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Metabolic and hormonal interactions between muscle and adipose tissue

Published online by Cambridge University Press:  05 March 2007

Eva Tomas
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
Meghan Kelly
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
Xiaoqin Xiang
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
Tsu-Shuen Tsao
Affiliation:
Whitehead Institute for Biomedical Research, Boston, MA, USA
Charlotte Keller
Affiliation:
The Copenhagen Muscle Research Center, University of Copenhagen, Copenhagen, Denmark
Pernille Keller
Affiliation:
The Copenhagen Muscle Research Center, University of Copenhagen, Copenhagen, Denmark
Zhijun Luo
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
Harvey Lodish
Affiliation:
Whitehead Institute for Biomedical Research, Boston, MA, USA Massachusetts Institute of Technology, Boston, MA, USA
Asish K. Saha
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
Roger Unger
Affiliation:
University of Texas Southwestern Medical Center and Veterans Affairs Medical Center, Dallas, TX, USA
Neil B. Ruderman*
Affiliation:
Department of Medicine, Physiology and Biophysics and Diabetes Unit, Boston University Medical Center, Boston MA, USA
*
*Corresponding author: Professor N. B. Ruderman, fax +1 617 6387094, email nruderman@medicine.bu.edu
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Abstract

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From the perspective of a muscle physiologist, adipose tissue has long been perceived predominantly as a fuel reservoir that provides muscle and other tissues with NEFA when exogenous nutrients are insufficient for their energy needs. Recently, studies have established that adipose tissue is also an endocrine organ. Among the hormones it releases are adiponectin and leptin, both of which can activate AMP-activated protein kinase and increase fatty acid oxidation in skeletal muscle and probably other tissues. Deficiencies of leptin or leptin receptor, adiponectin and IL-6 are associated with obesity, insulin resistance and a propensity to type 2 diabetes. In addition, a lack of adiponectin has been linked to atherosclerosis. Whether this pathology reflects a deficient activation of AMP-activated protein kinase in peripheral tissues remains to be determined. Finally, recent studies have suggested that skeletal muscle may also function as an endocrine organ when it releases the cytokine IL-6 into the circulation during sustained exercise. Interestingly, one of the apparent effects of IL-6 is to stimulate lipolysis, causing the release of NEFA from the adipocyte. Thus, hormonal communications exist between the adipocyte and muscle that could enable them to talk to each other. The physiological relevance of this cross talk clearly warrants further study.

Type
Symposium 6: Adipose tissue–liver–muscle interactions leading to insulin resistance
Copyright
Copyright © The Nutrition Society 2004

References

Arita, Y, Kihara, S, Ouchi, N, Takahashi, M, Meada, K, Miyagawa, J, Hotta, K, Shimomura, I, Nakamura, I & Miyaoka, K (1999) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochemical and Biophysical Research Communications 257, 7983.CrossRefGoogle ScholarPubMed
Arner, P (2003) The adipocyte in insulin resistance: key molecules and the impact of the thiazolidinediones. Trends in Endocrinology and Metabolism 14, 137145.CrossRefGoogle ScholarPubMed
Berg, A, Combs, TP, Du, X, Brownlee, M & Scherer, PE (2001) The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nature Medicine 7, 947952.Google Scholar
Berg, AH, Combs, TP & Scherer, E (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends in Endocrinology and Metabolism 13, 8489.Google Scholar
Fruebis, J, Tsao, T-S, Javorschi, S, Ebbets-Reed, D, Erickson, MR, Yen, FT, Bihain, BE & Lodish, H (2001) Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proceedings of the National Academy of Sciences USA 4, 20052010.CrossRefGoogle Scholar
Gong, D, Yang, R, Munir, KM, Horenstein, RB & Shuldiner, AR (2003) New progress in adipocytokine research. Current Opinion in Endocrinology and Diabetes 10, 115121.CrossRefGoogle Scholar
Halaas, JL, Gajiwala, KS, Maffei, M, Cohen, SL, Chait, BT, Rabinowitz, D, Lallone, RL, Burley, SK & Friedman, JM (1995) Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269, 543546.Google Scholar
Hotta, K, Funahashi, T, Arita, Y, Takahashi, M, Matsuda, M, Okamoto, Y, Iwahashi, H, Kuriyama, H, Ouchi, N & Maeda, K (2000) Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arteriosclerosis, Thrombosis and Vascular Biology 20, 15951599.Google Scholar
Hu, E, Liang, P & Spiegelman, BM (1996) AdipoQ is a novel adipose-specific gene dysregulated in obesity. Journal of Biological Chemistry 18, 1069710703.Google Scholar
Keller, C, Steensberg, A, Pilegaard, H, Osada, T, Saltin, B, Pedersen, BK & Neufer, PD (2001) Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB Journal 15, 27482750.CrossRefGoogle ScholarPubMed
Lee, Y, Hirose, H, Ohneda, M, Johnson, JH, McGarry, JD & Unger, RH (1994) Beta-cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus: impairment in adipocyte-beta cell relationships. Proceedings of the National Academy of Sciences USA 91, 1087810882.Google Scholar
Maeda, N, Shimomurs, I, Kishida, K, Nishizawa, H, Matsuda, M, Nagaretani, H, et al. (2002) Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nature Medicine 7, 731737.CrossRefGoogle Scholar
Minokoshi, Y, Kim, YB, Peroni, OD, Fryer, LG, Muller, C, Carling, D & Kahn, BB (2002) Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415, 339343.CrossRefGoogle ScholarPubMed
Muoio, DM, Seefeld, K, Witters, LA & Coleman, RA (1999) AMP-activated kinase reciprocally regulates triacylglycerol synthesis and fatty acid oxidation in liver and muscle: evidence that sn-glycerol-3-phosphate acyltransferase is a novel target. Biochemical Journal 338, 783791.Google Scholar
Okamoto, Y, Kihara, S, Ouchi, N, Nishida, M, Arita, Y, Kumada, M, et al. (2002) Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 106, 27672770.CrossRefGoogle ScholarPubMed
Park, H, Kaushik, VK, Constant, S, Prentki, M, Przybytkowski, E, Ruderman, NB & Saha, AK (2002) Coordinate regulation of malonyl-CoA decarboxylase, sn-glycerol-3-phosphate acyltransferase, and acetyl-CoA carboxylase by AMP-activated kinase in rat tissues in response to exercise. Journal of Biological Chemistry 277, 3257132577.Google Scholar
Scherer, PE, Suzanne, W, Fogliano, M, Baldini, G & Lodish, HF (1995) A novel serum protein similar to C1q, produced exclusively in adipocytes. Journal of Biological Chemistry 45, 2674626749.CrossRefGoogle Scholar
Spiegelman, BM & Flier, JS (2001) Obesity and the regulation of energy balance. Cell 104, 531543.CrossRefGoogle ScholarPubMed
Starkie, R, Ostrowski, SR, Jauffred, S, Febbraio, M & Pedersen, BK (2003) Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB Journal 8, 884886.Google Scholar
Steensberg, A, Keller, C, Starkie, RL, Osada, T, Febbraio, MA & Pedersen, BK (2002) IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. American Journal of Physiology 283, E1272E1278.Google ScholarPubMed
Steensberg, A, Van Hall, G, Osada, T, Sacchetti, M, Saltin, B & Pedersen, KB (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. Journal of Physiology (London) 529, 237242.CrossRefGoogle ScholarPubMed
Tomas, E, Tsao, T-S, Saha, AK, Murrey, HE, Zhang, CC, Itani, SI, Lodish, HF & Ruderman, NB (2002) Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: Acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proceedings of the National Academy of Sciences USA 99, 1630916313.Google Scholar
Tsao, TS, Murrey, HE, Hug, C, Lee, DH & Lodish, HF (2002) Oligomerization state-dependent activation of NF-kappa B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). Journal of Biological Chemistry 277, 2935929362.CrossRefGoogle ScholarPubMed
Van Hall, G, Steensberg, A, Sacchetti, M, Fischer, C, Keller, C, Schjerling, P, Hiscock, N, Moller, K, Saltin, B, Febbraio, MA & Pedersen, BK (2003) Interleukin-6 stimulates lipolysis and fat oxidation in humans. Journal of Clinical Endocrinology and Metabolism 88, 30053010.CrossRefGoogle ScholarPubMed
Wallenius, V, Wallenius, K, Ahren, B, Rudling, M, Carlsten, H, Dickson, SL, Ohlsson, C & Jansson, JO (2002) Interleukin-6 deficient mice develop mature-onset obesity. Nature Medicine 1, 7579.CrossRefGoogle Scholar
Wu, X, Motoshina, H, Mahadev, K, Stalker, TJ, Scalia, R & Goldstein, BJ (2003) Involvement of AMP-activated protein kinase in glucose stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 52, 13551363.Google Scholar
Yamauchi, T, Kamon, J, Minokoshi, Y, Ito, Y, Tsuchida, A, Yokomizo, T, et al. (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature Medicine 423, 762768.Google Scholar
Yamauchi, T, Kamon, J, Minokoshi, Y, Ito, Y, Waki, H, Uchida, S, et al. (2002) Adiponectin stimulated glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nature Medicine 11, 18.Google Scholar
Yamauchi, T, Kamon, J, Waki, H, Terauchi, Y, Kubota, N, Hara, K, et al. (2001) The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nature Medicine 8, 941946.Google Scholar