Characterization of glucose-related metabolic pathways in differentiated rat oligodendrocyte lineage cells

GLIA

Volumn 64, Issue 1, 2016, Pages 21-34

  Amaral, Ana I ^a   Hadera, Mussie G ^b   Tavares, Joana M ^a   Kotter, Mark R N ^a   Sonnewald, Ursula ^b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

13C; Acetate; Energy metabolism; Glucose; Glycolysis; Mitochondria; Oligodendroglia; Pyruvate carboxylation

Indexed keywords

GLUCOSE; GLUTAMIC ACID; ACETIC ACID DERIVATIVE; ACETYL COENZYME A; CARBON; LACTIC ACID; MALIC ACID; MALIC ACID DERIVATIVE; OXALOACETIC ACID; PHOSPHOENOLPYRUVATE; PYRUVIC ACID; RADIOPHARMACEUTICAL AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXYLATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL VIABILITY; CONTROLLED STUDY; GLUCOSE INTAKE; GLUCOSE METABOLISM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOCYTOCHEMISTRY; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; MITOCHONDRION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGODENDROCYTE PRECURSOR CELL; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; ANIMAL; CELL CULTURE; CITRIC ACID CYCLE; CYTOSOL; METABOLISM; NEURAL STEM CELL; OLIGODENDROGLIA; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACETATES; ACETYL COENZYME A; ANIMALS; CARBON RADIOISOTOPES; CELLS, CULTURED; CITRIC ACID CYCLE; CYTOSOL; GLUCOSE; LACTIC ACID; MALATES; MITOCHONDRIA; NEURAL STEM CELLS; OLIGODENDROGLIA; OXALOACETIC ACID; PENTOSE PHOSPHATE PATHWAY; PHOSPHOENOLPYRUVATE; PYRUVIC ACID; RADIOPHARMACEUTICALS; RATS, SPRAGUE-DAWLEY;

EID: 84954402887     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22900     Document Type: Article

References (74)

1. Almeida A, Delgado-Esteban M, Bolanos JP, Medina JM. 2002. Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture. J Neurochem 81:207-217.
2. Amaral AI, Alves PM, Teixeira AP. 2014. Metabolic fux analysis tools to investigate brain metabolism in vitro. In: Hirrlinger J, Waagepertersen HS, editor. Brain energy metabolism. New York: Humana Press. pp 107-144.
3. Amaral AI, Meisingset TW, Kotter MR, Sonnewald U. 2013. Metabolic aspects of neuron-oligodendrocyte-astrocyte interactions. Front Endocrinol (Lausanne) 4:54
4. 13C-labeled glucose. Front Neuroenerg 3:5
5. 13C NMR spectroscopy and metabolic flux analysis. J Neurochem 113:735-748.
6. Amaral AI, Teixeira AP, Sonnewald U, Alves PM. 2011b. Estimation of intracellular fluxes in cerebellar neurons after hypoglycemia: Importance of the pyruvate recycling pathway and glutamine oxidation. J Neurosci Res 89:700-710.
7. Ariyannur PS, Moffett JR, Madhavarao CN, Arun P, Vishnu N, Jacobowitz DM, Hallows WC, Denu JM, Namboodiri AM. 2010. Nuclear-cytoplasmic localization of acetyl coenzyme a synthetase-1 in the rat brain. J Comp Neurol 518:2952-2977.
8. Armstrong RC, Mierzwa AJ, Sullivan GM, Sanchez MA. 2015. Myelin and oligodendrocyte lineage cells in white matter pathology and plasticity after traumatic brain injury. Neuropharmacology. pii: S0028-3908(15)00158-6 (Epub ahead of print).
9. Attwell D, Laughlin SB. 2001. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
10. Baer AS, Syed YA, Kang SU, Mitteregger D, Vig R, Ffrench-Constant C, Franklin RJ, Altmann F, Lubec G, Kotter MR. 2009. Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132:465-481.
11. 13C]lactate in co-cultures of cerebellar neurons and astrocytes. Neurochem Res 32:671-680.
12. 13C]aspartate in cultured astrocytes: Compartmentation of pyruvate metabolism. Neurosci Lett 237:117-120.
13. Banki K, Colombo E, Sia F, Halladay D, Mattson DH, Tatum AH, Massa PT, Phillips PE, Perl A. 1994. Oligodendrocyte-specific expression and autoantigenicity of transaldolase in multiple sclerosis. J Exp Med 180:1649-1663.
14. Baslow MH, Guilfoyle DN. 2006. Functions of N-acetylaspartate and N-acetylaspartyl-glutamate in brain-Evidence of a role in maintenance of higher brain integrative activities of information processing and cognition. In: Moffett JR, Tieman SB, Weinberger DR, Coyle JT, Namboodiri AMA, editors. N-acetylaspartate: A unique neuronal molecule in the central nervous system. Bethesda, MD: Springer. pp 95-112.
15. Biemann K. 1962. The mass spectra of isotopically labeled molecules. Mass spectrometry; Organic chemical applications. New York: McGraw-Hill. pp 223-227.
16. Bolanos JP, Almeida A. 2010. The pentose-phosphate pathway in neuronal survival against nitrosative stress. IUBMB Life 62:14-18.
17. Brekke EM, Morken TS, Wideroe M, Haberg AK, Brubakk AM, Sonnewald U. 2014. The pentose phosphate pathway and pyruvate carboxylation after neonatal hypoxic-ischemic brain injury. J Cereb Blood Flow Metab 34:724-734.
18. 13C from [2-13C]- and [3-13C]glucose into TCA cycle intermediates and neurotransmitter amino acids in functionally intact neurons. J Cereb Blood Flow Metab 32:1788-1799.
19. 13C NMR. J Biol Chem 265:12916-12926.
20. Cesar M, Hamprecht B. 1995. Immunocytochemical examination of neural rat and mouse primary cultures using monoclonal antibodies raised against pyruvate carboxylase. J Neurochem 64:2312-2318.
21. Chakraborty G, Mekala P, Yahya D, Wu G, Ledeen RW. 2001. Intraneuronal N-acetylaspartate supplies acetyl groups for myelin lipid synthesis: Evidence for myelin-associated aspartoacylase. J Neurochem 78:736-745.
22. Cruz F, Scott SR, Barroso I, Santisteban P, Cerdan S. 1998. Ontogeny and cellular localization of the pyruvate recycling system in rat brain. J Neurochem 70:2613-2619.
23. Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA. 2006. Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26:10967-10983.
24. 2]glucose labeling study in humans. J Cereb Blood Flow Metab 27:1593-1602.
25. Edmond J, Robbins RA, Bergstrom JD, Cole RA, de Vellis J. 1987. Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes, and oligodendrocytes from developing brain in primary culture. J Neurosci Res 18:551-561.
26. Francis JS, Strande L, Markov V, Leone P. 2012. Aspartoacylase supports oxidative energy metabolism during myelination. J Cereb Blood Flow Metab 32:1725-1736.
27. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Mobius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA. 2012. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517-521.
28. Gamberino WC, Berkich DA, Lynch CJ, Xu B, LaNoue KF. 1997. Role of pyruvate carboxylase in facilitation of synthesis of glutamate and glutamine in cultured astrocytes. J Neurochem 69:2312-2325.
29. Garcia-Nogales P, Almeida A, Bolanos JP. 2003. Peroxynitrite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J Biol Chem 278:864-874.
30. Geddes JW, Wood JD. 1984. Changes in the amino acid content of nerve endings (synaptosomes) induced by drugs that alter the metabolism of glutamate and gamma-aminobutyric acid. J Neurochem 42:16-24.
31. Gegelashvili G, Schousboe A. 1997. High affinity glutamate transporters: Regulation of expression and activity. Mol Pharmacol 52:6-15.
32. Gegelashvili G, Schousboe A. 1998. Cellular distribution and kinetic properties of high-affinity glutamate transporters. Brain Res Bull 45:233-238.
33. 13C-NMR spectroscopy studies of pyruvate recycling in brain. Dev Neurosci 20:389-398.
34. 13C NMR spectroscopic study. J Neurochem 64:2773-2782.
35. Hertz L, Yu A, Svenneby G, Kvamme E, Fosmark H, Schousboe A. 1980. Absence of preferential glutamine uptake into neurons-An indication of a net transfer of TCA constituents from nerve endings to astrocytes? Neurosci Lett 16:103-109.
36. Hofmann U, Maier K, Niebel A, Vacun G, Reuss M, Mauch K. 2008. Identification of metabolic fluxes in hepatic cells from transient 13C-labeling experiments: Part I. Experimental observations. Biotechnol Bioeng 100:344-354.
37. Kostic M, Zivkovic N, Stojanovic I. 2013. Multiple sclerosis and glutamate excitotoxicity. Rev Neurosci 24:71-88.
38. 13C NMR spectroscopy. NMR Biomed 6:264-277.
39. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD. 2012. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 26:443-448.
40. Lyons SA, Kettenmann H. 1998. Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J Cereb Blood Flow Metab 18:521-530.
41. Martinez-Hernandez A, Bell KP, Norenberg MD. 1977. Glutamine synthetase: Glial localization in brain. Science 195:1356-1358.
42. Mawhinney TP, Robinett RS, Atalay A, Madson MA. 1986. Analysis of amino acids as their tert.-butyldimethylsilyl derivatives by gas-liquid chromatography and mass spectrometry. J Chromatogr 358:231-242.
43. McCarthy KD, de Vellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
44. McKenna M, Gruetter R, Sonnewald U, Waagepetersen HS, Schousboe A. S. 2012. Energy metabolism of the brain. In: Brady ST, Siegel GJ, Albers RW, Price DL, editors. Basic neurochemistry: Principles of molecular, cellular, and medical neurobiology, 8th ed., Oxford, UK: Elsevier Academic Press. pp 200-231.
45. McKenna MC, Stevenson JH, Huang X, Tildon JT, Zielke CL, Hopkins IB. 2000. Mitochondrial malic enzyme activity is much higher in mitochondria from cortical synaptic terminals compared with mitochondria from primary cultures of cortical neurons or cerebellar granule cells. Neurochem Int 36:451-459.
46. McKenna MC, Tildon JT, Stevenson JH, Huang X, Kingwell KG. 1995. Regulation of mitochondrial and cytosolic malic enzymes from cultured rat brain astrocytes. Neurochem Res 20:1491-1501.
47. 13C NMR study of neuronal-glial interactions in a model of temporal lobe epilepsy. J Cereb Blood Flow Metab 25:1254-1264.
48. Mifsud G, Zammit C, Muscat R, Di Giovanni G, Valentino M. 2014. Oligodendrocyte pathophysiology and treatment strategies in cerebral ischemia. CNS Neurosci Ther 20:603-612.
49. Moffett JR, Arun P, Ariyannur PS, Garbern JY, Jacobowitz DM, Namboodiri AM. 2011. Extensive aspartoacylase expression in the rat central nervous system. Glia 59:1414-1434.
50. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AM. 2007. N-acetylaspartate in the CNS: From neurodiagnostics to neurobiology. Prog Neurobiol 81:89-131.
51. Morken TS, Brekke E, Haberg A, Wideroe M, Brubakk AM, Sonnewald U. 2014. Altered astrocyte-neuronal interactions after hypoxia-ischemia in the neonatal brain in female and male rats. Stroke 45:2777-2785.
52. Muir D, Berl S, Clarke DD. 1986. Acetate and fluoroacetate as possible markers for glial metabolism in vivo. Brain Res 380:336-340.
53. Murin R, Cesar M, Kowtharapu BS, Verleysdonk S, Hamprecht B. 2009. Expression of pyruvate carboxylase in cultured oligodendroglial, microglial and ependymal cells. Neurochem Res 34:480-489.
54. Nilsen LH, Witter MP, Sonnewald U. 2014. Neuronal and astrocytic metabolism in a transgenic rat model of Alzheimer's disease. J Cereb Blood Flow Metab 34:906-914.
55. Norenberg MD, Martinez-Hernandez A. 1979. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 161:303-310.
56. Olstad E, Olsen GM, Qu H, Sonnewald U. 2007. Pyruvate recycling in cultured neurons from cerebellum. J Neurosci Res 85:3318-3325.
57. 2-fixing enzymes in the metabolism of rat brain. J Neurochem 22:717-724.
58. Pitt D, Werner P, Raine CS. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70.
59. Reubi JC, van den Berg C, Cuenod M. 1978. Glutamine as precursor for the GABA and glutamate trasmitter pools. Neurosci Lett 10:171-174.
60. Rinholm JE, Bergersen LH. 2014. White matter lactate-does it matter? Neuroscience 276:109-116.
61. Sa Santos S, Sonnewald U, Carrondo MJ, Alves PM. 2011. The role of glia in neuronal recovery following anoxia: In vitro evidence of neuronal adaptation. Neurochem Int 58:665-675.
62. Sanchez-Abarca LI, Tabernero A, Medina JM. 2001. Oligodendrocytes use lactate as a source of energy and as a precursor of lipids. Glia 36:321-329.
63. Schoenfeld R, Wong A, Silva J, Li M, Itoh A, Horiuchi M, Itoh T, Pleasure D, Cortopassi G. 2010. Oligodendroglial differentiation induces mitochondrial genes and inhibition of mitochondrial function represses oligodendroglial differentiation. Mitochondrion 10:143-150.
64. Shank RP, Bennett GS, Freytag SO, Campbell GL. 1985. Pyruvate carboxylase: An astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res 329:364-367.
65. Simonishvili S, Jain MR, Li H, Levison SW, Wood TL. 2013. Identification of Bax-interacting proteins in oligodendrocyte progenitors during glutamate excitotoxicity and perinatal hypoxia-ischemia. ASN Neuro 5(5):e00131
66. Sonnewald U. 2014. Glutamate synthesis has to be matched by its degradation-Where do all the carbons go? J Neurochem 131:399-406.
67. 13C MRS. Neurochem Res 35:1916-1921.
68. 13C glucose metabolism in neocortical astrocytes: Evidence for mitochondrial heterogeneity. Dev Neurosci 15:351-358.
69. 13C NMR spectroscopy that glutamine from astrocytes is a precursor for GABA synthesis in neurons. Neurochem Int 22:19-29.
70. Sykes JE, Lopes-Cardozo M, Van Den Bergh SG. 1986. Relationship between the pentose-phosphate pathway and the de novo synthesis of fatty acids and cholesterol in oligodendrocyte-enriched glial cultures. Neurochem Int 8:77-82.
71. van den Berg CJ, Garfinkel D. 1971. A stimulation study of brain compartments. Metabolism of glutamate and related substances in mouse brain. Biochem J 123:211-218.
72. Waagepetersen HS, Sonnewald U, Larsson OM, Schousboe A. 2001. Multiple compartments with different metabolic characteristics are involved in biosynthesis of intracellular and released glutamine and citrate in astrocytes. Glia 35:246-252.
73. Yan H, Rivkees SA. 2006. Hypoglycemia influences oligodendrocyte development and myelin formation. Neuroreport 17:55-59.
74. Ziabreva I, Campbell G, Rist J, Zambonin J, Rorbach J, Wydro MM, Lassmann H, Franklin RJ, Mahad D. 2010. Injury and differentiation following inhibition of mitochondrial respiratory chain complex IV in rat oligodendrocytes. Glia 58:1827-1837.