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Can food factors provide Us with the similar beneficial effects of physical exercise?

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Abstract

Metabolic diseases have got global health issues. Physical exercise as well as diet therapy is a potent strategy for fighting against the diseases. However, it is often difficult to continue to keep exercise regularly enough to take sufficient effect. Thus, good substitutes for the therapeutic exercise would be greatly beneficial. Recent studies have suggested that 5′AMP-activated protein kinase (AMPK) play important roles in the metabolic alterations by muscle contraction. The notion that AMPK mediates broad effects of physical exercise has been widely accepted, though it has been challenged by observations in some genetically AMPK-disrupted animals. We have demonstrated metabolome-wide significance of AMPK activation in contracting muscles. Thus, pharmacological activation of AMPK can be a promising way to obtain similar effects of the exercise. The relevance of AMPK will be introduced, and possible strategies for obtaining similar effects to the exercise from food factors will be discussed in the current review.

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References

  1. International Diabetes Federation. IDF Diabetes Atlas. 6th ed. International Diabetes Federation, Brussel, Belgium (2014)

  2. American Diabetes Association. (4) Foundations of care: Education, nutrition, physical activity, smoking cessation, psychosocial care, and immunization. Diabetes Care 38: S20-S30 (2015)

  3. American Diabetes Association. (5) Prevention or delay of type 2 diabetes. Diabetes Care 38: S31-S32 (2015)

  4. Berger M, Hagg S, Ruderman NB. Glucose metabolism in perfused skeletal muscle. Interaction of insulin and exercise on glucose uptake. Biochem. J. 146: 231–238 (1975)

    Article  CAS  Google Scholar 

  5. Brozinick JT Jr, Etgen GJ Jr, Yaspelkis BB 3rd, Kang HY, Ivy JL. Effects of exercise training on muscle GLUT-4 protein content and translocation in obese Zucker rats. Am. J. Physiol. 265: 419–427 (1993)

    Google Scholar 

  6. Roy D, Johannsson E, Bonen A, Marette A. Electrical stimulation induces fiber type-specific translocation of GLUT-4 to T tubules in skeletal muscle. Am. J. Physiol. 273: 688–694 (1997)

    Google Scholar 

  7. Carling D, Zammit VA, Hardie DG. A common bicyclic protein kinase cascade inactivates the regulatory enzymes of fatty acid and cholesterol biosynthesis. FEBS Lett. 223: 217–222 (1987)

    Article  CAS  Google Scholar 

  8. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47: 1369–1373 (1998)

    CAS  Google Scholar 

  9. Musi N, Hayashi T, Fujii N, Hirshman MF, Witters LA, Goodyear LJ. AMPactivated protein kinase activity and glucose uptake in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 280: 677–684 (2001)

    Google Scholar 

  10. Miyamoto L, Toyoda T, Hayashi T, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Ogawa Y, Inoue G, Fushiki T, Nakao K. Effect of acute activation of 5′-AMP-activated protein kinase on glycogen regulation in isolated rat skeletal muscle. J. Appl. Physiol. 102: 1007–1013 (2007)

    Article  CAS  Google Scholar 

  11. Miyamoto L, Ebihara K, Kusakabe T, Aotani D, Yamamoto-Kataoka S, Sakai T, Aizawa-Abe M, Yamamoto Y, Fujikura J, Hayashi T, Hosoda K, Nakao K. Leptin activates hepatic 5′-AMP-activated protein kinase through sympathetic nervous system and a1-adrenergic receptor: A potential mechanism for improvement of fatty liver in lipodystrophy by leptin. J. Biol. Chem. 287: 40441–40447 (2012)

    Article  CAS  Google Scholar 

  12. Nakano M, Hamada T, Hayashi T, Yonemitsu S, Miyamoto L, Toyoda T, Tanaka S, Masuzaki H, Ebihara K, Ogawa Y, Hosoda K, Inoue G, Yoshimasa Y, Otaka A, Fushiki T, Nakao K. α2 isoform-specific activation of 5′adenosine monophosphate-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-β-D-ribonucleoside at a physiological level activates glucose transport and increases glucose transporter 4 in mouse skeletal muscle. Metabolism 55: 300–308 (2006)

    Article  CAS  Google Scholar 

  13. Fujii N, Hirshman MF, Kane EM, Ho RC, Peter LE, Seifert MM, Goodyear LJ. AMP-activated protein kinase alpha2 activity is not essential for contractionand hyperosmolarity-induced glucose transport in skeletal muscle. J. Biol. Chem. 280: 39033–39041 (2005)

    Article  CAS  Google Scholar 

  14. Jorgensen SB, Viollet B, Andreelli F, Frosig C, Birk JB, Schjerling P, Vaulont S, Richter EA, Wojtaszewski JF. Knockout of the alpha2 but not alpha1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside but not contraction-induced glucose uptake in skeletal muscle. J. Biol. Chem. 279: 1070–1079 (2004)

    Article  CAS  Google Scholar 

  15. Miura S, Kai Y, Kamei Y, Bruce CR, Kubota N, Febbraio MA, Kadowaki T, Ezaki O. Alpha2-AMPK activity is not essential for an increase in fatty acid oxidation during low-intensity exercise. Am. J. Physiol. Endocrinol. Metab. 296: 47–55 (2009)

    Article  Google Scholar 

  16. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ. A role for AMPactivated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell 7: 1085–1094 (2001)

    Article  CAS  Google Scholar 

  17. Miyamoto L. Significance of 5’AMP-activated protein kinase in metabolomic regulation by skeletal muscle contraction. J. Sports Med. Phys. Fitness 4: 93–102 (2015)

    Article  Google Scholar 

  18. Miyamoto L, Egawa T, Oshima R, Kurogi E, Tomida Y, Tsuchiya K, Hayashi T. AICAR stimulation metabolome widely mimics electrical contraction in isolated rat epitrochlearis muscle. Am. J. Physiol. Cell Physiol. 305: 1214–1222 (2013)

    Article  Google Scholar 

  19. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. P. Natl. Acad. Sci. USA 101: 3329–3335 (2004)

    Article  CAS  Google Scholar 

  20. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 13: 2004–2008 (2003)

    Article  CAS  Google Scholar 

  21. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J. Biol. 2: 28 (2003)

    Article  Google Scholar 

  22. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG. Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2: 9–19 (2005)

    Article  CAS  Google Scholar 

  23. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 280: 29060–29066 (2005)

    Article  CAS  Google Scholar 

  24. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2: 21–33 (2005)

    Article  CAS  Google Scholar 

  25. Scott JW, Ross FA, Liu JK, Hardie DG. Regulation of AMP-activated protein kinase by a pseudosubstrate sequence on the gamma subunit. EMBO J. 26: 806–815 (2007)

    Article  CAS  Google Scholar 

  26. Davies SP, Helps NR, Cohen PT, Hardie DG. 5′-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase-2C alpha and native bovine protein phosphatase-2AC. FEBS Lett. 377: 421–425 (1995)

    Article  CAS  Google Scholar 

  27. Xie M, Zhang D, Dyck JR, Li Y, Zhang H, Morishima M, Mann DL, Taffet GE, Baldini A, Khoury DS, Schneider MD. A pivotal role for endogenous TGF-betaactivated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. P. Natl. Acad. Sci. USA 103: 17378–17383 (2006)

    Article  CAS  Google Scholar 

  28. Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J. Biol. Chem. 281: 25336–25343 (2006)

    Article  CAS  Google Scholar 

  29. Ma X, Iwanaka N, Masuda S, Karaike K, Egawa T, Hamada T, Toyoda T, Miyamoto L, Nakao K, Hayashi T. Morus alba leaf extract stimulates 5′-AMP-activated protein kinase in isolated rat skeletal muscle. J. Ethnopharmacol. 122: 54–59 (2009)

    Article  Google Scholar 

  30. Lee SM, Do HJ, Shin MJ, Seong SI, Hwang KY, Lee JY, Kwon O, Jin T, Chung JH. 1-Deoxynojirimycin isolated from a Bacillus subtilis stimulates adiponectin and GLUT4 expressions in 3T3-L1 adipocytes. J. Microbiol. Biotechn. 23: 637–643 (2013)

    Article  CAS  Google Scholar 

  31. Jensen TE, Rose AJ, Hellsten Y, Wojtaszewski JF, Richter EA. Caffeine-induced Ca2+ release increases AMPK-dependent glucose uptake in rodent soleus muscle. Am. J. Physiol. Endocrinol. Metab. 293: 286–292 (2007)

    Article  Google Scholar 

  32. Egawa T, Hamada T, Ma X, Karaike K, Kameda N, Masuda S, Iwanaka N, Hayashi T. Caffeine activates preferentially a1-isoform of 5′AMP-activated protein kinase in rat skeletal muscle. Acta Physiol. 201: 227–238 (2011)

    Article  CAS  Google Scholar 

  33. Egawa T, Hamada T, Kameda N, Karaike K, Ma X, Masuda S, Iwanaka N, Hayashi T. Caffeine acutely activates 5′adenosine monophosphate-activated protein kinase and increases insulin-independent glucose transport in rat skeletal muscles. Metabolism 58: 1609–1617 (2009)

    Article  CAS  Google Scholar 

  34. Turner N, Li JY, Gosby A, To SW, Cheng Z, Miyoshi H, Taketo MM, Cooney GJ, Kraegen EW, James DE, Hu LH, Li J, Ye JM. Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: A mechanism for the action of berberine to activate AMP-activated protein kinase and improve insulin action. Diabetes 57: 1414–1418 (2008)

    Article  CAS  Google Scholar 

  35. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, Hohnen-Behrens C, Gosby A, Kraegen EW, James DE, Kim JB. Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55: 2256–2264 (2006)

    Article  CAS  Google Scholar 

  36. Brusq JM, Ancellin N, Grondin P, Guillard R, Martin S, Saintillan Y, Issandou M. Inhibition of lipid synthesis through activation of AMP kinase: An additional mechanism for the hypolipidemic effects of berberine. J. Lipid Res. 47: 1281–1288 (2006)

    Article  CAS  Google Scholar 

  37. Zheng J, Ramirez VD. Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. Br. J. Pharmacol. 130: 1115–1123 (2000)

    Article  CAS  Google Scholar 

  38. Hwang JT, Kwon DY, Yoon SH. AMP-activated protein kinase: A potential target for the diseases prevention by natural occurring polyphenols. N. Biotechnol. 26: 17–22 (2009)

    Article  CAS  Google Scholar 

  39. Murase T, Misawa K, Haramizu S, Hase T. Catechin-induced activation of the LKB1/AMP-activated protein kinase pathway. Biochem. Pharmacol. 78: 78–84 (2009)

    Article  CAS  Google Scholar 

  40. Lin CL, Lin JK. Epigallocatechin gallate (EGCG) attenuates high glucose-induced insulin signaling blockade in human hepG2 hepatoma cells. Mol. Nutr. Food Res. 52: 930–939 (2008)

    Article  CAS  Google Scholar 

  41. Moon HS, Chung CS, Lee HG, Kim TG, Choi YJ, Cho CS. Inhibitory effect of (-)-epigallocatechin-3-gallate on lipid accumulation of 3T3-L1 cells. Obesity 15: 2571–2582 (2007)

    Article  CAS  Google Scholar 

  42. Hwang JT, Park IJ, Shin JI, Lee YK, Lee SK, Baik HW, Ha J, Park OJ. Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 338: 694–699 (2005)

    Article  CAS  Google Scholar 

  43. Lu J, Wu DM, Zheng YL, Hu B, Zhang ZF, Shan Q, Zheng ZH, Liu CM, Wang YJ. Quercetin activates AMP-activated protein kinase by reducing PP2C expression protecting old mouse brain against high cholesterol-induced neurotoxicity. J. Pathol. 222: 199–212 (2010)

    Article  CAS  Google Scholar 

  44. Hawley SA, Selbert MA, Goldstein EG, Edelman AM, Carling D, Hardie DG. 5′-AMP activates the AMP-activated protein kinase cascade, and Ca2+/calmodulin activates the calmodulin-dependent protein kinase I cascade, via three independent mechanisms. J. Biol. Chem. 270: 27186–27191 (1995)

    Article  CAS  Google Scholar 

  45. Hawley SA, Ross FA, Chevtzoff C, Green KA, Evans A, Fogarty S, Towler MC, Brown LJ, Ogunbayo OA, Evans AM, Hardie DG. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab. 11: 554–565 (2010)

    Article  CAS  Google Scholar 

  46. Ahn J, Lee H, Kim S, Park J, Ha T. The anti-obesity effect of quercetin is mediated by the AMPK and MAPK signaling pathways. Biochem. Biophys. Res. Commun. 373: 545–549 (2008)

    Article  CAS  Google Scholar 

  47. Suchankova G, Nelson LE, Gerhart-Hines Z, Kelly M, Gauthier MS, Saha AK, Ido Y, Puigserver P, Ruderman NB. Concurrent regulation of AMP-activated protein kinase and SIRT1 in mammalian cells. Biochem. Biophys. Res. Commun. 378: 836–841 (2009)

    Article  CAS  Google Scholar 

  48. de Boer VC, de Goffau MC, Arts IC, Hollman PC, Keijer J. SIRT1 stimulation by polyphenols is affected by their stability and metabolism. Mech. Ageing Dev. 127: 618–627 (2006)

    Article  Google Scholar 

  49. Kaeberlein M, McDonagh T, Heltweg B, Hixon J, Westman EA, Caldwell SD, Napper A, Curtis R, DiStefano PS, Fields S, Bedalov A, Kennedy BK. Substratespecific activation of sirtuins by resveratrol. J. Biol. Chem. 280: 17038–17045 (2005)

    Article  CAS  Google Scholar 

  50. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191–196 (2003)

    Article  CAS  Google Scholar 

  51. Pacholec M, Bleasdale JE, Chrunyk B, Cunningham D, Flynn D, Garofalo RS, Griffith D, Griffor M, Loulakis P, Pabst B, Qiu X, Stockman B, Thanabal V, Varghese A, Ward J, Withka J, Ahn K. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J. Biol. Chem. 285: 8340–8351 (2010)

    Article  CAS  Google Scholar 

  52. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458: 1056–1060 (2009)

    Article  CAS  Google Scholar 

  53. Um JH, Park SJ, Kang H, Yang S, Foretz M, McBurney MW, Kim MK, Viollet B, Chung JH. AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59: 554–563 (2010)

    Article  CAS  Google Scholar 

  54. Miyamoto L, Watanabe M, Kono M, Matsushita T, Hattori H, Ishizawa K, Nemoto H, Tsuchiya K. Cytotoxicity evaluation of symmetrically branched glycerol trimer in human hepatocellular carcinoma HepG2 cells. J. Toxicol. Sci. 37: 1059–1063 (2012)

    Article  CAS  Google Scholar 

  55. Miyamoto L, Watanabe M, Taoka C, Kono M, Tomida Y, Matsushita T, Kamiya M, Hattori H, Ishizawa K, Abe S, Nemoto H, Tsuchiya K. A novel prodrug strategy for extremely hydrophobic agents: Conjugation to symmetrically branched glycerol trimer improves pharmacological and pharmacokinetic properties of fenofibrate. Mol. Pharmacol. 10: 2723–2729 (2013)

    Article  CAS  Google Scholar 

  56. Nemoto H, Katagiri A, Kamiya M, Kawamura T, Matsushita T, Matsumura K, Itou T, Hattori H, Tamaki M, Ishizawa K, Miyamoto L, Abe S, Tsuchiya K. Synthesis of paclitaxel-BGL conjugates. Bioorgan. Med. Chem. 20: 5559–5567 (2012)

    Article  CAS  Google Scholar 

  57. Miyamoto L, Watanabe M, Tomida Y, Kono M, Fujii S, Matsushita T, Hattori H, Ishizawa K, Nemoto H, Tsuchiya K. Acute oral toxicity evaluation of symmetrically branched glycerol trimer in ddY mice. J. Toxicol. Sci. 37: 1253–1259 (2012)

    Article  CAS  Google Scholar 

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  1. Laboratory of Pharmacology and Physiological Sciences, Frontier Laboratories for Pharmaceutical Sciences, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, Japan

    Licht Miyamoto

  2. Department of Medical Pharmacology, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, Japan

    Licht Miyamoto

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Miyamoto, L. Can food factors provide Us with the similar beneficial effects of physical exercise?. Food Sci Biotechnol 25 (Suppl 1), 9–13 (2016). https://doi.org/10.1007/s10068-016-0092-9

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