Diet-induced obesity alters anabolic signalling in mice at the onset of skeletal muscle regeneration

Acta Physiologica

Volumn 215, Issue 1, 2015, Pages 46-57

  Brown, L A ^a   Lee, D E ^a   Patton, J F ^a   Perry, R A ^a   Brown, J L ^a   Baum, J I ^a   Smith Blair, N ^a   Greene, N P ^a   Washington, T A ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Diet induced obesity; Inflammation; Protein synthesis; Regeneration; Skeletal muscle

Indexed keywords

BUPIVACAINE; CYCLIN D1; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MYOD PROTEIN; MYOGENIC FACTOR; PROTEIN; PROTEIN KINASE B; S6 KINASE; SOMATOMEDIN C; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANABOLIC SIGNALING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; INFLAMMATION; LEAN BODY WEIGHT; LIPID DIET; MALE; MOUSE; MUSCLE INJURY; MUSCLE METABOLISM; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGENERATIVE ABILITY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; ANIMAL; C57BL MOUSE; DISEASE MODEL; METABOLISM; OBESITY; PHYSIOLOGY; REGENERATION;

ANIMALS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR I; MICE, INBRED C57BL; MUSCLE, SKELETAL; OBESITY; REGENERATION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84937821245     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12537     Document Type: Article

References (44)

1. Akhmedov, D. & Berdeaux, R. 2013. The effects of obesity on skeletal muscle regeneration. Front Physiol 4, 371.
2. Bellanger, T.M. & Bray, G.A. 2005. Obesity related morbidity and mortality. J La State Med Soc 157, S42-S49.
3. Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J.C., Glass, D.J. & Yancopoulos, G.D. 2001. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
4. Carlson, B.M. 1973. The regeneration of skeletal muscle. A review. Am J Anat 137, 119-149.
5. Chen, S.E., Gerken, E., Zhang, Y., Zhan, M., Mohan, R.K., Li, A.S., Reid, M.B. & Li, Y.P. 2005. Role of TNF-(Ohtani et al.) signaling in regeneration of cardiotoxin-injured muscle. Am J Physiol Cell Physiol, 289, C1179-C1187.
6. Chmelar, J., Chung, K.J. & Chavakis, T. 2013. The role of innate immune cells in obese adipose tissue inflammation and development of insulin resistance. Thromb Haemost 109, 399-406.
7. Cusi, K., Maezono, K., Osman, A., Pendergrass, M., Patti, M.E., Pratipanawatr, T., DeFronzo, R.A., Kahn, C.R. & Mandarino, L.J. 2000. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105, 311-320.
8. De Bleecker, J.L. & Engel, A.G. 1994. Expression of cell adhesion molecules in inflammatory myopathies and Duchenne dystrophy. J Neuropathol Exp Neurol 53, 369-376.
9. DeFronzo, R.A. & Tripathy, D. 2009. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32, S157-S163.
10. Drake, J.C., Alway, S.E., Hollander, J.M. & Williamson, D.L. 2010. AICAR treatment for 14 days normalizes obesity-induced dysregulation of TORC1 signaling and translational capacity in fasted skeletal muscle. Am J Physiol Regul Integr Comp Physiol 299, R1546-R1554.
11. Finkelstein, E.A., Khavjou, O.A., Thompson, H., Trogdon, J.G., Pan, L., Sherry, B. & Dietz, W. 2012. Obesity and severe obesity forecasts through 2030. Am J Prev Med 42, 563-570.
12. Ge, Y., Wu, A.L., Warnes, C., Liu, J., Zhang, C., Kawasome, H., Terada, N., Boppart, M.D., Schoenherr, C.J. & Chen, J. 2009. mTOR regulates skeletal muscle regeneration in vivo through kinase-dependent and kinase-independent mechanisms. Am J Physiol Cell Physiol 297, C1434-C1444.
13. Goodman, C.A., Frey, J.W., Mabrey, D.M., Jacobs, B.L., Lincoln, H.C., You, J.S. & Hornberger, T.A. 2011. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589, 5485-5501.
14. Greene, N.P., Nilsson, M.I., Washington, T.A., Lee, D.E., Brown, L.A., Papineau, A.M., Shimkus, K.L., Greene, E.S., Crouse, S.F. & Fluckey, J.D. 2014. Impaired exercise-induced mitochondrial biogenesis in the obese Zucker rat, despite PGC-1alpha induction, is due to compromised mitochondrial translation elongation. Am J Physiol Endocrinol Metab 306, E503-E511.
15. Gregor, M.F. & Hotamisligil, G.S. 2011. Inflammatory mechanisms in obesity. Annu Rev Immunol 29, 415-445.
16. Hotamisligil, G.S., Peraldi, P., Budavari, A., Ellis, R., White, M.F. & Spiegelman, B.M. 1996. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271, 665-668.
17. Hu, Z., Wang, H., Lee, I.H., Modi, S., Wang, X., Du, J. & Mitch, W.E. 2010. PTEN inhibition improves muscle regeneration in mice fed a high-fat diet. Diabetes 59, 1312-1320.
18. Kharraz, Y., Guerra, J., Mann, C.J., Serrano, A.L. & Munoz-Canoves, P. 2013. Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediators Inflamm 2013, 491-497.
19. Leger, B., Cartoni, R., Praz, M., Lamon, S., Deriaz, O., Crettenand, A., Gobelet, C., Rohmer, P., Konzelmann, M., Luthi, F. & Russell, A.P. 2006. Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 576, 923-933.
20. McClung, J.M., Mehl, K.A., Thompson, R.W., Lowe, L.L. & Carson, J.A. 2005. Nandrolone decanoate modulates cell cycle regulation in functionally overloaded rat soleus muscle. Am J Physiol Regul Integr Comp Physiol 6, R1543-R1552.
21. Megeney, L.A., Kablar, B., Garrett, K., Anderson, J.E. & Rudnicki, M.A. 1996. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10, 1173-1183.
22. Nguyen, M.H., Cheng, M. & Koh, T.J. 2011. Impaired muscle regeneration in ob/ob and db/db mice. ScientificWorldJournal 11, 1525-1535.
23. Nilsson, M.I., Dobson, J.P., Greene, N.P., Wiggs, M.P., Shimkus, K.L., Wudeck, E.V., Davis, A.R., Laureano, M.L. & Fluckey, J.D. 2013. Abnormal protein turnover and anabolic resistance to exercise in sarcopenic obesity. FASEB J 27, 3905-3916.
24. Nimmo, M.A., Leggate, M., Viana, J.L. & King, J.A. 2013. The effect of physical activity on mediators of inflammation. Diabetes Obes Metab 15, 51-60.
25. Ohtani, T., Ishihara, K., Atsumi, T., Nishida, K., Kaneko, Y., Miyata, T., Itoh, S., Narimatsu, M., Maeda, H., Fukada, T., Itoh, M., Okano, H., Hibi, M. & Hirano, T. 2000. Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12, 95-105.
26. Peterson, J.M., Bryner, R.W. & Alway, S.E. 2008. Satellite cell proliferation is reduced in muscles of obese Zucker rats but restored with loading. Am J Physiol Cell Physiol 295, C521-C528.
27. Relaix, F. & Zammit, P.S. 2012. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139, 2845-2856.
28. Rigamonti, E. & Zordan, P. 2014. Macrophage plasticity in skeletal muscle repair. Biomed Res Int 2014, 560-629.
29. Rommel, C., Bodine, S.C., Clarke, B.A., Rossman, R., Nunez, L., Stitt, T.N., Yancopoulos, G.D. & Glass, D.J. 2001. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3, 1009-1013.
30. Schiaffino, S., Dyar, K.A., Ciciliot, S., Blaauw, B. & Sandri, M. 2013. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280, 4294-4314.
31. Seidell, J.C. 2000. Obesity, insulin resistance and diabetes - a worldwide epidemic. Br J Nutr 83, S5-S8.
32. Sitnick, M., Bodine, S.C. & Rutledge, J.C. 2009. Chronic high fat feeding attenuates load-induced hypertrophy in mice. J Physiol 587, 5753-5765.
33. Svanberg, E., Zachrisson, H., Ohlsson, C., Iresjo, B.M. & Lundholm, K.G. 1996. Role of insulin and IGF-I in activation of muscle protein synthesis after oral feeding. Am J Physiol 270, E614-E620.
34. Tamilarasan, K.P., Temmel, H., Das, S.K., Al Zoughbi, W., Schauer, S., Vesely, P.W. & Hoefler, G. 2012. Skeletal muscle damage and impaired regeneration due to LPL-mediated lipotoxicity. Cell Death Dis 3, e354.
35. Tierney, M.T., Aydogdu, T., Sala, D., Malecova, B., Gatto, S., Puri, P.L., Latella, L. & Sacco, A. 2014. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med 20, 1182-1186.
36. Unsold, B., Bremen, E., Didie, M., Hasenfuss, G. & Schafer, K. 2015. Differential PI3-kinase signal transduction in obesity-associated cardiac hypertrophy and response to ischemia. Obesity (Silver Spring) 23, 90-99.
37. Venuti, J.M., Morris, J.H., Vivian, J.L., Olson, E.N. & Klein, W.H. 1995. Myogenin is required for late but not early aspects of myogenesis during mouse development. J Cell Biol 128, 563-576.
38. Villalta, S.A., Nguyen, H.X., Deng, B., Gotoh, T. & Tidball, J.G. 2009. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet 18, 482-496.
39. Vincent, H.K., Horodyski, M., Gearen, P., Vlasak, R., Seay, A.N., Conrad, B.P. & Vincent, K.R. 2012. Obesity and long term functional outcomes following elective total hip replacement. J Orthop Surg Res 7, 16.
40. Washington, T.A., White, J.P., Davis, J.M., Wilson, L.B., Lowe, L.L., Sato, S. & Carson, J.A. 2011. Skeletal muscle mass recovery from atrophy in IL-6 knockout mice. Acta Physiol (Oxf) 202, 657-669.
41. Washington, T.A., Brown, L., Smith, D.A., Davis, G., Baum, J. & Bottje, W. 2013. Monocarboxylate transporter expression at the onset of skeletal muscle regeneration. Physiol Rep 1, e00075.
42. Washington, T.A., Healey, J.M., Thompson, R.W., Lowe, L.L. & Carson, J.A. 2014. Lactate dehydrogenase regulation in aged skeletal muscle: regulation by anabolic steroids and functional overload. Exp Gerontol 57, 66-74.
43. Yang, H., Li, F., Kong, X., Yuan, X., Wang, W., Huang, R., Li, T., Geng, M., Wu, G. & Yin, Y. 2012. Chemerin regulates proliferation and differentiation of myoblast cells via ERK1/2 and mTOR signaling pathways. Cytokine 60, 646-652.
44. Zhang, C., Li, Y., Wu, Y., Wang, L., Wang, X. & Du, J. 2013. Interleukin-6/signal transducer and activator of transcription 3 (STAT3) pathway is essential for macrophage infiltration and myoblast proliferation during muscle regeneration. J Biol Chem 288, 1489-1499.