Measurement of unidirectional Pi to ATP flux in human visual cortex at 7 T by using in vivo 31P magnetic resonance spectroscopy

Taking advantage of the high NMR detection sensitivity and the large chemical shift dispersion offered by ultra-high field strength of 7 T, the effect of magnetization transfer on inorganic phosphate (Pi) resonance during saturation of γ-ATP resonance, mediated by the ATP synthesis reaction, was observed noninvasively in the human primary visual cortex by using in vivo 31P magnetic resonance spectroscopy. The unidirectional flux from Pi to ATP was measured by using progressive saturation transfer experiments. The cerebral ATP synthesis rate in the human primary visual cortex measured by 31P magnetic resonance spectroscopy in this study was 12.1 ± 2.8 μmol ATP/g per min, which agreed well with the value that was calculated indirectly from the cerebral metabolic rate of glucose consumption reported previously.

[1]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[2]  P. Magistretti,et al.  Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  K. Uğurbil,et al.  In vivo 31P magnetic resonance spectroscopy of human brain at 7 T: An initial experience , 2003, Magnetic resonance in medicine.

[4]  G. Bodenhausen,et al.  Principles of nuclear magnetic resonance in one and two dimensions , 1987 .

[5]  Jean-Louis Martiel,et al.  Uptake of locally applied deoxyglucose, glucose and lactate by axons and schwann cells of rat vagus nerve , 2003, The Journal of physiology.

[6]  A. From,et al.  31P NMR studies of ATP synthesis and hydrolysis kinetics in the intact myocardium. , 1987, Biochemistry.

[7]  R. Balaban,et al.  Metabolic Network Control of Oxidative Phosphorylation , 2003, Journal of Biological Chemistry.

[8]  M. Weiner,et al.  31P NMR saturation transfer measurements of phosphorus exchange reactions in rat heart and kidney in situ. , 1986, Biochemistry.

[9]  K Uğurbil,et al.  Measurement of an individual rate constant in the presence of multiple exchanges: application to myocardial creatine kinase reaction. , 1986, Biochemistry.

[10]  A. From,et al.  Measurement of ATP synthesis rates by 31P‐NMR spectroscopy in the intact myocardium in vivo , 1990, Magnetic resonance in medicine.

[11]  R. Shulman,et al.  31P NMR saturation-transfer measurements in Saccharomyces cerevisiae: characterization of phosphate exchange reactions by iodoacetate and antimycin A inhibition. , 1987, Biochemistry.

[12]  J. Hatazawa,et al.  Measurement of the Ratio of Cerebral Oxygen Consumption to Glucose Utilization by Positron Emission Tomography: Its Consistency with the Values Determined by the Kety-Schmidt Method in Normal Volunteers , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[13]  E. Shoubridge,et al.  31P NMR saturation transfer measurements of the steady state rates of creatine kinase and ATP synthetase in the rat brain , 1982, FEBS letters.

[14]  K. Uğurbil,et al.  31P nuclear magnetic resonance measurements of ATPase kinetics in aerobic Escherichia coli cells. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[15]  K Ugurbil,et al.  Increase of creatine kinase activity in the visual cortex of human brain during visual stimulation: A 31p NMR magnetization transfer study , 1997, Magnetic resonance in medicine.

[16]  M. Portman.  Measurement of unidirectional P(i)-->ATP flux in lamb myocardium in vivo. , 1994, Biochimica et biophysica acta.

[17]  R Gruetter,et al.  Automatic, localized in Vivo adjustment of all first‐and second‐order shim coils , 1993, Magnetic resonance in medicine.

[18]  J. Balschi,et al.  ATP synthesis and degradation rates in the perfused rat heart. 31P-nuclear magnetic resonance double saturation transfer measurements. , 1988, Biophysical journal.

[19]  R. Shulman,et al.  In vivo 31P nuclear magnetic resonance saturation transfer measurements of phosphate exchange reactions in the yeast Saccharomyces cerevisiae , 1985, FEBS letters.

[20]  C. Hardy,et al.  Mapping creatine kinase reaction rates in human brain and heart with 4 tesla saturation transfer 31P NMR , 1992 .

[21]  A. From,et al.  31P NMR measurement of mitochondrial uncoupling in isolated rat hearts. , 1990, The Journal of biological chemistry.

[22]  P. Magistretti,et al.  How to balance the brain energy budget while spending glucose differently , 2003, The Journal of physiology.

[23]  R. P. Shockley,et al.  Determination of rat cerebral cortical blood volume changes by capillary mean transit time analysis during hypoxia, hypercapnia and hyperventilation , 1988, Brain Research.

[24]  A. From,et al.  31P NMR measurement of ATP synthesis rate in perfused intact rat hearts , 1986, FEBS letters.

[25]  P. Narasimhan,et al.  31P magnetization transfer studies in the monkey brain , 1992, Magnetic resonance in medicine.

[26]  K. Uğurbil.  Magnetization transfer measurements of creatine kinase and ATPase rates in intact hearts. , 1985, Circulation.

[27]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[28]  I. Silver,et al.  ATP and Brain Function , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  A. From,et al.  ATP synthesis kinetics and mitochondrial function in the postischemic myocardium as studied by 31P NMR. , 1988, The Journal of biological chemistry.

[30]  I. Campbell,et al.  31P-NMR saturation transfer studies of aerobic Escherichia coli cells. , 1988, Biochimica et biophysica acta.

[31]  J. Ingwall,et al.  Reaction rates of creatine kinase and ATP synthesis in the isolated rat heart. A 31P NMR magnetization transfer study. , 1985, The Journal of biological chemistry.

[32]  P. Barker,et al.  Magnesium and pH imaging of the human brain at 3.0 Tesla , 1999, Magnetic resonance in medicine.

[33]  I. Gribbestad,et al.  Nuclear magnetic resonance spectroscopy: biochemical evaluation of brain function in vivo and in vitro. , 1994, Neurotoxicology.

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

[35]  R G Shulman,et al.  NMR studies of enzymatic rates in vitro and in vivo by magnetization transfer , 1984, Quarterly Reviews of Biophysics.

[36]  M. Garwood,et al.  B1-insensitive, single-shot localization and water suppression. , 1996, Journal of magnetic resonance. Series B.

[37]  G. Radda,et al.  31P NMR magnetization-transfer measurements of ATP turnover during steady-state isometric muscle contraction in the rat hind limb in vivo. , 1989, Biochemistry.

[38]  K. Uğurbil,et al.  Saturation-transfer studies of ATP-Pi exchange in isolated perfused rat liver. , 1987, Biochimica et biophysica acta.