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Temporal responses of protein synthesis in human skeletal muscle to feeding

Published online by Cambridge University Press:  09 March 2007

M. A. McNurlan ,
P. Essen ,
E. Milne ,
E. Vinnars ,
P. J. Garlick  and
J. Wernerman
M. A. McNurlan
Affiliation:
The Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
P. Essen
Affiliation:
Department of Anesthesiology and Intensive Care, Huddinge University Hospital, Stockholm, Sweden
E. Milne
Affiliation:
The Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
E. Vinnars
Affiliation:
Department of Anesthesiology and Intensive Care, St Görans Hospital, Stockholm, Sweden
P. J. Garlick
Affiliation:
The Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
J. Wernerman
Affiliation:
Department of Anesthesiology and Intensive Care, St Görans Hospital, Stockholm, Sweden
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Abstract

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In attempting to evaluate alterations in metabolic responses to dietary nutrients that occur in pathological conditions in man, it is first necessary to understand normal metabolic responses. The present study set out to determine the temporal responses of protein synthesis in the skeletal muscle of healthy subjects to the consumption of food. Sequential measurements of protein synthesis in quadriceps muscle were made in eight subjects by injection of 0.05 g L-[l-13C]leucine/kg body-weight. The rate of protein synthesis after an overnight fast (i.e. in the post-absorptive state) was 2.2% muscle protein. After 1 h of eating, protein synthesis was unaltered (2.2%/d), but after 10 h of consuming small hourly meals the rate had risen to 2.9%/d, with a variation in response among individuals. The response of muscle to 10 h of feeding was also investigated in subjects who underwent only one measurement each, either after 10 h of eating small meals or after the same time-period when no food was given. Protein synthesis rates were only slightly elevated in the group of fed individuals (2.3%/d, n 6) compared with the fasted group (2.1%/d, n 6). Taken together the two studies suggest that in healthy adults muscle protein synthesis does not respond quickly to the influx of dietary nutrients and that even after 10 h of feeding any stimulation of protein synthesis is small.

Keywords

Protein synthesisHuman skeletal muscleResponse to feeding
Type
Metabolic Effects of Nutrient Intakes
Information
British Journal of Nutrition , Volume 69 , Issue 1 , January 1993 , pp. 117 - 126
Copyright
Copyright © The Nutrition Society 1993

References

REFERENCES

Baillie, A. G. S. & Garlick, P. J. (1991). Attenuated responses of muscle protein synThesis to fasting and insulin in adult female rats. American Journal of Physiology 262 (Endocrin. Metab. 25), E1–E5.Google Scholar
Banauch, D., Brümmer, W., Ebeling, W., Metz, H., Rindfrey, H. & Laung, H. (1975). Eine glucose-dehydrogenase für die glucose-bestimmung in körperflüssigkeiten (Glucose determination in body fluids by glucose dehydrogenase). Journal of Clinical Chemistry and Clinical Biochemistry 13, 101–107.Google ScholarPubMed
Bruce, A. C., McNurlan, M. A., McHardy, K. C., Broom, J., Buchanan, K. D., Calder, A. G., Milne, E., McGaw, B. A., Garlick, P. J. & James, W. P. T. (1990). Nutrient oxidation patterns and protein metabolism in lean and obese subjects. International Journal of Obesity 14, 631–646.Google ScholarPubMed
Calder, A. G. & Smith, A. (1988). Stable isotope ratio analysis of leucine and ketoisocaproic acid in blood plasma by gas chromatography/mass spectrometry. Use of the tertiary butyldimethylsilyl derivatives. Rapid Communications in Mass Spectrometry 2, 14–16.CrossRefGoogle ScholarPubMed
Conway, J. M., Marable, N. L. & Bodwell, C. E. (1988). Whole-body leucine and energy metabolism in adult women. European Journal of Clinical Nutrition 42, 661–669.Google ScholarPubMed
Dash, R. J., England, B. J., Midgley, J. A. R. & Niswender, G. D. (1975). A specific, non-chromatographic radioimmunoassay for human plasma cortisol. Steroids 26, 647–661.CrossRefGoogle ScholarPubMed
Eisentraut, A., Ohneda, A., Parada, E. & Unger, R. H. (1968). Immunological discrimination between pancreatic and enteric glucagon-like immunoreactivity (GLI) in tissues and plasma. Diabetes 177, 321–322.Google Scholar
Essen, P., McNurlan, M. A., Wernerman, J., Milne, E., Vinnars, E. & Garlick, P. J. (1992). Short-term starvation decreases skeletal muscle protein synThesis rate in man. Clinical Physiology 12, 287–299.CrossRefGoogle ScholarPubMed
Ford, G. C., Cheng, K. N. & Halliday, D. (1985). Analysis of [l-13C]leucine and [13C]KIC in plasma by capillary gas chromatography/mass spectrometry in protein turnover studies. Biomedical Mass Spectrometry 12, 432–436.CrossRefGoogle ScholarPubMed
Garlick, P. J., Fern, M. & Preedy, V. R. (1983). The effect of insulin infusion and food intake on muscle protein synThesis in postabsorptive rats. Biochemical Journal 210, 669–676.CrossRefGoogle ScholarPubMed
Garlick, P. J., McNurlan, M. A. & Preedy, V. R. (1980). A rapid and convenient method for measuring the rate of protein synThesis in tissues by injection of [3H]phenylalanine. Biochemical Journal 192, 719–723.CrossRefGoogle ScholarPubMed
Garlick, P. J., Wernerman, J., McNurlan, M. A., Essen, P., Lobley, G. E., Milne, E., Calder, A. G. & Vinnars, E. (1989). Measurement of the rate of protein synThesis in muscle of postabsorptive young men by injection of a ‘flooding dose’ of [l-13C]1eucine. Clinical Science 77, 329–336.CrossRefGoogle Scholar
Hagenfeldt, L., Eriksson, S. & Wahren, J. (1980). Influence of leucine on arterial concentrations and regional exchange of amino acids in healthy subjects. Clinical Science 59, 173–181.CrossRefGoogle ScholarPubMed
Halliday, D., Pacy, P. J., Cheng, K. N., Dworzak, F., Gibson, J. N. A. & Rennie, M. J. (1988). Rate of protein synThesis in skeletal muscle of normal man and patients with muscular dystrophy: a reassessment. Clinical Science 74, 237–240.CrossRefGoogle ScholarPubMed
Hoffer, L. J., Yang, R. D., Matthews, D. E., Bistrian, B. R., Bier, D. M. & Young, V. R. (1985). Effects of meal consumption on whole body leucine and alanine kinetics in young adult man. British Journal of Nutrition 53, 31–38.CrossRefGoogle Scholar
Li, J. B. & Jefferson, L. S. (1978). Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochimica et Biophysica Acta 544, 351–359.CrossRefGoogle ScholarPubMed
Louard, R. J., Barrett, E. J. & Gelfand, R. A. (1990). Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man. Clinical Science 79, 457–466.CrossRefGoogle ScholarPubMed
Low, R. B., Stirewalt, W. S., Rittling, S. R. & Woodworth, R. C. (1984). Amino acid pools in cultured muscle cells. Journal of Cellular Biochemistry 25, 123–129.CrossRefGoogle ScholarPubMed
McHardy, K. C., McNurlan, M. A., Fearns, L. M., Broom, J. & Garlick, P. J. (1987). The use of somatostatin infusion to study the role of insulin in the regulation of nutrient oxidation in man. Endocrinology 112, Suppl., 79A.Google Scholar
MacKenzie, S. L. & Tenaschuk, D. (1974). Gas-liquid chromatography of N-heptafluorobutyryl isobutyryl esters of amino acids. Journal of Chromatography 97, 19–24.CrossRefGoogle Scholar
McNurlan, M. A., Essen, P., Heys, S. D., Buchan, V., Garlick, P. J. & Wernerman, J. (1991). Measurement of protein synThesis in human skeletal muscle: Further investigation of the flooding technique. Clinical Science 81, 557–564.CrossRefGoogle ScholarPubMed
McNurlan, M. A., Essen, P., Vinnars, E., Garlick, P. J. & Wernerman, J. (1990). Delayed response to feeding on protein synThesis in human skeletal muscle measured by the flooding dose technique. Clinical Nutrition 9, Special Suppl., 12.CrossRefGoogle Scholar
McNurlan, M. A., McHardy, K. C., Broom, J., Calder, A. G., Milne, E. & Garlick, P. J. (1989). Responses of whole-body protein turnover in man to feeding: lack of dependence on insulin. FEBS Journal 3, A1259.Google Scholar
McNurlan, M. A., Tomkins, A. M. & Garlick, P. J. (1979). The effect of starvation on the rate of protein synThesis in rat liver and small intestine. Biochemical Journal 178, 373–379.CrossRefGoogle ScholarPubMed
Matthews, D. E., Schwartz, H. P., Young, R. D., Motil, K. J. & Young, V. R. (1982). Relationship of plasma leucine and 2 ketoisocaproate during a L-[13C]leucine infusion in man: a method for measuring human intracellular leucine tracer enrichment. Metabolism 31, 1105–1112.CrossRefGoogle Scholar
Melville, S., McNurlan, M. A., McHardy, K. C., Broom, J., Milne, E., Calder, A. G. & Garlick, P. J. (1989). The role of degradation in the acute control of protein balance in adult man: Failure of feeding to stimulate protein synThesis as assessed by L-[l-13C]leucine infusion. Metabolism 38, 248–255.CrossRefGoogle Scholar
Midgley, A. R., Rabau, R. W. & Niswender, G. D. (1969). Rddioimmunoassays employing double antibody techniques. Acta Endocrinologica 142, Suppl., 247–254.Google ScholarPubMed
Motil, K. J., Bier, D. M., Matthews, D. E., Burke, J. F. & Young, V. R. (1981 a). Whole body leucine and lysine metabolism studied with [l-13C]leucine and (α-15N]lysine: Response in healthy young men given excess energy intake. Metabolism 30, 783–791.CrossRefGoogle ScholarPubMed
Motil, K. J., Matthews, D. E., Bier, D. M., Burke, J. G., Munro, H. N. & Young, V. R. (1981 b). Whole body leucine and lysine metabolism: Response to dietary protein intake in young men. American Journal of Physiology 240, E712–E721.Google ScholarPubMed
Pacy, P. J., Nair, K. S., Ford, C. & Halliday, D. (1989). Failure of insulin infusion to stimulate fractional muscle protein synThesis in type 1 diabetic patients. Diabetes 38, 618–624.CrossRefGoogle Scholar
Pozefsky, T., Felig, P., Tobin, J. D., Soeldner, J. S. & Cahill, J. G. F. (1969). Amino acid balance across tissues of the forearm in postabsorptive man, effects of insulin at two dose levels. Journal of Clinical Investigation 48, 2273–2282.CrossRefGoogle ScholarPubMed
Read, W. W., Read, M., Rennie, M. J., Griggs, R. C. & Halliday, D. (1984). Preparation ofCO2, from blood and protein-bound amino acid carboxyl groups for quantitation of 13C-isotope enrichments. Biomedical Mass Spectrometry 11, 348–352.CrossRefGoogle Scholar
Rennie, M. J., Edwards, R. H. T., Halliday, D., Matthews, D. E., Wolman, S. L. & Millward, D. J. (1982). Muscle protein synThesis measured by stable isotope techniques in man: The effects of feeding and fasting, Clinical Science 63, 519–523.CrossRefGoogle ScholarPubMed
Smith, K., Barua, J. M., Watt, P. W., Scrimgeour, C. M., Rickhuss, P. K. & Rennie, M. J. (1991). Preliminary evidence of artefactually high values of muscle protein synThesis obtained by the flooding dose technique compared with the constant infusion method. Clinical Nutrition 10, 7.CrossRefGoogle Scholar
Watt, P. W., Stenhouse, M. G., Corbett, M. E. & Rennie, M. J. (1989). t-RNA charging in pig muscle measured by [113C]leucine during fasting and infusion of amino acids. Clinical Nutrition 8, 47.Google Scholar
Wernerman, J., von der Decken, A. & Vinnars, E. (1985). The diurnal pattern of protein synThesis in human skeletal muscle. Clinical Nutrition 4, 203–205.CrossRefGoogle ScholarPubMed
Young, V. R., Gucalp, C., Rand, W. M., Matthews, D. E. & Bier, D. M. (1987). Leucine kinetics during three weeks at submaintenance-to-maintenance intakes of leucine in men: Adaptation and accommodation. Human Nutrition: Clinical Nutrition 41C, 1–18.Google Scholar