Introduction to in vivo 31P magnetic resonance spectroscopy of (human) skeletal muscle

31P magnetic resonance spectroscopy (MRS) offers a unique non-invasive window on energy metabolism in skeletal muscle, with possibilities for longitudinal studies and of obtaining important bioenergetic data continuously and with sufficient time resolution during muscle exercise. The present paper provides an introductory overview of the current status of in vivo 31P MRS of skeletal muscle, focusing on human applications, but with some illustrative examples from studies on transgenic mice. Topics which are described in the present paper are the information content of the 31P magnetic resonance spectrum of skeletal muscle, some practical issues in the performance of this MRS methodology, related muscle biochemistry and the validity of interpreting results in terms of biochemical processes, the possibility of investigating reaction kinetics in vivo and some indications for fibre-type heterogeneity as seen in spectra obtained during exercise.

[1]  R. Kearney,et al.  Fitting cytosolic ADP recovery after exercise with a step response function , 1999, Magnetic resonance in medicine.

[2]  R. B. Moon,et al.  Determination of intracellular pH by 31P magnetic resonance. , 1973, The Journal of biological chemistry.

[3]  R. Shulman,et al.  31P nuclear magnetic resonance measurements of muscle glucose-6-phosphate. Evidence for reduced insulin-dependent muscle glucose transport or phosphorylation activity in non-insulin-dependent diabetes mellitus. , 1992, The Journal of clinical investigation.

[4]  G K Radda,et al.  Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. , 1994, Magnetic resonance quarterly.

[5]  M. Sibomana,et al.  31P NMR saturation transfer study of the creatine kinase reaction in human skeletal muscle at rest and during exercise , 1997, Magnetic resonance in medicine.

[6]  B. Massie,et al.  Dissociation of [H+] from fatigue in human muscle detected by high time resolution 31P‐NMR , 1993, Muscle & nerve.

[7]  D. Gadian,et al.  Mapping of metabolites in whole animals by 31P NMR using surface coils , 1980, Nature.

[8]  P R Luyten,et al.  Broadband proton decoupling in human 31p NMR spectroscopy , 1989, NMR in biomedicine.

[9]  S. Confort-Gouny,et al.  Heterogeneity of metabolic response to muscular exercise in humans , 1990, FEBS letters.

[10]  Britton Chance,et al.  An in vivo phosphorus nuclear magnetic resonance study of the variations with age in the phosphodiers' content of human muscle , 1988, Mechanisms of Ageing and Development.

[11]  J. Haselgrove,et al.  Functional pools of oxidative and glycolytic fibers in human muscle observed by 31P magnetic resonance spectroscopy during exercise. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Kushmerick,et al.  Creatine Kinase Equilibration Follows Solution Thermodynamics in Skeletal Muscle. , 1995, The Journal of Biological Chemistry.

[13]  S Nioka,et al.  Multiple controls of oxidative metabolism in living tissues as studied by phosphorus magnetic resonance. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Robert J. Gillies,et al.  NMR in physiology and biomedicine , 1994 .

[15]  P. Zaniol,et al.  Inorganic phosphate is transported into mitochondria in the absence of ATP biosynthesis: an in vivo 31P NMR study in the human skeletal muscle. , 1996, Biochemical and biophysical research communications.

[16]  D. I. Hoult,et al.  Observation of tissue metabolites using 31P nuclear magnetic resonance , 1974, Nature.

[17]  V. Saks,et al.  Cellular Bioenergetics: Role of Coupled Creatine Kinases , 1994, Developments in Molecular and Cellular Biochemistry.

[18]  R. Gupta,et al.  31P NMR studies of intracellular free Mg2+ in intact frog skeletal muscle. , 1980, The Journal of biological chemistry.

[19]  R. Kreis,et al.  Effect of exercise on the creatine resonances in 1H MR spectra of human skeletal muscle. , 1999, Journal of magnetic resonance.

[20]  I. Smith,et al.  Magnetic resonance spectroscopy in biology and medicine. , 1989, Clinical biochemistry.

[21]  R. Shulman,et al.  Nuclear Magnetic Resonance Studies of Muscle and Applications to Exercise and Diabetes , 1996, Diabetes.

[22]  L. Ploutz-Snyder,et al.  Energy-rich phosphates in slow and fast human skeletal muscle. , 1995, The American journal of physiology.

[23]  P J Geiger,et al.  Transport of energy in muscle: the phosphorylcreatine shuttle. , 1981, Science.

[24]  G K Radda,et al.  Examination of a case of suspected McArdle's syndrome by 31P nuclear magnetic resonance. , 1981, The New England journal of medicine.

[25]  P. Matthews,et al.  Energetics of human muscle: Exercise‐induced ATP depletion , 1986, Magnetic resonance in medicine.

[26]  N. Secher,et al.  31P-NMR spectroscopy, rsEMG, and histochemical fiber types of human wrist flexor muscles. , 1994, Journal of applied physiology.

[27]  M. Kushmerick.  Bioenergetics and muscle cell types. , 1995, Advances in experimental medicine and biology.

[28]  M J Kushmerick,et al.  A simple analysis of the "phosphocreatine shuttle". , 1984, The American journal of physiology.

[29]  A. van den Boogaart,et al.  Quantitative data analysis of in vivo MRS data sets , 1997 .

[30]  T R Brown,et al.  NOE Enhancements and T1 Relaxation Times of Phosphorylated Metabolites in Human Calf Muscle at 1.5 Tesla , 1995, Magnetic resonance in medicine.

[31]  B Chance,et al.  Mitochondrial regulation of phosphocreatine/inorganic phosphate ratios in exercising human muscle: a gated 31P NMR study. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[32]  T R Brown,et al.  Practical applications of chemical shift imaging , 1992, NMR in biomedicine.

[33]  J. J. van Vaals,et al.  Alterations in relative phosphocreatine concentrations in preclinical mouse muscular dystrophy revealed by in vivo nmr , 1988, NMR in biomedicine.

[34]  Keith R Thulborn,et al.  Absolute molar concentrations by NMR in inhomogeneous B1. A scheme for analysis of in vivo metabolites , 1983 .

[35]  G. Radda,et al.  In Vivo functioning of creatine phosphokinase in human forearm muscle, studied by 31P NMR saturation transfer , 1989, Magnetic Resonance in Medicine.

[36]  P. Jehenson,et al.  Phosphorus NMR spectroscopy study of muscular enzyme deficiencies involving glycogenolysis and glycolysis , 1987, Neurology.

[37]  Kevin M. Brindle,et al.  NMR methods for measuring enzyme kinetics in vivo , 1988 .

[38]  E. Achten,et al.  31P-NMR spectroscopy and the metabolic properties of different muscle fibers. , 1990, Journal of applied physiology.

[39]  A. Heerschap,et al.  Effects of ischemia on skeletal muscle energy metabolism in mice lacking creatine kinase monitored by in vivo 31P nuclear magnetic resonance spectroscopy , 1999, NMR in biomedicine.

[40]  D. Gadian,et al.  Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study. , 1983, Molecular biology & medicine.

[41]  R. Shulman,et al.  In vivo regulation of muscle glycogen synthase and the control of glycogen synthesis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[42]  K. Sahlin,et al.  Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. , 1993, The Biochemical journal.

[43]  G. Radda,et al.  Assessment of mitochondrial function and control in normal and diseased states. , 1995, Biochimica et biophysica acta.

[44]  Truman R. Brown,et al.  Application of Principal-Component Analysis for NMR Spectral Quantitation , 1995 .

[45]  M. Wyss,et al.  Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. , 1992, The Biochemical journal.

[46]  M. Rudin,et al.  Measurement of Reaction Rates In Vivo Using Magnetization Transfer Techniques , 1992 .

[47]  B. Chance,et al.  Energy metabolism of the untrained muscle of elite runners as observed by 31P magnetic resonance spectroscopy: evidence suggesting a genetic endowment for endurance exercise. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Arend Heerschap,et al.  Altered Ca2+ Responses in Muscles with Combined Mitochondrial and Cytosolic Creatine Kinase Deficiencies , 1997, Cell.

[49]  R. Briggs,et al.  A 31P NMR study of mitochondrial inorganic phosphate visibility: effects of Ca2+, Mn2+, and the pH gradient. , 1992, Biochemistry.

[50]  G. Goelman,et al.  pH heterogeneity during exercise in localized spectra from single human muscles. , 1993, The American journal of physiology.

[51]  T. Brown,et al.  Application of 31P-NMR spectroscopy to the study of striated muscle metabolism. , 1982, The American journal of physiology.

[52]  J. Fleg,et al.  The relationship between creatine kinase kinetics and exercise intensity in human forearm is unchanged by age. , 2000, American journal of physiology. Endocrinology and metabolism.

[53]  P. Cozzone,et al.  23 – 31P NMR Spectroscopy of Metabolic Changes Associated with Muscle Exercise: Physiopathological Applications , 1994 .

[54]  P. Bachert,et al.  Kinetics of the in vivo31P1H nuclear overhauser effect of the human-calf-muscle phosphocreatine resonance , 1992 .

[55]  D. van Ormondt,et al.  Analysis of NMR Data Using Time Domain Fitting Procedures , 1992 .

[56]  Arend Heerschap,et al.  Metabolic changes in reflex sympathetic dystrophy: A 31P NMR spectroscopy study , 1993, Muscle & nerve.

[57]  Roger J. Ordidge,et al.  Image-selected in Vivo spectroscopy (ISIS). A new technique for spatially selective nmr spectroscopy , 1986 .

[58]  Britton Chance,et al.  Magnetic Resonance Spectroscopy of Muscle Bioenergetics , 1994 .