CNTF reverses obesity-induced insulin resistance by activating skeletal muscle AMPK

Nature Medicine

Volumn 12, Issue 5, 2006, Pages 541-548

  Watt, Matthew J ^a   Dzamko, Nicolas ^b   Thomas, Walter G ^c   Rose John, Stefan ^d   Ernst, Matthias ^e   Carling, David ^f   Kemp, Bruce E ^b,g   Febbraio, Mark A ^a   Steinberg, Gregory R ^b  

^a RMIT UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^d UNIVERSITY OF KIEL   (Germany)

^e ROYAL MELBOURNE HOSPITAL   (Australia)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

^g CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVATION; FATTY ACID OXIDATION; FOOD INTAKE; GENE EXPRESSION REGULATION; GENETIC MODEL; GLUCOSE TOLERANCE; INSULIN RESISTANCE; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OBESITY; PRIORITY JOURNAL; SKELETAL MUSCLE; TREATMENT OUTCOME; WEIGHT REDUCTION;

ANIMALS; BODY WEIGHT; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; CYTOKINE RECEPTOR GP130; ENZYME ACTIVATION; FATTY ACIDS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INSULIN RESISTANCE; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; OBESITY; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTORS, CYTOKINE; RECEPTORS, INTERLEUKIN-6; RECEPTORS, OSM-LIF; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

ANIMALIA; RODENTIA;

EID: 33646570554     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm1383     Document Type: Article

References (49)

1. Lambert, P.D. et al. Ciliary neurotrophic factor activates leptin-like pathways and reduces body fat, without cachexia or rebound weight gain, even in leptin-resistant obesity. Proc. Natl. Acad. Sci. USA 98, 4652-4657 (2001).
2. Gloaguen, I. et al. Ciliary neurotrophic factor corrects obesity and diabetes associated with leptin deficiency and resistance. Proc. Natl. Acad. Sci. USA 94, 6456-6461 (1997).
3. Sleeman, M.W. et al. Ciliary neurotrophic factor improves diabetic parameters and hepatic steatosis and increases basal metabolic rate in db/db mice. Proc. Natl. Acad. Sci. USA 100, 14297-14302 (2003).
4. Kokoeva, M.V., Yin, H. & Flier, J.S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310, 679-683 (2005).
5. MacLennan, A.J. et at. Immunohistochemical localization of ciliary neurotrophic factor receptor alpha expression in the rat nervous system. J. Neurosci. 16, 621-630 (1996).
6. Lee, M.Y., Hofmann, H.D. & Kirsch, M. Expression of ciliary neurotrophic factor receptor-alpha messenger RNA in neonatal and adult rat brain: an in situ hybridization study. Neuroscience 77, 233-246 (1997).
7. Davis, S. et al. LIFR beta and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science 260, 1805-1808 (1993).
8. Boulton, T.G., Stahl, N. & Yancopoulos, G.D. Ciliary neurotrophic factor/leukemia inhibitory factor/interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J. Biol. Chem. 269, 11648-11655 (1994).
9. Ziotopoulou, M., Erani, D.M., Hileman, S.M., Bjorbaek, C. & Mantzoros, C.S. Unlike leptin, ciliary neurotrophic factor does not reverse the starvation-induced changes of serum corticosterone and hypothalamic neuropeptide levels but induces expression of hypothalamic inhibitors of leptin signaling. Diabetes 49, 1890-1896 (2000).
10. Cohen, P. et al. Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss. Science 297, 240-243 (2002).
11. Zurlo, F., Larson, K., Bogardus, C. & Ravussin, E. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J. Clin. Invest. 86, 1423-1427 (1990).
12. Bonen, A. et al. Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J. 18, 1144-1146 (2004).
13. Shulman, G.I. Cellular mechanisms of insulin resistance. J. Clin. Invest. 106, 171-176 (2000).
14. Minokoshi, Y. et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415, 339-343 (2002).
15. Kahn, B.B., Alquier, T., Carling, D. & Hardie, D.G. AMP-activated protein kinase: Ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15-25 (2005).
16. Halaas, J.L. et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269, 543-546 (1995).
17. Considine, R.V. et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N. Engl. J. Med. 334, 292-295 (1996).
18. Frederich, R.C. et al. Leptin and the regulation of body weight in mammals. Nat. Med. 1, 1311-1314 (1995).
19. Steinberg, G.R. et al. Endurance training partially reverses dietary-induced leptin resistance in rodent skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286, E57-E63 (2004).
20. Starr, R. et al. A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921 (1997).
21. Bjorbaek, C., Elmquist, J.K., Frantz, J.D., Shoelson, S.E. & Flier, J.S. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell 1, 619-625 (1998).
22. Howard, J.K. et al. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat. Med. 10, 734-738 (2004).
23. Mori, H. et al. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 10, 739-743 (2004).
24. Ernst, M. et al. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J. Exp. Med. 194, 189-203 (2001).
25. Woods, A. et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 13, 2004-2008 (2003).
26. Hawley, S. et al. Complexes between the LKB1 tumor suppressor, STRADalpha/beta and MO25alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J. Biol. 2, 28 (2003).
27. Schuster, B. et al. Signalling of human CNTF revisited: the interleukin-6 (IL-6) receptor can serve as an α-receptor for ciliary neurotrophic factor (CNTF). J. Biol. Chem. 278, 9528-9535 (2003).
28. Shibata, R. et al. Inhibition of STAT3 prevents neointima formation by inhibiting proliferation and promoting apoptosis of neointimal smooth muscle cells. Hum. Gene Ther. 14, 601-610 (2003).
29. Bluher, S. et al. Ciliary neurotrophic factorAx15 alters energy homeostasis, decreases body weight, and improves metabolic control in diet-induced obese and UCP1-DTA mice. Diabetes 53, 2787-2796 (2004).
30. Sinha, S., Perdomo, G., Brown, N.F. & O'Doherty, R.M. Fatty acid-induced insulin resistance in L6 myotubes is prevented by inhibition of activation and nuclear localization of nuclear factor κB. J. Biol. Chem. 279, 41294-41301 (2004).
31. Tartaglia, L. et al. Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263-1271 (1995).
32. Baumann, H. et al. The full-length leptin receptor has signaling capabilities of interleukin 6-type cytokine receptors. Proc. Natl. Acad. Sci. USA 93, 8374-8378 (1996).
33. Bates, S.H. et al. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 42, 856-860 (2003).
34. Tartaglia, L.A. The leptin receptor. J. Biol. Chem. 272, 6093-6096 (1997).
35. Bjorbaek, C., El-Haschimi, K., Frantz, J.D. & Flier, J.S. The role of SOCS-3 in leptin signaling and leptin resistance. J. Biol. Chem. 274, 30059-30065 (1999).
36. Steinberg, G.R., Bonen, A. & Dyck, D.J. Fatty acid oxidation and triacylglycerol hydrolysis are enhanced following chronic leptin treatment in rats. Am. J. Physiol. 282, E593-E600 (2002).
37. Steinberg, G.R. et al. Chronic leptin administration decreases fatty acid uptake and fatty acid transporters in rat skeletal muscle. J. Biol. Chem. 277, 8854-8860 (2002).
38. Nicholson, S.E. et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA 97, 6493-6498 (2000).
39. Kelly, M. et al. AMPK activity is diminished in tissues of IL-6 knockout mice: the effect of exercise. Biochem. Biophys. Res. Commun. 320, 449-454 (2004).
40. Muoio, D.M., Dohm, G.L., Fiedorek, F.T.J., Tapscott, E.B. & Coleman, R.A. Leptin directly alters lipid partitioning in skeletal muscle. Diabetes 46, 1360-1363 (1997).
41. Brozinick, J.T., Jr. & Birnbaum, M.J. Insulin, but not contraction, activates Akt/PKB in isolated rat skeletal muscle. J. Biol. Chem. 273, 14679-14682 (1998).
42. Watt, M.J. et al. Beta-adrenergic stimulation of skeletal muscle HSL can be overridden by AMPK signaling. FASEB J. 18, 1445-1446 (2004).
43. Blau, H.M. & Webster, C. Isolation and charcterization of human skeletal muscle cells. Proc. Natl. Acad. Sci. USA 78, 5623-5627 (1981).
44. Petersen, E.W. et al. Acute IL-6 treatment increases fatty acid turnover in elderly humans in vivo and in tissue culture in vitro. Am. J. Physiol. Endocrinol. Metab. 288, E155-E162 (2005).
45. Kallen, K.-J. et al. Receptor recognition sites of cytokines are organized as exchangeable modules. Transfer of the leukemia inhibitory factor receptor-binding site from ciliary neurotrophic factor to interleukin-6. J. Biol. Chem. 274, 11859-11867 (1999).
46. Chen, Z.P. et al. AMPK signaling in contracting human skeletal muscle: aceyl-CoA carboxylase and NO synthase phosphorylation. Am. J. Physiol. Endocrinol. Metab. 279, E1202-E1206 (2000).
47. Preiss, J. et al. Quantitative measurement of sn-1,2-diacylglycerols present in platelets, hepatocytes, and ras- and sis-transformed normal rat kidney cells. J. Biol. Chem. 261, 8597-8600 (1986).
48. Bergmeyer, H.U. Co-enzymes and related compounds, in Methods of Enzymatic Analysis 2nd edn Vol 5, Ch 3 (ed. Bergmeyer, H.U.) 1967-2200 (Academic Press Inc., New York, 1974).
49. Dudley, G., Tullson, P. & Terjung, R. Influence of mitochondrial content on the sensitivity of respiratory control. J. Biol. Chem. 262, 9109-9114 (1987).