Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes

Journal of Neuroscience

Volumn 31, Issue 10, 2011, Pages 3550-3559

  Azarias, Guillaume ^a   Perreten, Hélène ^b   Lengacher, Sylvain ^b   Poburko, Damon ^c   Demaurex, Nicolas ^c   Magistretti, Pierre J ^b,d   Chatton, Jean Yves ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b EPFL   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d Center for Psychiatric Neuroscience Lausanne   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; OXYGEN; REACTIVE OXYGEN METABOLITE; SODIUM ION;

ACIDIFICATION; AEROBIC METABOLISM; AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; ASTROCYTE; CELL PH; CONTROLLED STUDY; CYTOSOL; ENERGY METABOLISM; FLUORESCENCE ANALYSIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MITOCHONDRION PH; MOUSE; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SODIUM CELL LEVEL; SYNAPTIC TRANSMISSION;

AMINO ACID TRANSPORT SYSTEM X-AG; ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CEREBRAL CORTEX; ENERGY METABOLISM; GLUTAMIC ACID; HYDROGEN-ION CONCENTRATION; MICE; MITOCHONDRIA; NEURONS; OXYGEN;

EID: 79952427057     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4378-10.2011     Document Type: Article

References (47)

1. Abad MF, Di Benedetto G, Magalhães PJ, Filippin L, Pozzan T (2004) Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J Biol Chem 279:11521-11529. (Pubitemid 38401652)
2. Alle H, Roth A, Geiger JR (2009) Energy-efficient action potentials in hippocampal mossy fibers. Science 325:1405-1408.
3. Amato A, Ballerini L, Attwell D (1994) Intracellular pH changes produced by glutamate uptake in rat hippocampal slices. J Neurophysiol 72:1686-1696. (Pubitemid 24325095)
4. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483-495. (Pubitemid 40269763)
5. Bernardi P (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79:1127-1155.
6. + responses in astrocytes. Glia 54:460-470.
7. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhäuser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7:613-620. (Pubitemid 38691900)
8. Blachly-Dyson E, Forte M (2001) VDACchannels. IUBMB Life 52:113-118.
9. Casey JR, Grinstein S, Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11:50-61.
10. + dynamics in mouse cortical astrocytes: implications for cellular bioenergetics. Eur J Neurosci 12:3843-3853.
11. Chatton JY, Idle JR, Vågbø CB, Magistretti PJ (2001) Insights into the mechanisms of ifosfamide encephalopathy: drug metabolites have agonistic effects on alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptors and induce cellular acidification in mouse cortical neurons. J Pharmacol Exp Ther 299:1161-1168. (Pubitemid 33104990)
12. Chatton JY, Pellerin L, Magistretti PJ (2003) GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci U S A 100:12456-12461. (Pubitemid 37271581)
13. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
14. Chesler M, Kraig RP (1989) Intracellular pH transients of mammalian astrocytes. J Neurosci 9:2011-2019. (Pubitemid 19156989)
15. 2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem J 283:41-50.
16. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139-143. (Pubitemid 30491313)
17. Hajnó czky G, Robb-Gaspers LD, Seitz MB, Thomas AP (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82:415-424.
18. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honoré T, Nielsen M, Lehre KP, Danbolt NC (1996) Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722. (Pubitemid 26367342)
19. Herrero-Mendez A, Almeida A, Fernández E, Maestre C, Moncada S, Bolaños 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.
20. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/ glycogenolysis. J Cereb Blood Flow Metab 27:219-249. (Pubitemid 46148451)
21. Kahlert S, Zündorf G, Reiser G (2008) Detection of de-and hyperpolarization of mitochondria of cultured astrocytes and neurons by the cationic fluorescent dye rhodamine 123. J Neurosci Methods 171:87-92.
22. Langer J, Rose CR (2009) Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859-5877.
23. Levy LM, Warr O, Attwell D (1998) Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J Neurosci 18:9620-9628. (Pubitemid 28543743)
24. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, Han X, Takano T, Wang S, Sim FJ, Goldman SA, Nedergaard M (2007) The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-12266. (Pubitemid 350085462)
25. Magistretti PJ (2009) Neuroscience. Low-cost travel in neurons. Science 325:1349-1351.
26. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-497.
27. Mitchell P (1979) Keilin's respiratory chain concept and its chemiosmotic consequences. Science 206:1148-1159.
28. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276-3287.
29. Pawelczyk T, Olson MS (1995) Changes in the structure of pyruvate dehydrogenase complex induced by mono-and divalent ions. Int J Biochem Cell Biol 27:513-521.
30. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625-10629. (Pubitemid 24329051)
31. Pellerin L, Magistretti PJ (2003) Food for thought: challenging the dogmas. J Cereb Blood Flow Metab 23:1282-1286. (Pubitemid 37409790)
32. Poburko D, Santo-Domingo J, Demaurex N (2011) Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevation. J Biol Chem. Advance online publication. Retrieved Feb 14, 2011. doi:10.1074/jbc.M110.159962.
33. Porcelli AM, Ghelli A, Zanna C, Pinton P, Rizzuto R, Rugolo M (2005) pH difference across the outer mitochondrial membrane measured with a green fluorescent protein mutant. Biochem Biophys Res Commun 326:799-804. (Pubitemid 39655990)
34. Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A 103:15038-15043. (Pubitemid 44583160)
35. + changes induced by glutamate, kainate, and D-aspartate in rat hippocampal astrocytes. J Neurosci 16:5393-5404.
36. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551-1555.
37. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638-1643. (Pubitemid 351931254)
38. Selivanov VA, Zeak JA, Roca J, Cascante M, Trucco M, Votyakova TV (2008) The role of external and matrix pH in mitochondrial reactive oxygen species generation. J Biol Chem 283:29292-29300.
39. Serres S, Raffard G, Franconi JM, Merle M (2008) Close coupling between astrocytic and neuronal metabolisms to fulfill anaplerotic and energy needs in the rat brain. J Cereb Blood Flow Metab 28:712-724. (Pubitemid 351432784)
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 U S A 95:316-321. (Pubitemid 28103951)
41. Sorg O, Magistretti PJ (1992) Vasoactive intestinal peptide and noradrenaline exert long-term control on glycogen levels in astrocytes: blockade by protein synthesis inhibition. J Neurosci 12:4923-4931.
42. Strathmann J, Klimo K, Sauer SW, Okun JG, Prehn JH, Gerhäuser C (2010) Xanthohumol-induced transient superoxide anion radical formation triggers cancer cells into apoptosis via a mitochondria-mediated mechanism. FASEB J 24:2938-2950.
43. Tsacopoulos M, Magistretti PJ (1996) Metabolic coupling between glia and neurons. J Neurosci 16:877-885. (Pubitemid 26140843)
44. Verkhratsky A, Steinhäuser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380-412. (Pubitemid 30171314)
45. Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton JY, Magistretti PJ, Pellerin L (2003) Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37:275-286. (Pubitemid 36143822)
46. Wiederkehr A, Park KS, Dupont O, Demaurex N, Pozzan T, Cline GW, Wollheim CB (2009) Matrix alkalinization: a novel mitochondrial signal for sustained pancreatic beta-cell activation. EMBO J 28:417-428.
47. Wyss MT, Weber B, Treyer V, Heer S, Pellerin L, Magistretti PJ, Buck A (2009) Stimulation-induced increases of astrocytic oxidative metabolism in rats and humans investigated with 1-11C-acetate. J Cereb Blood Flow Metab 29:44-56.