Advertisement

Muscle endocrinology and its relation with nutrition

  • Cecilia Romagnoli
  • Barbara Pampaloni
  • Maria Luisa BrandiEmail author
Review Article

Abstract

Recent years have demonstrated clear evidence that skeletal muscle is an active endocrine organ. During contraction of muscle fibers, the skeletal muscle produces and releases, into the blood stream, cytokines and other peptides, called myokines, thanks to which it can both communicate with cells locally within the muscle, in an autocrine and paracrine fashion, or with other distant tissues, exerting its endocrine effects. With the progress of sophisticated technologies, the interest towards the skeletal muscle secretome is rapidly grown and the discovery of new myokines represents a prolific field for the identification of new pharmacological approaches for the management and treatment of many clinical diseases. Considering the importance of the muscle proteome and the cross-talk with other organs, the preservation of a skeletal muscle in good health represents a fundamental aspect in life, especially in ageing. Sarcopenia is the age-dependent loss of skeletal muscle mass and strength, bringing to increases of the risk of adverse outcomes, such as physical disability and poor quality of life, as well as alteration of several hormonal networks. For that reasons, the scientific community has risen its interest to find new interventions to prevent and manage the sarcopenia. Adequate nutrition during ages plays a fundamental role in the health and function of the skeletal muscle and it can represents, alone or in combination with physical exercise, a possible preventive measure against sarcopenia. This review will overview the endocrinology of the skeletal muscle, making a focus on food intake as a strategy for preventing skeletal muscle decay.

Keywords

Skeletal muscle endocrinology Myokine Protein intake Nutrition Sarcopenia 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Statement of human and animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study, informed consent is not required.

References

  1. 1.
    Pedersen BK (2013) Muscle as a secretory organ. Compr Physiol 3:1337–1362.  https://doi.org/10.1002/cphy.c120033 Google Scholar
  2. 2.
    Pedersen I, Hojman P (2012) Muscle-to-organ cross talk mediated by myokines. Adipocyte 1:164–167.  https://doi.org/10.4161/adip.20344 CrossRefGoogle Scholar
  3. 3.
    Marzetti E, Calvani R, Tosato M et al (2017) Sarcopenia: an overview. Aging Clin Exp Res 29:11–17.  https://doi.org/10.1007/s40520-016-0704-5 CrossRefGoogle Scholar
  4. 4.
    Goldstein MS (1961) Humoral nature of the hypoglycemic factor of muscular work. Diabetes 10:232–234.  https://doi.org/10.2337/diab.10.3.232 CrossRefGoogle Scholar
  5. 5.
    Ostrowski K, Rohde T, Zacho M et al (1998) Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J Physiol 508:949–953.  https://doi.org/10.1111/j.1469-7793.1998.949bp.x CrossRefGoogle Scholar
  6. 6.
    Steensberg A, van Hall G, Osada T et al (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529:237–242.  https://doi.org/10.1111/j.1469-7793.2000.00237.x CrossRefGoogle Scholar
  7. 7.
    Bruunsgaard H, Galbo H, Halkjaer-Kristensen J et al (1997) Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol 499:833–841CrossRefGoogle Scholar
  8. 8.
    Pedersen B, Steensberg A, Fischer C et al (2003) Searching for the exercise factor: is IL-6 a candidate? J Muscle Res Cell Motil 24:113–119CrossRefGoogle Scholar
  9. 9.
    Fischer CP (2006) Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev 12:6–33Google Scholar
  10. 10.
    MacIntyre D, Sorichter S, Mair J et al (2001) Markers of inflammation and myofibrillar proteins following eccentric exercise in humans. Eur J Appl Physiol 84:180–186.  https://doi.org/10.1007/s004210170002 CrossRefGoogle Scholar
  11. 11.
    Weigert C, Hennige A, Brodbeck K et al (2005) Interleukin-6 acts as insulin sensitizer on glycogen synthesis in human skeletal muscle cells by phosphorylation of Ser473 of Akt. Am J Physiol Endocrinol Metab 289:E251–E257.  https://doi.org/10.1152/ajpendo.00448.2004 CrossRefGoogle Scholar
  12. 12.
    Glund S, Deshmukh A, Long Y et al (2007) Interleukin-6 directly increases glucose metabolism in resting human skeletal muscle. Diabetes 56:1630–1637.  https://doi.org/10.2337/db06-1733 CrossRefGoogle Scholar
  13. 13.
    Carey A, Steinberg G, Macaulay S et al (2006) Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 55:2688–2697.  https://doi.org/10.2337/db05-1404 CrossRefGoogle Scholar
  14. 14.
    Pedersen B, Akerström T, Nielsen A et al (2007) Role of myokines in exercise and metabolism. J Appl Physiol 103:1093–1098.  https://doi.org/10.1152/japplphysiol.00080.2007 CrossRefGoogle Scholar
  15. 15.
    So B, Kim H, Kim J et al (2014) Exercise-induced myokines in health and metabolic diseases. Integr Med Res 3:172–179.  https://doi.org/10.1016/j.imr.2014.09.007 CrossRefGoogle Scholar
  16. 16.
    Jy H (2018) The role of exercise-induced myokines in regulating metabolism. Arch Pharm Res 41:14–29.  https://doi.org/10.1007/s12272-017-0994-y CrossRefGoogle Scholar
  17. 17.
    X’avia Chan C, McDermott J, Siu K (2011) Secretome analysis of skeletal myogenesis using SILAC and shotgun proteomics. Int J Proteom 32:7.  https://doi.org/10.1155/2011/329467 Google Scholar
  18. 18.
    X’avia Chan C, Masui O, Krakovska O et al (2011) Identification of differentially regulated secretome components during skeletal myogenesis. Mol Cell Proteom 10:M110.004804.  https://doi.org/10.1074/mcp.m110.004804 CrossRefGoogle Scholar
  19. 19.
    Yoon J, Kim J, Song P et al (2012) Secretomics for skeletal muscle cells: a discovery of novel regulators? Adv Biol Regul 52:340–350.  https://doi.org/10.1016/j.jbior.2012.03.001 CrossRefGoogle Scholar
  20. 20.
    Ohlendieck K (2013) Proteomic identification of biomarkers of skeletal muscle disorders. Biomark Med 7:169–186.  https://doi.org/10.2217/bmm.12.96 CrossRefGoogle Scholar
  21. 21.
    Brown K, Formolo C, Seol H et al (2012) Advances in the proteomic investigation of the cell secretome. Expert Rev Proteom 9:337–345.  https://doi.org/10.1586/epr.12.21 CrossRefGoogle Scholar
  22. 22.
    Yoon J, Song P, Jang J et al (2009) Comparative proteomic analysis of the insulin-induced L6 myotube secretome. Proteomics 10:5315–5325.  https://doi.org/10.1021/pr200573b Google Scholar
  23. 23.
    Hartwig S, Raschke S, Knebel B et al (1844) (2913) Secretome profiling of primary human skeletal muscle cells. Biochim Biophys Acta 5:1011–1017.  https://doi.org/10.1016/j.bbapap.2013.08.004 Google Scholar
  24. 24.
    Henningsen J, Rigbolt K, Blagoev B et al (2010) Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol Cell Proteom 9:2482–2496.  https://doi.org/10.1074/mcp.M110.002113 CrossRefGoogle Scholar
  25. 25.
    Deshmukh A, Cox J, Jensen L et al (2015) Secretome analysis of lipid-induced insulin resistance in skeletal muscle cells by a combined experimental and bioinformatics workflow. J Proteome Res 14:4885–4895.  https://doi.org/10.1021/acs.jproteome.5b00720 CrossRefGoogle Scholar
  26. 26.
    Grube L, Dellen R, Kruse F et al (2018) Mining the secretome of C2C12 muscle cells: data dependent experimental approach to analyze protein secretion using label-free quantification and peptide based analysis. J Proteome Res 17:879–890.  https://doi.org/10.1021/acs.jproteome.7b00684 CrossRefGoogle Scholar
  27. 27.
    Raschke S, Eckardt K, Bjørklund Holven K et al (2013) Identification and validation of novel contraction-regulated myokines released from primary human skeletal muscle cells. PLoS One 8:e62008.  https://doi.org/10.1371/journal.pone.0062008 CrossRefGoogle Scholar
  28. 28.
    Norheim F, Raastad T, Thiede B et al (2011) Proteomic identification of secreted proteins from human skeletal muscle cells and expression in response to strength training. Am J Physiol Endocrinol Metab 301:E1013–E1021.  https://doi.org/10.1152/ajpendo.00326.2011 CrossRefGoogle Scholar
  29. 29.
    Pourteymour S, Eckardt K, Holen T et al (2017) Global mRNA sequencing of human skeletal muscle: search for novel exercise-regulated myokines. Mol Metab 6:352–365.  https://doi.org/10.1016/j.molmet.2017.01.007 CrossRefGoogle Scholar
  30. 30.
    McPherron A, Lawler A, Lee S (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90.  https://doi.org/10.1038/387083a0 CrossRefGoogle Scholar
  31. 31.
    Rodgers B, Garikipati D (2008) Clinical, agricultural, and evolutionary biology of myostatin: a comparative review. Endocr Rev 29:513–534.  https://doi.org/10.1210/er.2008-0003 CrossRefGoogle Scholar
  32. 32.
    Hansen J, Brandt C, Nielsen A et al (2011) Exercise induces a marked increase in plasma follistatin: evidence that follistatin is a contraction-induced hepatokine. Endocrinology 152:164–171.  https://doi.org/10.1210/en.2010-0868 CrossRefGoogle Scholar
  33. 33.
    Pedersen B (2012) «Muscular interleukin-6 and its role as an energy sensor. Med Sci Sports Exerc 44:392–396.  https://doi.org/10.1249/MSS.0b013e31822f94ac CrossRefGoogle Scholar
  34. 34.
    Pedersen B, Febbraio M (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88:1379–1406.  https://doi.org/10.1152/physrev.90100.2007 CrossRefGoogle Scholar
  35. 35.
    Quinn L, Anderson B, Strait-Bodey L et al (2009) Oversecretion of interleukin-15 from skeletal muscle reduces adiposity. Am J Physiol Endocrinol Metab 296:E191–E202.  https://doi.org/10.1152/ajpendo.90506.2008 CrossRefGoogle Scholar
  36. 36.
    Allen T, Whitham M, Febbraio M (2012) IL-6 muscles in on the gut and pancreas to enhance insulin secretion. Cell Metab 15:8–9.  https://doi.org/10.1016/j.cmet.2011.12.004 CrossRefGoogle Scholar
  37. 37.
    Boström P, Wu J, Jedrychowski M et al (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–468.  https://doi.org/10.1038/nature10777 CrossRefGoogle Scholar
  38. 38.
    Jeremic N, Chaturvedi P, Tyagi S (2017) Browning of white fat: novel insight into factors, mechanisms, and therapeutics. J Cell Physiol 232:61–68.  https://doi.org/10.1002/jcp.25450 CrossRefGoogle Scholar
  39. 39.
    Colaianni G, Cuscito C, Mongelli T et al (2014) Irisin enhances osteoblast differentiation in vitro. Int J Endocrinol 2014:902186.  https://doi.org/10.1155/2014/902186 CrossRefGoogle Scholar
  40. 40.
    Colaianni G, Cuscito C, Mongelli T et al (2015) The myokine irisin increases cortical bone mass. Proc Natl Acad Sci USA 112:E5763.  https://doi.org/10.1073/pnas CrossRefGoogle Scholar
  41. 41.
    Hamrick M (2012) The skeletal muscle secretome: an emerging player in muscle-bone crosstalk. Bonekey Rep 1:60.  https://doi.org/10.1038/bonekey.2012.60 CrossRefGoogle Scholar
  42. 42.
    Wei K, Serpooshan V, Hurtado C et al (2015) Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature 525:479–485.  https://doi.org/10.1038/nature15372 CrossRefGoogle Scholar
  43. 43.
    Ouchi N, Oshima Y, Ohashi K et al (2008) Follistatin-like 1, a secreted muscle protein, promotes endothelial cell function and revascularization in ischemic tissue through a nitric-oxide synthase-dependent mechanism. J Biol Chem 283:32802–32811.  https://doi.org/10.1074/jbc.M803440200 CrossRefGoogle Scholar
  44. 44.
    McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94:12457–12461.  https://doi.org/10.1073/pnas.94.23.12457 CrossRefGoogle Scholar
  45. 45.
    White TA, LeBrasseur NK (2014) Myostatin and sarcopenia: opportunities and challenges—a mini-review. Gerontology 60:289–293.  https://doi.org/10.1159/000356740 CrossRefGoogle Scholar
  46. 46.
    Trendelenburg AU, Meyer A, Rohner D et al (2009) Myostatin reduces Akt/TORC1/p70S6 K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296:C1258–C1270.  https://doi.org/10.1152/ajpcell.00105.2009 CrossRefGoogle Scholar
  47. 47.
    Schuelke M, Wagner KR, Stolz LE et al (2004) Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350:2682–2688.  https://doi.org/10.1056/NEJMoa040933 CrossRefGoogle Scholar
  48. 48.
    Mosher DS, Quignon P, Bustamante CD et al (2007) A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 3:e79.  https://doi.org/10.1371/journal.pgen.0030079 CrossRefGoogle Scholar
  49. 49.
    Clop A, Marcq F, Takeda H et al (2006) A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38:813–818.  https://doi.org/10.1038/ng1810 CrossRefGoogle Scholar
  50. 50.
    Saitoh M, Ishida J, Ebner N et al (2017) Myostatin inhibitors as pharmacological treatment for muscle wasting and muscular dystrophy. JCSM Clin Rep 2:1e00037–10e00037.  https://doi.org/10.17987/jcsm-cr.v2i1.37 Google Scholar
  51. 51.
    Hoogaars WMH, Jaspers RT (2018) Past, present, and future perspective of targeting myostatin and related signaling pathways to counteract muscle atrophy (Chapter 8). In: Xiao J (ed) Muscle atrophy, advances in experimental medicine and biology, vol 1088. Springer, Singapore.  https://doi.org/10.1007/978-981-13-1435-3_8 Google Scholar
  52. 52.
    Reginster JY, Cooper C, Rizzoli R et al (2016) Recommendations for the conduct of clinical trials for drugs to treat or prevent sarcopenia. Aging Clin Exp Res 28:47–58.  https://doi.org/10.1007/s40520-015-0517-y CrossRefGoogle Scholar
  53. 53.
    Cruz-Jentoft A, Baeyens J, Bauer J et al (2010) European Working Group on Sarcopenia in Older People, Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–423.  https://doi.org/10.1093/ageing/afq034 CrossRefGoogle Scholar
  54. 54.
    Reginster J, Cooper C, Rizzoli R et al (2016) Recommendations for the conduct of clinical trials for drugs to treat or prevent sarcopenia. Aging Clin Exp Res 28:47–58.  https://doi.org/10.1007/s40520-015-0517-y CrossRefGoogle Scholar
  55. 55.
    Vitale G, Cesari M, Mari D (2016) Aging of the endocrine system and its potential impact on sarcopenia. Eur J Intern Med 35:10–15.  https://doi.org/10.1016/j.ejim.2016.07.017 CrossRefGoogle Scholar
  56. 56.
    Landi F, Calvani R, Cesari M et al (2015) Sarcopenia as the biological substrate of physical frailty. Clin Geriatr Med 31:367–374.  https://doi.org/10.1016/j.cger.2015.04.005 CrossRefGoogle Scholar
  57. 57.
    Calvani R, Miccheli A, Landi F et al (2013) Current nutritional recommendations and novel dietary strategies to manage sarcopenia. J Frailty Aging 2:38–53Google Scholar
  58. 58.
    Malafarina V, Uriz-Otano F, Gil-Guerrero L et al (2013) The anorexia of ageing: physiopathology, prevalence, associated comorbidity and mortality. A systematic review. Maturitas 74:293–302.  https://doi.org/10.1016/j.maturitas.2013.01.016 CrossRefGoogle Scholar
  59. 59.
    Wolfe RR (2002) Regulation of muscle protein by amino acids. J Nutr 132:3219S–3224S.  https://doi.org/10.1093/jn/131.10.3219S CrossRefGoogle Scholar
  60. 60.
    Wolfe RR, Miller S, Miller K (2008) Optimal protein intake in the elderly. Clin Nutr 27:675–684.  https://doi.org/10.1016/j.clnu.2008.06.008 CrossRefGoogle Scholar
  61. 61.
    Katsanos C, Kobayashi H, Sheffield-Moore M et al (2006) A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am J Physiol Endocrinol Metab 291:E381–E387.  https://doi.org/10.1152/ajpendo.00488.2005 CrossRefGoogle Scholar
  62. 62.
    Katsanos C, Kobayashi H, Sheffield-Moore S et al (2005) Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 82:1065–1073.  https://doi.org/10.1093/ajcn/82.5.1065 CrossRefGoogle Scholar
  63. 63.
    Panel on Macronutrients, Panel on the Definition of Dietary Fibers, Subcommittees on Upper Reference Levels of Nutrients and Interpretation and Uses of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. Food and Nutrition Board. Institute of Medicine of the National Academies (2005) Protein and amino acids. In: Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. The National Academies Press, Washington DC, pp. 589–768.  https://doi.org/10.17226/10490
  64. 64.
    Morley J, Argiles J, Evans W et al (2010) Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc 11:391–396.  https://doi.org/10.1016/j.jamda.2010.04.014 CrossRefGoogle Scholar
  65. 65.
    Bauer J, Biolo G, Cederholm T et al (2013) Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J Am Med Dir Assoc 14:542–559.  https://doi.org/10.1016/j.jamda.2013.05.021 CrossRefGoogle Scholar
  66. 66.
    Symons T, Sheffield-Moore M et al (2009) A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. J Am Diet Assoc 109:1582–1586.  https://doi.org/10.1016/j.jada.2009.06.369 CrossRefGoogle Scholar
  67. 67.
    Kim I, Schutzler S, Schrader A et al (2015) Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am J Physiol Endocrinol Metab 308:E21–E28.  https://doi.org/10.1152/ajpendo.00382.2014 CrossRefGoogle Scholar
  68. 68.
    Mitchell W, Wilkinson D, Phillips B et al (2016) Human skeletal muscle protein metabolism responses to amino acid nutrition. Adv Nutr 7:828S–838S.  https://doi.org/10.3945/an.115.011650 CrossRefGoogle Scholar
  69. 69.
    Anthony J, Anthony T, Kimball S et al (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr 131:856S–860S.  https://doi.org/10.1093/jn/131.3.856S CrossRefGoogle Scholar
  70. 70.
    Anthony J, Yoshizawa F, Anthony T et al (2000) Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J Nutr 130:2413–2419.  https://doi.org/10.1093/jn/130.10.2413 CrossRefGoogle Scholar
  71. 71.
    Nakashima K, Ishida A, Yamazaki M et al (2005) Leucine suppresses myofibrillar proteolysis by down-regulating ubiquitin-proteasome pathway in chick skeletal muscles. Biochem Biophys Res Commun 336:660–666.  https://doi.org/10.1016/j.bbrc.2005.08.138 CrossRefGoogle Scholar
  72. 72.
    Landi F, Calvani R, Tosato M et al (2016) Protein intake and muscle health in old age: from biological plausibility to clinical evidence. Nutrients 8:295.  https://doi.org/10.3390/nu8050295 CrossRefGoogle Scholar
  73. 73.
    Xu Z, Tan Z, Zhang Q, Gui Q, Yang Y (2014) The effectiveness of leucine on muscle protein synthesis, lean body mass and leg lean mass accretion in older people: a systematic review and meta-analysis. Br J Nutr 113:25–34.  https://doi.org/10.1017/S0007114514002475 CrossRefGoogle Scholar
  74. 74.
    van Vliet S, Burd N, van Loon L (2015) The skeletal muscle anabolic response to plant- versus animal-based protein consumption. J Nutr 145:1981–1991.  https://doi.org/10.3945/jn.114.204305 CrossRefGoogle Scholar
  75. 75.
    Yang Y, Churchward-Venne T, Burd N et al (2012) Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutr Metab (Lond) 9:57.  https://doi.org/10.1186/1743-7075-9-57 CrossRefGoogle Scholar
  76. 76.
    Rondanelli M, Perna S, Faliva M et al (2015) Novel insights on intake of meat and prevention of sarcopenia: all reasons for an adequate consumption. Nutr Hosp 32:2136–2143.  https://doi.org/10.3305/nh.2015.32.5.9638 Google Scholar
  77. 77.
    Wu H, Xia Y, Jiang J et al (2015) Effect of beta-hydroxy-beta-methylbutyrate supplementation on muscle loss in older adults: a systematic review and meta-analysis. Arch Gerontol Geriatr 61:168–175.  https://doi.org/10.1016/j.archger.2015.06.020 CrossRefGoogle Scholar
  78. 78.
    Robinson R, Reginster J, Rizzoli R et al (2018) Does nutrition play a role in the prevention and management of sarcopenia? Clin Nutr 37:1121–1132.  https://doi.org/10.1016/j.clnu.2017.08.016 CrossRefGoogle Scholar
  79. 79.
    Pedersen BK (2009) The diseasome of physical inactivity–and the role of myokines in muscle–fat cross talk. J Physiol 587:5559–5568.  https://doi.org/10.1113/jphysiol.2009.179515 CrossRefGoogle Scholar
  80. 80.
    Plomgaard P, Bouzakri K, Krogh-Madsen R et al (2005) Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54:2939–2945.  https://doi.org/10.2337/diabetes.54.10.2939 CrossRefGoogle Scholar
  81. 81.
    Landi F, Marzetti E, Martone A et al (2014) Exercise as a remedy for sarcopenia. Curr Opin Clin Nutr Metab Care 17:25–31.  https://doi.org/10.1097/MCO.0000000000000018 Google Scholar
  82. 82.
    Marzetti E, Calvani R, Tosato M et al (2017) Physical activity and exercise as countermeasures to physical frailty and sarcopenia. Aging Clin Exp Res 29:35–42.  https://doi.org/10.1007/s40520-016-0705-4 CrossRefGoogle Scholar
  83. 83.
    Chesley A, MacDougall J, Tarnopolsky M et al (1992) Changes in human muscle protein synthesis after resistance exercise. J Appl Physiol 73:1383–1388.  https://doi.org/10.1152/jappl.1992.73.4.1383 CrossRefGoogle Scholar
  84. 84.
    Beaudart C, Dawson A, Shaw S et al (2017) Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int 28:1817–1833.  https://doi.org/10.1007/s00198-017-3980-9 CrossRefGoogle Scholar
  85. 85.
    Deutz N, Bauer J, Barazzoni R et al (2014) Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Nutr 33:929–936.  https://doi.org/10.1016/j.clnu.2014.04.007 Google Scholar
  86. 86.
    Landi F, Cesari M, Calvani R et al (2017) The “Sarcopenia and Physical fRailty IN older people: multi-componenT Treatment strategies” (SPRINTT) randomized controlled trial: design and methods. Aging Clin Exp Res 29:89–100.  https://doi.org/10.1007/s40520-016-0715-2 CrossRefGoogle Scholar
  87. 87.
    Marzetti E, Cesari M, Calvani R et al (2018) The “Sarcopenia and Physical fRailty IN older people: multi-componenT Treatment strategies” (SPRINTT) randomized controlled trial: case finding, screening and characteristics of eligible participants. Exp Gerontol 113:48–57.  https://doi.org/10.1016/j.exger.2018.09.017 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Experimental and Clinical Biomedical SciencesUniversity of FlorenceFlorenceItaly

Personalised recommendations