L-lactate-mediated neuroprotection against glutamate- induced excitotoxicity requires ARALAR/AGC1

Journal of Neuroscience

Volumn 36, Issue 16, 2016, Pages 4443-4456

  Llorente Folch, Irene ^a,b,c   Rueda, Carlos B ^a,b,c,d   Pérez Liébana, Irene ^a,b,c   Satrústegui, Jorgina ^a,b,c   Pardo, Beatriz ^a,b,c  

^a CSIC   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c Sanitaria Fundación Jiménez Díaz   (Spain)

^d Howard Hughes Medical Institute   (United States)

Author keywords

ARALAR AGC1; Glutamate excitotoxicity; Kainic acid; L lactate; Malate aspartate NADH shuttle; Neuroprotection

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ADENINE NUCLEOTIDE TRANSLOCASE; ARALAR; EXCITATORY AMINO ACID TRANSPORTER; GLUCOSE; GLUTAMIC ACID; KAINIC ACID; LACTIC ACID; REACTIVE OXYGEN METABOLITE; RESPIRATORY STIMULANT AGENT; UNCLASSIFIED DRUG; AGC1 PROTEIN, MOUSE; AGGRECAN; CARRIER PROTEIN; SLC25A12 PROTEIN, MOUSE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL CULTURE; CELL VIABILITY ASSAY; CONTROLLED STUDY; EXCITOTOXICITY; IMAGING; IMMUNODETECTION; LASER MICROSCOPY; MALATE ASPARTATE SHUTTLE; MALE; MEMBRANE POTENTIAL; MOUSE; NERVE INJURY; NEUROPROTECTION; NONHUMAN; OXYGEN CONSUMPTION; PH; PRIORITY JOURNAL; 129 MOUSE; ANIMAL; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

AGGRECANS; ANIMALS; CELLS, CULTURED; GLUTAMIC ACID; LACTIC ACID; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NEUROPROTECTION;

EID: 84964091869     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3691-15.2016     Document Type: Article

References (87)

1. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA (2010) NAD+depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30:2967-2978. CrossRef Medline
2. Andrabi SA, Umanah GK, Chang C, Stevens DA, Karuppagounder SS, Gagné JP, Poirier GG, Dawson VL, Dawson TM (2014) Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc Natl Acad Sci U S A 111:10209-10214. CrossRef Medline
3. Barja G, Herrero A (2000) Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14:312-318. Medline
4. Barros LF (2013) Metabolic signaling by lactate in the brain. Trends Neurosci 36:396-404. CrossRef Medline
5. Ben-Ari Y, Tremblay E, Ottersen OP (1979a) [Primary and secondary cerebral lesions produced by kainic acid injections in the rat]. Comptes rendus des seances de l'Academie des sciences Serie D, Sciences naturelles 288:991-994. Medline
6. Ben-Ari Y, Lagowska J, Tremblay E, Le Gal La Salle G (1979b) A new model of focal status epilepticus: intra-amygdaloid application of kainic acid elicits repetitive secondarily generalized convulsive seizures. Brain Res 163:176-179. CrossRef Medline
7. Berthet C, Lei H, Thevenet J, Gruetter R, Magistretti PJ, Hirt L (2009) Neuroprotective role of lactate after cerebral ischemia. J Cereb Blood Flow Metab 29:1780-1789. CrossRef Medline
8. Boumezbeur F, Petersen KF, Cline GW, Mason GF, Behar KL, Shulman GI, Rothman DL (2010) The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J Neurosci 30:13983-13991. CrossRef Medline
9. Bouzat P, Magistretti PJ, OddoM (2014) Hypertonic lactate and the injured brain: facts and the potential for positive clinical implications. Intensive Care Med 40:920-921. CrossRef Medline
10. Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297-312. CrossRef Medline
11. Brennan-Minnella AM, Shen Y, El-Benna J, Swanson RA (2013) Phosphoinositide 3-kinase couples NMDA receptors to superoxide release in excitotoxic neuronal death. Cell Death Dis 4:e580. CrossRef Medline
12. Castillo X, Rosafio K, Wyss MT, Drandarov K, Buck A, Pellerin L, Weber B, Hirt L (2015) A probable dual mode of action for both L-and D-lactate neuroprotection in cerebral ischemia. J Cereb Blood Flow Metab 35: 1561-1569. CrossRef Medline
13. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634. CrossRef Medline
14. Contreras L, Satrú stegui J (2009) Calcium signaling in brain mitochondria: interplay of malate aspartate NADH shuttle and calcium uniporter/mitochondrial dehydrogenase pathways. J Biol Chem 284:7091-7099. CrossRef Medline
15. Duchen MR (2012) Mitochondria, calcium-dependent neuronal death and neurodegenerative disease. Pflugers Arch 464:111-121. CrossRef Medline
16. Duchen MR, Pearce RJ, Biscoe TJ (1990) Use of microfluorimetry to monitor mitochondrial membrane potential in single dissociated mammalian cells. J Physiol 426:2P.
17. Emaus RK, Grunwald R, Lemasters JJ (1986) Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties. Biochim Biophys Acta 850:436-448. CrossRef Medline
18. Farooqui T, Farooqui AA (2009) Aging: an ant factor for the pathogenesis of neurodegenerative diseases. Mech Ageing Dev 130:203-215. CrossRef Medline
19. Fouquerel E, Goellner EM, Yu Z, Gagné JP, Barbi de Moura M, Feinstein T, Wheeler D, Redpath P, Li J, Romero G, Migaud M, Van Houten B, Poirier GG, Sobol RW (2014) ARTD1/PARP1 negatively regulates glycolysis by inhibiting hexokinase 1 independent of NAD+ depletion. Cell Rep 8:1819-1831. CrossRef Medline
20. Gerdts J, Brace EJ, Sasaki Y, DiAntonio A, Milbrandt J (2015) SARM1 activation triggers axon degeneration locally via NAD(+) destruction. Science 348:453-457. CrossRef Medline
21. Gleichmann M, Collis LP, Smith PJ, Mattson MP (2009) Simultaneous single neuron recording of O2 consumption, [Ca 2+]i and mitochondrial membrane potential in glutamate toxicity. J Neurochem 109:644-655. CrossRef Medline
22. Hack N, Balázs R (1994) Selective stimulation of excitatory amino acid receptor subtypes and the survival of granule cells in culture: effect of quisqualate and AMPA. Neurochem Int 25:235-241. CrossRef Medline
23. Hu Y, Wilson GS (1997) A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J Neurochem 69:1484-1490. CrossRef Medline
24. Jalil MA, Begum L, Contreras L, Pardo B, Iijima M, Li MX, Ramos M, Marmol P, Horiuchi M, Shimotsu K, Nakagawa S, Okubo A, Sameshima M, Isashiki Y, Del Arco A, Kobayashi K, Satrú stegui J, Saheki T (2005) Reduced N-acetylaspartate levels in mice lacking Aralar, a brain-and muscle-type mitochondrial aspartate-glutamate carrier. J Biol Chem 280: 31333-31339. CrossRef Medline
25. Jean-Quartier C, Bondarenko AI, Alam MR, Trenker M, Waldeck-Weiermair M, Malli R, Graier WF (2012) Studying mitochondrial Ca(2+) uptake: a revisit. Mol Cell Endocrinol 353:114-127. CrossRef Medline
26. Jekabsons MB, Nicholls DG (2004) In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J Biol Chem 279:32989-33000. CrossRef Medline
27. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103. CrossRef Medline
28. Kauppinen RA, Taipale HT, Komulainen H (1989) Interrelationships between glucose metabolism, energy state, and the cytosolic free calcium concentration in cortical synaptosomes from the guinea pig. J Neurochem 53:766-771. CrossRef Medline
29. Kim SH, Lu HF, Alano CC (2011) Neuronal Sirt3 protects against excitotoxic injury in mouse cortical neuron culture. PLoS One 6:e14731. CrossRef Medline
30. Lauritzen KH, Morland C, Puchades M, Holm-Hansen S, Hagelin EM, Lauritzen F, Attramadal H, Storm-Mathisen J, Gjedde A, Bergersen LH (2014) Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism. Cereb Cortex 24:2784-2795. CrossRef Medline
31. Llorente-Folch I, Rueda CB, Amigo I, del Arco A, Saheki T, Pardo B, Satrú-stegui J (2013) Calcium-regulation of mitochondrial respiration maintains ATP homeostasis and requires ARALAR/AGC1-malate aspartate shuttle in intact cortical neurons. J Neurosci 33:13957-13971. CrossRef Medline
32. Loaiza A, Porras OH, Barros LF (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337-7342. Medline
33. Lothman EW, Collins RC (1981) Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218:299-318. CrossRef Medline
34. Lund P, Bergmeyer HU (1986) Glutamine and L-glutamate: UV-method with glutaminase and glutamate dehydrogenase. In: Methods of enzymatic analysis, Vol. 8, pp 357-363. Weinheim: Verlagsgesellschaft.
35. Mattson MP, Barger SW, Begley JG, Mark RJ (1995) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 46:187-216. CrossRef Medline
36. Maus M, Marin P, Israël M, Glowinski J, Prémont J (1999) Pyruvate and lactate protect striatal neurons against N-methyl-D-aspartate-induced neurotoxicity. Eur J Neurosci 11:3215-3224. CrossRef Medline
37. Mayer ML, Westbrook GL (1987) Permeation and block of N-methyl-Daspartic acid receptor channels by divalent cations in mouse cultured central neurones. J Physiol 394:501-527. CrossRef Medline
38. Menga A, Iacobazzi V, Infantino V, Avantaggiati ML, Palmieri F (2015) The mitochondrial aspartate/glutamate carrier isoform 1 gene expression is regulated by CREB in neuronal cells. Int J Biochem Cell Biol 60:157-166. CrossRef Medline
39. Mosienko V, Teschemacher AG, Kasparov S (2015) Is L-lactate a novel signaling molecule in the brain? J Cereb Blood Flow Metab 35:1069-1075. CrossRef Medline
40. Nicholls DG (2008) Oxidative stress and energy crises in neuronal dysfunction. Ann N Y Acad Sci 1147:53-60. CrossRef Medline
41. Nicholls DG, Vesce S, Kirk L, Chalmers S (2003) Interactions between mitochondrial bioenergetics and cytoplasmic calcium in cultured cerebellar granule cells. Cell Calcium 34:407-424. CrossRef Medline
42. Nicholls DG, Johnson-Cadwell L, Vesce S, Jekabsons M, Yadava N (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J Neurosci Res 85:3206-3212. CrossRef Medline
43. Olney JW, Fuller T, de Gubareff T (1979) Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res 176:91-100. CrossRef Medline
44. Palmer AE, Tsien RY (2006) Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc 1:1057-1065. CrossRef Medline
45. Pardo B, Contreras L, Serrano A, Ramos M, Kobayashi K, Iijima M, Saheki T, Satrú stegui J (2006) Essential role of Aralar in the transduction of small Ca2+ signals to neuronal mitochondria. J Biol Chem 281:1039-1047. CrossRef Medline
46. 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. CrossRef Medline
47. Pellerin L, Magistretti PJ (1996) Excitatory amino acids stimulate aerobic glycolysis in astrocytes via an activation of the Na+/K+ ATPase. Dev Neurosci 18:336-342. CrossRef Medline
48. Pellerin L, Magistretti PJ (2004) Neuroscience: let there be (NADH) light. Science 305:50-52. CrossRef Medline
49. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL, Stella N, Magistretti PJ (1998) Evidence supporting the existence of an activitydependent astrocyte-neuron lactate shuttle. Dev Neurosci 20:291-299. CrossRef Medline
50. Porras OH, Ruminot I, Loaiza A, Barros LF (2008) Na(+)-Ca(2+) cosignaling in the stimulation of the glucose transporter GLUT1 in cultured astrocytes. Glia 56:59-68. CrossRef Medline
51. Prichard J, Rothman D, Novotny E, Petroff O, Kuwabara T, Avison M, Howseman A, Hanstock C, Shulman R (1991) Lactate rise detected by 1H NMR in human visual cortex during physiologic stimulation. Proc Natl Acad Sci U S A 88:5829-5831. CrossRef Medline
52. Qian W, Van Houten B (2010) Alterations in bioenergetics due to changes in mitochondrial DNA copy number. Methods 51:452-457. CrossRef Medline
53. Qiu J, Tan YW, Hagenston AM, Martel MA, Kneisel N, Skehel PA, Wyllie DJ, Bading H, Hardingham GE (2013) Mitochondrial calcium uniporter Mcu controls excitotoxicity and is transcriptionally repressed by neuroprotective nuclear calcium signals. Nat Commun 4:2034. CrossRef Medline
54. Racine RJ (1972) Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294. CrossRef Medline
55. Ramos M, del Arco A, Pardo B, Martínez-Serrano A, Martínez-Morales JR, Kobayashi K, Yasuda T, Bogó nez E, Bovolenta P, Saheki T, Satrú stegui J (2003) Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier Aralar1 in brain and prominent expression in the spinal cord. Brain Res Dev Brain Res 143:33-46. CrossRef Medline
56. Rodriguez-Rodriguez P, Almeida A, Bolaños JP (2013) Brain energy metabolism in glutamate-receptor activation and excitotoxicity: role for APC/ C-Cdh1 in the balance glycolysis/pentose phosphate pathway. Neurochem Int 62:750-756. CrossRef Medline
57. Ros J, Pecinska N, Alessandri B, Landolt H, FillenzM (2001) Lactate reduces glutamate-induced neurotoxicity in rat cortex. J Neurosci Res 66:790-794. CrossRef Medline
58. Rose CR, Ransom BR (1997) Regulation of intracellular sodium in cultured rat hippocampal neurones. J Physiol 499:573-587. CrossRef Medline
59. Rueda CB, Llorente-Folch I, Amigo I, Contreras L, González-Sánchez P, Martínez-Valero P, Juaristi I, Pardo B, del Arco A, Satrú stegui J (2014) Ca(2+) regulation of mitochondrial function in neurons. Biochim Biophys Acta 1837:1617-1624. CrossRef Medline
60. Rueda CB, Traba J, Amigo I, Llorente-Folch I, González-Sánchez P, Pardo B, Esteban JA, del Arco A, Satrú stegui J (2015) Mitochondrial ATP-Mg/Pi carrier SCaMC-3/Slc25a23 counteracts PARP-1-dependent fall in mitochondrial ATP caused by excitotoxic insults in neurons. J Neurosci 35: 3566-3581. CrossRef Medline
61. Ruiz F, Alvarez G, Pereira R, Hernández M, Villalba M, Cruz F, Cerdán S, Bogó nez E, Satrú stegui J (1998) Protection by pyruvate and malate against glutamate-mediated neurotoxicity. Neuroreport 9:1277-1282. Medline San
62. Martín A, Ceballo S, Ruminot I, Lerchundi R, Frommer WB, Barros LF (2013) A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells. PLoS One 8:e57712. CrossRef Medline
63. Satrú stegui J, Bak LK (2015) Fluctuations in cytosolic calcium regulate the neuronal malate-aspartate NADH shuttle: implications for neuronal energy metabolism. Neurochem Res 40:2425-2430. CrossRef Medline
64. Satrú stegui J, Pardo B, Del Arco A (2007) Mitochondrial transporters as novel targets for intracellular calcium signaling. Physiol Rev 87:29-67. CrossRef Medline
65. Schauwecker PE (2011) The relevance of individual genetic background and its role in animal models of epilepsy. Epilepsy Res 97:1-11. CrossRef Medline
66. Schauwecker PE, Steward O (1997) Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc Natl Acad Sci U S A 94:4103-4108. CrossRef Medline
67. Schmued LC, Albertson C, SlikkerWJr (1997) Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751:37-46. CrossRef Medline
68. Schurr A, Payne RS, Miller JJ, Rigor BM (1997a) Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res 744:105-111. CrossRef Medline
69. Schurr A, Payne RS, Miller JJ, Rigor BM (1997b) Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69:423-426. CrossRef Medline
70. Schurr A, Payne RS, Tseng MT, Gozal E, Gozal D (2001a) Excitotoxic preconditioning elicited by both glutamate and hypoxia and abolished by lactate transport inhibition in rat hippocampal slices. Neurosci Lett 307: 151-154. CrossRef Medline
71. Schurr A, Payne RS, Miller JJ, Tseng MT, Rigor BM (2001b) Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia. Brain Res 895:268-272. CrossRef Medline
72. Serres S, Bezancon E, Franconi JM, Merle M (2004) Ex vivo analysis of lactate and glucose metabolism in the rat brain under different states of depressed activity. J Biol Chem 279:47881-47889. CrossRef Medline
73. Shulman RG, Hyder F, Rothman DL (2001) Cerebral energetics and the glycogen shunt: neurochemical basis of functional imaging. Proc Natl Acad Sci U S A 98:6417-6422. CrossRef Medline
74. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK, Amiel SA (2003) Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 23:658-664. CrossRef Medline
75. Sokoloff L (1992) The brain as a chemical machine. Prog Brain Res 94: 19-33. CrossRef Medline
76. Soultanakis RP, Melamede RJ, Bespalov IA, Wallace SS, Beckman KB, Ames BN, Taatjes DJ, Janssen-HeiningerYM (2000) Fluorescence detection of 8-oxoguanine in nuclear and mitochondrialDNAof cultured cells using a recombinant Fab and confocal scanning laser microscopy. Free Radic Biol Med 28:987-998. CrossRef Medline
77. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373. CrossRef Medline
78. Tantama M, Martínez-Francois JR, Mongeon R, Yellen G (2013) Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATP-to-ADP ratio. Nat Commun 4:2550. CrossRef Medline
79. Tildon JT, McKenna MC, Stevenson J, Couto R (1993) Transport of L-lactate by cultured rat brain astrocytes. Neurochem Res 18:177-184. CrossRef Medline
80. Vergun O, Sobolevsky AI, Yelshansky MV, Keelan J, Khodorov BI, Duchen MR (2001) Exploration of the role of reactive oxygen species in glutamate neurotoxicity in rat hippocampal neurones in culture. J Physiol 531:147-163. CrossRef Medline
81. Walls AB, Eyjolfsson EM, Schousboe A, Sonnewald U, Waagepetersen HS (2014) A subconvulsive dose of kainate selectively compromises astrocytic metabolism in the mouse brain in vivo. J Cereb Blood Flow Metab 34:1340-1346. CrossRef Medline
82. Wang GJ, Randall RD, Thayer SA (1994) Glutamate-induced intracellular acidification of cultured hippocampal neurons demonstrates altered energy metabolism resulting from Ca2+ loads. J Neurophysiol 72:2563-2569. Medline
83. Wang Y, Qin ZH (2010) Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 15:1382-1402. CrossRef Medline
84. Wong EH, Kemp JA, Priestley T, Knight AR, Woodruff GN, Iversen LL (1986) The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc Natl Acad Sci U S A 83:7104-7108. CrossRef Medline
85. Yang J, Ruchti E, Petit JM, Jourdain P, Grenningloh G, Allaman I, Magistretti PJ (2014) Lactate promotes plasticity gene expression by potentiating NMDAsignaling in neurons. Proc Natl Acad SciU S A 111:12228-12233. CrossRef Medline
86. Yano S, Tokumitsu H, Soderling TR (1998) Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396:584-587. CrossRef Medline
87. Zhang J, Dawson VL, Dawson TM, Snyder SH (1994) Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263: 687-689. CrossRef Medline