Elevated lactate suppresses neuronal firing in vivo and inhibits glucose metabolism in hippocampal slice cultures

Brain Research

Volumn 1117, Issue 1, 2006, Pages 213-223

  Gilbert, Erin ^a   Tang, J Michael ^a   Ludvig, Nandor ^a   Bergold, Peter J ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

ATP; Cerebral metabolism; Ischemia; Lactate; Microdialysis; Oxidation reduction

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTRODE; GLUCOSE METABOLISM; GLUCOSE OXIDATION; HIPPOCAMPUS; MALE; NERVE CELL; NONHUMAN; OXIDATION REDUCTION REACTION; PERFUSION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; TISSUE CULTURE;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG INTERACTIONS; ENERGY METABOLISM; GLUCOSE; HIPPOCAMPUS; LACTIC ACID; MALE; NAD; NEURONS; ORGAN CULTURE TECHNIQUES; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; PYRAMIDAL CELLS; PYRUVIC ACID; RATS; RATS, LONG-EVANS; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 33749983983     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.07.107     Document Type: Article

References (69)

1. Ahmed S.M., Rzigalinski B.A., Willoughby K.A., Sitterding H.A., and Ellis E.F. Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J. Neurochem. 74 (2000) 1951-1960
2. Allen N.J., Karadottir R., and Attwell D. A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells. J. Neurosci. 25 (2005) 848-859
3. Andrews Z.B., Diano S., and Horvath T.L. Mitochondrial uncoupling proteins in the CNS: in support of function and survival. Nat. Rev., Neurosci. 6 (2005) 829-840
4. Bittar P.G., Charnay Y., Pellerin L., Bouras C., and Magistretti P.J. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J. Cereb. Blood Flow Metab. 16 (1996) 1079-1089
5. Borowsky I.W., and Collins R.C. Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities. J. Comp. Neurol. 288 (1989) 401-413
6. Cerdan S., Rodrigues T.B., Sierra A., Benito M., Fonseca L.L., Fonseca C.P., and Garcia-Martin M.L. The redox switch/redox coupling hypothesis. Neurochem. Int. 48 (2006) 523-530
7. Chen T., Qian Y.Z., Di X., Zhu J.P., and Bullock R. Evidence for lactate uptake after rat fluid percussion injury. Acta Neurochir., Suppl. 76 (2000) 359-364
8. Chih C.P., and Roberts Jr. E.L. Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis. J. Cereb. Blood Flow Metab. 23 (2003) 1263-1281
9. Chih C.P., Lipton P., and Roberts Jr. E.L. Do active cerebral neurons really use lactate rather than glucose?. TINS 24 (2001) 573-578
10. Chih C.P., He J., Sly T.S., and Roberts Jr. E.L. Comparison of glucose and lactate as substrates during NMDA-induced activation of hippocampal slices. Brain Res. 893 (2001) 143-154
11. Choi I.Y., Lee S.P., Kim S.G., and Gruetter R. In vivo measurements of brain glucose transport using the reversible Michaelis-Menten model and simultaneous measurements of cerebral blood flow changes during hypoglycemia. J. Cereb. Blood Flow Metab. 21 (2001) 653-663
12. Crumrine R.C., and LaManna J.C. Regional cerebral metabolites, blood flow, plasma volume, and mean transit time in total cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 11 (1991) 272-282
13. Debernardi R., Pierre K., Lengacher S., Magistretti P.J., and Pellerin L. Cell-specific expression pattern of monocarboxylate transporters in astrocytes and neurons observed in different mouse brain cortical cell cultures. J. Neurosci. Res. 73 (2003) 141-155
14. Dirnagl U., Iadecola C., and Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22 (1999) 391-397
15. Fox P.T., and Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 1140-1144
16. Fox S.E., and Ranck Jr. J.B. Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp. Brain Res. 41 (1981) 399-410
17. Gewirtz R.J., Dhillon H.S., Goes S.E., DeAtley S.M., and Scheff S.W. Lactate and free fatty acids after subarachnoid hemorrhage. Brain Res. 840 (1999) 84-91
18. 14C-labeled substrates by hippocampal slice cultures. Brain Res. Protoc. 15 (2005) 135-141
19. Glenn T.C., Kelly D.F., Boscardin W.J., McArthur D.L., Vespa P., Oertel M., Hovda D.A., Bergsneider M., Hillered L., and Martin N.A. Energy dysfunction as a predictor of outcome after moderate or severe head injury: indices of oxygen, glucose, and lactate metabolism. J. Cereb. Blood Flow Metab. 23 (2003) 1239-1250
20. Gramsbergen J.B., Leegsma-Vogt G., Venema K., Noraberg J., and Korf J. Quantitative on-line monitoring of hippocampus glucose and lactate metabolism in organotypic cultures using biosensor technology. J. Neurochem. 85 (2003) 399-408
21. Gruetter R. Glycogen: the forgotten cerebral energy store. J. Neurosci. Res. 74 (2003) 179-183
22. Hassen G.W., Tian D., Ding D., and Bergold P.J. A new model of ischemic preconditioning using young adult hippocampal slice cultures. Brain Res. Brain Res. Protoc. 13 (2004) 135-143
23. Hertz L., and Dienel G.A. Energy metabolism in the brain. Int. Rev. Neurobiol. 51 (2002) 1-102
24. Hertz L. Intercellular metabolic compartmentation in the brain: past, present and future. Neurochem. Int. 45 (2004) 285-296
25. Inao S., Marmarou A., Clarke G.D., Andersen B.J., Fatouros P.P., and Young H.F. Production and clearance of lactate from brain tissue, cerebrospinal fluid, and serum following experimental brain injury. J. Neurosurg. 69 (1988) 736-744
26. Itoh Y., Esaki T., Shimoji K., Cook M., Law M.J., Kaufman E., and Sokoloff L. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4879-4884
27. Izumi Y., Benz A.M., Katsuki H., and Zorumski C.F. Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J. Neurosci. 17 (1997) 9448-9457
28. Kanatani T., Mizuno K., and Okada Y. Effects of glycolytic metabolites on preservation of high energy phosphate level and synaptic transmission in the granule cells of guinea pig hippocampal slices. Experientia 51 (1995) 213-216
29. Kaplan J.H. Biochemistry of Na,K-ATPase. Annu. Rev. Biochem. 71 (2002) 511-535
30. Kasischke K.A., Vishwasrao H.D., Fisher P.J., Zipfel W.R., and Webb W.W. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305 (2004) 99-103
31. Klaus S., Heringlake M., Gliemroth J., Pagel H., Staubach K., and Bahlmann L. Biochemical tissue monitoring during hypoxia and reoxygenation. Resuscitation 56 (2003) 299-305
32. Koehler-Stec E.M., Simpson I.A., Vannucci S.J., Landschulz K.T., and Landschulz W.H. Monocarboxylate transporter expression in mouse brain. Am. J. Physiol. 275 (1998) E516-E524
33. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 79 (1999) 1431-1568
34. Lowry J.P., and Fillenz M. Evidence for uncoupling of oxygen and glucose utilization during neuronal activation in rat striatum. J. Physiol. 498 Pt 2 (1997) 497-501
35. Ludvig N., and Tang H.M. Cellular electrophysiological changes in the hippocampus of freely behaving rats during local microdialysis with epileptogenic concentration of N-methyl-d-aspartate. Brain Res. Bull. 51 (2000) 233-240
36. Ludvig N., Potter P.E., and Fox S.E. Simultaneous single-cell recording and microdialysis within the same brain site in freely behaving rats: a novel neurobiological method. J. Neurosci. Methods 55 (1994) 31-40
37. Ludvig N., Chao K., Altura B.T., Altura B.M., and Fox S.E. Manipulation of pyramidal cell firing in the hippocampus of freely behaving rats by local application of K+ via microdialysis. Hippocampus 6 (1996) 97-108
38. Ludvig N., Kovacs L., Kando L., Medveczky G., Tang H.M., Eberle L.P., and Lemon C.R. The use of a remote-controlled minivalve, carried by freely moving animals on their head, to achieve instant pharmacological effects in intracerebral drug-perfusion studies. Brain Res. Brain Res. Protoc. 9 (2002) 23-31
39. Magistretti P.J., Pellerin L., Rothman D.L., and Shulman R.G. Energy on demand. Science 283 (1999) 496-497
40. McEwen B.S., and Reagan L.P. Glucose transporter expression in the central nervous system: relationship to synaptic function. Eur. J. Pharmacol. 490 (2004) 13-24
41. McKenna M.C., Tildon J.T., Stevenson J.H., Boatright R., and Huang S. Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: differences revealed using aminooxyacetate. Dev. Neurosci. 15 (1993) 320-329
42. McKenna M.C., Tildon J.T., Stevenson J.H., and Hopkins I.B. Energy metabolism in cortical synaptic terminals from weanling and mature rat brain: evidence for multiple compartments of tricarboxylic acid cycle activity. Dev. Neurosci. 16 (1994) 291-300
43. McKenna M.C., Tildon J.T., Stevenson J.H., Hopkins I.B., Huang X., and Couto R. Lactate transport by cortical synaptosomes from adult rat brain: characterization of kinetics and inhibitor specificity. Dev. Neurosci. 20 (1998) 300-309
44. McKenna M.C., Hopkins I.B., and Carey A. Alpha-cyano-4-hydroxycinnamate decreases both glucose and lactate metabolism in neurons and astrocytes: implications for lactate as an energy substrate for neurons. J. Neurosci. Res. 66 (2001) 747-754
45. Mintun M.A., Vlassenko A.G., Rundle M.M., and Raichle M.E. Increased lactate/pyruvate ratio augments blood flow in physiologically activated human brain. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 659-664
46. Pearson T., Damian K., Lynas R.E., and Frenguelli B.G. Sustained elevation of extracellular adenosine and activation of A1 receptors underlie the post-ischaemic inhibition of neuronal function in rat hippocampus in vitro. J. Neurochem. 97 (2006) 1357-1368
47. Pellerin L., and Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10625-10629
48. Pellerin L., and Magistretti P.J. Food for thought: challenging the dogmas. J. Cereb. Blood Flow Metab. 23 (2003) 1282-1286
49. Pierre K., and Pellerin L. Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J. Neurochem. 94 (2005) 1-14
50. Raichle M.E. Functional brain imaging and human brain function. J. Neurosci. 23 (2003) 3959-3962
51. Saitoh M., Okada Y., and Nabetani M. Effect of mannose, fructose and lactate on the preservation of synaptic potentials in hippocampal slices. Neurosci. Lett. 171 (1994) 125-128
52. Schurr A. Glucose and the ischemic brain: a sour grape or a sweet treat?. Curr. Opin. Clin. Nutr. Metab. Care 4 (2001) 287-292
53. Schurr A. Lactate, glucose and energy metabolism in the ischemic brain. Int. J. Mol. Med. 10 (2002) 131-136
54. Schurr A., West C.A., and Rigor B.M. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240 (1988) 1326-1328
55. Schurr A., Payne R.S., Miller J.J., and Rigor B.M. Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J. Neurochem. 69 (1997) 423-426
56. Schurr A., Payne R.S., Miller J.J., and Rigor B.M. Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res. 774 (1997) 221-224
57. 14C) 2-deoxyglucose. J. Comp. Neurol. 177 (1978) 335-359
58. Shulman R.G., Rothman D.L., Behar K.L., and Hyder F. Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci. 27 (2004) 489-495
59. Sokoloff L. Energetics of functional activation in neural tissues. Neurochem. Res. 24 (1999) 321-329
60. Tabernero A., Vicario C., and Medina J.M. Lactate spares glucose as a metabolic fuel in neurons and astrocytes from primary culture. Neurosci. Res. 26 (1996) 369-376
61. Takata T., Sakurai T., Yang B., Yokono K., and Okada Y. Effect of lactate on the synaptic potential, energy metabolism, calcium homeostasis and extracellular glutamate concentration in the dentate gyrus of the hippocampus from guinea-pig. Neuroscience 104 (2001) 371-378
62. Tsacopoulos M., and Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16 (1996) 877-885
63. Tseng M.T., Chan S.A., and Schurr A. Ischemia-induced changes in monocarboxylate transporter 1 reactive cells in rat hippocampus. Neurol. Res. 25 (2003) 83-86
64. Waagepetersen H.S., Bakken I.J., Larsson O.M., Sonnewald U., and Schousboe A. Comparison of lactate and glucose metabolism in cultured neocortical neurons and astrocytes using 13C-NMR spectroscopy. Dev. Neurosci. 20 (1998) 310-320
65. Wada H., Okada Y., Nabetani M., and Nakamura H. The effects of lactate and beta-hydroxybutyrate on the energy metabolism and neural activity of hippocampal slices from adult and immature rat. Brain Res. Dev. Brain Res. 101 (1997) 1-7
66. Wada H., Okada Y., Uzuo T., and Nakamura H. The effects of glucose, mannose, fructose and lactate on the preservation of neural activity in the hippocampal slices from the guinea pig. Brain Res. 788 (1998) 144-150
67. Xiang Z.-M., and Bergold P.J. Synaptic depression and neuronal loss in transiently acidic hippocampal slice cultures. Brain Res. 881 (2000) 77-87
68. Xiang Z.-M., Hrabetova S., Moskowitz S.I., Casaccia-Bonnefil P., Young S.R., Nimmrich V.C., Tiedge H., Einheber S., Karnup S., Bianchi R., and Bergold P.J. Long-term maintenance of mature hippocampal slices in vitro. J. Neurosci. Methods 98 (2000) 145-154
69. Xiang Z.-M., Yuan M., Hassan G.W., Gampel M., and Bergold P.J. Lactate-induced excitotoxicity in hippocampal slice cultures. Exp. Neurol. 186 (2004) 70-77