Caffeine and contraction synergistically stimulate 5′‐AMP‐activated protein kinase and insulin‐independent glucose transport in rat skeletal muscle
5′‐Adenosine monophosphate‐activated protein kinase (AMPK) has been identified as a key mediator of contraction‐stimulated insulin‐independent glucose transport in skeletal muscle. Caffeine acutely stimulates AMPK in resting skeletal muscle, but it is unknown whether caffeine affects AMPK in contracting muscle. Isolated rat epitrochlearis muscle was preincubated and then incubated in the absence or presence of 3 mmol/L caffeine for 30 or 120 min. Electrical stimulation (ES) was used to evoke tetanic contractions during the last 10 min of the incubation period. The combination of caffeine plus contraction had additive effects on AMPKα Thr172 phosphorylation, α‐isoform‐specific AMPK activity, and 3‐O‐methylglucose (3MG) transport. In contrast, caffeine inhibited basal and contraction‐stimulated Akt Ser473 phosphorylation. Caffeine significantly delayed muscle fatigue during contraction, and the combination of caffeine and contraction additively decreased ATP and phosphocreatine contents. Caffeine did not affect resting tension. Next, rats were given an intraperitoneal injection of caffeine (60 mg/kg body weight) or saline, and the extensor digitorum longus muscle was dissected 15 min later. ES of the sciatic nerve was performed to evoke tetanic contractions for 5 min before dissection. Similar to the findings from isolated muscles incubated in vitro, the combination of caffeine plus contraction in vivo had additive effects on AMPK phosphorylation, AMPK activity, and 3MG transport. Caffeine also inhibited basal and contraction‐stimulated Akt phosphorylation in vivo. These findings suggest that caffeine and contraction synergistically stimulate AMPK activity and insulin‐independent glucose transport, at least in part by decreasing muscle fatigue and thereby promoting energy consumption during contraction.
Keywords:
50-AMP-activated protein kinase, energy deprivation, glucose metabolism, muscle contraction, muscle fatigue.
Autoři:
Satoshi Tsuda *,1; Tatsuro Egawa 1,2; Kazuto Kitani 1; Rieko Oshima 1; Xiao Ma 3; Tatsuya Hayashi 1
Působiště autorů:
Laboratory of Sports and Exercise Medicine, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, 606‐8501, Japan
1; Department of Physiology, Graduate School of Health Sciences, Toyohashi SOZO University, Toyohashi, 440‐0016, Japan
2; Key Laboratory of Puer Tea Science, Ministry of Education, Yunnan Agricultural University, Kunming, 650201, Yunnan Province, China
3
Vyšlo v časopise:
Physiological Reports, 3, 2015, č. 10, s. 1-12
Kategorie:
Original Research
prolekare.web.journal.doi_sk:
https://doi.org/10.14814/phy2.12592
© 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Souhrn
5′‐Adenosine monophosphate‐activated protein kinase (AMPK) has been identified as a key mediator of contraction‐stimulated insulin‐independent glucose transport in skeletal muscle. Caffeine acutely stimulates AMPK in resting skeletal muscle, but it is unknown whether caffeine affects AMPK in contracting muscle. Isolated rat epitrochlearis muscle was preincubated and then incubated in the absence or presence of 3 mmol/L caffeine for 30 or 120 min. Electrical stimulation (ES) was used to evoke tetanic contractions during the last 10 min of the incubation period. The combination of caffeine plus contraction had additive effects on AMPKα Thr172 phosphorylation, α‐isoform‐specific AMPK activity, and 3‐O‐methylglucose (3MG) transport. In contrast, caffeine inhibited basal and contraction‐stimulated Akt Ser473 phosphorylation. Caffeine significantly delayed muscle fatigue during contraction, and the combination of caffeine and contraction additively decreased ATP and phosphocreatine contents. Caffeine did not affect resting tension. Next, rats were given an intraperitoneal injection of caffeine (60 mg/kg body weight) or saline, and the extensor digitorum longus muscle was dissected 15 min later. ES of the sciatic nerve was performed to evoke tetanic contractions for 5 min before dissection. Similar to the findings from isolated muscles incubated in vitro, the combination of caffeine plus contraction in vivo had additive effects on AMPK phosphorylation, AMPK activity, and 3MG transport. Caffeine also inhibited basal and contraction‐stimulated Akt phosphorylation in vivo. These findings suggest that caffeine and contraction synergistically stimulate AMPK activity and insulin‐independent glucose transport, at least in part by decreasing muscle fatigue and thereby promoting energy consumption during contraction.
Keywords:
50-AMP-activated protein kinase, energy deprivation, glucose metabolism, muscle contraction, muscle fatigue.
Zdroje
1. Abbott, M. J., A. M. Edelman, and L. P. Turcotte. 2009. CaMKK is an upstream signal of AMP-activated protein kinase in regulation of substrate metabolism in contracting skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R1724–R1732.
2. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11:36–42.
3. Allen, D. G., and H. Westerblad. 1995. The effects of caffeine on intracellular calcium, force and the rate of relaxation of mouse skeletal muscle. J. Physiol. 487(Pt 2):331–342.
4. Bassoli, B. K., P. Cassolla, G. R. Borba-Murad, J. Constantin, C. L. Salgueiro-Pagadigorria, R. B. Bazotte, et al. 2008. Chlorogenic acid reduces the plasma glucose peak in the oral glucose tolerance test: effects on hepatic glucose release and glycaemia. Cell Biochem. Funct. 26:320–328.
5. Bianchi, C. P. 1962. Kinetics of radiocaffeine uptake and release in frog sartorius. J. Pharmacol. Exp. Ther. 138:41–47.
6. Canto, C., Z. Gerhart-Hines, J. N. Feige, M. Lagouge, L. Noriega, J. C. Milne, et al. 2009. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458:1056–1060.
7. Cheng, J. T., I. M. Liu, T. F. Tzeng, W. C. Chen, S. Hayakawa, and T. Yamamoto. 2003. Release of beta-endorphin by caffeic acid to lower plasma glucose in streptozotocin- induced diabetic rats. Horm. Metab. Res. 35:251–258.
8. Cheung, P. C., I. P. Salt, S. P. Davies, D. G. Hardie, and D. Carling. 2000. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem. J. 346(Pt 3):659–669.
9. Costill, D. L., G. P. Dalsky, and W. J. Fink. 1978. Effects of caffeine ingestion on metabolism and exercise performance. Med. Sci. Sports 10:155–158.
10. Ding, M., S. N. Bhupathiraju, M. Chen, R. M. van Dam, and F. B. Hu. 2014. Caffeinated and decaffeinated coffee consumption and risk of type 2 diabetes: a systematic review and a dose-response meta-analysis. Diabetes Care 37:569– 586.
11. Egawa, T., T. Hamada, N. Kameda, K. Karaike, X. Ma, S. Masuda, et al. 2009. Caffeine acutely activates 50adenosine monophosphate-activated protein kinase and increases insulin-independent glucose transport in rat skeletal muscles. Metabolism 58:1609–1617.
12. Egawa, T., T. Hamada, X. Ma, K. Karaike, N. Kameda, S. Masuda, et al. 2011a. Caffeine activates preferentially alpha1-isoform of 50AMP-activated protein kinase in rat skeletal muscle. Acta Physiol. (Oxf.) 201:227–238.
13. Egawa, T., S. Tsuda, X. Ma, T. Hamada, and T. Hayashi. 2011b. Caffeine modulates phosphorylation of insulin receptor substrate-1 and impairs insulin signal transduction in rat skeletal muscle. J. Appl. Physiol. 111:1629–1636.
14. Fisher, J. S., J. Gao, D. H. Han, J. O. Holloszy, and L. A. Nolte. 2002. Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin. Am. J. Physiol. Endocrinol. Metab. 282:E18–E23.
15. Foukas, L. C., N. Daniele, C. Ktori, K. E. Anderson, J. Jensen, and P. R. Shepherd. 2002. Direct effects of caffeine and theophylline on p110 delta and other phosphoinositide 3- kinases. Differential effects on lipid kinase and protein kinase activities. J. Biol. Chem. 277:37124–37130.
16. Friedrichsen, M., B. Mortensen, C. Pehmoller, J. B. Birk, and J. F. Wojtaszewski. 2013. Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol. Cell. Endocrinol. 366:204–214.
17. Fujii, N., N. Jessen, and L. J. Goodyear. 2006. AMP-activated protein kinase and the regulation of glucose transport. Am. J. Physiol. Endocrinol. Metab. 291:E867–E877.
18. Funai, K., and G. D. Cartee. 2009. Inhibition of contraction- stimulated AMP-activated protein kinase inhibits contraction-stimulated increases in PAS-TBC1D1 and glucose transport without altering PAS-AS160 in rat skeletal muscle. Diabetes 58:1096–1104.
19. Graham, T. E., and L. L. Spriet. 1995. Metabolic, catecholamine, and exercise performance responses to various doses of caffeine. J. Appl. Physiol. (1985) 78:867– 874.
20. Hardie, D. G. 2011. Sensing of energy and nutrients by AMP- activated protein kinase. Am. J. Clin. Nutr. 93:891S–896S.
21. Hayashi, T., M. F. Hirshman, N. Fujii, S. A. Habinowski, L. A. Witters, and L. J. Goodyear. 2000. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49:527–531.
22. Hsu, F. L., Y. C. Chen, and J. T. Cheng. 2000. Caffeic acid as active principle from the fruit of Xanthium strumarium to lower plasma glucose in diabetic rats. Planta Med. 66:228– 230.
23. Hunter, R. W., J. T. Treebak, J. F. Wojtaszewski, and K. Sakamoto. 2011. Molecular mechanism by which AMP- activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 60:766–774.
24. Huxley, R., C. M. Lee, F. Barzi, L. Timmermeister, S. Czernichow, V. Perkovic, et al. 2009. Coffee, decaffeinated coffee, and tea consumption in relation to incident type 2 diabetes mellitus: a systematic review with meta-analysis. Arch. Intern. Med. 169:2053–2063.
25. Iglesias, M. A., J. M. Ye, G. Frangioudakis, A. K. Saha, E. Tomas, N. B. Ruderman, et al. 2002. AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats. Diabetes 51:2886–2894.
26. Iwanaka, N., T. Egawa, N. Satoubu, K. Karaike, X. Ma, S. Masuda, et al. 2010. Leucine modulates contraction- and insulin-stimulated glucose transport and upstream signaling events in rat skeletal muscle. J. Appl. Physiol. 108:274–282.
27. Jager, S., C. Handschin, J. St-Pierre, and B. M. Spiegelman. 2007. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. USA 104:12017–12022.
28. Jensen, T. E., A. J. Rose, Y. Hellsten, J. F. Wojtaszewski, and E. A. Richter. 2007. Caffeine-induced Ca(2+) release increases AMPK-dependent glucose uptake in rodent soleus muscle. Am. J. Physiol. Endocrinol. Metab. 293:E286–E292.
29. Jung, U. J., M. K. Lee, Y. B. Park, S. M. Jeon, and M. S. Choi. 2006. Antihyperglycemic and antioxidant properties of caffeic acid in db/db mice. J. Pharmacol. Exp. Ther. 318:476–483.
30. Kolnes, A. J., A. Ingvaldsen, A. Bolling, J. T. Stuenaes, M. Kreft, R. Zorec, et al. 2010. Caffeine and theophylline block insulin-stimulated glucose uptake and PKB phosphorylation in rat skeletal muscles. Acta Physiol. (Oxf.) 200:65–74.
31. Magkos, F., and S. A. Kavouras. 2005. Caffeine use in sports, pharmacokinetics in man, and cellular mechanisms of action. Crit. Rev. Food Sci. Nutr. 45:535–562.
32. Miyamoto, L., T. Toyoda, T. Hayashi, S. Yonemitsu, M. Nakano, S. Tanaka, et al. 2007. Effect of acute activation of 5’-AMP-activated protein kinase on glycogen regulation in isolated rat skeletal muscle. J. Appl. Physiol. 102:1007–1013.
33. Miyazaki, E., H. Yabu, and M. Takahashi. 1962. Increasing effect of caffeine on the oxygen consumption of the skeletal muscle. Jpn. J. Physiol. 12:113–123.
34. Musi, N., T. Hayashi, N. Fujii, M. F. Hirshman, L. A. Witters, and L. J. Goodyear. 2001. AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 280:E677–E684.
35. Nakano, M., T. Hamada, T. Hayashi, S. Yonemitsu, L. Miyamoto, T. Toyoda, et al. 2006. alpha2 Isoform-specific activation of 50adenosine monophosphate-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-beta-D- ribonucleoside at a physiological level activates glucose transport and increases glucose transporter 4 in mouse skeletal muscle. Metabolism 55:300–308.
36. Nesher, R., I. E. Karl, K. E. Kaiser, and D. M. Kipnis. 1980. Epitrochlearis muscle. I. Mechanical performance, energetics, and fiber composition. Am. J. Physiol. 239:E454–E460.
37. Raney, M. A., and L. P. Turcotte. 2008. Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. J. Appl. Physiol. (1985) 104:1366–1373.
38. Rockl, K. S., M. F. Hirshman, J. Brandauer, N. Fujii, L. A. Witters, and L. J. Goodyear. 2007. Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56:2062–2069.
39. Ryu, S., S. K. Choi, S. S. Joung, H. Suh, Y. S. Cha, S. Lee,et al. 2001. Caffeine as a lipolytic food component increases endurance performance in rats and athletes. J. Nutr. Sci. Vitaminol. (Tokyo) 47:139–146.
40. Sakamoto, K., M. F. Hirshman, W. G. Aschenbach, and L. J. Goodyear. 2002. Contraction regulation of Akt in rat skeletal muscle. J. Biol. Chem. 277:11910–11917.
41. Sakamoto, K., D. E. Arnolds, N. Fujii, H. F. Kramer, M. F. Hirshman, and L. J. Goodyear. 2006. Role of Akt2 in contraction-stimulated cell signaling and glucose uptake in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 291: E1031–E1037.
42. Simmonds, M. J., C. L. Minahan, and S. Sabapathy. 2010. Caffeine improves supramaximal cycling but not the rate of anaerobic energy release. Eur. J. Appl. Physiol. 109:287–295.
43. Stapleton, D., K. I. Mitchelhill, G. Gao, J. Widmer, B. J. Michell, T. Teh, et al. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611–614.
44. Stein, S. C., A. Woods, N. A. Jones, M. D. Davison, and D. Carling. 2000. The regulation of AMP-activated protein kinase by phosphorylation. Biochem. J. 345(Pt 3):437–443.
45. Tarnopolsky, M., and C. Cupido. 2000. Caffeine potentiates low frequency skeletal muscle force in habitual and nonhabitual caffeine consumers. J. Appl. Physiol. (1985) 89:1719–1724.
46. Toyoda, T., T. Hayashi, L. Miyamoto, S. Yonemitsu, M. Nakano, S. Tanaka, et al. 2004. Possible involvement of the alpha1 isoform of 50AMP-activated protein kinase in oxidative stress-stimulated glucose transport in skeletal
47. muscle. Am. J. Physiol. Endocrinol. Metab. 287:E166–
48. E173.Tsuda, S., T. Egawa, X. Ma, R. Oshima, E. Kurogi, and T.
49. Hayashi. 2012. Coffee polyphenol caffeic acid but not chlorogenic acid increases 5’AMP-activated protein kinase and insulin-independent glucose transport in rat skeletal muscle. J. Nutr. Biochem. 23:1403–1409.
50. Vavvas, D., A. Apazidis, A. K. Saha, J. Gamble, A. Patel, B. E. Kemp, et al. 1997. Contraction-induced changes in acetyl- CoA carboxylase and 50-AMP-activated kinase in skeletal muscle. J. Biol. Chem. 272:13255–13261.
51. Winder, W. W., and D. G. Hardie. 1996. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am. J. Physiol. 270 (2 Pt 1):E299–E304.
52. Wojtaszewski, J. F., J. B. Birk, C. Frosig, M. Holten, H. Pilegaard, and F. Dela. 2005. 5’AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J. Physiol. 564(Pt 2):563–573.
53. Wright, D. C., K. A. Hucker, J. O. Holloszy, and D. H. Han. 2004. Ca2+ and AMPK both mediate stimulation of glucose transport by muscle contractions. Diabetes 53:330–335.
54. Wu, M., M. Falasca, and E. R. Blough. 2011. Akt/protein kinase B in skeletal muscle physiology and pathology. J. Cell. Physiol. 226:29–36.
55. Young, D. A., J. J. Uhl, G. D. Cartee, and J. O. Holloszy. 1986. Activation of glucose transport in muscle by prolonged exposure to insulin. Effects of glucose and insulin concentrations. J. Biol. Chem. 261:16049–16053.
56. Zheng, D., P. S. MacLean, S. C. Pohnert, J. B. Knight, A. L. Olson, W. W. Winder, et al. 2001. Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J. Appl. Physiol. 91:1073–1083.
57. Zheng, X., S. Takatsu, H. Wang, and H. Hasegawa. 2014. Acute intraperitoneal injection of caffeine improves endurance exercise performance in association with increasing brain dopamine release during exercise. Pharmacol. Biochem. Behav. 122:136–143.
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