Skip to main content
Top
Published in: The journal of nutrition, health & aging 10/2017

01-12-2017

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

Authors: J. Verney, V. Martin, S. Ratel, V. Chavanelle, M. Bargetto, M. Etienne, E. Chaplais, P. Le Ruyet, C. Bonhomme, L. Combaret, C. Guillet, N. Boisseau, P. Sirvent, Dominique Dardevet

Published in: The journal of nutrition, health & aging | Issue 10/2017

Login to get access

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.
Literature
1.
go back to reference Harris T. Muscle mass and strength:relation to function in population studies, J Nutr, 1997, 127, 1004S–1006SCrossRefPubMed Harris T. Muscle mass and strength:relation to function in population studies, J Nutr, 1997, 127, 1004S–1006SCrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
5.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
6.
go back to reference 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 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
7.
go back to reference 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, 1772–1774CrossRefPubMed 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, 1772–1774CrossRefPubMed
8.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
9.
go back to reference 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.PubMed 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.PubMed
10.
go back to reference 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):14–23CrossRefPubMed 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):14–23CrossRefPubMed
11.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference 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.PubMed 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.PubMed
14.
go back to reference Anthony JC, Anthony TG, Layman DK. Leucine supplementation enhances skeletal muscle recovery in rats following exercise, J Nutr 1999;129: 1102–1106.CrossRefPubMed Anthony JC, Anthony TG, Layman DK. Leucine supplementation enhances skeletal muscle recovery in rats following exercise, J Nutr 1999;129: 1102–1106.CrossRefPubMed
15.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
18.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference 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.PubMed 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.PubMed
21.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
22.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
25.
go back to reference 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.PubMed 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.PubMed
26.
go back to reference 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.PubMed 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.PubMed
27.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
28.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
29.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
30.
go back to reference 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. 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.
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
33.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
34.
go back to reference 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):e75408CrossRef 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):e75408CrossRef
35.
go back to reference 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):437–46CrossRefPubMed 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):437–46CrossRefPubMed
36.
go back to reference 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. 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.
37.
go back to reference 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):958CrossRefPubMed 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):958CrossRefPubMed
39.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
40.
go back to reference 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: 630–635CrossRefPubMed 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: 630–635CrossRefPubMed
41.
go back to reference 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: 723–748CrossRefPubMedPubMedCentral 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: 723–748CrossRefPubMedPubMedCentral
42.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
43.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
44.
go back to reference 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):323–31PubMed 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):323–31PubMed
45.
go back to reference 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):997–1005CrossRefPubMed 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):997–1005CrossRefPubMed
46.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
47.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
48.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
49.
go back to reference 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.CrossRef 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.CrossRef
50.
go back to reference 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.PubMed 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.PubMed
51.
go back to reference 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):549–54PubMed 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):549–54PubMed
52.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
53.
go back to reference 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, 2014CrossRefPubMed 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, 2014CrossRefPubMed
54.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
55.
go back to reference Sun X, Zemel MB. Leucine modulation of mitochondrial mass and oxygen consumption in skeletal Sun X, Zemel MB. Leucine modulation of mitochondrial mass and oxygen consumption in skeletal
56.
go back to reference 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. 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.
go back to reference Wei-jian Jiang. Sirtuins: Novel targets for metabolic disease in drug development, Biochem Biophys Res Commun. 2008 Aug 29;373(3):341–4 Wei-jian Jiang. Sirtuins: Novel targets for metabolic disease in drug development, Biochem Biophys Res Commun. 2008 Aug 29;373(3):341–4
58.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
59.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
Metadata
Title
Soluble milk proteins improve muscle mass recovery after immobilization-induced muscle atrophy in old rats but do not improve muscle functional property restoration
Authors
J. Verney
V. Martin
S. Ratel
V. Chavanelle
M. Bargetto
M. Etienne
E. Chaplais
P. Le Ruyet
C. Bonhomme
L. Combaret
C. Guillet
N. Boisseau
P. Sirvent
Dominique Dardevet
Publication date
01-12-2017
Publisher
Springer Paris
Published in
The journal of nutrition, health & aging / Issue 10/2017
Print ISSN: 1279-7707
Electronic ISSN: 1760-4788
DOI
https://doi.org/10.1007/s12603-016-0855-2

Other articles of this Issue 10/2017

The journal of nutrition, health & aging 10/2017 Go to the issue