Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 33, 2014, Pages 12228-12233

  Yang, Jiangyan ^a   Ruchti, Evelyne ^a,b,c   Petit, Jean Marie ^a,c   Jourdain, Pascal ^a,c   Grenningloh, Gabriele ^a   Allaman, Igor ^a   Magistretti, Pierre J ^a,b,c  

^a EPFL   (Switzerland)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Astrocyte neuron interaction; Astrocyte neuron lactate shuttle; Brain energy metabolism; Learning and memory

Indexed keywords

ARC PROTEIN; CALCIUM; CELL PROTEIN; LACTIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN C FOS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ZIF2687 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CELL LEVEL; CONTROLLED STUDY; GENE EXPRESSION; IN VIVO STUDY; INTRACELLULAR SIGNALING; LONG TERM MEMORY; LONG TERM POTENTIATION; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SENSORIMOTOR CORTEX;

ASTROCYTE-NEURON INTERACTION; ASTROCYTE-NEURON LACTATE SHUTTLE; BRAIN ENERGY METABOLISM; LEARNING AND MEMORY;

ANIMALS; CALCIUM; CELLS, CULTURED; GENE EXPRESSION; LACTIC ACID; MICE; N-METHYLASPARTATE; NEURONAL PLASTICITY; NEURONS; SIGNAL TRANSDUCTION;

EID: 84906308932     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322912111     Document Type: Article

References (35)

1. Suzuki A, et al. (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144(5):810-823.
2. Gibbs ME, Anderson DG, Hertz L (2006) Inhibition of glycogenolysis in astrocytes interrupts memory consolidation in young chickens. Glia 54(3):214-222. (Pubitemid 44230858)
3. Newman LA, Korol DL, Gold PE (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS ONE 6(12):e28427.
4. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89(1):121-145.
5. Bramham CR, et al. (2010) The Arc of synaptic memory. Exp Brain Res 200(2):125-140.
6. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84(1):87-136. (Pubitemid 38049877)
7. Caroni P, Donato F, Muller D (2012) Structural plasticity upon learning: Regulation and functions. Nat Rev Neurosci 13(7):478-490.
8. Zhou X, et al. (2009) N-methyl-D-aspartate-stimulated ERK1/2 signaling and the transcriptional up-regulation of plasticity-related genes are developmentally regulated following in vitro neuronal maturation. J Neurosci Res 87(12):2632-2644.
9. Cammarota M, et al. (2000) Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade. Brain Res Mol Brain Res 76(1):36-46. (Pubitemid 30133231)
10. Giovannini MG (2006) The role of the extracellular signal-regulated kinase pathway in memory encoding. Rev Neurosci 17(6):619-634.
11. Sweatt JD (2001) The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76(1):1-10.
12. Mullasseril P, et al. (2010) A subunit-selective potentiator of NR2C- and NR2D-containing NMDA receptors. Nat Commun 1:90.
13. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004(255):re16.
14. Hashimoto T, Hussien R, Oommen S, Gohil K, Brooks GA (2007) Lactate sensitive transcription factor network in L6 cells: Activation of MCT1 and mitochondrial biogenesis. FASEB J 21(10):2602-2612. (Pubitemid 47230688)
15. Milovanova TN, et al. (2008) Lactate stimulates vasculogenic stem cells via the thioredoxin system and engages an autocrine activation loop involving hypoxia-inducible factor 1. Mol Cell Biol 28(20):6248-6261.
16. Zieker D, et al. (2008) Lactate modulates gene expression in human mesenchymal stem cells. Langenbecks Arch Surg 393(3):297-301.
17. Formby B, Stern R (2003) Lactate-sensitive response elements in genes involved in hyaluronan catabolism. Biochem Biophys Res Commun 305(1):203-208. (Pubitemid 36535428)
18. Zilberter Y, Zilberter T, Bregestovski P (2010) Neuronal activity in vitro and the in vivo reality: The role of energy homeostasis. Trends Pharmacol Sci 31(9):394-401.
19. Lau CG, Zukin RS (2007) NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8(6):413-426. (Pubitemid 46789232)
20. Bergersen LH, Gjedde A (2012) Is lactate a volume transmitter of metabolic states of the brain? Front Neuroenergetics 4:5.
21. Sullivan JM, et al. (1994) Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13(4):929-936. (Pubitemid 24347305)
22. Köhr G, Eckardt S, Lüddens H, Monyer H, Seeburg PH (1994) NMDA receptor channels: Subunit-specific potentiation by reducing agents. Neuron 12(5):1031-1040. (Pubitemid 24178195)
23. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci 6(8):626-640. (Pubitemid 41059337)
24. Allaman I, Bélanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: For better and for worse. Trends Neurosci 34(2):76-87.
25. Bélanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: Focus on astrocyte-neuron metabolic cooperation. Cell Metab 14(6):724-738.
26. Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62(6):649-671.
27. Magistretti PJ (2006) Neuron-glia metabolic coupling and plasticity. J Exp Biol 209(Pt 12):2304-2311.
28. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91(22):10625-10629. (Pubitemid 24329051)
29. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32(7):1152-1166.
30. Tsacopoulos M, Magistretti PJ (1996) Metabolic coupling between glia and neurons. J Neurosci 16(3):877-885. (Pubitemid 26140843)
31. Choi HB, et al. (2012) Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 75(6):1094-1104.
32. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: Possible function as lactate supply for neighboring cells. Brain Res 623(2):208-214. (Pubitemid 23275402)
33. Magistretti PJ, Morrison JH (1988) Noradrenaline- and vasoactive intestinal peptide-containing neuronal systems in neocortex: Functional convergence with contrasting morphology. Neuroscience 24(2):367-378. (Pubitemid 18062260)
34. Bozzo L, Puyal J, Chatton JY (2013) Lactate modulates the activity of primary cortical neurons through a receptor-mediated pathway. PLoS ONE 8(8):e71721.
35. Tang F, et al. (2014) Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5:3284.