Metabolic mapping of astrocytes and neurons in culture using stable isotopes and gas chromatography-mass spectrometry (GC-MS)

Neuromethods

Volumn 90, Issue , 2014, Pages 73-105

  Walls, Anne B ^a   Bak, Lasse K ^a   Sonnewald, Ursula ^a   Schousboe, Arne ^a   Waagepetersen, Helle S ^a  

^a NONE

Author keywords

13 C glucose glutamate glutamine; 15 N glutamate glutamine; Astrocytes; Calculations of isotopic enrichment; Co cultures; Glycogen; Mass spectrometry; Neurons; Pentose phosphate pathway

Indexed keywords

AMINO ACID; CARBON 13; GLUTAMIC ACID; GLUTAMINE; GLYCOGEN; ISOTOPE; NITROGEN 15; PENTOSE PHOSPHATE; PYRUVIC ACID;

ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN MAPPING; CARBOXYLATION; CELL LABELING; CELL METABOLISM; CEREBELLUM; CLINICAL PROTOCOL; COCULTURE; ENRICHMENT CULTURE; EXPERIMENTAL STUDY; EXTRACTION; GAS CHROMATOGRAPHY; IN VITRO STUDY; INCUBATION TIME; MASS SPECTROMETRY; NERVE CELL CULTURE; NONHUMAN; PRIMARY CULTURE; PRIORITY JOURNAL; STUDY DESIGN;

EID: 84921832164     PISSN: 08932336     EISSN: 19406045     Source Type: Book Series    
DOI: 10.1007/978-1-4939-1059-5_4     Document Type: Article

References (65)

1. Schousboe A (2012) Studies of brain metabolism: a historical perspective. In: Choi I-Y, Gruetter R (eds) Advances in neurobiology. Springer Science, New York, NY, pp 909–920
2. Mc Kenna MC, Dienel GA, Sonnewald U, Waagepetersen HS, Schousboe A (2012) Energy metabolism in the brain. In: Brady ST, Siegel GJ, Albers RW, Price DL (eds) Basic neurochemistry. Elsevier-Academic, London, pp 223–258
3. Yudkoff M, Nissim I, Kim SU, Pleasure D, Segal S (1984) Metabolism of 15 NH 3 in organotypic cerebellar explants and cultured astrocytes: studies with gas chromatography-mass spectrometry. J Neurochem 42:283–286
4. Sonnewald U, Westergaard N, Petersen SB, Unsgard G, Schousboe A (1993) Metabolism of [U- 13 C]glutamate in astrocytes studied by 13 C NMR spectroscopy: Incorporation of more label into lactate than into glutamine demonstrates the importance of the tricarboxylic acid cycle. J Neurochem 61:1179–1182
5. Sonnewald U, Westergaard N, Jones P, Taylor A, Bachelard HS, Schousboe A (1996) Metabolism of [U- 13 C 5] glutamine in cultured astrocytes studied by NMR spectroscopy: First evidence of astrocytic pyruvate recycling. J Neurochem 67:2566–2572
6. Sonnewald U, Westergaard N, Krane J, Unsgard G, Petersen SB, Schousboe A (1991) First direct demonstration of preferential release of citrate from astrocytes using [13 C]NMR spectroscopy of cultured neurons and astrocytes. Neurosci Lett 128:235–239
7. Leo GC, Driscoll BF, Shank RP, Kaufman E (1993) Analysis of [1- 13 C] D -glucose metabolism in cultured astrocytes and neurons using nuclear magnetic resonance spectroscopy. Dev Neurosci 15:282–288
8. Badar-Goffer RS, Bachelard HS, Morris PG (1990) Cerebral metabolism of acetate and glucose studied by 13 C-n.m.r. Spectroscopy. A technique for investigating metabolic compartmentation in the brain. Biochem J 266: 133–139
9. Badar-Goffer R, Bachelard H (1991) Metabolic studies using 13 C nuclear magnetic resonance spectroscopy. Essays Biochem 26:105–119
10. Lange SC, Bak LK, Waagepetersen HS, Schousboe A, Norenberg MD (2012) Primary cultures of astrocytes: their value in understanding astrocytes in health and disease. Neurochem Res 37:2569–2588
11. Booher J, Sensenbrenner M (1972) Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask cultures. Neurobiology 2:97–105
12. Messer A (1977) The maintenance and identification of mouse cerebellar granule cells in monolayer culture. Brain Res 130:1–12
13. Dichter MA (1978) Rat cortical neurons in cell culture: Culture methods, cell morphology, electrophysiology, and synapse formation. Brain Res 149:279–293
14. Drejer J, Larsson OM, Schousboe A (1982) Characterization of L-glutamate uptake into and release from astrocytes and neurons cultured from different brain regions. Exp Brain Res 47:259–269
15. Yu AC, Hertz E, Hertz L (1984) Alterations in uptake and release rates for GABA, glutamate, and glutamine during biochemical maturation of highly purified cultures of cerebral cortical neurons, a GABAergic preparation. J Neurochem 42:951–960
16. Hertz L, Juurlink BH, Szuchet S (1985) Cell cultures. In: Lajtha A (ed) Handbook of neurochemistry, vol 8. Plenum, New York, NY, pp 603–661
17. Schousboe A, Drejer J, Hansen GH, Meier E (1985) Cultured neurons as model systems for biochemical and pharmacological studies on receptors for neurotransmitter amino acids. Dev Neurosci 7:252–262
18. Drejer J, Larsson OM, Kvamme E, Svenneby G, Hertz L, Schousboe A (1985) Ontogenetic development of glutamate metabolizing enzymes in cultured cerebellar granule cells and in cerebellum in vivo. Neurochem Res 10:49–62
19. Drejer J, Schousboe A (1989) Selection of a pure cerebellar granule cell culture by kainate treatment. Neurochem Res 14:751–754
20. Schousboe A, Meier E, Drejer J, Hertz L (1989) Preparation of primary cultures of mouse (rat) cerebellar granule cells. In: Shahar A, de Vellis J, Vernadakis A, Haber B (eds) A dissection and tissue culture manual for the nervous system. Alan R. Liss, New York, NY, pp 183–186
21. Sonnewald U, Olstad E, Qu H, Babot Z, Cristofòfol R, Suñol C, Schousboe A, Waagepetersen H (2004) First direct demonstration of extensive GABA synthesis in mouse cerebellar neuronal cultures. J Neurochem 91:796–803
22. Westergaard N, Fosmark H, Schousboe A (1991) Metabolism and release of glutamate in cerebellar granule cells cocultured with astrocytes from cerebellum or cerebral cortex. J Neurochem 56:59–66
23. Larsson OM, Drejer J, Kvamme E, Svenneby G, Hertz L, Schousboe A (1985) Ontogenetic development of glutamate and GABA metabolizing enzymes in cultured cerebral cortex interneurons and in cerebral cortex in vivo. Int J Dev Neurosci 3:177–185
24. Sonnewald U, Kortner TM, Qu H, Olstad E, Sunol C, Bak LK, Schousboe A, Waagepetersen HS (2006) Demonstration of extensive GABA synthesis in the small population of GAD positive neurons in cerebellar cultures by the use of pharmacological tools. Neurochem Int 48:572–578
25. Larsson OM, Gram L, Schousboe I, Schousboe A (1986) Differential effect of gamma-vinyl GABA and valproate on GABA-transaminase from cultured neurones and astrocytes. Neuropharmacology 25:617–625
26. Snodgrass SR, White WF, Biales B, Dichter M (1980) Biochemical correlates of GABA function in rat cortical neurons in culture. Brain Res 190:123–138
27. Larsson OM, Drejer J, Hertz L, Schousboe A (1983) Ion dependency of uptake and release of GABA and (RS)-nipecotic acid studied in cultured mouse brain cortex neurons. J Neurosci Res 9:291–302
28. Drejer J, Honore T, Schousboe A (1987) Excitatory amino acid-induced release of 3 H-GABA from cultured mouse cerebral cortex interneurons. J Neurosci 7:2910–2916
29. Dichter MA (1980) Physiological identifi cation of GABA as the inhibitory transmitter for mammalian cortical neurons in cell culture. Brain Res 190:111–121
30. Yu AC, Hertz L (1982) Uptake of glutamate, GABA, and glutamine into a predominantly GABA-ergic and a predominantly glutamatergic nerve cell population in culture. J Neurosci Res 7:23–35
31. Leke R, Bak LK, Schousboe A, Waagepetersen HS (2008) Demonstration of neuron-glia transfer of precursors for GABA biosynthesis in a co-culture system of dissociated mouse cerebral cortex. Neurochem Res 33:2629–2635
32. Wu DK, Scully S, de Vellis J (1988) Induction of glutamine synthetase in rat astrocytes by cocultivation with embryonic chick neurons. J Neurochem 50:929–935
33. Schousboe A, Hertz L, Svenneby G (1977) Uptake and metabolism of GABA in astrocytes cultured from dissociated mouse-brain hemispheres. Neurochem Res 2:217–229
34. Schousboe A, Svenneby G, Hertz L (1977) Uptake and metabolism of glutamate in astrocytes cultured from dissociated mouse brain hemispheres. J Neurochem 29:999–1005
35. Schousboe A (1980) Primary cultures of astrocytes from mammalian brain as a tool in neurochemical research. Cell Mol Biol Incl Cyto Enzymol 26:505–513
36. Hogstad S, Svenneby G, Torgner IA, Kvamme E, Hertz L, Schousboe A (1988) Glutaminase in neurons and astrocytes cultured from mouse brain: Kinetic properties and effects of phosphate, glutamate, and ammonia. Neurochem Res 13:383–388
37. Hoogland TM, Kuhn B (2010) Recent developments in the understanding of astrocyte function in the cerebellum in vivo. Cerebellum 9:264–271
38. Skytt DM, Madsen KK, Pajecka K, Schousboe A, Waagepetersen HS (2010) Characterization of primary and secondary cultures of astrocytes prepared from mouse cerebral cortex. Neurochem Res 35:2043–2052
39. Moonen G, Cam Y, Sensenbrenner M, Mandel P (1975) Variability of the effects of serumfree medium, dibutyryl-cyclic AMP or theophylline on the morphology of cultured new-born rat astroblasts. Cell Tissue Res 163:365–372
40. Moonen G, Heinen E, Goessens G (1976) Comparative ultrastructural study of the effects of serum-free medium and dibutyryl-cyclic AMP on newborn rat astroblasts. Cell Tissue Res 167:221–227
41. Kimelberg HK, Narumi S, Bourke RS (1978) Enzymatic and morphological properties of primary rat brain astrocyte cultures, and enzyme development in vivo. Brain Res 153:55–77
42. Hertz L, Juurlink BHJ, Fosmark H, Schousboe A (1982) Astrocytes in primary cultures. In: Pfeiffer SE (ed) Neuroscience approached through cell culture, vol 1. CRC, Boca Raton, FL, pp 175–186
43. Bachelard H, Badar-Goffer R (1993) NMR spectroscopy in neurochemistry. J Neurochem 61:412–429
44. McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR (1996) Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 66:386–393
45. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105
46. Mc Gale EH, Pye IF, Stonier C, Hutchinson EC, Aber GM (1977) Studies of the interrelationship between cerebrospinal fluid and plasma amino acid concentrations in normal individuals. J Neurochem 29:291–297
47. Choi IY, Gruetter R (2003) In vivo 13 C NMR assessment of brain glycogen concentration and turnover in the awake rat. Neurochem Int 43:317–322
48. Slais K, Vorisek I, Zoremba N, Homola A, Dmytrenko L, Sykova E (2008) Brain metabolism and diffusion in the rat cerebral cortex during pilocarpine-induced status epilepticus. Exp Neurol 209:145–154
49. Schousboe A, Westergaard N, Waagepetersen HS, Larsson OM, Bakken IJ, Sonnewald U (1997) Traffi cking between glia and neurons of TCA cycle intermediates and related metabolites. Glia 21:99–105
50. Brekke EM, Walls AB, Schousboe A, Waagepetersen HS, Sonnewald U (2012) Quantitative importance of the pentose phosphate pathway determined by incorporation of 13 C from [2- 13 C]- and [3- 13 C]glucose into TCA cycle intermediates and neurotransmitter amino acids in functionally intact neurons. J Cereb Blood Flow Metab 32:1788–1799
51. Walls AB, Heimburger CM, Bouman SD, Schousboe A, Waagepetersen HS (2009) Robust glycogen shunt activity in astrocytes: Effects of glutamatergic and adrenergic agents. Neuroscience 158:284–292
52. 2+ homeostasis and metabolism of glucose in astrocytes with an emphasis on pyruvate carboxylation, oxidative decarboxylation and recycling: implications for glutamate neurotransmission and excitotoxicity. Neurotox Res 21:405–417
53. 13 CNMR spectroscopy. Dev Neurosci 20:310–320
54. Biemann K (1962) Mass spectrometry in organic chemistry applications. McGraw, New York, NY, pp 223–227
55. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
56. Walls AB, Sickmann HM, Brown A, Bouman SD, Ransom B, Schousboe A, Waagepetersen HS (2008) Characterization of 1,4-dideoxy- 1,4-imino-d-arabinitol (DAB) as an inhibitor of brain glycogen shunt activity. J Neurochem 105:1462–1470
57. Mawhinney TP, Robinett RS, Atalay A, Madson MA (1986) Gas-liquid chromatography and mass spectral analysis of mono-, di- and tricarboxylates as their tert.-butyldimethylsilyl derivatives. J Chromatogr 361:117–130
58. Brekke E, Walls AB, Norfeldt L, Schousboe A, Waagepetersen HS, Sonnewald U (2012) Direct measurement of backfl ux between oxaloacetate and fumarate following pyruvate carboxylation. Glia 60:147–158
59. Katz J, Wood HG (1960) The use of glucose- C14 for the evaluation of the pathways of glucose metabolism. J Biol Chem 235: 2165–2177
60. Wood HG, Katz J, Landau BR (1963) Estimation of pathways of carbohydrate metabolism. Biochem Z 338:809–847
61. Katz J, Landau BR, Bartsch GE (1966) The pentose cycle, triose phosphate isomerization, and lipogenesis in rat adipose tissue. J Biol Chem 241:727–740
62. Herrero-Mendez A, Almeida A, Fernandez E, Maestre C, Moncada S, Bolanos JP (2009) The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/CCdh1. Nat Cell Biol 11:747–752
63. Sickmann HM, Schousboe A, Fosgerau K, Waagepetersen HS (2005) Compartmentation of lactate originating from glycogen and glucose in cultured astrocytes. Neurochem Res 30:1295–1304
64. Olstad E, Olsen GM, Qu H, Sonnewald U (2007) Pyruvate recycling in cultured neurons from cerebellum. J Neurosci Res 85: 3318–3325
65. DeJongh DC, Radford T, Hribar JD, Hanessian S, Bieber M, Dawson G, Sweeley CC (1969) Analysis of trimethylsilyl derivatives of carbohydrates by gas chromatography and mass spectrometry. J Am Chem Soc 91:1728–1740