Cerebral glutamine metabolism under hyperammonemia determined in vivo by localized 1H and 15N NMR spectroscopy

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 4, 2012, Pages 696-708

  Cudalbu, Cristina ^a   Lanz, Bernard ^a   Duarte, João M N ^b   Morgenthaler, Florence D ^a   Pilloud, Yves ^a   Mlynárik, Vladimir ^a   Gruetter, Rolf ^a,c,d  

^a EPFL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

15N and 1H MRS; glutamate dehydrogenase; glutamine synthetase; hyperammonemia; net glutamine accumulation

Indexed keywords

AMMONIA; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; GLUTAMINE; NITROGEN 15;

AMINO ACID BRAIN LEVEL; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERAMMONEMIA; IN VIVO STUDY; MALE; NEUROTRANSMISSION; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT;

AMMONIA; ANIMALS; BRAIN; GLUTAMATE-AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE; HYPERAMMONEMIA; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MODELS, BIOLOGICAL; NITROGEN ISOTOPES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84859432226     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.173     Document Type: Article

References (49)

1. Aoki C, Milner TA, Sheu KF, Blass JP, Pickel VM (1987) Regional distribution of astrocytes with intense immunoreactivity for glutamate dehydrogenase in rat brain: implications for neuron-glia interactions in glutamate transmission. J Neurosci 7:2214-31
2. Berl S, Nicklas WJ, Clarke DD (1968) Compartmentation of glutamic acid metabolism in brain slices. J Neurochem 15:131-40
3. Berl S, Takagaki G, Clarke DD, Waelsch H (1962) Metabolic compartments in vivo. Ammonia and glutamic acid metabolism in brain and liver. J Biol Chem 237:2562-9
4. Butterworth RF, Girard G, Giguere JF (1988) Regional differences in the capacity for ammonia removal by brain following portocaval anastomosis. J Neurochem 51:486-90
5. Choi IY, Lei H, Gruetter R (2002) Effect of deep pentobarbital anesthesia on neurotransmitter metabolism in vivo: on the correlation of total glucose consumption with glutamatergic action. J Cereb Blood Flow Metab 22:1343-51 (Pubitemid 35285092)
6. Choi IY, Tkac I, Gruetter R (2000) Single-shot, threedimensional 'non-echo' localization method for in vivo NMR spectroscopy. Magn Reson Med 44:387-94
7. Clarke DD, Nicklas WJ, Berl S (1970) Tricarboxylic acidcycle metabolism in brain. Effect of fluoroacetate and fluorocitrate on the labelling of glutamate, aspartate, glutamine and gamma-aminobutyrate. Biochem J 120:345-51
8. Cooper AJ, McDonald JM, Gelbard AS, Gledhill RF, Duffy TE (1979) The metabolic fate of 13N-labeled ammonia in rat brain. J Biol Chem 254:4982-92 (Pubitemid 9227452)
9. Cooper AJ, Plum F (1987) Biochemistry and physiology of brain ammonia. Physiol Rev 67:440-519 (Pubitemid 17063608)
10. Du Ruisseau JP, Greenstein JP, Winitz M, Birnbaum SM (1957) Studies on the metabolism of amino acids and related compounds in vivo. VI. Free amino acid levels in the tissues of rats protected against ammonia toxicity. Arch Biochem Biophys 68:161-71
11. Duarte JMN, Cunha RA, Carvalho RA (2007) Different metabolism of glutamatergic and GABAergic compartments in superfused hippocampal slices characterized by nuclear magnetic resonance spectroscopy. Neuroscience 144:1305-13 (Pubitemid 46123825)
12. Duarte JMN, Lanz B, Gruetter R (2011) Compartmentalised cerebral metabolism of [1,6-13C]glucose determined by in vivo 13C NMR spectroscopy at 14.1 T. Front Neuroenergetics 3:3
13. Erecinska M, Silver IA (1990) Metabolism and role of glutamate in mammalian brain. Prog Neurobiol 35:245-96 (Pubitemid 20304100)
14. Fitzpatrick SM, Hetherington HP, Behar KL, Shulman RG (1989) Effects of acute hyperammonemia on cerebral amino acid metabolism and pHi in vivo, measured by 1H and 31P nuclear magnetic resonance. J Neurochem 52:741-9 (Pubitemid 19067530)
15. Govindaraju V, Young K, Maudsley AA (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13:129-53 (Pubitemid 30414704)
16. Gruetter R (2004) Principles of the measurment of neuroglial metabolism using in vivo 13C NMR spectroscopy. Adv Mol Cell Biol 31:409-33
17. Gruetter R, Adriany G, Choi IY, Henry PG, Lei H, Oz G (2003) Localized in vivo 13C NMR spectroscopy of the brain. NMR Biomed 16:313-38 (Pubitemid 38008361)
18. Gruetter R, Novotny EJ, Boulware SD, Mason GF, Rothman DL, Shulman GI, Prichard JW, Shulman RG (1994) Localized 13C NMR spectroscopy in the human brain of amino acid labeling from D-[1-13C]glucose. J Neurochem 63:1377-85
19. Gruetter R, Seaquist ER, Ugurbil K (2001) A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am J Physiol Endocrinol Metab 281:E100-12
20. Gruetter R, Tkac I (2000) Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med 43:319-23 (Pubitemid 30075458)
21. Kanamori K, Parivar F, Ross BD (1993) A 15N NMR study of in vivo cerebral glutamine synthesis in hyperammonemic rats. NMR Biomed 6:21-6
22. Kanamori K, Ross BD (1993) 15N n.m.r. measurement of the in vivo rate of glutamine synthesis and utilization at steady state in the brain of the hyperammonaemic rat. Biochem J 293(Part 2):461-8 (Pubitemid 23233928)
23. Kanamori K, Ross BD (1995) Steady-state in vivo glutamate dehydrogenase activity in rat brain measured by 15N NMR. J Biol Chem 270:24805-9
24. Kanamori K, Ross BD, Chung JC, Kuo EL (1996) Severity of hyperammonemic encephalopathy correlates with brain ammonia level and saturation of glutamine synthetase in vivo. J Neurochem 67:1584-94 (Pubitemid 26314216)
25. Kunz N, Cudalbu C, Mlynarik V, Huppi PS, Sizonenko SV, Gruetter R (2010) Diffusion-weighted spectroscopy: a novel approach to determine macromolecule resonances in short-echo time 1H-MRS. Magn Reson Med 64:939-46
26. Martinez-Hernandez A, Bell KP, Norenberg MD (1977) Glutamine synthetase: glial localization in brain. Science 195:1356-8 (Pubitemid 8056735)
27. McKenna MC (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J Neurosci Res 85:3347-58 (Pubitemid 350058523)
28. Mlynarik V, Cudalbu C, Xin L, Gruetter R (2008) 1H NMR spectroscopy of rat brain in vivo at 14.1Tesla: improvements in quantification of the neurochemical profile. J Magn Reson 194:163-8
29. Mlynarik V, Gambarota G, Frenkel H, Gruetter R (2006) Localized short-echo-time proton MR spectroscopy with full signal-intensity acquisition. Magn Reson Med 56:965-70 (Pubitemid 44691337)
30. Morgenthaler FD, Koski DM, Kraftsik R, Henry PG, Gruetter R (2006) Biochemical quantification of total brain glycogen concentration in rats under different glycemic states. Neurochem Int 48:616-22
31. Mulkern R, Bowers J (1994) Density matrix calculations of AB spectra from multipulse sequences: quantum mechanics meets in vivo spectroscopy. Concepts Magn Reson 6:1-23
32. Norenberg MD, Martinez-Hernandez A (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 161:303-10 (Pubitemid 9087410)
33. Oz G, Berkich DA, Henry PG, Xu Y, LaNoue K, Hutson SM, Gruetter R (2004) Neuroglial metabolism in the awake rat brain: CO2 fixation increases with brain activity. J Neurosci 24:11273-9 (Pubitemid 39658262)
34. Pfeuffer J, Tkac I, Provencher SW, Gruetter R (1999) Toward an in vivo neurochemical profile: quantification of 18 metabolites in short-echo-time (1)H NMR spectra of the rat brain. J Magn Reson 141:104-20 (Pubitemid 129608901)
35. Rothman DL, Sibson NR, Hyder F, Shen J, Behar KL, Shulman RG (1999) In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. Philos Trans R Soc Lond B Biol Sci 354:1165-77 (Pubitemid 29400899)
36. Schmitt A, Kugler P (1999) Cellular and regional expression of glutamate dehydrogenase in the rat nervous system: non-radioactive in situ hybridization and comparative immunocytochemistry. Neuroscience 92:293-308 (Pubitemid 29249039)
37. Shank RP, Aprison MH (1981) Present status and significance of the glutamine cycle in neural tissues. Life Sci 28:837-42 (Pubitemid 11099940)
38. Shen J, Sibson NR, Cline G, Behar KL, Rothman DL, Shulman RG (1998) 15N-NMR spectroscopy studies of ammonia transport and glutamine synthesis in the hyperammonemic rat brain. Dev Neurosci 20:434-43 (Pubitemid 28495539)
39. Sibson NR, Dhankhar A, Mason GF, Behar KL, Rothman DL, Shulman RG (1997) In vivo 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc Natl Acad Sci USA 94:2699-704
40. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 95:316-21 (Pubitemid 28103951)
41. Sibson NR, Mason GF, Shen J, Cline GW, Herskovits AZ, Wall JE, Behar KL, Rothman DL, Shulman RG (2001) In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during. J Neurochem 76:975-89 (Pubitemid 32167371)
42. Tkac I, Starcuk Z, Choi IY, Gruetter R (1999) In vivo 1H NMR spectroscopy of rat brain at 1ms echo time. Magn Reson Med 41:649-56 (Pubitemid 29205710)
43. Uffmann K, Gruetter R (2007) Mathematical modeling of (13)C label incorporation of the TCA cycle: the concept of composite precursor function. J Neurosci Res 85:3304-17 (Pubitemid 350058518)
44. Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129:35-43 (Pubitemid 127454051)
45. Xin L, Gambarota G, Duarte JM, Mlynarik V, Gruetter R (2010) Direct in vivo measurement of glycine and the neurochemical profile in the rat medulla oblongata. NMR Biomed 23:1097-102
46. Yudkoff M, Nissim I, Hummeler K, Medow M, Pleasure D (1986) Utilization of [15N]glutamate by cultured astrocytes. Biochem J 234:185-92
47. Zaganas I, Waagepetersen HS, Georgopoulos P, Sonnewald U, Plaitakis A, Schousboe A (2001) Differential expression of glutamate dehydrogenase in cultured neurons and astrocytes from mouse cerebellum and cerebral cortex. J Neurosci Res 66:909-13 (Pubitemid 33126393)
48. Zwingmann C (2007) The anaplerotic flux and ammonia detoxification in hepatic encephalopathy. Metab Brain Dis 22:235-49 (Pubitemid 47624321)
49. Zwingmann C, Leibfritz D (2003) Regulation of glial metabolism studied by 13C-NMR. NMR Biomed 16:370-99 (Pubitemid 38008364)