Cellular mitochondrial heterogeneity in cultured astrocytes as demonstrated by immunogold labeling of α-ketoglutarate dehydrogenase

GLIA

Volumn 53, Issue 2, 2006, Pages 225-231

  Waagepetersen, Helle S ^a   Hansen, Gert H ^b   Fenger, Kirsten ^b   Lindsay, J Gordon ^c   Gibson, Gary ^d   Schousboe, Arne ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Citrate; Compartmentation; Electron microscopy; Glutamate; Glutamine; Metabolism

Indexed keywords

ANTIBODY; GOLD; OXOGLUTARATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN CORTEX; BRAIN METABOLISM; BRAIN MITOCHONDRION; CELL COMPARTMENTALIZATION; CEREBELLUM; CITRIC ACID CYCLE; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOGOLD LABELING; METABOLITE; MOUSE; NEWBORN; NONHUMAN; POISSON DISTRIBUTION; PRIORITY JOURNAL; ALGORITHM; ANIMAL; CELL CULTURE; ENZYMOLOGY; GENETICS; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

ALGORITHMS; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CITRIC ACID CYCLE; IMMUNOHISTOCHEMISTRY; KETOGLUTARATE DEHYDROGENASE COMPLEX; MICE; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; POISSON DISTRIBUTION;

EID: 33644792251     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20276     Document Type: Article

References (58)

1. +-induced stimulation of glucose utilization in rat brain. J Cereb Blood Flow Metab 15:97-110.
2. Berl S, Clarke DD. 1983. The metabolic compartmentation concept. In: Hertz L, Kvamme E, McGeer EG, Schousboe A, editors. Glutamine, glutamate and GABA in the central nervous system. New York: Alan R Liss, p 205-217.
3. Calingasan NY, Baker H, Sheu KF, Gibson GE. 1994. Distribution of the alpha-ketoglutarate dehydrogenase complex in rat brain. J Comp Neurol 346:461-479.
4. 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.
5. 13C labels. J Neurosci Res 66:771-781.
6. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
7. Danielsen EM, Hansen GH, Niels-Christiansen LL. 1995. Localization and biosynthesis of aminopeptidase N in pig fetal small intestine. Gastroenterology 109:1039-1050.
8. De Marcucci OG, Gibb GM, Dick J, Lindsay JG. 1988. Biosynthesis, import and processing of precursor polypeptides of mammalian mitochondrial pyruvate dehydrogenase complex. Biochem J 251:817-823.
9. Faff-Michalak L, Albrecht J. 1991. Aspartate-aminotransferase, malate-dehydrogenase, and pyruvate-carboxylase activities in rat cerebral synaptic and nonsynaptic mitochondria-effects of in vitro treatment with ammonia, hyperammonemia and hepatic-encephalopathy. Metab Brain Dis 6:187-197.
10. 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.
11. Garseth M, Sonnewald U, White LR, Rod M, Zwart JA, Nygaard O, Aasly J. 2000. Proton magnetic resonance spectroscopy of cerebrospinal fluid in neurodegenerative disease: indication of glial energy impairment in Huntington chorea, but not Parkinson disease. J Neurosci Res 60:779-782.
12. Gibson GE, Park LC, Sheu KF, Blass JP, Calingasan NY. 2000. The alpha-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem Int 36:97-112.
13. 13C-NMR spectroscopy studies of pyruvate recycling in brain. Dev Neurosci 20:389-398.
14. Hawkins RA, Miller AL, Nielsen RC, Veech RL. 1973. The acute action of ammonia on rat brain metabolism in vivo. Biochem J 134:1001-1008.
15. Hertz L, Juurlink BHJ, Fosmark H, Schousboe A. 1982. Astrocytes in primary cultures. In: Pfeiffer SE, editor. Neuroscience approached through cell culture. Boca Raton, FL: CRC Press, p 175-186.
16. Hertz L, Juurlink BHJ, Hertz E, Fosmark H, Schousboe A. 1989. Preparation of primary cultures of mouse (rat) astrocytes. In: Shahar A, De Vellis J, Vernadakis A, Haber B, editors. A dissection and tissue culture manual for the nervous system. New York: Alan R Liss. p 105-108.
17. Hertz L, Peng L, Westergaard N, Yudkoff M, Schousboe A. 1992. Neuronal-astrocytic interactions in metabolism of transmitter amino acids of the glutamate family. In: Schousboe A, Diemer NH, Kofod H, editors. Drug research related to neuroactive amino acids. Alfred Benzon Symposium 32. Copenhagen: Munksgaard. p 30-48.
18. Hertz L, Dringen R, Schousboe A, Robinson SR. 1999. Astrocytes: glutamate producers for neurons. J Neurosci Res 57:417-428.
19. Huang HM, Fowler C, Zhang H, Gibson GE. 2004. Mitochondrial heterogeneity within and between different cell types. Neurochem Res 29:651-658.
20. Laake JH, Takumi Y, Eidet J, Torgner IA, Roberg B, Kvamme E, Ottersen OP. 1999. Postembedding immunogold labelling reveals subcellular localization and pathway-specific enrichment of phosphate activated glutaminase in rat cerebellum. Neuroscience 88:1137-1151.
21. Lai JC, Walsh JM, Dennis SC, Clark JB. 1977. Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J Neurochem 28:625-631.
22. Lai JC. 1992. Oxidative metabolism in neuronal and non-neuronal mitochondria. Can J Physiol Pharmacol 70(suppl):S130-S137.
23. 1H NMR. J Biol Chem 271:10648-10653.
24. 13C]glucose. Eur J Biochem 231:697-703.
25. McKenna MC. 2003. Glutamate metabolism in primary cultures of rat brain astrocytes: rationale and initial efforts toward developing a compartimental model. Adv Exp Med Biol 537:317-341.
26. McKenna MC, Tildon JT, Couto R, Stevenson JH, Caprio FJ. 1990. The metabolism of malate by cultured rat brain astrocytes. Neurochem Res 15:1211-1220.
27. 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.
28. McKenna MC, Stevenson JH, Huang X, Hopkins IB. 2000. Differential distribution of the enzymes glutamate dehydrogenase and aspartate aminotransferase in cortical synaptic mitochondria contributes to metabolic compartmentation in cortical synaptic terminals. Neurochem Int 37:229-241.
29. Medina JM, Tabernero A. 2002. Astrocyte-synthesized oleic acid behaves as a neurotrophic factor for neurons. J Physiol Paris 96:265-271.
30. Norenberg MD, Martinez-Hernandez A. 1979. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 161:303-310.
31. Oh YJ, Markelonis GJ, Oh TH. 1991. Immunocytochemical localization of mitochondrial malate dehydrogenase in primary cultures of rat astrocytes and oligodendrocytes. J Histochem Cytochem 39:681-688.
32. Ottersen OP. 1989a. Postembedding immunogold labelling of fixed glutamate: an electron microscopic analysis of the relationship between gold particle density and antigen concentration. J Chem Neuroanat 2:57-66.
33. Ottersen OP. 1989b. Quantitative electron microscopic immunocytochemistry of neuroactive amino acids. Anat Embryol (Berl) 180:1-15.
34. Perkins GA, Renken CW, Frey TG, Ellisman MH. 2001. Membrane architecture of mitochondria in neurons of the central nervous system. J Neurosci Res 66:857-865.
35. Qu H, Faero E, Jorgensen P, Dale O, Gisvold SE, Unsgard G, Sonnewald U. 1999. Decreased glutamate metabolism in cultured astrocytes in the presence of thiopental. Biochem Pharmacol 58:1075-1080.
36. Schousboe A, Divac I. 1979. Difference in glutamate uptake in astrocytes cultured from different brain regions. Brain Res 177:407-409.
37. Schousboe A, Waagepetersen HS. 2004. Role of astrocytes in homeostasis of glutamate and GABA during physiological and pathophysiological conditions. Adv Mol Cell Biol 31:461-474.
38. Schousboe A, Svenneby G, Hertz L. 1977a. Uptake and metabolism of glutamate in astrocytes cultured from dissociated mouse brain hemispheres. J Neurochem 29:999-1005.
39. Schousboe A, Hertz L, Svenneby G. 1977b. Uptake and metabolism of GABA in astrocytes cultured from dissociated mouse-brain hemispheres. Neurochem Res 2:217-229.
40. Schousboe A, Westergaard N, Sonnewald U, Petersen SB, Yu AC, Hertz L. 1992. Regulatory role of astrocytes for neuronal biosynthesis and homeostasis of glutamate and GABA. Prog Brain Res 94:199-211.
41. Schousboe A, Westergaard N, Sonnewald U, Petersen SB, Huang R, Peng L, Hertz L. 1993. Glutamate and glutamine metabolism and compartmentation in astrocytes. Dev Neurosci 15:359-366.
42. 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.
43. 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 28:897-916.
44. 13C glucose metabolism in neocortical astrocytes: evidence for mitochondrial heterogeneity. Dev Neurosci 15:351-358.
45. 13C NMR spectroscopy: incorporation of more label into lactate than into glutamine demonstrates the importance of the tricarboxylic acid cycle. J Neurochem 61:1179-1182.
46. Sonnewald U, Westergaard N, Schousboe A. 1997. Glutamate transport and metabolism in astrocytes. Glia 21:56-63.
47. Sonnewald U, Hertz L, Schousboe A. 1998. Mitochondrial heterogeneity in the brain at the cellular level. J Cereb Blood Flow Metab 18:231-237.
48. 13C-NMR spectroscopy. Dev Neurosci 20:310-320.
49. 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.
50. Waagepetersen HS, Qu H, Hertz L, Sonnewald U, Schousboe A. 2002. Demonstration of pyruvate recycling in primary cultures of neocortical astrocytes but not in neurons. Neurochem Res 27:1431-1437.
51. Waagepetersen HS, Sonnewald U, Schousboe A. 2003. Compartmentation of glutamine, glutamate, and GABA metabolism in neurons and astrocytes: functional implications. Neuroscientist 9:398-403.
52. Waniewski RA. 1992. Physiological levels of ammonia regulate glutamine synthesis from extracellular glutamate in astrocyte cultures. J Neurochem 58:167-174.
53. Westergaard N, Sonnewald U, Unsgard G, Peng L, Hertz L, Schousboe A. 1994. Uptake, release, and metabolism of citrate in neurons and astrocytes in primary cultures. J Neurochem 62:1727-1733.
54. 2+ of N-methyl-D-aspartate receptor-mediated channel current and neurotransmitter release. Proc Natl Acad Sci USA 92:3367-3370.
55. Yu AC, Drejer J, Hertz L, Schousboe A. 1983. Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J Neurochem 41:1484-1487.
56. 15N]glutamate. J Neurochem 55:137-145.
57. Zhang H, Huang HM, Carson RC, Mahmood J, Thomas HM, Gibson GE. 2001. Assessment of membrane potentials of mitochondrial populations in living cells. Anal Biochem 298:170-180.
58. 13C isotopomer analysis of glucose and alanine metabolism reveals cytosolic pyruvate compartmentation as part of energy metabolism in astrocytes. Glia 34:200-212.