Integrating muscle cell biochemistry and whole-body physiology in humans:(31)P-MRS data from the InSight trial

Lindsay M Edwards, Graham J Kemp, Renee M Dwyer, Justin T Walls, Huddy Fuller, Steven R Smith, Conrad P Earnest, Lindsay M Edwards, Graham J Kemp, Renee M Dwyer, Justin T Walls, Huddy Fuller, Steven R Smith, Conrad P Earnest

Abstract

We acquired (31)P-MRS data from skeletal muscle of subjects of mixed gender and ethnicity, combined with a panel of physiological characteristics, and tested several long-standing hypotheses regarding relationships between muscle cell biochemistry and whole-body physiology with unusually high statistical power. We hypothesized that i) whole-body VO(2)max would correlate with muscle respiratory capacity, ii) resting muscle phosphocreatine concentration ([PCr]) would negatively correlate with delta efficiency and iii) muscle mitochondrial function would positively correlate with both resting VO(2) and total daily energy expenditure (TDEE). Muscle respiratory capacity explained a quarter of the variation in VO(2)max (r(2) = 26, p < .001, n = 87). There was an inverse correlation between muscle [PCr] and delta efficiency (r = -23, p = 046, n = 87). There was also a correlation between [PCr] recovery halftime and TDEE (r = -23, p = 035, n = 87). Our data not only provide insights into muscle cell chemistry and whole-body physiology but our mixed cohort means that our findings are broadly generalizable.

Figures

Figure 1. Correlations between 31 P-MRS estimates…
Figure 1. Correlations between 31P-MRS estimates of mitochondrial function and either absolute (left column) or mass-adjusted (right column) VO2max (n = 86).
Absolute VO2max is in L min−1, mass-adjusted VO2max is in mL min−1 kg−1.
Figure 2. Correlation between PCr 1/2t (see…
Figure 2. Correlation between PCr1/2t (see main text for details) and total daily energy expenditure (TDEE); relationship is significant at p < .05.
Figure 3. Correlations between 31 P-MRS estimates…
Figure 3. Correlations between 31P-MRS estimates of mitochondrial function and percent body fat (left column) or fat mass (right column, in kg) (n = 86).
Figure 4. Principle components analysis scores biplot…
Figure 4. Principle components analysis scores biplot for 31P-MRS data from 87 subjects of mixed gender and ethnicity.

References

    1. Kemp G. J. & Radda G. K. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q 10, 43–63 (1994).
    1. Coyle E. F., Sidossis L. S., Horowitz J. F. & Beltz J. D. Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sports Exerc 24, 782–788 (1992).
    1. Livingstone M. B. & Black A. E. Markers of the validity of reported energy intake. J Nutr 133 Suppl 3, 895S–920S (2003).
    1. Schoeller D. A. How accurate is self-reported dietary energy intake? Nutr Rev 48, 373–379 (1990).
    1. Schulz L. O., Alger S., Harper I., Wilmore J. H. & Ravussin E. Energy expenditure of elite female runners measured by respiratory chamber and doubly labeled water. J Appl Physiol 72, 23–28 (1992).
    1. Forbes G. B. in Human body composition. Growth, aging, nutrition, and activity. 209–247 (Springer-Verlag, 1987).
    1. Forbes G. B., Brown M. R., Welle S. L. & Lipinski B. A. Deliberate overfeeding in women and men: energy cost and composition of the weight gain. Br J Nutr 56, 1–9 (1986).
    1. Pullar J. D. & Webster A. J. The energy cost of fat and protein deposition in the rat. Br J Nutr 37, 355–363 (1977).
    1. Spady D. W., Payne P. R., Picou D. & Waterlow J. C. Energy balance during recovery from malnutrition. Am J Clin Nutr 29, 1073–1088 (1976).
    1. Tataranni P. A. et al. Body weight gain in free-living Pima Indians: effect of energy intake vs expenditure. Int J Obes Relat Metab Disord 27, 1578–1583 (2003).
    1. de Jonge L. et al. Validation study of energy expenditure and intake during calorie restriction using doubly labeled water and changes in body composition. Am J Clin Nutr 85, 73–79 (2007).
    1. Jubrias S. A., Crowther G. J., Shankland E. G., Gronka R. K. & Conley K. E. Vol. 553, 589–599 (2003).
    1. Naressi A., Couturier C., Castang I., de Beer R. & Graveron-Demilly D. Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput Biol Med 31, 269–286 (2001).
    1. Vanhamme L., van den Boogaart A. & Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129, 35–43 (1997).
    1. Kemp G. J., Meyerspeer M. & Moser E. Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by 31P MRS: a quantitative review. NMR Biomed 20, 555–565 (2007).
    1. Golding E. M., Teague W. E. & Dobson G. P. Adjustment of K' to varying pH and pMg for the creatine kinase, adenylate kinase and ATP hydrolysis equilibria permitting quantitative bioenergetic assessment. J Exp Biol 198, 1775–1782 (1995).
    1. Braun M. Differential Equations and their Applications. 4 edn, (Springer, 1941).
    1. Amara C. E. et al. Mitochondrial function in vivo: Spectroscopy provides window on cellular energetics. Methods 46, 312–318 (2008).
    1. Jeneson J. A. L., Wiseman R. W., Westerhoff H. V. & Kushmerick M. J. The signal transduction function for oxidative phosphorylationiIs at least second order in ADP. J. Biol. Chem. 271, 27995–27998 (1996).
    1. Rodgers J. L. & Nicewander W. A. Thirteen ways to look at the correlation coefficient. The American Statistician 42, 59–66 (1988).
    1. Larson-Meyer D. E., Newcomer B. R., Hunter G. R., Hetherington H. P. & Weinsier R. L. 31P MRS measurement of mitochondrial function in skeletal muscle: reliability, force-level sensitivity and relation to whole body maximal oxygen uptake. NMR Biomed 13, 14–27 (2000).
    1. McCully K. K., Fielding R. A., Evans W. J., Leigh J. S. & Posner J. D. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. Journal of Applied Physiology 75, 813–819 (1993).
    1. Conley K. E. et al. Ageing, muscle properties and maximal O(2) uptake rate in humans. J Physiol 526 Pt 1, 211–217 (2000).
    1. Wyss M. & Wallimann T. Creatine metabolism and the consequences of creatine depletion in muscle. Mol Cell Biochem 133–134, 51–66 (1994).
    1. Madhu B., Lagerwall K. & Soussi B. Phosphorus metabolites in different muscles of the rat leg by 31P image-selected in vivo spectroscopy. NMR Biomed 9, 327–332 (1996).
    1. Takahashi H. et al. Relationships between fiber composition and NMR measurements in human skeletal muscle. NMR Biomed 9, 8–12 (1996).
    1. Wasserman K., Hansen J. E., Sue D. Y., Stringer W. W. & Whipp B. J. in Principles of Exercise Testing and Interpretation (Lipincott Williams and Wilkins., 2005).
    1. Mallory L. A. et al. Influence of peak VO2 and muscle fiber type on the efficiency of moderate exercise. Med Sci Sports Exerc 34, 1279–1287 (2002).
    1. Hunter G. R. et al. Inverse relationship between exercise economy and oxidative capacity in muscle. Eur J Appl Physiol 94, 558–568 (2005).
    1. Lucia A., Hoyos J., Perez M., Santalla A. & Chicharro J. L. Inverse relationship between VO2max and economy/efficiency in world-class cyclists. Med Sci Sports Exerc 34, 2079–2084 (2002).
    1. Edwards L. M. et al. Uncoupling protein 3 inversely correlates with resting metabolic rate in fit, young men. Proc Physiol Soc 11, C49 (2008).
    1. Vaughan-Jones R. D., Spitzer K. W. & Swietach P. Intracellular pH regulation in heart. J Mol Cell Cardiol 46, 318–331 (2009).
    1. Kampert J. B., Blair S. N., Barlow C. E.& Kohl H. W., 3rd. Physical activity, physical fitness, and all-cause and cancer mortality: a prospective study of men and women. Ann Epidemiol 6, 452–457 (1996).
    1. Mogensen M., Bagger M., Pedersen P. K., Fernstrom M. & Sahlin K. Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency. J Physiol 571, 669–681 (2006).

Source: PubMed

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