Abstract
Nutrient stimulation of muscle protein synthesis (MPS) is regulated by the change in extracellular essential amino acid (EAA) concentration. In vivo microdialysis (MD) is a minimally invasive sampling technique, capable of sampling solute in the interstitial space of a target tissue. In a contralateral limb design (REST vs. EX), this study utilised in vivo MD to examine the change in skeletal muscle dialysate amino acid concentration following ingestion of whey protein isolate (WPI) and flavoured water (CON). Four male subjects undertook unilateral, concentric lower limb knee extensor resistance exercise (RE) on two occasions. After RE, an MD catheter (CMA 63) was inserted into m. vastus lateralis of the exercise and resting leg and sampled serially over 7 h. Following a 2.5 h equilibration period subjects consumed either 0.55 g/kg WPI or CON. Peak plasma EAA (2656 ± 152 µM) preceded the peak in dialysate EAA (2345 ± 164 µM) by 30 min in response to WPI ingestion; however, the post-prandial elevation in dialysate EAA extended beyond that of the plasma. This resulted in no difference in the dialysate EAA area under the curve (ΔAUC270) relative to plasma in response to WPI ingestion [220 ± 29 vs. 206 ± 7.9 mmol min/L (p = 0.700)]. A bout of unilateral lower limb RE had no effect of the subsequent dialysate amino acid concentration in response to either WPI or CON ingestion. These data represent a novel report describing the time course and magnitude of change in skeletal muscle dialysate concentration of key nutrient regulators of MPS sampled by in vivo MD, in response to nutrient ingestion with and without RE.
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Abbreviations
- EAA:
-
Essential amino acids
- FSR:
-
Fractional synthetic rate
- LTM:
-
Lean tissue mass
- MPS:
-
Muscle protein synthesis
- MD:
-
Microdialysis
- RE:
-
Resistance exercise
References
Arner P (1999) Microdialysis: use in human exercise studies. Proc Nutr Soc 58(4):913–917
Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A, Rankin D, Smith K, Rennie MJ (2010a) Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr 92(5):1080–1088
Atherton PJ, Smith K, Etheridge T, Rankin D, Rennie MJ (2010b) Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Amino Acids 38(5):1533–1539
Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 268(3 Pt 1):E514–E520
Bohe J, Low A, Wolfe RR, Rennie MJ (2003) Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol 552(Pt 1):315–324
Breen L, Churchward-Venne TA (2012) Leucine: a nutrient ‘trigger’ for muscle anabolism, but what more? J Physiol 590(Pt 9):2065–2066
Carson BP, McCormack WG, Conway C, Cooke J, Saunders J, O’Connor WT, Jakeman PM (2015) An in vivo microdialysis characterization of the transient changes in the interstitial dialysate concentration of metabolites and cytokines in human skeletal muscle in response to insertion of a microdialysis probe. Cytokine 71(2):327–333
Chesley A, MacDougall JD, Tarnopolsky MA, Atkinson SA, Smith K (1992) Changes in human muscle protein synthesis after resistance exercise. J Appl Physiol (Bethesda, Md: 1985) 73(4):1383–1388
Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ (2005) Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19(3):422–424
Durham WJ, Casperson SL, Dillon EL, Keske MA, Paddon-Jones D, Sanford AP, Hickner RC, Grady JJ, Sheffield-Moore M (2010) Age-related anabolic resistance after endurance-type exercise in healthy humans. FASEB J
Ekberg NR, Wisniewski N, Brismar K, Ungerstedt U (2005) Measurement of glucose and metabolites in subcutaneous adipose tissue during hyperglycemia with microdialysis at various perfusion flow rates. Clin Chim Acta 359(1–2):53–64
Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR (1996) Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 270(4 Pt 1):E627–E633
Filho JC, Bergstrom J, Stehle P, Furst P (1997) Simultaneous measurements of free amino acid patterns of plasma, muscle and erythrocytes in healthy human subjects. Clin Nutr (Edinburgh, Scotland) 16(6):299–305
Frossard M, Blank D, Joukhadar C, Bayegan K, Schmid R, Luger A, Muller M (2005) Interstitial glucose in skeletal muscle of diabetic patients during an oral glucose tolerance test. Diabet Med 22(1):56–60
Fryburg DA, Barrett EJ, Louard RJ, Gelfand RA (1990) Effect of starvation on human muscle protein metabolism and its response to insulin. Am J Physiol 259(4 Pt 1):E477–E482
Glynn EL, Fry CS, Drummond MJ, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB (2010) Excess leucine intake enhances muscle anabolic signaling but not net protein anabolism in young men and women. J Nutr 140(11):1970–1976
Gutierrez A, Anderstam B, Alvestrand A (1999) Amino acid concentration in the interstitium of human skeletal muscle: a microdialysis study. Eur J Clin Invest 29(11):947–952
Henriksson J (1999) Microdialysis of skeletal muscle at rest. Proc Nutr Soc 58(4):919–923
Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR (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(2):E381–E387
Maggs DG, Jacob R, Rife F, Lange R, Leone P, During MJ, Tamborlane WV, Sherwin RS (1995) Interstitial fluid concentrations of glycerol, glucose, and amino acids in human quadricep muscle and adipose tissue. Evidence for significant lipolysis in skeletal muscle. J Clin Investig 96(1):370–377
Mannion AF, Jakeman PM, Dunnett M, Harris RC, Willan PL (1992) Carnosine and anserine concentrations in the quadriceps femoris muscle of healthy humans. Eur J Appl Physiol 64(1):47–50
Miller S, Chinkes D, MacLean DA, Gore D, Wolfe RR (2004) In vivo muscle amino acid transport involves two distinct processes. Am J Physiol Endocrinol Metab 287(1):E136–E141
Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM (2009) Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89(1):161–168
Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273(1 Pt 1):E99–E107
Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR (2000) An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol (Bethesda, Md: 1985) 88(2):386–392
Rosdahl H, Hamrin K, Ungerstedt U, Henriksson J (1998) Metabolite levels in human skeletal muscle and adipose tissue studied with microdialysis at low perfusion flow. Am J Physiol 274(5 Pt 1):E936–E945
Siklova-Vitkova M, Polak J, Klimcakova E, Vrzalova J, Hejnova J, Kovacikova M, Kovacova Z, Bajzova M, Rossmeislova L, Hnevkovska Z, Langin D, Stich V (2009) Effect of hyperinsulinemia and very-low-calorie diet on interstitial cytokine levels in subcutaneous adipose tissue of obese women. Am J Physiol Endocrinol Metab 297(5):E1154–E1161
Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR (1999) Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Physiol 276(4 Pt 1):E628–E634
Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR (2003) Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 78(2):250–258
Witard OC, Tieland M, Beelen M, Tipton KD, van Loon LJ, Koopman R (2009) Resistance exercise increases postprandial muscle protein synthesis in humans. Med Sci Sports Exerc 41(1):144–154
Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD (2014) Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr 99(1):86–95
Wolfe RR (2002) Regulation of muscle protein by amino acids. J Nutr 132(10):3219S–3224S
Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, Tarnopolsky MA, Phillips SM (2012) Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr 108(10):1780–1788
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This work has been supported by an EMBARK postgraduate scholarship from the Irish Research Council for Science, Engineering and Technology (IRCSET) awarded to WGM and Higher Education Association Research Facilities Enhancement Scheme awarded to PMJ.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the University of Limerick Research Ethics Committee (ULREC Approval 09/07) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
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McCormack, W.G., Cooke, J.P., O’Connor, W.T. et al. Dynamic measures of skeletal muscle dialysate and plasma amino acid concentration in response to exercise and nutrient ingestion in healthy adult males. Amino Acids 49, 151–159 (2017). https://doi.org/10.1007/s00726-016-2343-8
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DOI: https://doi.org/10.1007/s00726-016-2343-8