MAPK phosphatase-1 facilitates the loss of oxidative myofibers associated with obesity in mice

Journal of Clinical Investigation

Volumn 119, Issue 12, 2009, Pages 3817-3829

  Roth, Rachel J ^a   Le, Annie M ^a   Zhang, Lei ^a   Kahn, Mario ^a   Samuel, Varman T ^a   Shulman, Gerald I ^a   Bennett, Anton M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; ENERGY EXPENDITURE; FAT INTAKE; GENE OVEREXPRESSION; HEALTH; LIPID DIET; MALE; METABOLIC SYNDROME X; MOUSE; MUSCLE CELL; MUSCLE TWITCH; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SKELETAL MUSCLE; STRESS; WILD TYPE;

ANIMALS; BASE SEQUENCE; DIETARY FATS; DNA PRIMERS; DUAL SPECIFICITY PHOSPHATASE 1; ENERGY METABOLISM; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUSCLE FIBERS, SLOW-TWITCH; OBESITY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RNA, MESSENGER; TRANS-ACTIVATORS; UP-REGULATION;

EID: 72849125839     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI39054     Document Type: Article

References (63)

1. Raman, M., Chen, W., and Cobb, M.H. 2007. Differential regulation and properties of MAPKs. Oncogene. 26:3100-3112.
2. Weston, C.R., and Davis, R.J. 2007. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19:142-149.
3. Cuenda, A., and Rousseau, S. 2007. p38 MAPKinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta. 1773:1358-1375. (Pubitemid 47125981)
4. Murphy, L.O., and Blenis, J. 2006. MAPK signal specificity: the right place at the right time. Trends Biochem. Sci. 31:268-275. (Pubitemid 43674354)
5. Weston, C.R., and Davis, R.J. 2007. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19:142-149.
6. Dickinson, R.J., and Keyse, S.M. 2006. Diverse physiological functions for dual-specificity MAP kinase phosphatases. J. Cell Sci. 119:4607-4615.
7. Boutros, T., Chevet, E., and Metrakos, P. 2008. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 60:261-310.
8. Karlsson, M., Mandl, M., and Keyse, S.M. 2006. Spatio- temporal regulation of mitogen-activated protein kinase (MAPK) signalling by protein phosphatases. Biochem. Soc. Trans. 34:842-845.
9. Cuevas, B.D., Abell, A.N., and Johnson, G.L. 2007. Role of mitogen-activated protein kinase kinase kinases in signal integration. Oncogene. 26:3159-3171. (Pubitemid 46763012)
10. Keyse, S.M. 2008. Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev. 27:253-261.
11. Jeffrey, K.L., Camps, M., Rommel, C., and Mackay, C.R. 2007. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 6:391-403.
12. Liu, Y., Shepherd, E.G., and Nelin, L.D. 2007. MAPK phosphatases [mdash] regulating the immune response. Nat. Rev. Immunol. 7:202-212.
13. Owens, D.M., and Keyse, S.M. 2007. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene. 26:3203-3213. (Pubitemid 46763015)
14. Wu, J.J., et al. 2006. Mice lacking MAP kinase phosphatase-1 have enhanced MAP kinase activity and resistance to diet-induced obesity. Cell Metab. 4:61-73.
15. Bassel-Duby, R., and Olson, E.N. 2006. Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 75:19-37.
16. Zierath, J.R., and Hawley, J.A. 2004. Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol. 2:e348.
17. Zurlo, F., Larson, K., Bogardus, C., and Ravussin, E. 1990. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J. Clin. Invest. 86:1423-1427.
18. He, J., Watkins, S., and Kelley, D.E. 2001. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes. 50:817-823. (Pubitemid 32242639)
19. Simoneau, J.A., Veerkamp, J.H., Turcotte, L.P., and Kelley, D.E. 1999. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J. 13:2051-2060.
20. Handschin, C., and Spiegelman, B.M. 2006. Peroxisome proliferator- activated receptor {gamma} coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27:728-735.
21. Handschin, C., and Spiegelman, B.M. 2008. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature. 454:463-469.
22. Lin, J., et al. 2002. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature. 418:797-801.
23. Handschin, C., et al. 2007. Skeletal muscle fibertype switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J. Biol. Chem. 282:30014-30021.
24. Mootha, V.K., et al. 2003. PGC-1[alpha]-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:267-273.
25. Patti, M.E., et al. 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.
26. Sparks, L.M., et al. 2005. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes. 54:1926-1933.
27. Crunkhorn, S., et al. 2007. Peroxisome proliferator activator receptor {gamma}çesity: potential pathogenic role of saturated fatty acids and p38 mitogena-ctivated protein kinase activation. J. Biol. Chem. 282:15439-15450.
28. Coll, T., et al. 2006. Palmitate-mediated downregulation of peroxisome proliferator-activated receptor- gamma coactivator 1alpha in skeletal muscle cells involves MEK1/2 and nuclear factor-kappaB activation. Diabetes. 55:2779-2787.
29. Puigserver, P., et al. 2001. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol. Cell. 8:971-982.
30. Akimoto, T., et al. 2005. Exercise stimulates Pgc-1{alpha} transcription in skeletal muscle through activation of the p38 MAPK pathway. J. Biol. Chem. 280:19587-19593.
31. Dorfman, K., et al. 1996. Disruption of the erp/mkp-1 gene does not affect mouse development: normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene. 13:925-931. (Pubitemid 26329078)
32. Kwak, S.P., and Dixon, J.E. 1995. Multiple dual specificity protein tyrosine phosphatases are expressed and regulated differentially in liver cell lines. J. Biol. Chem. 270:1156-1160.
33. Cao, H., et al. 2008. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell. 134:933-944.
34. Shi, H., et al. 2006. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116:3015-3025.
35. Fan, M., et al. 2004. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK. Genes Dev. 18:278-289.
36. Knutti, D., Kressler, D., and Kralli, A. 2001. Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a repressor. Proc. Natl. Acad. Sci. U. S. A. 98:9713-9718.
37. Wells, G.D., Noseworthy, M.D., Hamilton, J., Tarnopolski, M., and Tein, I. 2008. Skeletal muscle metabolic dysfunction in obesity and metabolic syndrome. Can. J. Neurol. Sci. 35:31-40.
38. Kelley, D.E., Goodpaster, B., Wing, R.R., and Simoneau, J.A. 1999. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am. J. Physiol. 277:E1130-E1141.
39. Kim, J.Y., Hickner, R.C., Cortright, R.L., Dohm, G.L., and Houmard, J.A. 2000. Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279:E1039-E1044.
40. Chi, H., et al. 2006. Dynamic regulation of proand anti-inf lammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103:2274-2279.
41. Garcia-Roves, P., et al. 2007. Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 104:10709-10713.
42. Turner, N., et al. 2007. Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes. 56:2085-2092. (Pubitemid 47195821)
43. Hancock, C.R., et al. 2008. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc. Natl. Acad. Sci. U. S. A. 105:7815-7820.
44. Bonnard, C., et al. 2008. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118:789-800.
45. Choi, C.S., et al. 2007. Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J. Clin. Invest. 117:1995-2003.
46. Cha, S.H., Rodgers, J.T., Puigserver, P., Chohnan, S., and Lane, M.D. 2006. Hypothalamic malonyl-CoA triggers mitochondrial biogenesis and oxidative gene expression in skeletal muscle: Role of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 103:15410-15415.
47. 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. U. S. A. 104:12017-12022.
48. Li, X., Monks, B., Ge, Q., and Birnbaum, M.J. 2007. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature. 447:1012-1016. (Pubitemid 46975750)
49. Gerhart-Hines, Z., et al. 2007. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J. 26:1913-1923. (Pubitemid 46624046)
50. Teyssier, C., Ma, H., Emter, R., Kralli, A., and Stallcup, M.R. 2005. Activation of nuclear receptor coactivator PGC-1alpha by arginine methylation. Genes Dev. 19:1466-1473. (Pubitemid 41003013)
51. Sano, M., et al. 2007. Intramolecular control of protein stability, subnuclear compartmentalization, and coactivator function of peroxisome proliferator- activated receptor {gamma} coactivator 1{alpha}. J. Biol. Chem. 282:25970-25980. (Pubitemid 47372787)
52. Choi, C.S., et al. 2008. Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc. Natl. Acad. Sci. U. S. A. 105:19926-19931.
53. Leone, T.C., et al. 2005. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 3:e101.
54. Benton, C.R., et al. 2008. Modest PGC-1alpha over-expression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J. Biol. Chem. 283:4228-4240.
55. Richardson, D.K., et al. 2005. Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J. Biol. Chem. 280:10290-10297.
56. Lin, J., et al. 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell. 119:121-135. (Pubitemid 39349325)
57. Handschin, C., et al. 2007. PGC-1{alpha} regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev. 21:770-783. (Pubitemid 46572357)
58. Jackson, K.A., Snyder, D.S., and Goodell, M.A. 2004. Skeletal muscle fiber-specific green autofluorescence: potential for stem cell engraftment artifacts. Stem Cells. 22:180-187.
59. Handschin, C., Rhee, J., Lin, J., Tarr, P.T., and Spiegelman, B.M. 2003. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc. Natl. Acad. Sci. U. S. A. 100:7111-7116.
60. Puigserver, P., et al. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 92:829-839. (Pubitemid 28155321)
61. Kwak, S.P., Hakes, D.J., Martell, K.J., and Dixon, J.E. 1994. Isolation and characterization of a human dual specificity protein-tyrosine phosphatase gene. J. Biol. Chem. 269:3596-3604.
62. Monsalve, M., et al. 2000. Direct coupling of transcription and mRNA processing through the thermogenic coactivator PGC-1. Mol. Cell. 6:307-316.
63. Neschen, S., et al. 2002. Contrasting effects of fish oil and safflower oil on hepatic peroxisomal and tissue lipid content. Am. J. Physiol. Endocrinol. Metab. 282:E395-E401.