The use of doubly labeled milk protein to measure postprandial muscle protein synthesis rates in vivo in humans

Journal of Applied Physiology

Volumn 117, Issue 11, 2014, Pages 1363-1370

  Burd, Nicholas A ^a   Cermak, Naomi M ^a   Kouw, Imre W K ^a   Gorissen, Stefan H ^a   Gijsen, Annemie P ^a   Van Loon, Luc J C ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Dietary protein; Hypertrophy; Nutrition; Stable isotopes

Indexed keywords

CARBON; CASEIN; LEUCINE; MUSCLE PROTEIN; PHENYLALANINE;

AGED; BIOSYNTHESIS; BLOOD; DIAGNOSTIC USE; HUMAN; MALE; METABOLISM; MUSCLE FIBRIL;

AGED; CARBON ISOTOPES; CASEINS; HUMANS; LEUCINE; MALE; MUSCLE PROTEINS; MYOFIBRILS; PHENYLALANINE;

EID: 84914125523     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00411.2014     Document Type: Article

References (37)

1. Bechshoeft R, Dideriksen KJ, Reitelseder S, Scheike T, Kjaer M, Holm L. The anabolic potential of dietary protein intake on skeletal muscle is prolonged by prior light-load exercise. Clinical nutrition 32: 236-244, 2013.
2. Bequette BJ, Kyle CE, Crompton LA, Anderson SE, Hanigan MD. Protein metabolism in lactating goats subjected to the insulin clamp. J Dairy Sci 85: 1546-1555, 2002.
3. Boirie Y, Fauquant J, Rulquin H, Maubois JL, Beaufrere B. Production of large amounts of [13C]leucine-enriched milk proteins by lactating cows. J Nutr 125: 92-98, 1995.
4. Boirie Y, Gachon P, Corny S, Fauquant J, Maubois JL, Beaufrere B. Acute postprandial changes in leucine metabolism as assessed with an intrinsically labeled milk protein. Am J Physiol Endocrinol Metab 271: E1083-E1091, 1996.
5. Borno A, Hulston CJ, van Hall G. Determination of human muscle protein fractional synthesis rate: An evaluation of different mass spectrometry techniques and considerations for tracer choice. J Mass Spectrom 49: 674-680, 2014.
6. Burd NA, Hamer HM, Pennings B, Pellikaan WF, Senden JMG, Gijsen AP, van Loon LJC. Substantial differences between organ and muscle specific tracer incorporation rates in a lactating dairy cow. PloS One 8: E68109, 2013.
7. Burd NA, Pennings B, Groen BB, Gijsen AP, Senden JM, van Loon LJ. The single biopsy approach is reliable for the measurement of muscle protein synthesis rates in vivo in older men. J Appl Physiol 113: 896-902, 2012.
8. Burd NA, West DW, Rerecich T, Prior T, Baker SK, Phillips SM. Validation of a single biopsy approach and bolus protein feeding to determine myofibrillar protein synthesis in stable isotope tracer studies in humans. Nutr Metab 8: 15, 2011.
9. Calder AG, Anderson SE, Grant I, McNurlan MA, Garlick PJ. The determination of low d5-phenylalanine enrichment (0.002-009 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography/electron ionization mass spectrometry. Rapid Commun Mass Spectrom 6: 421-424, 1992.
10. Evenepoel P, Hiele M, Luypaerts A, Geypens B, Buyse J, Decuypere E, Rutgeerts P, Ghoos Y. Production of egg proteins, enriched with L-leucine-13C1, for the study of protein assimilation in humans using the breath test technique. J Nutr 127: 327-331, 1997.
11. Garlick PJ, Wernerman J, McNurlan MA, Essen P, Lobley GE, Milne E, Calder GA, Vinnars E. Measurement of the rate of protein synthesis in muscle of postabsorptive young men by injection of a 'flooding dose' of [1-13C]leucine. Clin Sci 77: 329-336, 1989.
12. Gorissen SH, Burd NA, Hamer HM, Gijsen AP, Groen BB, van Loon LJ. Carbohydrate coingestion delays dietary protein digestion and absorption but does not modulate postprandial muscle protein accretion. J Clin Endocrinol Metab 99: 2250-2258, 2014.
13. Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, Layfield R, Wackerhage H, Smith K, Atherton P, Selby A, Rennie MJ. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 295: E595-E604, 2008.
14. Hamer HM, Wall BT, Kiskini A, de Lange A, Groen BB, Bakker JA, Gijsen AP, Verdijk LB, van Loon LJ. Carbohydrate co-ingestion with protein does not further augment post-prandial muscle protein accretion in older men. Nutr Metab 10: 15, 2013.
15. Kiskini A, Hamer HM, Wall BT, Groen BB, de Lange A, Bakker JA, Senden JM, Verdijk LB, van Loon LJ. The muscle protein synthetic response to the combined ingestion of protein and carbohydrate is not impaired in healthy older men. Age 35: 2389-2398, 2013.
16. Koopman R, Crombach N, Gijsen AP, Walrand S, Fauquant J, Kies AK, Lemosquet S, Saris WH, Boirie Y, van Loon LJ. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. Am J Clin Nutr 90: 106-115, 2009.
17. Koopman R, Verdijk L, Manders RJ, Gijsen AP, Gorselink M, Pijpers E, Wagenmakers AJ, van Loon LJ. Co-ingestion of protein and leucine stimulates muscle protein synthesis rates to the same extent in young and elderly lean men. Am J Clin Nutr 84: 623-632, 2006.
18. Koopman R, Walrand S, Beelen M, Gijsen AP, Kies AK, Boirie Y, Saris WH, van Loon LJ. Dietary protein digestion and absorption rates and the subsequent postprandial muscle protein synthetic response do not differ between young and elderly men. J Nutr 139: 1707-1713, 2009.
19. Koopman R, Zorenc AH, Gransier RJ, Cameron-Smith D, van Loon LJ. Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. Am J Physiol Endocrinol Metabol 290: E1245-E1252, 2006.
20. Ljungqvist OH, Persson M, Ford GC, Nair KS. Functional heterogeneity of leucine pools in human skeletal muscle. Am J Physiol Endocrinol Metab 273: E564-E570, 1997.
21. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89: 161-168, 2009.
22. Patterson BW, Zhao G, Klein S. Improved accuracy and precision of gas chromatography/mass spectrometry measurements for metabolic tracers. Metabolism 47: 706-712, 1998.
23. 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 93: 997-1005, 2011.
24. Pennings B, Groen B, de Lange A, Gijsen AP, Zorenc AH, Senden JM, van Loon LJ. Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am J Physiol Endocrinol Metab 302: E992-E999, 2012.
25. Pennings B, Koopman R, Beelen M, Senden JM, Saris WH, van Loon LJ. Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. Am J Clin Nutr 93: 322-331, 2011.
26. Pennings B, Pellikaan WF, Senden JM, van Vuuren AM, Sikkema J, van Loon LJ. The production of intrinsically labeled milk and meat protein is feasible and provides functional tools for human nutrition research. J Dairy Sci 94: 4366-4373, 2011.
27. Reeds PJ, Hachey DL, Patterson BW, Motil KJ, Klein PD. VLDL apolipoprotein B-100, a potential indicator of the isotopic labeling of the hepatic protein synthetic precursor pool in humans: Studies with multiple stable isotopically labeled amino acids. J Nutr 122: 457-466, 1992.
28. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Lund P, Kristensen NB, Frystyk J, Flyvbjerg A, Schjerling P, van Hall G, Kjaer M, Holm L. Whey and casein labeled with L-[1-13C]leucine and muscle protein synthesis: Effect of resistance exercise and protein ingestion. Am J Physiol Endocrinol Metab 300: E231-E242, 2011.
29. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Schjerling P, van Hall G, Kjaer M, Holm L. Positive muscle protein net balance and differential regulation of atrogene expression after resistance exercise and milk protein supplementation. Eur J Nutr 53: 321-333, 2014.
30. Rennie MJ, Smith K, Watt PW. Measurement of human tissue protein synthesis: An optimal approach. Am J Physiol Endocrinol Metab 266: E298-E307, 1994.
31. Schwenk WF, Beaufrere B, Haymond MW. Use of reciprocal pool specific activities to model leucine metabolism in humans. Am J Physiol Endocrinol Metab 249: E646-E650, 1985.
32. Schwenk WF, Berg PJ, Beaufrere B, Miles JM, Haymond MW. Use of t-butyldimethylsilylation in the gas chromatographic/mass spectrometric analysis of physiologic compounds found in plasma using electron-impact ionization. Anal Biochem 141: 101-109, 1984.
33. Slater C, Preston T, McMillan DC, Falconer JS, Fearon KCH. GC/MS analysis of [2H5]phenylalanine at very low enrichment: Measurement of protein synthesis in health and disease. J Mass Spectrom 30: 1325-1332, 1995.
34. van Loon LJ, Boirie Y, Gijsen AP, Fauquant J, de Roos AL, Kies AK, Lemosquet S, Saris WH, Koopman R. The production of intrinsically labeled milk protein provides a functional tool for human nutrition research. J Dairy Sci 92: 4812-4822, 2009.
35. Wall BT, Hamer HM, de Lange A, Kiskini A, Groen BB, Senden JM, Gijsen AP, Verdijk LB, van Loon LJ. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clin Nutr 32: 412-419, 2013.
36. Watt PW, Lindsay Y, Scrimgeour CM, Chien PA, Gibson JN, Taylor DJ, Rennie MJ. Isolation of aminoacyl-TRNA and its labeling with stable-isotope tracers: Use in studies of human tissue protein synthesis. Proc Natl Acad Sci U S A 88: 5892-5896, 1991.
37. Wolfe RR, Song J, Sun J, Zhang XJ. Total aminoacyl-Transfer RNA pool is greater in liver than muscle in rabbits. J Nutr 137: 2333-2338, 2007.