Extracellular growth factors and mitogens cooperate to drive mitochondrial biogenesis

Journal of Cell Science

Volumn 122, Issue 24, 2009, Pages 4516-4525

  Echave, Pedro ^a   Machado da Silva, Gisela ^a   Arkell, Rebecca S ^a   Duchen, Michael R ^a   Jacobson, Jake ^a   Mitter, Richard ^b   Lloyd, Alison C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

ERK; ERR ; Growth; Mitochondria; PI3K

Indexed keywords

APHIDICOLIN; CYTOCHROME C; DNA DIRECTED DNA POLYMERASE ALPHA; ESTROGEN RELATED RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; NEU DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROHIBITIN; RAS PROTEIN; SOMATOMEDIN C;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DENSITY; CELL GROWTH; CELL PROLIFERATION; CELL VOLUME; CONTROLLED STUDY; DNA REPLICATION; GENE ACTIVATION; GENE EXPRESSION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SCHWANN CELL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INSULIN-LIKE GROWTH FACTOR I; MITOCHONDRIA; MITOGENS; NEUREGULINS; RATS; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 71449126926     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.049734     Document Type: Article

References (61)

1. Alaynick, W. A., Kondo, R. P., Xie, W., He, W., Dufour, C. R., Downes, M., Jonker, J. W., Giles, W., Naviaux, R. K., Giguere, V. et al. (2007). ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab. 6, 13-24.
2. Ariazi, E. A., Kraus, R. J., Farrell, M. L., Jordan, V. C. and Mertz, J. E. (2007). Estrogen-related receptor alpha1 transcriptional activities are regulated in part via the ErbB2/HER2 signaling pathway. Mol. Cancer Res. 5, 71-85.
3. Bhaskar, P. T. and Hay, N. (2007). The two TORCs and Akt. Dev. Cell 12, 487-502.
4. Bonawitz, N. D., Chatenay-Lapointe, M., Pan, Y. and Shadel, G. S. (2007). Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 5, 265-277.
5. Canto, C., Pich, S., Paz, J. C., Sanches, R., Martinez, V., Orpinell, M., Palacin, M., Zorzano, A. and Guma, A. (2007). Neuregulins increase mitochondrial oxidative capacity and insulin sensitivity in skeletal muscle cells. Diabetes 56, 2185-2193.
6. Carrier, J. C., Deblois, G., Champigny, C., Levy, E. and Giguere, V. (2004). Estrogen-related receptor alpha (ERRalpha) is a transcriptional regulator of apolipoprotein A-IV and controls lipid handling in the intestine. J. Biol. Chem. 279, 52052-52058.
7. Casley, C. S., Land, J. M., Sharpe, M. A., Clark, J. B., Duchen, M. R. and Canevari, L. (2002). Beta-amyloid fragment 25-35 causes mitochondrial dysfunction in primary cortical neurons. Neurobiol. Dis. 10, 258-267.
8. Conlon, I. and Raff, M. (2003). Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J. Biol. 2, 7.
9. Conlon, I. J., Dunn, G. A., Mudge, A. W. and Raff, M. C. (2001). Extracellular control of cell size. Nat. Cell Biol. 3, 918-921.
10. Cunningham, J. T., Rodgers, J. T., Arlow, D. H., Vazquez, F., Mootha, V. K. and Puigserver, P. (2007). mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450, 736-740.
11. Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105.
12. Davis, P. D., Elliott, L. H., Harris, W., Hill, C. H., Hurst, S. A., Keech, E., Kumar, M. K., Lawton, G., Nixon, J. S. and Wilkinson, S. E. (1992). Inhibitors of protein kinase C. 2. Substituted bisindolylmaleimides with improved potency and selectivity. J. Med. Chem. 35, 994-1001.
13. DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G. and Thompson, C. B. (2008). The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7, 11-20.
14. Disatnik, M. H., Boutet, S. C., Lee, C. H., Mochly-Rosen, D. and Rando, T. A. (2002). Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: a role for MARCKS in an integrin signaling pathway. J. Cell Sci. 115, 2151-2163.
15. 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 ERRalpha and gamma. Cell Metab. 5, 345-356.
16. Echave, P., Conlon, I. J. and Lloyd, A. C. (2007). Cell size regulation in mammalian cells. Cell Cycle 6, 218-224.
17. Falcon, S. and Gentleman, R. (2007). Using GOstats to test gene lists for GO term association. Bioinformatics 23, 257-258.
18. 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.
19. Fromm, L. and Burden, S. J. (2001). Neuregulin-1-stimulated phosphorylation of GABP in skeletal muscle cells. Biochemistry 40, 5306-5312.
20. Gallant, C., You, J. Y., Sasaki, Y., Grabarek, Z. and Morgan, K. G. (2005). MARCKS is a major PKC-dependent regulator of calmodulin targeting in smooth muscle. J. Cell Sci. 118, 3595-3605.
21. Giraud, M. N., Fluck, M., Zuppinger, C. and Suter, T. M. (2005). Expressional reprogramming of survival pathways in rat cardiocytes by neuregulin-1beta. J. Appl. Physiol. 99, 313-322.
22. Gogvadze, V., Orrenius, S. and Zhivotovsky, B. (2008). Mitochondria in cancer cells: what is so special about them? Trends Cell Biol. 18, 165-173.
23. Guarente, L. (2008). Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 132, 171-176.
24. 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-1alpha muscle-specific knock-out animals. J. Biol. Chem. 282, 30014-30021.
25. Herzog, B., Cardenas, J., Hall, R. K., Villena, J. A., Budge, P. J., Giguere, V., Granner, D. K. and Kralli, A. (2006). Estrogen-related receptor alpha is a repressor of phosphoenolpyruvate carboxykinase gene transcription. J. Biol. Chem. 281, 99-106.
26. Hood, D. A. (2001). Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 90, 1137-1157.
27. Huss, J. M., Kopp, R. P. and Kelly, D. P. (2002). Peroxisome proliferator-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-alpha and -gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J. Biol. Chem. 277, 40265-40274.
28. Huss, J. M., Torra, I. P., Staels, B., Giguere, V. and Kelly, D. P. (2004). Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24, 9079-9091.
29. Huss, J. M., Imahashi, K., Dufour, C. R., Weinheimer, C. J., Courtois, M., Kovacs, A., Giguere, V., Murphy, E. and Kelly, D. P. (2007). The nuclear receptor ERRalpha is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab. 6, 25-37.
30. Jager, S., Handschin, C., St-Pierre, J. and Spiegelman, B. M. (2007). AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. USA 104, 12017-12022.
31. Kai, Y., Takamatsu, C., Tokuda, K., Okamoto, M., Irita, K. and Takahashi, S. (2006). Rapid and random turnover of mitochondrial DNA in rat hepatocytes of primary culture. Mitochondrion 6, 299-304.
32. Kelly, D. P. and Scarpulla, R. C. (2004). Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368.
33. Klionsky, D. J. and Emr, S. D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
34. Kohn, A. D., Barthel, A., Kovacina, K. S., Boge, A., Wallach, B., Summers, S. A., Birnbaum, M. J., Scott, P. H., Lawrence, J. C., Jr and Roth, R. A. (1998). Construction and characterization of a conditionally active version of the serine/threonine kinase Akt. J. Biol. Chem. 273, 11937-11943.
35. Lin, J., Handschin, C. and Spiegelman, B. M. (2005). Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370.
36. Lloyd, A. C., Obermuller, F., Staddon, S., Barth, C. F., McMahon, M. and Land, H. (1997). Cooperating oncogenes converge to regulate cyclin/cdk complexes. Genes Dev. 11, 663-677.
37. Luo, J., Sladek, R., Carrier, J., Bader, J. A., Richard, D. and Giguere, V. (2003). Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol. Cell. Biol. 23, 7947-7956.
38. Mathon, N. F., Malcolm, D. S., Harrisingh, M. C., Cheng, L. and Lloyd, A. C. (2001). Lack of replicative senescence in normal rodent glia. Science 291, 872-875.
39. Meirhaeghe, A., Crowley, V., Lenaghan, C., Lelliott, C., Green, K., Stewart, A., Hart, K., Schinner, S., Sethi, J. K., Yeo, G. et al. (2003). Characterization of the human, mouse and rat PGC1 beta (peroxisome-proliferator-activated receptor-gamma coactivator 1 beta) gene in vitro and in vivo. Biochem. J. 373, 155-165.
40. Merkwirth, C. and Langer, T. (2009). Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta 1793, 27-32.
41. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., St Pierre, J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N. et al. (2004). Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. USA 101, 6570-6575.
42. Moraes, C. T. (2001). What regulates mitochondrial DNA copy number in animal cells? Trends Genet. 17, 199-205.
43. Nicholls, D., Cunningham, S. and Wiesinger, H. (1986). Mechanisms of thermogenesis in brown adipose tissue. Biochem. Soc. Trans. 14, 223-225.
44. Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S. et al. (2003). Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299, 896-899.
45. O'Neill, B. T., Kim, J., Wende, A. R., Theobald, H. A., Tuinei, J., Buchanan, J., Guo, A., Zaha, V. G., Davis, D. K., Schell, J. C. et al. (2007). A conserved role for phosphatidylinositol 3-kinase but not Akt signaling in mitochondrial adaptations that accompany physiological cardiac hypertrophy. Cell Metab. 6, 294-306.
46. Puigserver, P. and Spiegelman, B. M. (2003). Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90.
47. 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.
48. Rozen, S. and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
49. Rush, J. S., Sweitzer, T., Kent, C., Decker, G. L. and Waechter, C. J. (1991). Biogenesis of the endoplasmic reticulum in activated B lymphocytes: temporal relationships between the induction of protein N-glycosylation activity and the biosynthesis of membrane protein and phospholipid. Arch. Biochem. Biophys. 284, 63-70.
50. Sarbassov, D. D., Ali, S. M. and Sabatini, D. M. (2005). Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603.
51. Scarpulla, R. C. (2006). Nuclear control of respiratory gene expression in mammalian cells. J. Cell Biochem. 97, 673-683.
52. Scarpulla, R. C. (2008). Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 88, 611-638.
53. Schieke, S. M., Phillips, D., McCoy, J. P., Jr., Aponte, A. M., Shen, R. F., Balaban, R. S. and Finkel, T. (2006). The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281, 27643-27652.
54. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225.
55. 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 alpha (ERRalpha). J. Biol. Chem. 278, 9013-9018.
56. Schreiber, S. N., Emter, R., Hock, M. B., Knutti, D., Cardenas, J., Podvinec, M., Oakeley, E. J. and Kralli, A. (2004). The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. USA 101, 6472-6477.
57. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
58. Vercauteren, K., Pasko, R. A., Gleyzer, N., Marino, V. M. and Scarpulla, R. C. (2006). PGC-1-related coactivator: immediate early expression and characterization of a CREB/NRF-1 binding domain associated with cytochrome c promoter occupancy and respiratory growth. Mol. Cell. Biol. 26, 7409-7419.
59. Villena, J. A., Hock, M. B., Chang, W. Y., Barcas, J. E., Giguere, V. and Kralli, A. (2007). Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc. Natl. Acad. Sci. USA 104, 1418-1423.
60. Wallace, D. C. (2005). A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407.
61. 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.