
32. Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Puigserver, P., Isotanni, E., Olson, E.N., et al. 2002b. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibers. Nature 418: 797-801.
33. Lin, J., Wu, P.-H., Tarr, P.T., Lindenberg, K.S., St-Pierre, J., Zhang, C.-Y., Mootha, V.K., Jãger, S., Vianna, C.R., Reznick, R.M., et al. 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119: 121-135.
34. Lin, J., Yang, R., Tarr, P.T., Wu, P.-H., Handschin, C, Li, S., Yang, W., Pei, L., Uldry, M., Tontonoz, P., et al. 2005. Hyperlipidemic effects of dietary saturated fats mediated through PGC-1β coactivation of SREBP. Cell 120: 261-273.
35. 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.
36. 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. 98: 3820-3825.
37. Mortensen, O.H., Frandsen, L., Schjerling, P., Nishimura, E., and Grunnet, N. 2006. PGC-1α and PGC-1β have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am. J. Phys. Endocrinol. Metab. 4: E807-E816. doi: 10.1152/ajpendo.00591.2005.
38. Puigserver, P. and Spiegelman, B.M. 2003. Peroxisome proliferator- activated receptor-γ coactivator 1α (PGC-1α): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 24: 78-90.
39. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M., and Spiegelman, B.M. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839.
40. Puigserver, P., Adelmant, G., Wu, Z., Fan, M., Xu, J., O'Malley, B., and Spiegelman, B.M. 1999. Activation of PPAR-γ coactivator-1 through transcription factor docking. Science 286: 1368-1371.
41. Puigserver, P., Rhee, J., Donovan, J., Walkey, C.J., Yoon, J.C., Oriente, F., Kitamura, Y., Altomonte, J., Dong, H., Accili, D., et al. 2003. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423: 550-555.
42. Rogers, J.H., Tamirisa, P., Kovacs, A., Weinheimer, C., Courtois, M., Blumer, K.J., Kelly, D.P., and Muslin, A.J. 1999. RGS4 causes increased mortality and reduced cardiac hypertrophy in response to pressure overload. J. Clin. Invest. 104: 567-576.
43. Russell, L.K., Mansfield, CM., Lehman, J.J., Kovacs, A., Courtois, M., Saffitz, J.E., Medeiros, D.M., Valencik, M.L., McDonald, J.A., and Kelly, D.P. 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.
44. Sano, M., Tokudome, S., Shimizu, N., Yoshikawa, N., Ogawa, C., Shirakawa, K., Endo, J., Katayama, T., Yuasa, S., Ieda, M., et al. 2007. Intramolecular control of protein stability, sub-nuclear compartmentalization, and coactivator function of peroxisome proliferator-activated receptor γ coactivator 1α. J. Biol. Chem. 282: 25970-25980.
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. 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. Phys. 257:1-9.
47. 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. 104: 5223-5228.
48. St-Pierre, J., Lin, J., Krauss, S., Tarr, P.T., Yang, R., Newgard, C.B., and Spiegelman, B.M. 2003. Bioenergetic analysis of peroxisome proliferator-activated receptor γ coactivators 1α and 1β (PGC-1α and PGC-1β) in muscle cells. J. Biol. Chem. 278: 26597-26603.
49. Taha, M. and Lopaschuk, G.D. 2007. Alterations in energy metabolism in cardiomyopathies. Ann. Med. 39: 594-607.
50. Tei, C., Ling, L.H., Hodge, D.O., Bailey, K.R., Oh, J.K., Rodehef-fer, R.J., Tajik, A.J., and Seward, J.B. 1995. New index of combined systolic and diastolic myocardial performance: A simple and reproducible measure of cardiac function-a study in normals and dilated cardiomyopathy. J. Cardiol. 26: 357-366.
51. Uldry, M., Yang, W., St-Pierre, J., Lin, J., Seale, P., and Spiegel-man, B.M. 2006. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 3: 333-341.
52. Vega, R.B., Huss, J.M., and Kelly, D.P. 2000. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor a in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20: 1868-1876.
53. Vianna, C.R., Huntgeburth, M., Coppari, R., Choi, C.S., Lin, J., Krauss, S., Barbatelli, G., Tzameli, I., Kim, Y.B., Cinti, S., et al. 2006. Hypomorphic mutation of PGC-1β causes mitochondrial dysfunction and liver insulin resistance. Cell Metab. 4: 453-464.
54. Wallberg, A.E., Yamamura, S., Malik, S., Spiegelman, B.M., and Roeder, R.G. 2003. Coordination of p300-mediated chromatin remodeling and TRAP/mediator function through coactivator PGC-1α. Mol. Cell 12: 1137-1149.
55. 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., et al. 2007. A role for the transcriptional coactivator PGC-1α in muscle refueling. J. Biol. Chem. 282: 36642-36651.
56. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R.C., et al. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
57. Yoon, J.C., Puigserver, P., Chen, G., Donovan, J., Wu, Z., Rhee, J., Adelmant, G., Stafford, J., Kahn, C.R., Granner, D.K., et al. 2001. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413: 131-138.