Learning-Induced gene expression in the hippocampus reveals a role of neuron -Astrocyte metabolic coupling in long term memory

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Tadi, Monika ^a   Allaman, Igor ^a   Lengacher, Sylvain ^a   Grenningloh, Gabriele ^a   Magistretti, Pierre J ^a,b  

^a EPFL   (Switzerland)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GLUCOSE TRANSPORTER 1; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; MONOCARBOXYLATE TRANSPORTER;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN MAPPING; CONTROLLED STUDY; ENERGY METABOLISM; GENE; GENE EXPRESSION; GLUT1 GENE; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; MCT1 GENE; MCT4 GENE; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NA K ATPASE ALPHA2 GENE; NEUROMODULATION; NEURON ASTROCYTE METABOLIC COUPLING; NONHUMAN; PASSIVE AVOIDANCE TEST; ANIMAL; ASTROCYTE; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; ASTROCYTES; AVOIDANCE LEARNING; GLUCOSE TRANSPORTER TYPE 1; HIPPOCAMPUS; MALE; MEMORY, LONG-TERM; MICE; MICE, INBRED C57BL; MONOCARBOXYLIC ACID TRANSPORTERS; NEURONS; RNA, MESSENGER; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84949974544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141568     Document Type: Article

References (82)

1. McGaugh JL. Memory-a century of consolidation. Science. 2000; 287: 248-51. PMID: 10634773
2. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science. 2001; 294: 1030-8. PMID: 11691980
3. Kandel ER, Dudai Y, Mayford MR. The molecular and systems biology of memory. Cell. 2014; 157: 163-86. doi: 10.1016/j.cell.2014.03.001 PMID: 24679534
4. Klann E, Sweatt JD. Altered protein synthesis is a trigger for long-term memory formation. Neurobiol Learn Mem. 2008; 89: 247-59. PMID: 17919940
5. Pellerin L, Magistretti PJ. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A. 1994; 91: 10625-9. PMID: 7938003
6. Magistretti PJ, Allaman I. A cellular perspective on brain energy metabolism and functional imaging. Neuron. 2015; 86: 883-901. doi: 10.1016/j.neuron.2015.03.035 PMID: 25996133
7. Pellerin L, Magistretti PJ. Sweet sixteen for ANLS. J Cereb Blood Flow Metab. 2012; 32: 1152-66. doi: 10.1038/jcbfm.2011.149 PMID: 22027938
8. Allaman I, Magistretti PJ. Brain Energy Metabolism. In: Squire LR, Berg D, Bloom FE, du Lac S, Ghosh A, Spitzer NC, editors. Fundamental Neuroscience. San Diego: Academic Press; 2013. pp. 261-84.
9. Magistretti PJ, Chatton JY. Relationship between L-glutamate-regulated intracellular Na+ dynamics and ATP hydrolysis in astrocytes. J Neural Transm. 2005; 112: 77-85. PMID: 15599606
10. Brown AM, Baltan Tekkok S, Ransom BR. Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem Int. 2004; 45: 529-36. PMID: 15186919
11. Allaman I. Glial Glycogen Metabolism. In: Squire LR, editor. Encyclopedia of Neuroscience. Oxford: Academic Press; 2009. pp. 811-8.
12. Vilchez D, Ros S, Cifuentes D, Pujadas L, Valles J, Garcia-Fojeda B, et al. Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci. 2007; 10: 1407-13. PMID: 17952067
13. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell. 2011; 144: 810-23. doi: 10.1016/j.cell. 2011.02.018 PMID: 21376239
14. Newman LA, Korol DL, Gold PE. Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS One. 2011; 6: e28427. doi: 10.1371/journal.pone.0028427 PMID: 22180782
15. Pierre K, Pellerin L. Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J Neurochem. 2005; 94: 1-14.
16. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature. 2012; 487: 443-8. doi: 10.1038/ nature11314 PMID: 22801498
17. Lengacher S, Nehiri-Sitayeb T, Steiner N, Carneiro L, Favrod C, Preitner F, et al. Resistance to dietinduced obesity and associated metabolic perturbations in haploinsufficient monocarboxylate transporter 1 mice. PLoS One. 2013; 8: e82505. doi: 10.1371/journal.pone.0082505 PMID: 24367518
18. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, et al. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem. 1977; 28: 897-916. PMID: 864466
19. Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR. Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains. Amsterdam: Elsevier; 2000.
20. Izquierdo I, Medina JH. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem. 1997; 68: 285-316. PMID: 9398590
21. Abel T, Lattal KM. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol. 2001; 11: 180-7. PMID: 11301237
22. Taubenfeld SM, Wiig KA, Bear MF, Alberini CM. A molecular correlate of memory and amnesia in the hippocampus. Nat Neurosci. 1999; 2: 309-10. PMID: 10204535
23. Jones D, Gonzalez-Lima F. Mapping Pavlovian conditioning effects on the brain: blocking, contiguity, and excitatory effects. J Neurophysiol. 2001; 86: 809-23. PMID: 11495952
24. Cybulska-Klosowicz A, Zakrzewska R, Kossut M. Brain activation patterns during classical conditioning with appetitive or aversive UCS. Behav Brain Res. 2009; 204: 102-11. doi: 10.1016/j.bbr.2009.05.024 PMID: 19477203
25. Toledo-Rodriguez M, Pitiot A, Paus T, Sandi C. Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex. Neurobiol Learn Mem. 2012; 98: 93-101. doi: 10.1016/j.nlm.2012.05.006 PMID: 22664720
26. Sybirska E, Davachi L, Goldman-Rakic PS. Prominence of direct entorhinal-CA1 pathway activation in sensorimotor and cognitive tasks revealed by 2-DG functional mapping in nonhuman primate. J Neurosci. 2000; 20: 5827-34. PMID: 10908624
27. Davachi L, Goldman-Rakic PS. Primate rhinal cortex participates in both visual recognition and working memory tasks: functional mapping with 2-DG. J Neurophysiol. 2001; 85: 2590-601. PMID: 11387403
28. Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M. Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain. 2005; 1: 6. PMID: 15813993
29. Izquierdo I, Quillfeldt JA, Zanatta MS, Quevedo J, Schaeffer E, Schmitz PK, et al. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci. 1997; 9: 786-93. PMID: 9153585
30. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000; 406: 722-6. PMID: 10963596
31. D'Agata V, Cavallaro S. Hippocampal gene expression profiles in passive avoidance conditioning. Eur J Neurosci. 2003; 18: 2835-41. PMID: 14656332
32. Zhang XH, Wu LJ, Gong B, Ren M, Li BM, Zhuo M. Induction- and conditioning-protocol dependent involvement of NR2B-containing NMDA receptors in synaptic potentiation and contextual fear memory in the hippocampal CA1 region of rats. Mol Brain. 2008; 1: 9. doi: 10.1186/1756-6606-1-9 PMID: 18826591
33. Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science. 1992; 256: 675-7. PMID: 1585183
34. Barkus C, McHugh SB, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM. Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur J Pharmacol. 2010; 626: 49-56. doi: 10.1016/j.ejphar.2009.10.014 PMID: 19836379
35. Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010; 65: 7-19. doi: 10.1016/j.neuron.2009.11.031 PMID: 20152109
36. Alberini CM. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev. 2009; 89: 121-45. doi: 10.1152/physrev.00017.2008 PMID: 19126756
37. Squire LR, Genzel L, Wixted JT, Morris RG. Memory Consolidation. Cold Spring Harb Perspect Biol. 2015; 7: a021766. doi: 10.1101/cshperspect.a021766 PMID: 26238360
38. Igaz LM, Bekinschtein P, Izquierdo I, Medina JH. One-trial aversive learning induces late changes in hippocampal CaMKIIalpha, Homer 1a, Syntaxin 1a and ERK2 protein levels. Brain Res Mol Brain Res. 2004; 132: 1-12. PMID: 15548423
39. Taubenfeld SM, Wiig KA, Monti B, Dolan B, Pollonini G, Alberini CM. Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [beta] and [delta] Co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J Neurosci. 2001; 21: 84-91. PMID: 11150323
40. Zhang Y, Fukushima H, Kida S. Induction and requirement of gene expression in the anterior cingulate cortex and medial prefrontal cortex for the consolidation of inhibitory avoidance memory. Mol Brain. 2011; 4: 4. doi: 10.1186/1756-6606-4-4 PMID: 21244716
41. Alberini CM. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev. 2009; 89: 121-45. doi: 10.1152/physrev.00017.2008 PMID: 19126756
42. Riedel G, Micheau J, Lam AG, Roloff EL, Martin SJ, Bridge H, et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci. 1999; 2: 898-905. PMID: 10491611
43. Holt W, Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci. 1999; 19: 9054-62. PMID: 10516322
44. Sandusky LA, Flint RW, McNay EC. Elevated glucose metabolism in the amygdala during an inhibitory avoidance task. Behav Brain Res. 2013; 245C: 83-7.
45. Kim JJ, Rison RA, Fanselow MS. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci. 1993; 107: 1093-8. PMID: 8136063
46. Holloway CM, McIntyre CK. Post-training disruption of Arc protein expression in the anterior cingulate cortex impairs long-term memory for inhibitory avoidance training. Neurobiol Learn Mem. 2011; 95: 425-32. doi: 10.1016/j.nlm.2011.02.002 PMID: 21315825
47. Chuquet J, Quilichini P, Nimchinsky EA, Buzsaki G. Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J Neurosci. 2010; 30: 15298-303. doi: 10.1523/JNEUROSCI.0762-10.2010 PMID: 21068334
48. Nehlig A. Brain uptake and metabolism of ketone bodies in animal models. Prostaglandins Leukot Essent Fatty Acids. 2004; 70: 265-75. PMID: 14769485
49. Jakoby P, Schmidt E, Ruminot I, Gutierrez R, Barros LF, Deitmer JW. Higher Transport and Metabolism of Glucose in Astrocytes Compared with Neurons: A Multiphoton Study of Hippocampal and Cerebellar Tissue Slices. Cereb Cortex. 2014; 24: 222-31. doi: 10.1093/cercor/bhs309 PMID: 23042735
50. Lundgaard I, Li B, Xie L, Kang H, Sanggaard S, Haswell JD, et al. Direct neuronal glucose uptake Heralds activity-dependent increases in cerebral metabolism. Nat Commun. 2015; 6: 6807. doi: 10.1038/ ncomms7807 PMID: 25904018
51. Kovar JL, Volcheck W, Sevick-Muraca E, Simpson MA, Olive DM. Characterization and performance of a near-infrared 2-deoxyglucose optical imaging agent for mouse cancer models. Anal Biochem. 2009; 384: 254-62. doi: 10.1016/j.ab.2008.09.050 PMID: 18938129
52. Cholet N, Pellerin L, Welker E, Lacombe P, Seylaz J, Magistretti P, et al. Local injection of antisense oligonucleotides targeted to the glial glutamate transporter GLAST decreases the metabolic response to somatosensory activation. J Cereb Blood Flow Metab. 2001; 21: 404-12. PMID: 11323526
53. Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton JY, et al. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron. 2003; 37: 275-86. PMID: 12546822
54. Schmidt S, Richter M, Montag D, Sartorius T, Gawlik V, Hennige AM, et al. Neuronal functions, feeding behavior, and energy balance in Slc2a3+/- mice. Am J Physiol Endocrinol Metab. 2008; 295: E1084-E1094. doi: 10.1152/ajpendo.90491.2008 PMID: 18780771
55. Stuart CA, Ross IR, Howell ME, McCurry MP, Wood TG, Ceci JD, et al. Brain glucose transporter (Glut3) haploinsufficiency does not impair mouse brain glucose uptake. Brain Res. 2011; 1384: 15-22. doi: 10.1016/j.brainres.2011.02.014 PMID: 21316350
56. Wang D, Pascual JM, Yang H, Engelstad K, Mao X, Cheng J, et al. A mouse model for Glut-1 haploinsufficiency. Hum Mol Genet. 2006; 15: 1169-79. PMID: 16497725
57. Vianna MR, Alonso M, Viola H, Quevedo J, de Paris F, Furman M, et al. Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem. 2000; 7: 333-40. PMID: 11040265
58. Dienel GA. Brain lactate metabolism: the discoveries and the controversies. J Cereb Blood Flow Metab. 2012; 32: 1107-38. doi: 10.1038/jcbfm.2011.175 PMID: 22186669
59. DiNuzzo M, Mangia S, Maraviglia B, Giove F. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling. J Cereb Blood Flow Metab. 2010; 30: 586-602. doi: 10.1038/jcbfm.2009.232 PMID: 19888285
60. Mangia S, Giove F, Tkac I, Logothetis NK, Henry PG, Olman CA, et al. Metabolic and hemodynamic events after changes in neuronal activity: current hypotheses, theoretical predictions and in vivo NMR experimental findings. J Cereb Blood Flow Metab. 2009; 29: 441-63. doi: 10.1038/jcbfm.2008.134 PMID: 19002199
61. Patel AB, Lai JC, Chowdhury GM, Hyder F, Rothman DL, Shulman RG, et al. Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle. Proc Natl Acad Sci U S A. 2014; 111: 5385-90. doi: 10.1073/pnas.1403576111 PMID: 24706914
62. Chenal J, Pierre K, Pellerin L. Insulin and IGF-1 enhance the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of the phosphoinositide 3-kinase-Aktmammalian target of rapamycin pathway. Eur J Neurosci. 2008; 27: 53-65. PMID: 18093179
63. Chenal J, Pellerin L. Noradrenaline enhances the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of PI3K/Akt and the mTOR/S6K pathway. J Neurochem. 2007; 102: 389-97. PMID: 17394554
64. Pierre K, Chatton JY, Parent A, Repond C, Gardoni F, Di Luca M., et al. Linking supply to demand: the neuronal monocarboxylate transporter MCT2 and the alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionic acid receptor GluR2/3 subunit are associated in a common trafficking process. Eur J Neurosci. 2009; 29: 1951-63. doi: 10.1111/j.1460-9568.2009.06756.x PMID: 19453627
65. Herrero-Mendez A, Almeida A, Fernandez E, Maestre C, Moncada S, Bolanos JP. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol. 2009; 11: 747-52. doi: 10.1038/ncb1881 PMID: 19448625
66. Rodriguez-Rodriguez P, Fernandez E, Bolanos JP. Underestimation of the pentose-phosphate pathway in intact primary neurons as revealed by metabolic flux analysis. J Cereb Blood Flow Metab. 2013; 33: 1843-5. doi: 10.1038/jcbfm.2013.168 PMID: 24064491
67. Moseley AE, Williams MT, Schaefer TL, Bohanan CS, Neumann JC, Behbehani MM, et al. Deficiency in Na,K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci. 2007; 27: 616-26. PMID: 17234593
68. Lingrel JB, Williams MT, Vorhees CV, Moseley AE. Na,K-ATPase and the role of alpha isoforms in behavior. J Bioenerg Biomembr. 2007; 39: 385-9. PMID: 18044013
69. Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE. Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci U S A. 1981; 78: 6535-9. PMID: 6118864
70. Allaman I, Pellerin L, Magistretti PJ. Protein targeting to glycogen mRNA expression is stimulated by noradrenaline in mouse cortical astrocytes. Glia. 2000; 30: 382-91. PMID: 10797618
71. Greenberg CC, Meredith KN, Yan L, Brady MJ. Protein targeting to glycogen overexpression results in the specific enhancement of glycogen storage in 3T3-L1 adipocytes. J Biol Chem. 2003; 278: 30835-42. PMID: 12805359
72. Duran J, Saez I, Gruart A, Guinovart JJ, Delgado-Garcia JM. Impairment in long-term memory formation and learning-dependent synaptic plasticity in mice lacking glycogen synthase in the brain. J Cereb Blood Flow Metab. 2013; 33: 550-6. doi: 10.1038/jcbfm.2012.200 PMID: 23281428
73. Gibbs ME, Lloyd HG, Santa T, Hertz L. Glycogen is a preferred glutamate precursor during learning in 1-day-old chick: biochemical and behavioral evidence. J Neurosci Res. 2007; 85: 3326-33. PMID: 17455305
74. Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A, et al. BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A. 2008; 105: 2711-6. doi: 10.1073/pnas.0711863105 PMID: 18263738
75. Katche C, Bekinschtein P, Slipczuk L, Goldin A, Izquierdo IA, Cammarota M, et al. Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc Natl Acad Sci U S A. 2010; 107: 349-54. doi: 10.1073/pnas.0912931107 PMID: 20018662
76. Miniaci MC, Kim JH, Puthanveettil SV, Si K, Zhu H, Kandel ER, et al. Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron. 2008; 59: 1024-36. doi: 10.1016/j.neuron.2008.07.036 PMID: 18817739
77. Dudai Y, Eisenberg M. Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron. 2004; 44: 93-100. PMID: 15450162
78. Miyashita T, Kubik S, Lewandowski G, Guzowski JF. Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem. 2008; 89: 269-84. PMID: 17931913
79. Yang J, Ruchti E, Petit JM, Jourdain P, Grenningloh G, Allaman I, et al. Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc Natl Acad Sci U S A. 2014; 111: 12228-33. doi: 10.1073/pnas.1322912111 PMID: 25071212
80. Stranahan AM, Mattson MP. Metabolic reserve as a determinant of cognitive aging. J Alzheimers Dis. 2012; 30 Suppl 2: S5-13. doi: 10.3233/JAD-2011-110899 PMID: 22045480
81. Kapogiannis D, Mattson MP. Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neurol. 2011; 10: 187-98. doi: 10.1016/S1474-4422(10) 70277-5 PMID: 21147038
82. Simpson JE, Ince PG, Lace G, Forster G, Shaw PJ, Matthews F, et al. Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain. Neurobiol Aging. 2010; 31: 578-90. doi: 10.1016/j. neurobiolaging.2008.05.015 PMID: 18586353