Advertisement

Sarcopenia in Diabetes Mellitus

  • Ken SugimotoEmail author
  • Chung-Chi Wang
  • Hiromi Rakugi
Chapter

Abstract

Sarcopenia is an age-related loss of skeletal muscle mass and strength. In this chapter, advances in the association of sarcopenia and diabetes mellitus are discussed. Falls in diabetic patients associate with decline of muscle mass or strength in the elderly. Insulin resistance impairs the protein regeneration in skeletal muscle and also induces the protein breakdown and muscle wasting, leading to development of sarcopenia. This insulin resistance suggests the most important linkage between sarcopenia and diabetes. Sarcopenia and obesity appear to have additive effects on insulin resistance and age-related changes in body composition. Loss of skeletal muscle mass affecting glucose disposal and impaired energy homeostasis affecting muscle protein content, together, might lead to a vicious cycle. Insulin resistance and inflammation leads to muscle wasting through the pathways involved in Akt/PKB, FoxOs, PGC-1α, and AMPK. The accumulation of AGEs through glucose intolerance enhanced by mitochondrial ROS with promotion of apoptosis leads to the development of muscle wasting. Exercise is known as the most efficient treatment of sarcopenia with diabetes but less information is known for nutritional replenishment or medications. Sarcopenia in diabetes mellitus would have higher physical dysfunction and mortality risks than those in nondiabetic older adults.

Keywords

Sarcopenia Diabetes mellitus Obesity Insulin resistance AGEs 

References

  1. 1.
    United Nations (2007) World population prospects, the 2006 revision: highlights. United Nations, New YorkGoogle Scholar
  2. 2.
    Smalley KJ, Knerr AN, Kendrick ZV, Colliver JA, Owen OE (1990) Reassessment of body-mass indexes. Am J Clin Nutr 52(3):405–408PubMedGoogle Scholar
  3. 3.
    Dutta C, Hadley EC, Lexell J (1997) Sarcopenia and physical performance in old age: overview. Muscle Nerve 5:S5–S9PubMedCrossRefGoogle Scholar
  4. 4.
    Kinney JM (2004) Nutritional frailty, sarcopenia and falls in the elderly. Curr Opin Clin Nutr Metab Care 7(1):15–20. doi: 10.1097/01.mco.0000109601.04238.46 PubMedCrossRefGoogle Scholar
  5. 5.
    Berger MJ, Doherty TJ (2010) Sarcopenia: prevalence, mechanisms, and functional consequences. Interdiscip Top Gerontol 37:94–114. doi: 10.1159/000319997 PubMedCrossRefGoogle Scholar
  6. 6.
    Villareal DT, Banks M, Siener C, Sinacore DR, Klein S (2004) Physical frailty and body composition in obese elderly men and women. Obes Res 12(6):913–920. doi: 10.1038/oby.2004.111 PubMedCrossRefGoogle Scholar
  7. 7.
    Goodman MN, Ruderman NB (1979) Insulin sensitivity of rat skeletal muscle: effects of starvation and aging. Am J Physiol 236(5):E519–E523PubMedGoogle Scholar
  8. 8.
    Sial S, Coggan AR, Carroll R, Goodwin J, Klein S (1996) Fat and carbohydrate metabolism during exercise in elderly and young subjects. Am J Physiol-Endocrinol Metab 271(6):E983–E989Google Scholar
  9. 9.
    Dardevet D, Sornet C, Balage M, Grizard J (2000) Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age. J Nutr 130(11):2630–2635PubMedGoogle Scholar
  10. 10.
    Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ et al (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378(9785):31–40. doi: 10.1016/s0140-6736(11)60679-x PubMedCrossRefGoogle Scholar
  11. 11.
    Styskal J, Van Remmen H, Richardson A, Salmon AB (2012) Oxidative stress and diabetes: what can we learn about insulin resistance from antioxidant mutant mouse models? Free Radic Biol Med 52(1):46–58. doi: 10.1016/j.freeradbiomed.2011.10.441 PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Laaksonen DE, Niskanen L, Lakka HM, Lakka TA, Uusitupa M (2004) Epidemiology and treatment of the metabolic syndrome. Ann Med 36(5):332–346. doi: 10.1080/07853890410031849 PubMedCrossRefGoogle Scholar
  13. 13.
    Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L (2008) Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care 11(6):693–700. doi: 10.1097/MCO.0b013e328312c37d PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Gillespie LD, Gillespie WJ, Robertson MC, Lamb SE, Cumming RG, Rowe BH (2003) Interventions for preventing falls in elderly people. Cochrane Database Syst Rev (4):Cd000340. doi:  10.1002/14651858.cd000340
  15. 15.
    Marzetti E, Leeuwenburgh C (2006) Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol 41(12):1234–1238. doi: 10.1016/j.exger.2006.08.011 PubMedCrossRefGoogle Scholar
  16. 16.
    Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol Ser A-Biol Sci Med Sci 61(10):1059–1064CrossRefGoogle Scholar
  17. 17.
    Leenders M, Verdijk LB, van der Hoeven L, Adam JJ, van Kranenburg J, Nilwik R et al (2013) Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 14(8):585–592. doi: 10.1016/j.jamda.2013.02.006 PubMedCrossRefGoogle Scholar
  18. 18.
    Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C et al (2007) Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 30(6):1507–1512. doi: 10.2337/dc06-2537 PubMedCrossRefGoogle Scholar
  19. 19.
    Corcoran MP, Lamon-Fava S, Fielding RA (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr 85(3):662–677PubMedGoogle Scholar
  20. 20.
    Russell ST, Rajani S, Dhadda RS, Tisdale MJ (2009) Mechanism of induction of muscle protein loss by hyperglycaemia. Exp Cell Res 315(1):16–25. doi: 10.1016/j.yexcr.2008.10.002 PubMedCrossRefGoogle Scholar
  21. 21.
    Lim S, Kim JH, Yoon JW, Kang SM, Choi SH, Park YJ et al (2010) Sarcopenic obesity: prevalence and association with metabolic syndrome in the Korean Longitudinal Study on Health and Aging (KLoSHA). Diabetes Care 33(7):1652–1654. doi: 10.2337/dc10-0107 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Srikanthan P, Hevener AL, Karlamangla AS (2010) Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One 5(5):e10805. doi: 10.1371/journal.pone.0010805 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    de Simone G, Pasanisi F, Ferrara AL, Roman MJ, Lee ET, Contaldo F et al (2013) Relative fat-free mass deficiency and left ventricular adaptation to obesity: the strong heart study. Int J Cardiol 168(2):729–733. doi: 10.1016/j.ijcard.2012.09.055 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Grimby G (1995) Muscle performance and structure in the elderly as studied cross-sectionally and longitudinally. J Gerontol A Biol Sci Med Sci 50(Spec No):17–22PubMedGoogle Scholar
  25. 25.
    Blough ER, Linderman JK (2000) Lack of skeletal muscle hypertrophy in very aged male Fischer 344 x Brown Norway rats. J Appl Physiol (Bethesda, Md: 1985) 88(4):1265–1270Google Scholar
  26. 26.
    Holloszy JO, Chen M, Cartee GD, Young JC (1991) Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech Ageing Dev 60(2):199–213PubMedCrossRefGoogle Scholar
  27. 27.
    Porter MM, Vandervoort AA, Lexell J (1995) Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports 5(3):129–142PubMedCrossRefGoogle Scholar
  28. 28.
    Lillioja S, Young AA, Culter CL, Ivy JL, Abbott WG, Zawadzki JK et al (1987) Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80(2):415–424. doi: 10.1172/jci113088 PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Ohlendieck K (2011) Skeletal muscle proteomics: current approaches, technical challenges and emerging techniques. Skelet Muscle 1(1):6. doi: 10.1186/2044-5040-1-6 PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Pedersen BK (2010) Muscle-to-fat interaction: a two-way street? J Physiol 588(Pt 1):21. doi: 10.1113/jphysiol.2009.184747 PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Briaud I, Lingohr MK, Dickson LM, Wrede CE, Rhodes CJ (2003) Differential activation mechanisms of Erk-1/2 and p70(S6K) by glucose in pancreatic beta-cells. Diabetes 52(4):974–983PubMedCrossRefGoogle Scholar
  32. 32.
    Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, Pedersen BK (2005) Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54(10):2939–2945PubMedCrossRefGoogle Scholar
  33. 33.
    Mikkelsen HB (2010) Interstitial cells of Cajal, macrophages and mast cells in the gut musculature: morphology, distribution, spatial and possible functional interactions. J Cell Mol Med 14(4):818–832. doi: 10.1111/j.1582-4934.2010.01025.x PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Yeh WC, Shahinian A, Speiser D, Kraunus J, Billia F, Wakeham A et al (1997) Early lethality, functional NF-kappaB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7(5):715–725PubMedCrossRefGoogle Scholar
  35. 35.
    Benito M (2011) Tissue specificity on insulin action and resistance: past to recent mechanisms. Acta Physiol 201(3):297–312. doi: 10.1111/j.1748-1716.2010.02201.x CrossRefGoogle Scholar
  36. 36.
    Yu H, Jove R (2004) The STATs of cancer – new molecular targets come of age. Nat Rev Cancer 4(2):97–105. doi: 10.1038/nrc1275 PubMedCrossRefGoogle Scholar
  37. 37.
    Boulton TG, Zhong Z, Wen Z, Darnell JE Jr, Stahl N, Yancopoulos GD (1995) STAT3 activation by cytokines utilizing gp130 and related transducers involves a secondary modification requiring an H7-sensitive kinase. Proc Natl Acad Sci U S A 92(15):6915–6919PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Penner G, Gang G, Sun X, Wray C, Hasselgren PO (2002) C/EBP DNA-binding activity is upregulated by a glucocorticoid-dependent mechanism in septic muscle. Am J Physiol Regul Integr Comp Physiol 282(2):R439–R444. doi: 10.1152/ajpregu.00512.2001 PubMedCrossRefGoogle Scholar
  39. 39.
    Toledo M, Busquets S, Ametller E, Lopez-Soriano FJ, Argiles JM (2011) Sirtuin 1 in skeletal muscle of cachectic tumour-bearing rats: a role in impaired regeneration? J Cachex Sarcopenia Muscle 2(1):57–62. doi: 10.1007/s13539-011-0018-6 CrossRefGoogle Scholar
  40. 40.
    Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280(5):E745–E751PubMedGoogle Scholar
  41. 41.
    Marzetti E, Carter CS, Wohlgemuth SE, Lees HA, Giovannini S, Anderson B et al (2009) Changes in IL-15 expression and death-receptor apoptotic signaling in rat gastrocnemius muscle with aging and life-long calorie restriction. Mech Ageing Dev 130(4):272–280PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Pedersen BK, Steensberg A, Keller P, Keller C, Fischer C, Hiscock N et al (2003) Muscle-derived interleukin-6: lipolytic, anti-inflammatory and immune regulatory effects. Pflugers Arch: Eur J Physiol 446(1):9–16. doi: 10.1007/s00424-002-0981-z CrossRefGoogle Scholar
  43. 43.
    Rui L, Yuan M, Frantz D, Shoelson S, White MF (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 277(44):42394–42398. doi: 10.1074/jbc.C200444200 PubMedCrossRefGoogle Scholar
  44. 44.
    Huang L, Gong L, Jiang X, Xing D (2014) Photoactivation of GLUT4 translocation promotes glucose uptake via PI3-K/Akt2 signaling in 3T3-L1 adipocytes. J Innov Opt Health Sci 7(3):1–10. doi:  10.1142/s1793545813500673
  45. 45.
    Hajduch E, Alessi DR, Hemmings BA, Hundal HS (1998) Constitutive activation of protein kinase B alpha by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47(7):1006–1013PubMedCrossRefGoogle Scholar
  46. 46.
    Andreozzi F, Procopio C, Greco A, Mannino GC, Miele C, Raciti GA et al (2011) Increased levels of the Akt-specific phosphatase PH domain leucine-rich repeat protein phosphatase (PHLPP)-1 in obese participants are associated with insulin resistance. Diabetologia 54(7):1879–1887. doi: 10.1007/s00125-011-2116-6 PubMedCrossRefGoogle Scholar
  47. 47.
    Inoki K, Li Y, Zhu T, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4(9):648–657. doi: 10.1038/ncb839 PubMedCrossRefGoogle Scholar
  48. 48.
    Nader GA (2007) Muscle growth learns new tricks from an old dog. Nat Med 13(9):1016–1018. doi: 10.1038/nm0907-1016 PubMedCrossRefGoogle Scholar
  49. 49.
    Sandri M (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23:160–170. doi: 10.1152/physiol.00041.2007 CrossRefGoogle Scholar
  50. 50.
    van der Velden JL, Langen RC, Kelders MC, Willems J, Wouters EF, Janssen-Heininger YM et al (2007) Myogenic differentiation during regrowth of atrophied skeletal muscle is associated with inactivation of GSK-3beta. Am J Physiol Cell Physiol 292(5):C1636–C1644. doi: 10.1152/ajpcell.00504.2006 PubMedCrossRefGoogle Scholar
  51. 51.
    Welch AA (2014) The 5th international symposium of the nutrition society nutritional influences on age-related skeletal muscle loss. Proc Nutr Soc 73(1):16–33. doi: 10.1017/s0029665113003698 PubMedCrossRefGoogle Scholar
  52. 52.
    Furuyama T, Kitayama K, Yamashita H, Mori N (2003) Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375(Pt 2):365–371. doi: 10.1042/bj20030022 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T et al (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279(39):41114–41123. doi: 10.1074/jbc.M400674200 PubMedCrossRefGoogle Scholar
  54. 54.
    Irwin ML, Yasui Y, Ulrich CM, Bowen D, Rudolph RE, Schwartz RS et al (2003) Effect of exercise on total and intra-abdominal body fat in postmenopausal women: a randomized controlled trial. JAMA 289(3):323–330PubMedCrossRefGoogle Scholar
  55. 55.
    McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, Esser KA (2009) FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am J Physiol Cell Physiol 297(3):C548–C555. doi: 10.1152/ajpcell.00502.2008 PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Cleasby ME, Jarmin S, Eilers W, Elashry M, Andersen DK, Dickson G et al (2014) Local overexpression of the myostatin propeptide increases glucose transporter expression and enhances skeletal muscle glucose disposal. Am J Physiol-Endocrinol Metab 306(7):E814–E823. doi: 10.1152/ajpendo.00586.2013 PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Henagan TM, Lenard NR, Gettys TW, Stewart LK (2014) Dietary quercetin supplementation in mice increases skeletal muscle PGC1 alpha expression, improves mitochondrial function and attenuates insulin resistance in a time-specific manner. Plos One 9(2):1–11. doi:  10.1371/journal.pone.0089365
  58. 58.
    Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34(3):267–273. doi: 10.1038/ng1180 PubMedCrossRefGoogle Scholar
  59. 59.
    Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S et al (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 100(14):8466–8471. doi: 10.1073/pnas.1032913100 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Crunkhorn S, Dearie F, Mantzoros C, Gami H, da Silva WS, Espinoza D et al (2007) Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J Biol Chem 282(21):15439–15450. doi: 10.1074/jbc.M611214200 PubMedCrossRefGoogle Scholar
  61. 61.
    Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA et al (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54(7):1926–1933PubMedCrossRefGoogle Scholar
  62. 62.
    Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O et al (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899):797–801. doi: 10.1038/nature00904 PubMedCrossRefGoogle Scholar
  63. 63.
    Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC et al (2012) A PGC-1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151(6):1319–1331. doi: 10.1016/j.cell.2012.10.050 PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Steinberg GR, Kemp BE (2009) AMPK in health and disease. Physiol Rev 89(3):1025–1078. doi: 10.1152/physrev.00011.2008 PubMedCrossRefGoogle Scholar
  65. 65.
    Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E et al (2005) Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 7(3):286–294. doi: 10.1038/ncb1231 PubMedCrossRefGoogle Scholar
  66. 66.
    Pehmoller C, Treebak JT, Birk JB, Chen S, Mackintosh C, Hardie DG et al (2009) Genetic disruption of AMPK signaling abolishes both contraction- and insulin-stimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am J Physiol Endocrinol Metab 297(3):E665–E675. doi: 10.1152/ajpendo.00115.2009 PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H et al (2012) AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 113(2):695–710. doi: 10.1002/jcb.23399 PubMedCrossRefGoogle Scholar
  68. 68.
    Tong JF, Yan X, Zhu MJ, Du M (2009) AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes. J Cell Biochem 108(2):458–468. doi: 10.1002/jcb.22272 PubMedCrossRefGoogle Scholar
  69. 69.
    Nakashima K, Yakabe Y (2007) AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71(7):1650–1656PubMedCrossRefGoogle Scholar
  70. 70.
    Birkenfeld AL, Lee HY, Guebre-Egziabher F, Alves TC, Jurczak MJ, Jornayvaz FR et al (2011) Deletion of the mammalian INDY homolog mimics aspects of dietary restriction and protects against adiposity and insulin resistance in mice. Cell Metab 14(2):184–195. doi: 10.1016/j.cmet.2011.06.009 PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Jager S, Handschin C, St-Pierre J, Spiegelman BM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 104(29):12017–12022. doi: 10.1073/pnas.0705070104 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Whaley-Connell A, McCullough PA, Sowers JR (2011) The role of oxidative stress in the metabolic syndrome. Rev Cardiovasc Med 12(1):21–29. doi: 10.3909/ricm0555 PubMedGoogle Scholar
  73. 73.
    Rooyackers OE, Adey DB, Ades PA, Nair KS (1996) Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc Natl Acad Sci U S A 93(26):15364–15369PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    de Cavanagh EMV, Inserra F, Ferder L (2011) Angiotensin II blockade: a strategy to slow ageing by protecting mitochondria? Cardiovasc Res 89(1):31–40. doi: 10.1093/cvr/cvq285 PubMedCrossRefGoogle Scholar
  75. 75.
    Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG et al (2004) IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 119(2):285–298. doi: 10.1016/j.cell.2004.09.027 PubMedCrossRefGoogle Scholar
  76. 76.
    Nicolson GL, Ash ME (2014) Lipid replacement therapy: a natural medicine approach to replacing damaged lipids in cellular membranes and organelles and restoring function. Biochim Biophys Acta Biomemb 1838(6):1657–1679. doi: 10.1016/j.bbamem.2013.11.010 CrossRefGoogle Scholar
  77. 77.
    Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL et al (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause charcot-marie-tooth neuropathy type 2A. Nat Genet 36(5):449–451. doi: 10.1038/ng1341 PubMedCrossRefGoogle Scholar
  78. 78.
    Thorpe SR, Baynes JW (2003) Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 25(3–4):275–281. doi: 10.1007/s00726-003-0017-9 PubMedCrossRefGoogle Scholar
  79. 79.
    Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS et al (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269(13):9889–9897PubMedGoogle Scholar
  80. 80.
    Teshima Y, Takahashi N, Nishio S, Saito S, Kondo H, Fukui A et al (2014) Production of reactive oxygen species in the diabetic heart – roles of mitochondria and NADPH oxidase. Circ J 78(2):300–306. doi: 10.1253/circj.CJ-13-1187 PubMedCrossRefGoogle Scholar
  81. 81.
    Van Puyvelde K, Mets T, Njemini R, Beyer I, Bautmans I (2014) Effect of advanced glycation end product intake on inflammation and aging: a systematic review. Nutr Rev 72(10):638–650. doi: 10.1111/nure.12141 PubMedCrossRefGoogle Scholar
  82. 82.
    Snow LM, Thompson LV (2009) Influence of insulin and muscle fiber type in nepsilon-(carboxymethyl)-lysine accumulation in soleus muscle of rats with streptozotocin-induced diabetes mellitus. Pathobiology J Immunopathol Mol Cell Biol 76(5):227–234. doi: 10.1159/000228898 CrossRefGoogle Scholar
  83. 83.
    Alves M, Calegari VC, Cunha DA, Saad MJ, Velloso LA, Rocha EM (2005) Increased expression of advanced glycation end-products and their receptor, and activation of nuclear factor kappa-B in lacrimal glands of diabetic rats. Diabetologia 48(12):2675–2681. doi: 10.1007/s00125-005-0010-9 PubMedCrossRefGoogle Scholar
  84. 84.
    Thornalley PJ (2005) Dicarbonyl intermediates in the maillard reaction. Ann N Y Acad Sci 1043:111–117. doi: 10.1196/annals.1333.014 PubMedCrossRefGoogle Scholar
  85. 85.
    Stadtman ER (2006) Protein oxidation and aging. Free Radic Res 40(12):1250–1258. doi: 10.1080/10715760600918142 PubMedCrossRefGoogle Scholar
  86. 86.
    Dhar A, Desai KM, Wu L (2010) Alagebrium attenuates acute methylglyoxal-induced glucose intolerance in Sprague-Dawley rats. Br J Pharmacol 159(1):166–175. doi: 10.1111/j.1476-5381.2009.00469.x PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Falone S, D’Alessandro A, Mirabilio A, Petruccelli G, Cacchio M, Di Ilio C et al (2012) Long term running biphasically improves methylglyoxal-related metabolism, redox homeostasis and neurotrophic support within adult mouse brain cortex. PLoS One 7(2):e31401. doi: 10.1371/journal.pone.0031401 PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Tanaka K, Kanazawa I, Yamaguchi T, Yano S, Kaji H, Sugimoto T (2014) Active vitamin D possesses beneficial effects on the interaction between muscle and bone. Biochem Biophys Res Commun 450(1):482–487. doi: 10.1016/j.bbrc.2014.05.145 PubMedCrossRefGoogle Scholar
  89. 89.
    Brownlee M (1995) The pathological implications of protein glycation. Clin Invest Med Clin Exp 18(4):275–281Google Scholar
  90. 90.
    Andersen H (2012) Motor dysfunction in diabetes. Diabetes Metab Res Rev 28:89–92. doi: 10.1002/dmrr.2257 PubMedCrossRefGoogle Scholar
  91. 91.
    El-Mesallamy HO, Hamdy NM, Ezzat OA, Reda AM (2011) Levels of soluble advanced glycation end product-receptors and other soluble serum markers as indicators of diabetic neuropathy in the foot. J Invest Med 59(8):1233–1238. doi: 10.231/JIM.0b013e318231db64 Google Scholar
  92. 92.
    Kim HK, Suzuki T, Saito K, Yoshida H, Kobayashi H, Kato H et al (2012) Effects of exercise and amino acid supplementation on body composition and physical function in community-dwelling elderly Japanese sarcopenic women: a randomized controlled trial. J Am Geriatr Soc 60(1):16–23. doi: 10.1111/j.1532-5415.2011.03776.x PubMedCrossRefGoogle Scholar
  93. 93.
    Castaneda C, Layne JE, Munoz-Orians L, Gordon PL, Walsmith J, Foldvari M et al (2002) A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care 25(12):2335–2341PubMedCrossRefGoogle Scholar
  94. 94.
    Lessard SJ, Chen ZP, Watt MJ, Hashem M, Reid JJ, Febbraio MA et al (2006) Chronic rosiglitazone treatment restores AMPKalpha2 activity in insulin-resistant rat skeletal muscle. Am J Physiol Endocrinol Metab 290(2):E251–E257. doi: 10.1152/ajpendo.00096.2005 PubMedCrossRefGoogle Scholar
  95. 95.
    Feinstein DL, Spagnolo A, Akar C, Weinberg G, Murphy P, Gavrilyuk V et al (2005) Receptor-independent actions of PPAR thiazolidinedione agonists: is mitochondrial function the key? Biochem Pharmacol 70(2):177–188. doi: 10.1016/j.bcp.2005.03.033 PubMedCrossRefGoogle Scholar
  96. 96.
    Miyazaki Y, He H, Mandarino LJ, DeFronzo RA (2003) Rosiglitazone improves downstream insulin receptor signaling in type 2 diabetic patients. Diabetes 52(8):1943–1950PubMedCrossRefGoogle Scholar
  97. 97.
    Bajaj M, Baig R, Suraamornkul S, Hardies LJ, Coletta DK, Cline GW et al (2010) Effects of pioglitazone on intramyocellular fat metabolism in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 95(4):1916–1923. doi: 10.1210/jc.2009-0911 PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Colca JR, Feinstein DL (2012) Altering mitochondrial dysfunction as an approach to treating Alzheimer’s disease. Adv Pharmacol 64:155–176. doi: 10.1016/b978-0-12-394816-8.00005-2, San Diego, CalifPubMedCrossRefGoogle Scholar
  99. 99.
    Marsh AP, Shea MK, Vance Locke RM, Miller ME, Isom S, Miller GD et al (2013) Resistance training and pioglitazone lead to improvements in muscle power during voluntary weight loss in older adults. J Gerontol A Biol Sci Med Sci 68(7):828–836. doi: 10.1093/gerona/gls258 PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Owen MR, Doran E, Halestrap AP (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 348(Pt 3):607–614PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  1. 1.Geriatric MedicineOsaka University Graduate School of MedicineSuitaJapan

Personalised recommendations