Physical and functional interaction of NCX1 and EAAC1 transporters leading to glutamate-enhanced ATP production in brain mitochondria

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Magi, Simona ^a   Lariccia, Vincenzo ^a   Castaldo, Pasqualina ^a   Arcangeli, Sara ^a   Nasti, Annamaria Assunta ^a   Giordano, Antonio ^a   Amoroso, Salvatore ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTISENSE OLIGONUCLEOTIDE; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; LUCIFERASE; LUCIFERIN; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG; ION; MALIC ACID; MALIC ACID DERIVATIVE; PYRUVIC ACID; SLC1A1 PROTEIN, HUMAN; SLC1A1 PROTEIN, RAT; SODIUM; SODIUM CALCIUM EXCHANGER 1; SODIUM-CALCIUM EXCHANGER 1;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; WESTERN BLOTTING; ANIMAL; BRAIN; CELL STRAIN; CHEMISTRY; METABOLISM; METHODOLOGY; MITOCHONDRION; NERVE CELL; OXIDATIVE STRESS; SWINE; WISTAR RAT;

MAMMALIA;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; HUMANS; IONS; MALATES; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; NEURONS; OXIDATIVE STRESS; PC12 CELLS; PYRUVIC ACID; RATS; RATS, WISTAR; SODIUM; SODIUM-CALCIUM EXCHANGER; SWINE;

EID: 84859131447     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034015     Document Type: Article

References (79)

1. Vanzetta I, Grinvald A, (1999) Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 286: 1555-1558.
2. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, et al. (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci U S A 95: 316-321.
3. Pellerin L, (2005) How astrocytes feed hungry neurons. Mol Neurobiol 32: 59-72.
4. Mangia S, Garreffa G, Bianciardi M, Giove F, Di Salle F, et al. (2003) The aerobic brain: lactate decrease at the onset of neural activity. Neuroscience 118: 7-10.
5. Chih CP, Roberts EL Jr, (2003) Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis. J Cereb Blood Flow Metab 23: 1263-1281.
6. Figley CR, (2011) Lactate transport and metabolism in the human brain: implications for the astrocyte-neuron lactate shuttle hypothesis. J Neurosci 31: 4768-4770.
7. Magistretti PJ, Pellerin L, (1999) Astrocytes Couple Synaptic Activity to Glucose Utilization in the Brain. News Physiol Sci 14: 177-182.
8. McKenna MC, Waagepetersen HS, Schousboe A, Sonnewald U, (2006) Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: current evidence and pharmacological tools. Biochem Pharmacol 71: 399-407.
9. Nehlig A, Coles JA, (2007) Cellular pathways of energy metabolism in the brain: is glucose used by neurons or astrocytes? Glia 55: 1238-1250.
10. Panov A, Schonfeld P, Dikalov S, Hemendinger R, Bonkovsky HL, et al. (2009) The neuromediator glutamate, through specific substrate interactions, enhances mitochondrial ATP production and reactive oxygen species generation in nonsynaptic brain mitochondria. J Biol Chem 284: 14448-14456.
11. Simpson IA, Carruthers A, Vannucci SJ, (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27: 1766-1791.
12. Danbolt NC, (2001) Glutamate uptake. Prog Neurobiol 65: 1-105.
13. Beart PM, O'Shea RD, (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol 150: 5-17.
14. Tzingounis AV, Wadiche JI, (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8: 935-947.
15. 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.
16. Yudkoff M, Nelson D, Daikhin Y, Erecinska M, (1994) Tricarboxylic acid cycle in rat brain synaptosomes. Fluxes and interactions with aspartate aminotransferase and malate/aspartate shuttle. J Biol Chem 269: 27414-27420.
17. Pisarenko OI, Solomatina ES, Ivanov VE, Studneva IM, Kapelko VI, et al. (1985) On the mechanism of enhanced ATP formation in hypoxic myocardium caused by glutamic acid. Basic Res Cardiol 80: 126-134.
18. Palmieri F, (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 447: 689-709.
19. Satrustegui J, Pardo B, Del Arco A, (2007) Mitochondrial transporters as novel targets for intracellular calcium signaling. Physiol Rev 87: 29-67.
20. Ralphe JC, Bedell K, Segar JL, Scholz TD, (2005) Correlation between myocardial malate/aspartate shuttle activity and EAAT1 protein expression in hyper- and hypothyroidism. Am J Physiol Heart Circ Physiol 288: H2521-2526.
21. Ralphe JC, Segar JL, Schutte BC, Scholz TD, (2004) Localization and function of the brain excitatory amino acid transporter type 1 in cardiac mitochondria. J Mol Cell Cardiol 37: 33-41.
22. Castaldo P, Cataldi M, Magi S, Lariccia V, Arcangeli S, et al. (2009) Role of the mitochondrial sodium/calcium exchanger in neuronal physiology and in the pathogenesis of neurological diseases. Prog Neurobiol 87: 58-79.
23. Gobbi P, Castaldo P, Minelli A, Salucci S, Magi S, et al. (2007) Mitochondrial localization of Na+/Ca2+ exchangers NCX1-3 in neurons and astrocytes of adult rat brain in situ. Pharmacol Res 56: 556-565.
24. Minelli A, Castaldo P, Gobbi P, Salucci S, Magi S, et al. (2007) Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 41: 221-234.
25. Blaustein MP, Lederer WJ, (1999) Sodium/calcium exchange: its physiological implications. Physiol Rev 79: 763-854.
26. Santo-Domingo J, Demaurex N, (2010) Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta 1797: 907-912.
27. Smets I, Caplanusi A, Despa S, Molnar Z, Radu M, et al. (2004) Ca2+ uptake in mitochondria occurs via the reverse action of the Na+/Ca2+ exchanger in metabolically inhibited MDCK cells. Am J Physiol Renal Physiol 286: F784-794.
28. Cervos-Navarro J, Diemer NH, (1991) Selective vulnerability in brain hypoxia. Crit Rev Neurobiol 6: 149-182.
29. Amoroso S, Schmid-Antomarchi H, Fosset M, Lazdunski M, (1990) Glucose, sulfonylureas, and neurotransmitter release: role of ATP-sensitive K+ channels. Science 247: 852-854.
30. Hirrlinger J, Dringen R, (2010) The cytosolic redox state of astrocytes: Maintenance, regulation and functional implications for metabolite trafficking. Brain Res Rev 63: 177-188.
31. Kanai Y, Smith CP, Hediger MA, (1993) A new family of neurotransmitter transporters: the high-affinity glutamate transporters. FASEB J 7: 1450-1459.
32. del Arco A, Satrustegui J, (1998) Molecular cloning of Aralar, a new member of the mitochondrial carrier superfamily that binds calcium and is present in human muscle and brain. J Biol Chem 273: 23327-23334.
33. Anderson CM, Bridges RJ, Chamberlin AR, Shimamoto K, Yasuda-Kamatani Y, et al. (2001) Differing effects of substrate and non-substrate transport inhibitors on glutamate uptake reversal. J Neurochem 79: 1207-1216.
34. Montiel T, Camacho A, Estrada-Sanchez AM, Massieu L, (2005) Differential effects of the substrate inhibitor l-trans-pyrrolidine-2,4-dicarboxylate (PDC) and the non-substrate inhibitor DL-threo-beta-benzyloxyaspartate (DL-TBOA) of glutamate transporters on neuronal damage and extracellular amino acid levels in rat brain in vivo. Neuroscience 133: 667-678.
35. Shigeri Y, Seal RP, Shimamoto K, (2004) Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Res Brain Res Rev 45: 250-265.
36. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, et al. (1998) DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53: 195-201.
37. Waagepetersen HS, Shimamoto K, Schousboe A, (2001) Comparison of effects of DL-threo-beta-benzyloxyaspartate (DL-TBOA) and L-trans-pyrrolidine-2,4-dicarboxylate (t-2,4-PDC) on uptake and release of [3 h]D-aspartate in astrocytes and glutamatergic neurons. Neurochem Res 26: 661-666.
38. Desagher S, Glowinski J, Premont J, (1997) Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J Neurosci 17: 9060-9067.
39. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, et al. (2004) Characterization of novel L-threo-beta-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65: 1008-1015.
40. Lee A, Anderson AR, Barnett AC, Chan A, Pow DV, (2011) Expression of multiple glutamate transporter splice variants in the rodent testis. Asian J Androl 13: 254-265.
41. Dedkova EN, Blatter LA, (2005) Modulation of mitochondrial Ca2+ by nitric oxide in cultured bovine vascular endothelial cells. Am J Physiol Cell Physiol 289: C836-845.
42. Nicholls DG, Ward MW, (2000) Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci 23: 166-174.
43. Perez-Ortiz JM, Tranque P, Vaquero CF, Domingo B, Molina F, et al. (2004) Glitazones differentially regulate primary astrocyte and glioma cell survival. Involvement of reactive oxygen species and peroxisome proliferator-activated receptor-gamma. J Biol Chem 279: 8976-8985.
44. Li S, Stys PK, (2001) Na(+)-K(+)-ATPase inhibition and depolarization induce glutamate release via reverse Na(+)-dependent transport in spinal cord white matter. Neuroscience 107: 675-683.
45. Pellerin L, Magistretti PJ, (1997) Glutamate uptake stimulates Na+,K+-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J Neurochem 69: 2132-2137.
46. O'Rourke B, (2007) Mitochondrial ion channels. Annu Rev Physiol 69: 19-49.
47. Masereel B, Pochet L, Laeckmann D, (2003) An overview of inhibitors of Na(+)/H(+) exchanger. Eur J Med Chem 38: 547-554.
48. Bernardinelli Y, Azarias G, Chatton JY, (2006) In situ fluorescence imaging of glutamate-evoked mitochondrial Na+ responses in astrocytes. Glia 54: 460-470.
49. Cox DA, Conforti L, Sperelakis N, Matlib MA, (1993) Selectivity of inhibition of Na(+)-Ca2+ exchange of heart mitochondria by benzothiazepine CGP-37157. J Cardiovasc Pharmacol 21: 595-599.
50. McCormack JG, Halestrap AP, Denton RM, (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70: 391-425.
51. Matlib MA, Zhou Z, Knight S, Ahmed S, Choi KM, et al. (1998) Oxygen-bridged dinuclear ruthenium amine complex specifically inhibits Ca2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J Biol Chem 273: 10223-10231.
52. Zhivotovsky B, Galluzzi L, Kepp O, Kroemer G, (2009) Adenine nucleotide translocase: a component of the phylogenetically conserved cell death machinery. Cell Death Differ 16: 1419-1425.
53. Magi S, Castaldo P, Carrieri G, Scorziello A, Di Renzo G, et al. (2005) Involvement of Na+-Ca2+ exchanger in intracellular Ca2+ increase and neuronal injury induced by polychlorinated biphenyls in human neuroblastoma SH-SY5Y cells. J Pharmacol Exp Ther 315: 291-296.
54. Quednau BD, Nicoll DA, Philipson KD, (1997) Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol 272: C1250-1261.
55. Kleizen B, Braakman I, (2004) Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16: 343-349.
56. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
57. Zambonin JL, Zhao C, Ohno N, Campbell GR, Engeham S, et al. (2011) Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis. Brain 134: 1901-1913.
58. Jung DW, Apel LM, Brierley GP, (1992) Transmembrane gradients of free Na+ in isolated heart mitochondria estimated using a fluorescent probe. Am J Physiol 262: C1047-1055.
59. Benveniste H, Drejer J, Schousboe A, Diemer NH, (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43: 1369-1374.
60. Ikonomidou C, Turski L, (2002) Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 1: 383-386.
61. Castaldo P, Magi S, Gaetani S, Cassano T, Ferraro L, et al. (2007) Prenatal exposure to the cannabinoid receptor agonist WIN 55,212-2 increases glutamate uptake through overexpression of GLT1 and EAAC1 glutamate transporter subtypes in rat frontal cerebral cortex. Neuropharmacology 53: 369-378.
62. Cuong DV, Kim N, Joo H, Youm JB, Chung JY, et al. (2005) Subunit composition of ATP-sensitive potassium channels in mitochondria of rat hearts. Mitochondrion 5: 121-133.
63. Yu WH, Wolfgang W, Forte M, (1995) Subcellular localization of human voltage-dependent anion channel isoforms. J Biol Chem 270: 13998-14006.
64. Babsky A, Doliba N, Savchenko A, Wehrli S, Osbakken M, (2001) Na+ effects on mitochondrial respiration and oxidative phosphorylation in diabetic hearts. Exp Biol Med (Maywood) 226: 543-551.
65. Guang HM, Du GH, (2006) Protections of pinocembrin on brain mitochondria contribute to cognitive improvement in chronic cerebral hypoperfused rats. Eur J Pharmacol 542: 77-83.
66. Gunter TE, Miller LM, Gavin CE, Eliseev R, Salter J, et al. (2004) Determination of the oxidation states of manganese in brain, liver, and heart mitochondria. J Neurochem 88: 266-280.
67. Almeida A, Medina JM, (1998) A rapid method for the isolation of metabolically active mitochondria from rat neurons and astrocytes in primary culture. Brain Res Brain Res Protoc 2: 209-214.
68. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, et al. (2002) Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125: 32-43.
69. Yu YX, Shen L, Xia P, Tang YW, Bao L, et al. (2006) Syntaxin 1A promotes the endocytic sorting of EAAC1 leading to inhibition of glutamate transport. J Cell Sci 119: 3776-3787.
70. Lomonosova E, Subramanian T, Chinnadurai G, (2005) Mitochondrial localization of p53 during adenovirus infection and regulation of its activity by E1B-19K. Oncogene 24: 6796-6808.
71. Wittig I, Schagger H, (2007) Electrophoretic methods to isolate protein complexes from mitochondria. Methods Cell Biol 80: 723-741.
72. Castaldo P, Magi S, Cataldi M, Arcangeli S, Lariccia V, et al. (2010) Altered regulation of glutamate release and decreased functional activity and expression of GLT1 and GLAST glutamate transporters in the hippocampus of adolescent rats perinatally exposed to Delta(9)-THC. Pharmacol Res 61: 334-341.
73. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, et al. (2002) Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5: 155-161.
74. Frontini A, Bertolotti P, Tonello C, Valerio A, Nisoli E, et al. (2008) Leptin-dependent STAT3 phosphorylation in postnatal mouse hypothalamus. Brain Res 1215: 105-115.
75. Chalmers S, McCarron JG, (2008) The mitochondrial membrane potential and Ca2+ oscillations in smooth muscle. J Cell Sci 121: 75-85.
76. Fiskum G, (1985) Intracellular levels and distribution of Ca2+ in digitonin-permeabilized cells. Cell Calcium 6: 25-37.
77. Giordano A, Calvani M, Petillo O, Grippo P, Tuccillo F, et al. (2005) tBid induces alterations of mitochondrial fatty acid oxidation flux by malonyl-CoA-independent inhibition of carnitine palmitoyltransferase-1. Cell Death Differ 12: 603-613.
78. Lartigue L, Kushnareva Y, Seong Y, Lin H, Faustin B, et al. (2009) Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol Biol Cell 20: 4871-4884.
79. Kirichok Y, Krapivinsky G, Clapham DE, (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427: 360-364.