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Soluble milk proteins improve muscle mass recovery after immobilization-induced muscle atrophy in old rats but do not improve muscle functional property restoration

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Abstract

Objectives

Effect of 3 different dairy protein sources on the recovery of muscle function after limb immobilization in old rats.

Design

Longitudinal animal study.

Setting

Institut National de la Recherche Agronomique (INRA). The study took part in a laboratory setting.

Intervention

Old rats were subjected to unilateral hindlimb immobilization for 8 days and then allowed to recover with 3 different dietary proteins: casein, soluble milk proteins or whey proteins for 49 days.

Measurements

Body weight, muscle mass, muscle fibre size, isometric, isokinetic torque, muscle fatigability and muscle oxidative status were measured before and at the end of the immobilization period and during the recovery period i.e 7, 21, 35 and 49 days post immobilization.

Results

In contrast to the casein diet, soluble milk proteins and whey proteins were efficient to favor muscle mass recovery after cast immobilization during aging. By contrast, none of the 3 diary proteins was able to improve muscle strength, power and fatigability showing a discrepancy between the recovery of muscle mass and function. However, the soluble milk proteins allowed a better oxidative capacity in skeletal muscle during the rehabilitation period.

Conclusion

Whey proteins and soluble milk proteins improve muscle mass recovery after immobilization-induced muscle atrophy in old rats but do not allow muscle functional property restoration.

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References

  1. Harris T. Muscle mass and strength:relation to function in population studies, J Nutr, 1997, 127, 1004S–1006S

    Article  CAS  PubMed  Google Scholar 

  2. Chakravarthy MV, Davis BS & Booth FW. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle, J Appl Physiol 2000;89, 1365–1379.

    Article  CAS  PubMed  Google Scholar 

  3. Suetta C, Hvid LG, Justesen L, Christensen U, Neergaard K, Simonsen L, Ortenblad N, Magnusson SP, Kjaer M, Aagaard P. Effects of ageing on human skeletal muscle after immobilization and retraining, J Appl Physiol, 2009, 107, 1172–1180.

    Article  CAS  PubMed  Google Scholar 

  4. Magne H, Savary-Auzeloux I, Vazeille E, Claustre A, Attaix D, Listrat A, Veronique SL, Philippe G, Dardevet D, Combaret L. Lack of muscle recovery after immobilization in old rats does not result from a defect in normalization of the ubiquitin-proteasome and the caspase-dependent apoptotic pathways, J Physiol, 2011, 589, 511–524.

    Article  CAS  PubMed  Google Scholar 

  5. Magne H, Savary-Auzeloux I, Migne C, Peyron MA, Combaret L, Remond D, Dardevet D. Contrarily to whey and high protein diets, dietary free leucine supplementation cannot reverse the lack of recovery of muscle mass after prolonged immobilization during ageing, J Physiol 2012;590: 2035–2049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Magne H, Savary-Auzeloux I, Remond D, Dardevet D. Nutritional strategies to counteract disuse muscle atrophy and improve following recovery, Nutrition Research Reviews 2013 Aug 9:1–17

    Google Scholar 

  7. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults, Jama 2007;297, 1772–1774

    Article  CAS  PubMed  Google Scholar 

  8. English KL & Paddon-Jones D. Protecting muscle mass and function in older adults during bed rest, Current opinion in clinical nutrition and metabolic care 2010;13, 34–39.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ferrucci L, Cavazzini C, Corsi A, Bartali B, Russo CR, Lauretani F, Ferrucci L, Cavazzini C, Corsi AM, Bartali B, Russo CR, Lauretani F, Bandinelli S, Bandinelli S, Guralnik JM. Biomarkers of frailty in older persons, J Endocrinol Invest. 2002;25(10 Suppl):10–5.

    CAS  PubMed  Google Scholar 

  10. Cooper R, Kuh D, Cooper C, Gale CR, Lawlor DA, Matthews F, Hardy R; FALCon and HALCyon Study Teams. Objective measures of physical capability and subsequent health: a systematic review, Age Ageing. 2011 Jan;40(1):14–23

    Article  PubMed  Google Scholar 

  11. Rieu, I., Sornet, C., Grizard, J., Dardevet, D. Glucocorticoid excess induces a prolonged leucine resistance on muscle protein synthesis in old rats, Experimental Gerontology, 2004, 39, 1315–1321.

    Article  CAS  PubMed  Google Scholar 

  12. Mosoni L, Malmezat T, Valluy MC, Houlier ML & Mirand PP. Muscle and liver protein synthesis adapt efficiently to food deprivation and refeeding in 12-month-old rats, J Nutr, 1996, 126, 516–522.

    Article  CAS  PubMed  Google Scholar 

  13. Dardevet D, Sornet C, Taillandier D, Savary I, Attaix D & Grizard J. Sensitivity and protein turnover response to glucocorticoids are different in skeletal muscle from adult and old rats, Lack of regulation of the ubiquitin-proteasome proteolytic pathway in ageing. The Journal of clinical investigation 1995;96, 2113–2119.

    CAS  PubMed  Google Scholar 

  14. Anthony JC, Anthony TG, Layman DK. Leucine supplementation enhances skeletal muscle recovery in rats following exercise, J Nutr 1999;129: 1102–1106.

    Article  CAS  PubMed  Google Scholar 

  15. Anthony TG, Anthony JC, Yoshizawa F, Kimball SR, Jefferson LS. Oral administration of leucine stimulates ribosomal protein mRNA translation but not global rates of protein synthesis in the liver of rats, J Nutr 2001;131: 1171–1176.

    Article  CAS  PubMed  Google Scholar 

  16. Koopman R, Wagenmakers AJ, Manders RJ, Zorenc AH, Senden JM, Gorselink M, Keizer HA, van Loon LJ. Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects, Am J Physiol Endocrinol Metab 2005;288: E645–E653.

    Article  CAS  PubMed  Google Scholar 

  17. Buse MG, Reid SS. Leucine, A possible regulator of protein turnover in muscle. J Clin Invest 1975;56: 1250–1261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Combaret L, Dardevet D, Rieu I, Pouch MN, Bechet D, Taillandier D, Grizard J, Attaix D. A leucine-supplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle, J Physiol 2005;569: 489–499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dardevet D, Sornet C, Bayle G, Prugnaud J, Pouyet C, Grizard J. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucinesupplemented meal, J Nutr 2002;132: 95–100.

    Article  CAS  PubMed  Google Scholar 

  20. Frexes-Steed M, Lacy DB, Collins J, Abumrad NN. Role of leucine and other amino acids in regulating protein metabolism in vivo, Am J Physiol 1992;262: E925–E935.

    CAS  PubMed  Google Scholar 

  21. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR; Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 2005;82: 1065–1073.

    Article  CAS  PubMed  Google Scholar 

  22. Li JB, Jefferson LS (1978) Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochim Biophys Acta 544: 351–359. 0304-4165(78)90103-4.

    Article  CAS  PubMed  Google Scholar 

  23. Nakashima K, Ishida A, Yamazaki M, Abe H. Leucine suppresses myofibrillar proteolysis by down-regulating ubiquitin-proteasome pathway in chick skeletal muscles, Biochem Biophys Res Commun 2005;336: 660–666.

    Article  CAS  PubMed  Google Scholar 

  24. Rieu I, Balage M, Sornet C, Giraudet C, Pujos E, Grizard J, Mosoni L, Dardevet D. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia, J Physiol 2006;575: 305–315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Smith K, Barua JM, Watt PW, Scrimgeour CM, Rennie MJ. Flooding with L-[1-13C] leucine stimulates human muscle protein incorporation of continuously infused L-[1-13C]valine, Am J Physiol 1992;262: E372–E376.

    CAS  PubMed  Google Scholar 

  26. Tischler ME, Desautels M, Goldberg AL. Does leucine, leucyl-tRNA, or some metabolite of leucine regulate protein synthesis and degradation in skeletal and cardiac muscle? J Biol Chem 1982;257: 1613–1621.

    CAS  PubMed  Google Scholar 

  27. Anthony JC, Anthony TG, Kimball SR, Vary TC, Jefferson LS. Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F formation, J Nutr 2000;130: 139–145.

    Article  CAS  PubMed  Google Scholar 

  28. Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A, Rankin D, Smith K, Rennie MJ. Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling, Am J Clin Nutr 2010;92: 1080–1088.

    Article  CAS  PubMed  Google Scholar 

  29. Peyrollier K, Hajduch E, Blair AS, Hyde R, Hundal HS. L-leucine availability regulates phosphatidylinositol 3-kinase, p70 S6 kinase and glycogen synthase kinase-3 activity in L6 muscle cells: evidence for the involvement of the mammalian target of rapamycin (mTOR) pathway in the L-leucine-induced up-regulation of system A amino acid transport, Biochem J 2000;350 Pt 2: 361–368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Dardevet D, Remond D, Peyron MA, Papet I, Savary-Auzeloux I, et al. Muscle wasting and resistance of muscle anabolism: the «anabolic threshold concept» for adapted nutritional strategies during sarcopenia, Scientific World Journal 2012: 269531.

    Google Scholar 

  31. Warren GL, Stallone JL, Allen MR, Bloomfield SA.Functional recovery of the plantarflexor muscle group after hindlimb unloading in the rat. Eur J Appl Physiol 2004;93: 130–138.

    Article  CAS  PubMed  Google Scholar 

  32. Papadakis MA, Grady D, Black D, Tierney MJ, Gooding GA, et al. Growth hormone replacement in healthy older men improves body composition but not functional ability, Ann Intern Med 1996;124: 708–716.

    Article  CAS  PubMed  Google Scholar 

  33. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R & Fiatarone Singh MA. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health, The journals of gerontology 2001;56, B209–217.

    Article  CAS  PubMed  Google Scholar 

  34. Martin V, S Ratel, J Siracusa, P. Leruyet, I Savary-Auzeloux, L Combaret, C Guillet and D Dardevet, Leucine-rich proteins are more efficient than casein in the recovery of muscle functional properties following a casting induced muscle atrophy. PlosOne, 2013a, Sep 19;8(9):e75408

    Article  Google Scholar 

  35. Komar B, Schwingshackl L, Hoffmann G. Effects of leucine-rich protein supplements on anthropometric parameter and muscle strength in the elderly: a systematic review and meta-analysis, J Nutr Health Aging. 2015 Apr;19(4):437–46

    Article  CAS  PubMed  Google Scholar 

  36. Martin V, S. Ratel, J. Siracusa, C. Bonhomme, L. Combaret, I. Savary-Auzeloux, C. Guillet, D. Dardevet. Les protéines solubles de lait accélèrent la récupération des aptitudes fonctionnelles musculaires à la suite d’une immobilisation, 10ème Journées Francophones de Nutrition, Lyon (France). Nutrition Clinique et Métabolisme, Cahiers de Nutrition et de Diététique, 2013b;26-47, S27.

    Google Scholar 

  37. Gryson C, Ratel S, Rance M, Penando S, Bonhomme C, Le Ruyet P, Duclos M, Boirie Y, Walrand S. Four-month course of soluble milk proteins interacts with exercise to improve muscle strength and delay fatigue in elderly participants, J Am Med Dir Assoc. 2014 Dec;15(12):958

    Article  PubMed  Google Scholar 

  38. Srere PA. Citrate synthase. Methods Enzymol. 1969, 13,:3–11

    Article  CAS  Google Scholar 

  39. Essén B, Jansson E, Henriksson J, Taylor AW, Saltin B. Metabolic characteristics of fibre types in human skeletal muscle, Acta Physiol Scand. 1975 Oct;95(2):153–65.

    Article  PubMed  Google Scholar 

  40. Varejao AS, Cabrita AM, Meek MF, Bulas-Cruz J, Gabriel RC, et al. Motion of the foot and ankle during the stance phase in rats, Muscle Nerve 2002;26: 630–635

    Article  PubMed  Google Scholar 

  41. Burke RE, Levine DN, Tsairis P, Zajac FE, 3rd; Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 1973;234: 723–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, et al. Slow and fast dietary proteins differently modulate postprandial protein accretion, Proc Natl Acad Sci U S A 1997;94: 14930–14935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, et al. The digestion rate of protein is an independent regulating factor of postprandial protein retention, Am J Physiol Endocrinol Metab 2001;280: E340–348.

    Article  CAS  PubMed  Google Scholar 

  44. Rieu I, Balage M, Sornet C, Debras E, Ripes S, Rochon-Bonhomme C, Pouyet C, Grizard J, Dardevet D. Increased availability of leucine with leucine-rich whey proteins improves postprandial muscle protein synthesis in aging rats Nutrition. 2007 Apr;23(4):323–31

    CAS  PubMed  Google Scholar 

  45. Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ.; Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr. 2011 May;93(5):997–1005

    Article  CAS  PubMed  Google Scholar 

  46. Dardevet D, Sornet C, Balage M, Grizard J. Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age, J Nutr 2000;130: 2630–2635.

    Article  CAS  PubMed  Google Scholar 

  47. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K & Rennie MJ. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion, The Journal of physiology 2008;586, 6049–6061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Järvinen TA, Józsa L, Kannus P, Järvinen TL, Järvinen M. Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles, An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil. 2002;23(3):245–54.

    Article  PubMed  Google Scholar 

  49. Canepari M, Pellegrino MA, D’Antona G, Bottinelli R. Skeletal muscle fibre diversity and the underlying mechanisms, Acta Physiol (Oxf). 2010 Aug;199(4):465–76.

    Article  Google Scholar 

  50. Holloszy JO. Biochemical adaptations in muscle, Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem. 1967 May 10;242(9):2278–82.

    CAS  PubMed  Google Scholar 

  51. Terjung RL, Baldwin KM, Molé PA, Klinkerfuss GH, Holloszy JO. Effect of running to exhaustion on skeletal muscle mitochondria: a biochemical study, Am J Physiol. 1972 Sep;223(3):549–54

    CAS  PubMed  Google Scholar 

  52. Wagatsuma A, Kotake N, Kawachi T, Shiozuka M, Yamada S, Matsuda R. Mitochondrial adaptations in skeletal muscle to hindlimb unloading, Mol Cell Biochem. 2011 Apr;350(1-2):1–11. 2010 Dec17.

    Article  CAS  PubMed  Google Scholar 

  53. Wall BT, Dirks ML, Snijders T, Stephens FB, Senden JM, Verscheijden ML, van Loon LJ. Short-term muscle disuse atrophy is not associated with increased intramuscular lipid deposition or a decline in the maximal activity of key mitochondrial enzymes in young and older males, Exp Gerontol. 2015 Jan;61:76–83, 2014

    Article  CAS  PubMed  Google Scholar 

  54. Oishi Y, Ogata T, Yamamoto KI, Terada M, Ohira T, Ohira Y, Taniguchi K, Roy RR. Cellular adaptations in soleus muscle during recovery after hindlimb unloading, Acta Physiol (Oxf). 2008 Mar;192(3):381–95. Epub 2007 Sep24.

    Article  CAS  PubMed  Google Scholar 

  55. Sun X, Zemel MB. Leucine modulation of mitochondrial mass and oxygen consumption in skeletal

  56. Liu J, Peng Y, Cui Z, Wu Z, Qian A, Shang P, Qu L, Li Y, Liu J, Long J. Depressed mitochondrial biogenesis and dynamic remodeling in mouse tibialis anterior and gastrocnemius induced by 4-week hindlimb unloading.

  57. Wei-jian Jiang. Sirtuins: Novel targets for metabolic disease in drug development, Biochem Biophys Res Commun. 2008 Aug 29;373(3):341–4

    Google Scholar 

  58. Lantier L, Fentz J, Mounier R, Leclerc J, Treebak JT, Pehmøller C, Sanz N, Sakakibara I, Saint-Amand E, Rimbaud S, Maire P, Marette A, Ventura-Clapier R, Ferry A, Wojtaszewski JF, Foretz M, Viollet B. AMPK controls exercise endurance, mitochondrial oxidative capacity, and skeletal muscle integrity, FASEB J. 2014 Jul;28(7):3211–24.

    Article  CAS  PubMed  Google Scholar 

  59. Westerblad H, Bruton JD, Katz A. Skeletal muscle: energy metabolism, fiber types, fatigue and adaptability, Exp Cell Res. 2010 Nov 1;316(18):3093–9.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Clermont Université, Université Blaise Pascal, EA 3533, Laboratoire des Adaptations Métaboliques à l’Exercice en Conditions Physiologiques et Pathologiques, CRNH Auvergne, Clermont Ferrand, France

    J. Verney, V. Martin, S. Ratel, V. Chavanelle, M. Bargetto, M. Etienne, E. Chaplais, N. Boisseau & P. Sirvent

  2. Lactalis Recherche et Développement, Lactalis Nutrition Santé, Torcé, France

    P. Le Ruyet & C. Bonhomme

  3. INRA, Unité de Nutrition Humaine (UNH, UMR 1019), CRNH Auvergne, Auvergne, France

    L. Combaret, C. Guillet & Dominique Dardevet

  4. Clermont Université, Université d’Auvergne, Clermont-Ferrand, France

    C. Guillet

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  1. J. Verney
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  2. V. Martin
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  3. S. Ratel
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  4. V. Chavanelle
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  5. M. Bargetto
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  6. M. Etienne
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  8. P. Le Ruyet
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  9. C. Bonhomme
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  10. L. Combaret
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  11. C. Guillet
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  13. P. Sirvent
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  14. Dominique Dardevet
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Correspondence to Dominique Dardevet.

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Verney, J., Martin, V., Ratel, S. et al. Soluble milk proteins improve muscle mass recovery after immobilization-induced muscle atrophy in old rats but do not improve muscle functional property restoration. J Nutr Health Aging 21, 1133–1141 (2017). https://doi.org/10.1007/s12603-016-0855-2

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  • DOI: https://doi.org/10.1007/s12603-016-0855-2

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