DOI QR코드

DOI QR Code

Lipid accumulation mediated by adiponectin in C2C12 myogenesis

  • Yin, Changjun (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Long, Qinqiang (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Lei, Ting (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Chen, Xiaodong (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Long, Huan (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Feng, Bin (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Peng, Yin (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Wu, Yanling (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University) ;
  • Yang, Zaiqing (Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Life Science and Technology, Huazhong Agricultural University)
  • Published : 2009.10.31

Abstract

Plasma concentrations of adiponectin have been shown to be decreased in patients with obesity, cardiovascular diseases, hypertension and metabolic syndrome. Recent studies have found that adiponectin reduces lipid accumulation in macrophage foam cells which may impact the development of atherosclerosis. However, it remains unclear whether adiponectin is involved in the process of lipid accumulation during myogenesis. Using C2C12 myoblasts, we investigated the effect of adiponectin on intramyocellular lipid accumulation during myogenesis. The results showed that intracellular lipid accumulation is significantly decreased during C2C12 differentiation, apparently due to increased fatty acid oxidation and decreased fatty acid synthesis during this process. C2C12 cells transiently transfected with adiponectin gene showed reduced lipid accumulation as compared to controls. Further experiments demonstrated that adiponectin can suppress lipid accumulation by increasing fatty acid oxidation during C2C12 myogenesis.

References

  1. Buckingham, M. (2006) Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr. Opin. Genet Dev. 16, 525-532 https://doi.org/10.1016/j.gde.2006.08.008
  2. Corcoran, M., Lamon-Fava, P. S. and Fielding, R. A. (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am. J. Clin. Nutr. 85, 662-677
  3. Schrauwen-Hinderling, V. B., Hesselink, M. K., Schrauwen, P. and Kooi, M. E. (2006) Intramyocellular lipid content in human skeletal muscle. Obesity (Silver Spring) 14, 357-367 https://doi.org/10.1038/oby.2006.47
  4. Goodpaster, B. H., He, J., Watkins, S. and Kelley, D. E. (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 86, 5755-5761
  5. Ye, J. M., Doyle, P. J., Iglesias, M. A., Watson, D. G., Cooney, G. J. and Kraegen, E. W. (2001) Peroxisome proliferator- activated receptor (PPAR)-alpha activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats: comparison with PPAR-gamma activation. Diabetes 50, 411-417 https://doi.org/10.2337/diabetes.50.2.411
  6. Kadowaki, T. and Yamauchi, T. (2005) Adiponectin and adiponectin receptors. Endocr. Rev. 26, 439-451 https://doi.org/10.1210/er.2005-0005
  7. Arita, Y., Kihara, S., Ouchi, N., Takahashi, M., Maeda, K., Miyagawa, J., Hotta, K., Shimomura, I., Nakamura, T., Miyaoka, K., Kuriyama, H., Nishida, M., Yamashita, S., Okubo, K., Matsubara, K., Muraguchi, M., Ohmoto, Y., Funahashi, T. and Matsuzawa, Y. (1999) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257, 79-83 https://doi.org/10.1006/bbrc.1999.0255
  8. Guerre-Millo, M. (2008) Adiponectin: an update. Diabetes Metab. 34, 12-18 https://doi.org/10.1016/j.diabet.2007.08.002
  9. Kadowaki, T., Yamauchi, T., Kubota, N., Hara, K., Ueki, K. and Tobe, K. (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest. 116, 1784-1792 https://doi.org/10.1172/JCI29126
  10. Yamauchi, T., Kamon, J., Ito, Y., Tsuchida, A., Yokomizo, T., Kita, S., Sugiyama, T., Miyagishi, M., Hara, K., Tsunoda, M., Murakami, K., Ohteki, T., Uchida, S., Takekawa, S., Waki, H., Tsuno, N.H., Shibata, Y., Terauchi, Y., Froguel, P., Tobe, K., Koyasu, S., Taira, K., Kitamura, T., Shimizu, T., Nagai, R. and Kadowaki, T. (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762-769 https://doi.org/10.1038/nature01705
  11. Yamauchi, T., Nio, Y., Maki, T., Kobayashi, M., Takazawa, T., Iwabu, M., Okada-Iwabu, M., Kawamoto, S., Kubota, N., Kubota, T., Ito, Y., Kamon, J., Tsuchida, A., Kumagai, K., Kozono, H., Hada, Y., Ogata, H., Tokuyama, K., Tsunoda, M., Ide, T., Murakami, K., Awazawa, M., Takamoto, I., Froguel, P., Hara, K., Tobe, K., Nagai, R., Ueki, K. and Kadowaki, T. (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332-339 https://doi.org/10.1038/nm1557
  12. Mao, X., Kikani, C. K., Riojas, R. A., Langlais, P., Wang, L., Ramos, F. J., Fang, Q., Christ-Roberts, C. Y., Hong, J. Y., Kim, R. Y., Liu, F. and Dong, L. Q. (2006) APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol. 8, 516-523 https://doi.org/10.1038/ncb1404
  13. Hug, C., Wang, J., Ahmad, N. S., Bogan, J. S., Tsao, T. S. and Lodish, H. F. (2004) T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. U.S.A. 101, 10308-10313 https://doi.org/10.1073/pnas.0403382101
  14. Yoon, M. J., Lee, G. Y., Chung, J. J., Ahn, Y. H., Hong, S. H. and Kim, J. B. (2006) Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 55, 2562-2570 https://doi.org/10.2337/db05-1322
  15. Tian, L., Luo, N., Klein, R. L., Chung, B. H., Garvey, W. T. and Fu, Y. (2009) Adiponectin reduces lipid accumulation in macrophage foam cells. Atherosclerosis 202, 152-161 https://doi.org/10.1016/j.atherosclerosis.2008.04.011
  16. Fu, Y., Luo, N., Klein, R. L. and Garvey, W. T. (2005) Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J. Lipid. Res. 46, 1369-1379 https://doi.org/10.1194/jlr.M400373-JLR200
  17. Fujita, T., Furukawa, S., Morita, K., Ishihara, T., Shiotani, M., Matsushita, Y., Matsuda, M. and Shimomura, I. (2005) Glucosamine induces lipid accumulation and adipogenic change in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 328, 369-374 https://doi.org/10.1016/j.bbrc.2004.12.185
  18. Shimokawa, T., Kato, M., Ezaki, O. and Hashimoto, S. (1998) Transcriptional regulation of muscle-specific genes during myoblast differentiation. Biochem. Biophys. Res. Commun 246, 287-292 https://doi.org/10.1006/bbrc.1998.8600
  19. Ouchi, N., Kihara, S., Arita, Y., Nishida, M., Matsuyama, A., Okamoto, Y., Ishigami, M., Kuriyama, H., Kishida, K., Nishizawa, H., Hotta, K., Muraguchi, M., Ohmoto, Y., Yamashita, S., Funahashi, T. and Matsuzawa, Y. (2001) Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation 103, 1057-1063 https://doi.org/10.1161/01.CIR.103.8.1057
  20. Krause, M. P., Liu, Y., Vu, V., Chan, L., Xu, A., Riddell, M. C., Sweeney, G. and Hawke., T. J. (2008) Adiponectin is expressed by skeletal muscle fibers and influences muscle phenotype and function. Am. J. Physiol. Cell Physiol. 295, C203-212 https://doi.org/10.1152/ajpcell.00030.2008
  21. Ingelsson, E., Arnlov, J., Zethelius, B., Vasan, R. S., Flyvbjerg, A., Frystyk, J., Berne, C., Hanni, A., Lind, L. and Sundstrom, J. (2009) Associations of Serum Adiponectin with Skeletal Muscle Morphology and Insulin Sensitivity. J. Clin. Endocrinol. Metab. 94, 953-957 https://doi.org/10.1210/jc.2008-1772
  22. Yamauchi, T., Kamon, J., Minokoshi, Y., Ito, Y., Waki, H., Uchida, S., Yamashita, S., Noda, M., Kita, S., Ueki, K., Eto, K., Akanuma, Y., Froguel, P., Foufelle, F., Ferre, P., Carling, D., Kimura, S., Nagai, R., Kahn, B. B. and Kadowaki, T. (2002) Adiponectin stimulates glucose utilization and fatty- acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288-1295 https://doi.org/10.1038/nm788
  23. Long, Y. C., Barnes, B. R., Mahlapuu, M., Steiler, T. L., Martinsson, S., Leng, Y., Wallberg-Henriksson, H., Andersson, L. and Zierath, J. R. (2005) Role of AMP-activated protein kinase in the coordinated expression of genes controlling glucose and lipid metabolism in mouse white skeletal muscle. Diabetologia 48, 2354-2364 https://doi.org/10.1007/s00125-005-1962-5
  24. Tugwood, J. D., Issemann, I., Anderson, R. G., Bundell, K. R., McPheat, W. L. and Green, S. (1992) The mouse peroxisome proliferator activated receptor recognizes a response element in the 5' flanking sequence of the rat acyl CoA oxidase gene. EMBO J. 11, 433-439
  25. Ceddia, R.B., Somwar, R., Maida, A., Fang, X., Bikopoulos, G. and Sweeney, G. (2005) Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 48, 132-139 https://doi.org/10.1007/s00125-004-1609-y
  26. Yamauchi, T., Kamon, J., Waki, H., Terauchi, Y., Kubota, N., Hara, K., Mori, Y., Ide, T., Murakami, K., Tsuboyama-Kasaoka, N., Ezaki, O., Akanuma, Y., Gavrilova, O., Vinson, C., Reitman, M. L., Kagechika, H., Shudo, K., Yoda, M., Nakano, Y., Tobe, K., Nagai, R., Kimura, S., Tomita, M., Froguel, P. and Kadowaki, T. (2001) The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7, 941-946 https://doi.org/10.1038/90984
  27. Takeuchi, T., Adachi, Y., Ohtsuki, Y. and Furihata, M. (2007) diponectin receptors, with special focus on the role of the third receptor, T-cadherin, in vascular disease. Med. Mol. Morphol. 40, 115-120 https://doi.org/10.1007/s00795-007-0364-9
  28. Ramirez-Zacarias, J. L., Castro-Munozledo, F. and Kuri-Harcuch, W. (1992) Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 97, 493-497 https://doi.org/10.1007/BF00316069

Cited by

  1. Relationships between serum adiponectin and soluble TNF-α receptors and glucose and lipid oxidation in lean and obese subjects vol.49, pp.1, 2012, https://doi.org/10.1007/s00592-010-0252-y
  2. Extracellular annexins and dynamin are important for sequential steps in myoblast fusion vol.200, pp.1, 2013, https://doi.org/10.1083/jcb.201207012
  3. CRF type 2 receptors mediate the metabolic effects of ghrelin in C2C12 cells vol.22, pp.2, 2014, https://doi.org/10.1002/oby.20535
  4. Relationships of serum soluble E-selectin concentration with insulin sensitivity and metabolic flexibility in lean and obese women vol.45, pp.3, 2014, https://doi.org/10.1007/s12020-013-0025-9
  5. Obese subcutaneous adipose tissue impairs human myogenesis, particularly in old skeletal muscle, via resistin-mediated activation of NFκB vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-33840-x