In vivo 1H-[13 C]-NMR spectroscopy of cerebral metabolism

NMR in Biomedicine

Volumn 16, Issue 6-7, 2003, Pages 339-357

  de Graaf, Robin A ^a   Mason, Graeme F ^a   Patel, Anant B ^a   Behar, Kevin L ^a   Rothman, Douglas L ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

13C substrates; 1H 13C NMR spectroscopy; Cerebral metabolism; GABA; Glutamate; Glutamine; Neurotransmitter cycle; TCA cycle

Indexed keywords

BRAIN; MAGNETIC FIELD EFFECTS; METABOLISM; NEUROLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

NEUROTRANSMISSION;

BIOMEDICAL ENGINEERING;

4 AMINOBUTYRIC ACID; CARBON 13; GLUCOSE; GLUTAMIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CARBON; DIAGNOSTIC AGENT; GLUTAMINE; PROTON;

BLOOD BRAIN BARRIER; BRAIN FUNCTION; BRAIN METABOLISM; CARBON NUCLEAR MAGNETIC RESONANCE; CELLULAR DISTRIBUTION; ENERGY METABOLISM; GABAERGIC SYSTEM; GRAY MATTER; HUMAN; IN VIVO STUDY; MAGNETIC FIELD; METABOLIC RATE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; RAT; REVIEW; SENSITIVITY ANALYSIS; SIGNAL PROCESSING; WHITE MATTER; ALGORITHM; ANIMAL; BRAIN; METABOLISM; METHODOLOGY; PHYSIOLOGY; STAINING; SYNAPTIC TRANSMISSION;

ALGORITHMS; ANIMALS; BRAIN; CARBON ISOTOPES; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; NEURONS; NEUROTRANSMITTER AGENTS; PROTONS; STAINING AND LABELING; SYNAPTIC TRANSMISSION;

EID: 0348149164     PISSN: 09523480     EISSN: None     Source Type: Journal    
DOI: 10.1002/nbm.847     Document Type: Review

References (80)

1. Siesjo B. Brain Energy Metabolism. Wiley: New York, 1978.
2. 11C. Am. J. Physiol. 1975; 228: 1936-1948.
3. 14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 1977; 28: 897-916.
4. 18F-2-fluoro-2-deoxy-D-glucose: validation of method. Ann. Neurol. 1979; 6: 371-388.
5. 18F]-fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circul. Res. 1979; 44: 127-137.
6. 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc. Natl Acad. Sci. USA 1997; 94: 2699-2704.
7. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl Acad. Sci. USA 1998; 95: 316-321.
8. 13C NMR for the assessment of human brain glucose metabolism in vivo. Biochemistry 1991; 30: 6362-6366.
9. 13C]glucose. J. Neurochem. 1994; 63: 1377-1385.
10. Gruetter R, Seaquist ER, Ugurbil K. A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am. J Physiol. Endocrinol. Metab. 2001; 281: E100-E112.
11. 13C NMR. Proc. Natl Acad. Sci. USA 1999; 96: 8235-8240.
12. Van den Berg CJ, Krzalic L, Mela P, Waetsch H. Compartmentation of glutamate metabolism in brain. Evidence for the existence of two different tricarboxylic acid cycles in brain. Biochem. J. 1969; 113: 281-290.
13. Berl S, Nicklas WJ, Clarke DD. Compartmentation of citric acid cycle metabolism in brain: labelling of glutamate, glutamine, aspartate and gaba by several radioactive tracer metabolites. J. Neurochem. 1970; 17: 1009-1015.
14. Mason GF, Rothman DL, Behar KL, Shulman RG. NMR determination of the TCA cycle rate and alpha-ketoglutarate/glutamate exchange rate in rat brain. J. Cereb. Blood Flow Metab. 1992; 12: 434-447.
15. Mason GF, Gruetter R, Rothman DL, Behar KL, Shulman RG, Novotny EJ. Simultaneous determination of the rates of the TCA cycle, glucose utilization, alpha-ketoglutarate/glutamate exchange, and glutamine synthesis in human brain by NMR. J. Cereb. Blood Flow Metab. 1995; 15: 12-25.
16. Pardridge WM, Boado RJ, Farrell CR. Brain-type glucose transporter (GLUT-1) is selectively localized to the blood-brain barrier. Studies with quantitative western blotting and in situ hybridization. J. Biol. Chem. 1990; 265: 18035-18040.
17. Erecinska M, Silver IA. Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 1990; 35: 245-296.
18. Fonnum F. Glutamate: a neurotransmitter in mammalian brain. J. Neurochem. 1984; 42: 1-11.
19. Kanai Y, Hediger MA. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 1992; 360: 467-471.
20. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. Localization of neuronal and glial glutamate transporters. Neuron 1994; 13: 713-725.
21. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 1995; 15: 711-720.
22. Martinez-Hernandez A, Bell KP, Norenberg MD. Glutamine synthetase: glial localization in brain. Science 1977; 195: 1356-1358.
23. Norenberg MD, Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res. 1979; 161: 303-310.
24. Chaudhry FA, Reimer RJ, Krizaj D, Barber D, Storm-Mathisen J, Copenhagen DR, Edwards RH. Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 1999; 99: 769-780.
25. Broer A, Brookes N, Ganapathy V, Dimmer KS, Wagner CA, Lang F, Broer S. The astroglial ASCT2 amino acid transporter as a mediator of glutamine efflux. J. Neurochem. 1999; 73: 2184-2194.
26. Varoqui H, Zhu H, Yao D, Ming H, Erickson JD. Cloning and functional identification of a neuronal glutamine transporter. J. Biol. Chem. 2000; 275: 4049-4054.
27. Kvamme E, Lenda K. Regulation of glutaminase by exogenous glutamate, ammonia and 2-oxoglutarate in synaptosomal enriched preparation from rat brain. Neurochem. Res. 1982; 7: 667-678.
28. 13C]-NMR spectroscopy. Magn. Reson. Med. 2003; 49: 37-46.
29. 15N-NMR spectroscopy studies of ammonia transport and glutamine synthesis in the hyperammonemic rat brain. Dev. Neurosci. 1998; 20: 434-443.
30. Shank RP, Bennett GS, Freytag SO, Campbell GL. Pyruvate carboxylase: an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res. 1985; 329: 364-367.
31. 13C]-glucose infusion. J. Neurochem. 2001; 76: 975-989.
32. Waniewski RA, Martin DL. Preferential utilization of acetate by astrocytes is attributable to transport. J. Neurosci. 1998; 18: 5225-5233.
33. 13C nuclear magnetic resonance spectroscopy: elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J. Neurosci. 2002; 22: 1523-1531.
34. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001; 21: 1133-1145.
35. 13C]glucose MRS in chronic hepatic encephalopathy in man. Magn. Reson. Med. 2001; 45: 981-993.
36. 13C]glucose. Brain Res. Brain Res. Protoc. 2003; 10: 181-190.
37. 2]-beta-hydroxybutyrate metabolism in human brain. J. Cereb. Blood Flow Metab. 2002; 22: 890-898.
38. Pan JW, Stein DT, Telang F, Lee JH, Shen J, Brown P, Cline G, Mason GF, Shulman GI, Rothman DL, Hetherington HP. Spectroscopic imaging of glutamate C4 turnover in human brain. Magn. Reson. Med. 2000; 44: 673-679.
39. 13C] magnetic resonance spectroscopy at 4.1 T. J. Cereb. Blood Flow Metab. 1999; 19: 1179-1188.
40. 13C] glutamate turnover in human brain. Proc. Natl Acad. Sci. USA 1992; 89: 9603-9606.
41. 13C] MRS and fMRI. Magn. Reson. Med. 2001; 45: 349-355.
42. 13C-decouple spectroscopic measurements of lactate and glutamate in the rat brain in vivo. Proc. Natl Acad. Sci. USA 1985; 82: 1633-1637.
43. 13C-edited NMR spectroscopy. J. Cereb. Blood Flow Metab. 1990; 10: 170-179.
44. 13C] D-glucose. Magn. Reson. Med. 1999; 41: 1077-1083.
45. de Graaf RA. In vivo NMR Spectroscopy. Principles and Techniques. Wiley: Chichester, 1998.
46. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993; 29: 804-811.
47. de Graaf RA, Brown PB, McIntyre S, Rothman DL, Nixon TW. Dynamic shim updating (DSU) for multislice signal acquisition. Magn. Reson. Med. 2003; 49: 409-416.
48. Shaka AJ, Keeler J, Frenkiel T, Freeman R. An improved sequence for broadband decoupling: WALTZ-16. J. Magn. Reson. 1983; 52: 335-338.
49. 1H NMR spectra by optimization of signal acquisition and processing and by incorporation of prior knowledge into the spectral fitting. Magn. Reson. Med. 1990; 15: 305-319.
50. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 1993; 30: 672-679.
51. 1H NMR spectra of the rat brain. J. Magn. Reson. 1999; 141: 104-120.
52. 1H NMR spectrum of rat brain. Magn. Reson. Med. 1993; 30: 38-44.
53. Hwang JH, Graham GD, Behar KL, Alger JR, Prichard JW, Rothman DL. Short echo time proton magnetic resonance spectroscopic imaging of macromolecule and metabolite signal intensities in the human brain. Magn. Reson. Med. 1996; 35: 633-639.
54. Hoult DI, Richards RE. The signal-to-noise ratio of the nuclear magnetic resonance experiment. J. Magn. Reson. 1976; 24: 71-85.
55. Hoult DI, Lauterbur PC. The sensitivity of the zeugmatographic experiment involving human samples. J. Magn. Reson. 1979; 34: 425-433.
56. Vaughan JT, Garwood M, Collins CM, Liu W, DelaBarre L, Adriany G, Andersen P, Merkle H, Goebel R, Smith MB, Ugurbil K. 7T vs. 4T: RF power, homogeneity, and signal-to-noise comparison in head images. Magn. Reson. Med. 2001; 46: 24-30.
57. 2 relaxation study of water, N-acetylaspartate, and creatine in human brain using Hahn and Carr-Purcell spin echoes at 4 T and 7 T. Magn. Reson. Med. 2002; 47: 629-633.
58. 1H spectroscopy at 1.5 and 4.0 Tesla. Magn. Reson. Med. 2000; 44: 185-192.
59. Barker PB, Hearshen DO, Boska MD. Single-voxel proton MRS of the human brain at 1.5 T and 3.0 T. Magn. Reson. Med. 2001; 45: 765-769.
60. 13C]-glucose and its metabolic products. Magn. Reson. Med. 1993; 30: 544-551.
61. 13C]NMR. Proc. Natl Acad. Sci. USA 1996; 93: 7612-7617.
62. 13C] nuclear magnetic resonance study. J. Cereb. Blood Flow Metab. 1997; 17: 1040-1047.
63. 2] glutamate/glutamine tomography in rat brain. Magn. Reson. Med. 1999; 42: 997-1003.
64. 13C] NMR spectroscopy. J. Neurochem. 2002; 82: 857-866.
65. de Graaf RA, Pan JW, Telang F, Lee JH, Brown P, Novotny EJ, Hetherington HP, Rothman DL. Differentiation of glucose transport in human brain gray and white matter. J. Cereb. Blood Flow Metab. 2001; 21: 483-492.
66. 1H spectroscopic imaging of human brain at 4.1 T using image segmentation. Magn. Reson. Med. 1996; 36: 21-29.
67. Roberts E, Chase TN, Tower DB. GABA in Nervous System Function. Raven Press: New York, 1976.
68. McCormick DA. GABA as an inhibitory neurotransmitter in human cerebral cortex. J. Neurophysiol. 1989; 62: 1018-1027.
69. 13C NMR studies of metabolic compartmentation in the adult mammalian brain. NMR Biomed. 1999; 12: 451-462.
70. Patel AB, Rothman DL, Cline GW, Behar KL. Glutamine is the major precursor for GABA synthesis in rat neocortex in vivo following acute GABA-transaminase inhibition. Brain Res. 2001; 919: 207-220.
71. 1H double-resonance difference spectroscopy of the rat brain in vivo. Proc. Natl Acad. Sci. USA 1984; 81: 6330-6334.
72. 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo. Proc. Natl Acad. Sci. USA 1993; 90: 5662-5666.
73. Petroff OA, Behar KL, Mattson RH, Rothman DL. Human brain gamma-aminobutyric acid levels and seizure control following initiation of vigabatrin therapy. J. Neurochem. 1996; 67: 2399-2404.
74. Sanacora G, Mason GF, Rothman DL, Behar KL, Hyder F, Petroff OA, Berman RM, Charney DS, Krystal JH. Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Arch. Gen. Psychiat. 1999; 56: 1043-1047.
75. Behar KL, Rothman DL, Petersen KF, Hooten M, Delaney R, Petroff OA, Shulman GI, Navarro V, Petrakis IL, Charney DS, Krystal JH. Preliminary evidence of low cortical GABA levels in localized 1H-MR spectra of alcohol-dependent and hepatic encephalopathy patients. Am. J. Psychiat. 1999; 156: 952-954.
76. Fox PT, Raichle ME. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl Acad. Sci. USA 1986; 83: 1140-1144.
77. Fox PT, Raichle ME, Mintun MA, Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988; 241: 462-464.
78. Rothman DL, Sibson NR, Hyder F, Shen J, Behar KL, Shulman RG. In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. Phil. Trans. R. Soc. Lond. B Biol. Sci. 1999; 354: 1165-1177.
79. 1H NMR in human visual cortex during physiologic stimulation. Proc. Natl Acad. Sci. USA 1991; 88: 5829-5831.
80. 13C magnetic resonance spectroscopy. J. Neurosci. Res. 2001; 66: 737-746.