Lactate Modulates the Activity of Primary Cortical Neurons through a Receptor-Mediated Pathway

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Bozzo, Luigi ^a   Puyal, Julien ^a   Chatton, Jean Yves ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA RESORCYLIC ACID; CALCIUM; G PROTEIN COUPLED RECEPTOR; GLUCOSE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LACTIC ACID; PERTUSSIS TOXIN; PYRUVIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL PH; CONTROLLED STUDY; EMBRYO; ENERGY METABOLISM; IC 50; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CEREBRAL CORTEX; ENERGY METABOLISM; GLUCOSE; HYDROGEN-ION CONCENTRATION; INTRACELLULAR SPACE; LACTATES; MICE; NEURONS; NEUROTRANSMITTER AGENTS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STEREOISOMERISM;

EID: 84881482883     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071721     Document Type: Article

References (46)

1. Abi-Saab WM, Maggs DG, Jones T, Jacob R, Srihari V, et al. (2002) Striking differences in glucose and lactate levels between brain extracellular fluid and plasma in conscious human subjects: effects of hyperglycemia and hypoglycemia. J Cereb Blood Flow Metab 22: 271-279.
2. Dienel GA, Ball KK, Cruz NF, (2007) A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover. J Neurochem 102: 466-478.
3. Gallagher CN, Carpenter KL, Grice P, Howe DJ, Mason A, et al. (2009) The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132: 2839-2849.
4. Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B, (2011) In vivo evidence for lactate as a neuronal energy source. J Neurosci 31: 7477-7485.
5. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C, (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322: 1551-1555.
6. Song Z, Routh VH, (2005) Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 54: 15-22.
7. Shimizu H, Watanabe E, Hiyama TY, Nagakura A, Fujikawa A, et al. (2007) Glial Nax channels control lactate signaling to neurons for brain [Na+] sensing. Neuron 54: 59-72.
8. Evans ML, McCrimmon RJ, Flanagan DE, Keshavarz T, Fan X, et al. (2004) Hypothalamic ATP-sensitive K+channels play a key role in sensing hypoglycemia and triggering counterregulatory epinephrine and glucagon responses. Diabetes 53: 2542-2551.
9. Song Z, Levin BE, McArdle JJ, Bakhos N, Routh VH, (2001) Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50: 2673-2681.
10. Murphy BA, Fakira KA, Song Z, Beuve A, Routh VH, (2009) AMP-activated protein kinase and nitric oxide regulate the glucose sensitivity of ventromedial hypothalamic glucose-inhibited neurons. Am J Physiol Cell Physiol 297: C750-758.
11. Parsons MP, Hirasawa M, (2010) ATP-sensitive potassium channel-mediated lactate effect on orexin neurons: implications for brain energetics during arousal. J Neurosci 30: 8061-8070.
12. Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA, (2002) Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544: 429-445.
13. Venner A, Karnani MM, Gonzalez JA, Jensen LT, Fugger L, et al. (2011) Orexin neurons as conditional glucosensors: paradoxical regulation of sugar sensing by intracellular fuels. J Physiol 589: 5701-5708.
14. Gonzalez JA, Jensen LT, Fugger L, Burdakov D, (2008) Metabolism-independent sugar sensing in central orexin neurons. Diabetes 57: 2569-2576.
15. Bergersen LH, Gjedde A, (2012) Is lactate a volume transmitter of metabolic states of the brain? Front Neuroenergetics 4: 5.
16. Blad CC, Ahmed K, AP IJ, Offermanns S, (2011) Biological and pharmacological roles of HCA receptors. Adv Pharmacol 62: 219-250.
17. Cai TQ, Ren N, Jin L, Cheng K, Kash S, et al. (2008) Role of GPR81 in lactate-mediated reduction of adipose lipolysis. Biochem Biophys Res Commun 377: 987-991.
18. Liu C, Wu J, Zhu J, Kuei C, Yu J, et al. (2009) Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81. J Biol Chem 284: 2811-2822.
19. Lauritzen KH, Morland C, Puchades M, Holm-Hansen S, Hagelin EM, et al. (2013) Lactate Receptor Sites Link Neurotransmission, Neurovascular Coupling, and Brain Energy Metabolism. Cereb Cortex (in press).
20. Barros LF (2013) Metabolic signaling by lactate in the brain. Trends Neurosci.
21. Chatton JY, Idle JR, Vagbo 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.
22. Grishchuk Y, Ginet V, Truttmann AC, Clarke PG, Puyal J, (2011) Beclin 1-independent autophagy contributes to apoptosis in cortical neurons. Autophagy 7: 1115-1131.
23. Cossart R, Ikegaya Y, Yuste R, (2005) Calcium imaging of cortical networks dynamics. Cell Calcium 37: 451-457.
24. Sasaki T, Takahashi N, Matsuki N, Ikegaya Y, (2008) Fast and accurate detection of action potentials from somatic calcium fluctuations. J Neurophysiol 100: 1668-1676.
25. Ewaschuk JB, Naylor JM, Zello GA, (2005) D-lactate in human and ruminant metabolism. J Nutr 135: 1619-1625.
26. Nedergaard M, Goldman SA, (1993) Carrier-mediated transport of lactic acid in cultured neurons and astrocytes. Am J Physiol 265: R282-289.
27. Kuei C, Yu J, Zhu J, Wu J, Zhang L, et al. (2011) Study of GPR81, the lactate receptor, from distant species identifies residues and motifs critical for GPR81 functions. Mol Pharmacol 80: 848-858.
28. Liu C, Kuei C, Zhu J, Yu J, Zhang L, et al. (2012) 3,5-Dihydroxybenzoic acid, a specific agonist for hydroxycarboxylic acid 1, inhibits lipolysis in adipocytes. J Pharmacol Exp Ther 341: 794-801.
29. Broer S, Broer A, Schneider HP, Stegen C, Halestrap AP, et al. (1999) Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341 (Pt 3): 529-535.
30. Lin RY, Vera JC, Chaganti RS, Golde DW, (1998) Human monocarboxylate transporter 2 (MCT2) is a high affinity pyruvate transporter. J Biol Chem 273: 28959-28965.
31. Gonzalez JA, Reimann F, Burdakov D, (2009) Dissociation between sensing and metabolism of glucose in sugar sensing neurones. J Physiol 587: 41-48.
32. Flick MJ, Konieczny SF, (2002) Identification of putative mammalian D-lactate dehydrogenase enzymes. Biochem Biophys Res Commun 295: 910-916.
33. Poole RC, Halestrap AP, (1993) Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol 264: C761-782.
34. Seino S, Shibasaki T, (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85: 1303-1342.
35. Bettler B, Kaupmann K, Mosbacher J, Gassmann M, (2004) Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 84: 835-867.
36. 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.
37. Dienel GA, (2012) Brain lactate metabolism: the discoveries and the controversies. J Cereb Blood Flow Metab 32: 1107-1138.
38. Dalsgaard MK, Quistorff B, Danielsen ER, Selmer C, Vogelsang T, et al. (2004) A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J Physiol 554: 571-578.
39. Ros J, Pecinska N, Alessandri B, Landolt H, Fillenz M, (2001) Lactate reduces glutamate-induced neurotoxicity in rat cortex. J Neurosci Res 66: 790-794.
40. Berthet C, Castillo X, Magistretti PJ, Hirt L, (2012) New evidence of neuroprotection by lactate after transient focal cerebral ischaemia: extended benefit after intracerebroventricular injection and efficacy of intravenous administration. Cerebrovasc Dis 34: 329-335.
41. Berthet C, Lei H, Thevenet J, Gruetter R, Magistretti PJ, et al. (2009) Neuroprotective role of lactate after cerebral ischemia. J Cereb Blood Flow Metab 29: 1780-1789.
42. Schurr A, Payne RS, Miller JJ, Tseng MT, Rigor BM, (2001) Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia. Brain Res 895: 268-272.
43. Schurr A, Dong WQ, Reid KH, West CA, Rigor BM, (1988) Lactic acidosis and recovery of neuronal function following cerebral hypoxia in vitro. Brain Res 438: 311-314.
44. Schurr A, Payne RS, Miller JJ, Rigor BM, (1997) Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69: 423-426.
45. Alessandri B, Schwandt E, Kamada Y, Nagata M, Heimann A, et al. (2012) The neuroprotective effect of lactate is not due to improved glutamate uptake after controlled cortical impact in rats. J Neurotrauma 29: 2181-2191.
46. Maran A, Cranston I, Lomas J, Macdonald I, Amiel SA, (1994) Protection by lactate of cerebral function during hypoglycaemia. Lancet 343: 16-20.