Stable isotope tracers and exercise physiology: past, present and future

Journal of Physiology

Volumn 595, Issue 9, 2017, Pages 2873-2882

  Wilkinson, Daniel J ^a   Brook, Matthew S ^a   Smith, Kenneth ^a   Atherton, Philip J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

exercise; metabolism; muscle; stable isotope

Indexed keywords

3 METHYLHISTIDINE; ALANINE; CHOLESTEROL; DEUTERIUM OXIDE; GLUCOSE; GLYCEROL; HISTIDINE; ISOTOPE TRACER; MUSCLE PROTEIN; PHENYLALANINE; TRACER; UNCLASSIFIED DRUG; VALINE;

COMPUTER ASSISTED TOMOGRAPHY; DIETARY INTAKE; DUAL ENERGY X RAY ABSORPTIOMETRY; EXERCISE; EXERCISE PHYSIOLOGY; FLUXOMICS; HUMAN; LIPID METABOLISM; METABOLOMICS; MUSCLE BIOPSY; MUSCLE HYPERTROPHY; MUSCLE MASS; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN SYNTHESIS; PROTEOMICS; RESISTANCE TRAINING; REVIEW; URINALYSIS; MASS FRAGMENTOGRAPHY; METABOLISM; PHYSIOLOGY; PROCEDURES; SKELETAL MUSCLE; TISSUE DISTRIBUTION; URINARY EXCRETION;

DEUTERIUM OXIDE; EXERCISE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMANS; MAGNETIC RESONANCE IMAGING; METABOLOMICS; MUSCLE, SKELETAL; RENAL ELIMINATION; TISSUE DISTRIBUTION;

EID: 84990889344     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP272277     Document Type: Review

References (62)

1. Baumann PQ, Stirewalt WS, O'Rourke BD, Howard D & Nair KS (1994). Precursor pools of protein synthesis: a stable isotope study in a swine model. Am J Physiol Endocrinol Metab 267, E203–E209.
2. 18O measurement by continuous-flow isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 10, 969–973.
3. Belloto E, Diraison F, Basset A, Allain G, Abdallah P & Beylot M (2007). Determination of protein replacement rates by deuterated water: validation of underlying assumptions. Am J Physiol Endocrinol Metab 292, E1340–E1347.
4. τ-methylhistidine. Metabolism 27, 525–530.
5. Biolo G, Gastaldelli A, Zhang XJ & Wolfe RR (1994). Protein synthesis and breakdown in skin and muscle: a leg model of amino acid kinetics. Am J Physiol Endocrinol Metab 267, E467–E474.
6. 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 Endocrinol Metab 268, E514–E520.
7. 2O)-derived measures of muscle protein synthesis and mTORc1-signaling. FASEB J 29, 4485–4496.
8. Burd NA, West DWD, Moore DR, Atherton PJ, Staples AW, Prior T, Tang JE, Rennie MJ, Baker SK & Phillips SM (2011). Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. J Nutr 141, 568–573.
9. Busch R, Kim Y-K, Neese RA, Schade-Serin V, Collins M, Awada M, Gardner JL, Beysen C, Marino ME, Misell LM & Hellerstein MK (2006). Measurement of protein turnover rates by heavy water labeling of nonessential amino acids. Biochim Biophys Acta 1760, 730–744.
10. Busch R, Neese RA, Awada M, Hayes GM & Hellerstein MK (2007). Measurement of cell proliferation by heavy water labeling. Nat Protoc 2, 3045–3057.
11. 2O labeling to quantify static and dynamic changes in cholesterol and cholesterol esters by high resolution LC/MS. J Lipid Res 52, 159–169.
12. Clark RV, Walker AC, O'Connor-Semmes RL, Leonard MS, Miller RR, Stimpson SA, Turner SM, Ravussin E, Cefalu WT, Hellerstein MK & Evans WJ (2014). Total body skeletal muscle mass: estimation by creatine (methyl-d3) dilution in humans. J Appl Physiol 116, 1605–1613.
13. Damas F, Phillips SM, Libardi CA, Vechin FC, Lixandrão ME, Jannig PR, Costa LAR, Bacurau AV, Snijders T, Parise G, Tricoli V, Roschel H & Ugrinowitsch C (2016). Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J Physiol 594, 5209–5222.
14. Decaris ML, Emson CL, Li K, Gatmaitan M, Luo F, Cattin J, Nakamura C, Holmes WE, Angel TE, Peters MG, Turner SM & Hellerstein MK (2015). Turnover rates of hepatic collagen and circulating collagen-associated proteins in humans with chronic liver disease. PLoS One 10, e0123311.
15. Diraison F, Pachiaudi C & Beylot M (1997). Measuring lipogenesis and cholesterol synthesis in humans with deuterated water: use of simple gas chromatographic/mass spectrometric techniques. J Mass Spectrom 32, 81–86.
16. 2O to study the influence of feeding on protein synthesis: effect of isotope equilibration in vivo vs. in cell culture. Am J Physiol Endocrinol Metab 288, E1277–E1283.
17. Dufner D & Previs SF (2003). Measuring in vivo metabolism using heavy water. Curr Opin Clin Nutr Metab Care 6, 511–517.
18. Friedlander AL, Jacobs KA, Fattor JA, Horning MA, Hagobian TA, Bauer TA, Wolfel EE & Brooks GA (2007). Contributions of working muscle to whole body lipid metabolism are altered by exercise intensity and training. Am J Physiol Endocrinol Metab 292, E107–E116.
19. 2O to measure skeletal muscle protein synthesis. Nutr Metab (Lond) 7, 31.
20. Gasier HG, Fluckey JD, Previs SF, Wiggs MP & Riechman SE (2012). Acute resistance exercise augments integrative myofibrillar protein synthesis. Metabolism 61, 153–156.
21. Goran MI, Peters EJ, Herndon DN & Wolfe RR (1990). Total energy expenditure in burned children using the doubly labeled water technique. Am J Physiol Endocrinol Metab 259, E576–E585.
22. Gundersen K (2016). Muscle memory and a new cellular model for muscle atrophy and hypertrophy. J Exp Biol 219, 235–242.
23. Guo Z & Jensen MD (1998). Intramuscular fatty acid metabolism evaluated with stable isotopic tracers. J Appl Physiol 84, 1674–1679.
24. Halliday D, Pacy PJ, Cheng KN, Dworzak F, Gibson JN & Rennie MJ (1988). Rate of protein synthesis in skeletal muscle of normal man and patients with muscular dystrophy: a reassessment. Clin Sci (Lond) 74, 237–240.
25. Hellerstein MK (2004). New stable isotope-mass spectrometric techniques for measuring fluxes through intact metabolic pathways in mammalian systems: introduction of moving pictures into functional genomics and biochemical phenotyping. Metab Eng 6, 85–100.
26. 2H labeling between body water and free amino acids: enabling studies of proteome synthesis. Anal Biochem 415, 197–199.
27. International Atomic Energy Agency (IAEA) (2011). Introduction to Body Composition Assessment Using the Deuterium Dilution Technique with Analysis of Saliva Samples by Fourier Transform Infrared Spectrometry. IAEA, Vienna.
28. 14C. J Appl Physiol 28, 264–267.
29. Kuksis A & Myher JJ (1995). Application of tandem mass spectrometry for the analysis of long-chain carboxylic acids. J Chromatogr B Biomed Sci Appl 671, 35–70.
30. Kumar V, Atherton P, Smith K & Rennie MJ (2009). Human muscle protein synthesis and breakdown during and after exercise. J Appl Physiol 106, 2026–2039.
31. MacDonald AJ, Small AC, Greig CA, Husi H, Ross JA, Stephens NA, Fearon KCH & Preston T (2013). A novel oral tracer procedure for measurement of habitual myofibrillar protein synthesis. Rapid Commun Mass Spectrom 27, 1769–1777.
32. Marliss EB, Wei CN & Dietrich LL (1979). The short-term effects of protein intake on 3-methylhistidine excretion. Am J Clin Nutr 32, 1617–1621.
33. Mitchell CJ, Churchward-Venne TA, Parise G, Bellamy L, Baker SK, Smith K, Atherton PJ & Phillips SM (2014). Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS One 9, e89431.
34. 13C fluxomics. Curr Opin Biotechnol 34C, 82–90.
35. Overmyer KA, Evans CR, Qi NR, Minogue CE, Carson JJ, Chermside-Scabbo CJ, Koch LG, Britton SL, Pagliarini DJ, Coon JJ & Burant CF (2015). Maximal oxidative capacity during exercise is associated with skeletal muscle fuel selection and dynamic changes in mitochondrial protein acetylation. Cell Metab 21, 468–478.
36. Pennings B, Koopman R, Beelen M, Senden JMG, Saris WHM & van Loon LJC (2011). 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.
37. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GF, Hill RE & Grant SM (1996). Effects of training duration on substrate turnover and oxidation during exercise. J Appl Physiol 81, 2182–2191.
38. Phillips SM, Tipton KD, Ferrando AA & Wolfe RR (1999). Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Physiol Endocrinol Metab. 276, E118–E124.
39. 15N]creatine. Pediatr Res 10, 184–188.
40. 2O: application to patients with end-stage renal disease. Am J Physiol Endocrinol Metab 286, E665–E672.
41. Previs SF, Herath K, Castro-Perez J, Mahsut A, Zhou H, McLaren DG, Shah V, Rohm RJ, Stout SJ, Zhong W, Wang S-P, Johns DG, Hubbard BK, Cleary MA & Roddy TP (2015). Effect of error propagation in stable isotope tracer studies: an approach for estimating impact on apparent biochemical flux. Methods Enzymol 561, 331–358.
42. 2O and liquid chromatography tandem mass spectrometry. Anal Biochem 420, 73–83.
43. Rennie MJ, Edwards RH, Halliday D, Matthews DE, Wolman SL & Millward DJ (1982). Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting. Clin Sci (Lond) 63, 519–523.
44. Rennie MJ & Halliday D (1984). The use of stable isotope tracers as metabolic probes of whole-body and limb metabolism. Proc Nutr Soc 43, 189–196.
45. Robinson MM, Turner SM, Hellerstein MK, Hamilton KL & Miller BF (2011). Long-term synthesis rates of skeletal muscle DNA and protein are higher during aerobic training in older humans than in sedentary young subjects but are not altered by protein supplementation. FASEB J 25, 3240–3249.
46. Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E & Wolfe RR (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol Endocrinol Metab 265, E380–E391.
47. Schoenheimer R & Rittenberg D (1936). Deuterium as an indicator in the study of intermediary metabolism – VI. Synthesis and destruction of fatty acids in the organism. J Biol Chem 114, 381–396.
48. Shankaran M, King CL, Angel TE, Holmes WE, Li KW, Colangelo M, Price JC, Turner SM, Bell C, Hamilton KL, Miller BF & Hellerstein MK (2016). Circulating protein synthesis rates reveal skeletal muscle proteome dynamics. J Clin Invest 126, 288.
49. Sheffield-Moore M, Dillon EL, Randolph KM, Casperson SL, White GR, Jennings K, Rathmacher J, Schuette S, Janghorbani M, Urban RJ, Hoang V, Willis M & Durham WJ (2014). Isotopic decay of urinary or plasma 3-methylhistidine as a potential biomarker of pathologic skeletal muscle loss. J Cachexia Sarcopenia Muscle 5, 19–25.
50. 3-creatine dilution method. J Cachexia Sarcopenia Muscle 4, 217–223.
51. 3) dilution in rats. J Appl Physiol 112, 1940–1948.
52. 2O. Am J Physiol Endocrinol Metab 286, E577–E588.
53. 2O incorporation into the glycerol moiety and application of MIDA. Am J Physiol Endocrinol Metab 285, E790–E803.
54. Ussing H (1937). The exchange of H and D atoms between water and protein in vivo and in vitro. Skand Arch Physiol 78, 225–241.
55. Ussing H (1938). The exchange of H and D atoms between water and protein in vivo and in vitro. Skand Arch Physiol 77, 107–122.
56. Ussing H (1941). The rate of protein renewal in mice and rats studied by means of heavy hydrogen. Acta Physiol Scand 2, 209–221.
57. Voogt JN, Awada M, Murphy EJ, Hayes GM, Busch R & Hellerstein MK (2007). Measurement of very low rates of cell proliferation by heavy water labeling of DNA and gas chromatography/pyrolysis/isotope ratio-mass spectrometric analysis. Nat Protoc 2, 3058–3062.
58. Watt PW, Lindsay Y, Scrimgeour CM, Chien PA, Gibson JN, Taylor DJ & Rennie MJ (1991). Isolation of aminoacyl-tRNA and its labeling with stable-isotope tracers: Use in studies of human tissue protein synthesis. Proc Natl Acad Sci USA 88, 5892–5896.
59. 6]phenylalanine for acute measurement of muscle protein synthesis in humans. Physiol Rep 3, e12433.
60. 2O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am J Physiol Endocrinol Metab 306, E571–E579.
61. Yang RD, Matthews DE, Bier DM, Lo C & Young VR (1984). Alanine kinetics in humans: influence of different isotopic tracers. Am J Physiol Endocrinol Metab 247, E634–E638.
62. Zhou H, Wang S-P, Herath K, Kasumov T, Sadygov RG, Previs SF & Kelley DE (2015). Tracer-based estimates of protein flux in cases of incomplete product renewal: evidence and implications of heterogeneity in collagen turnover. Am J Physiol Endocrinol Metab 309, E115–E121.