Microglial activation enhances associative taste memory through purinergic modulation of glutamatergic neurotransmission

Journal of Neuroscience

Volumn 35, Issue 7, 2015, Pages 3022-3033

  Delpech, Jean Christophe ^a,b   Saucisse, Nicolas ^a,b   Parkes, Shauna L ^a,b,c   Lacabanne, Chloe ^a,b   Aubert, Agnes ^a,b   Casenave, Fabrice ^a,b   Coutureau, Etienne ^b,c   Sans, Nathalie ^b,d   Layé, Sophie ^a,b   Ferreira, Guillaume ^a,b   Nadjar, Agnes ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UMR 5287   (France)

^d INSERM   (France)

Author keywords

AMPA; ATP; Cytokines; Lipopolysaccharide; Neuroinflammation

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; CORTICOSTERONE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PURINERGIC RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; SACCHARIN; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; LITHIUM CHLORIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; PURINERGIC RECEPTOR AFFECTING AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; CONDITIONED TASTE AVERSION TEST; CONTROLLED STUDY; HISTOLOGY; INSULA; MALE; MEMORY; MEMORY CONSOLIDATION; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TASTE AVERSION; TASTE DISCRIMINATION; TASTE MEMORY; WESTERN BLOTTING; ANIMAL; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENCEPHALITIS; LEARNING; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPTIC TRANSMISSION; TASTE; WISTAR RAT;

ANIMALS; ASSOCIATION LEARNING; CORTICOSTERONE; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; GLUTAMIC ACID; LIPOPOLYSACCHARIDES; LITHIUM CHLORIDE; MALE; MEMORY; MICROGLIA; PROTEIN TRANSPORT; PURINERGIC AGENTS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; TASTE;

EID: 84927170691     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3028-14.2015     Document Type: Article

References (59)

1. Adaikkan C, Rosenblum K (2012) The role of protein phosphorylation in the gustatory cortex and amygdala during taste learning. Exp Neurobiol 21:37-51. CrossRef Medline
2. Aubert A, Dantzer R (2005) The taste of sickness: lipopolysaccharide induced finickiness in rats. Physiol Behav 84:437-444. CrossRef Medline
3. Barki-Harrington L, Elkobi A, Tzabary T, Rosenblum K (2009) Tyrosine phosphorylation of the 2B subunit of the NMDA receptor is necessary for taste memory formation. J Neurosci 29:9219-9226. CrossRef Medline
4. Barrientos RM, Higgins EA, Sprunger DB, Watkins LR, Rudy JW, Maier SF (2002) Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav Brain Res 134: 291-298. CrossRef Medline
5. Barrientos RM, Sprunger DB, Campeau S, Watkins LR, Rudy JW, Maier SF (2004) BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J Neuroimmunol 155:119-126. CrossRef Medline
6. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, Von Zastrow M, Beattie MS, Malenka RC (2002) Control of synaptic strength by glial TNFalpha. Science 295:2282-2285. CrossRef Medline
7. Berman DE, Hazvi S, Neduva V, Dudai Y (2000) The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: activation of ERK1-2 and formation of a memory trace. J Neurosci 20: 7017-7023. Medline
8. Bermúdez-Rattoni F, Ramírez-Lugo L, Gutiérrez R, Miranda MI (2004) Molecular signals into the insular cortex and amygdala during aversive gustatory memory formation. Cell Mol Neurobiol 24:25-36. CrossRef Medline
9. Bessis A, Béchade C, Bernard D, Roumier A (2007) Microglial control of neuronal death and synaptic properties. Glia 55:233-238. CrossRef Medline
10. Brebner K, Hayley S, Zacharko R, Merali Z, Anisman H (2000) Synergistic effects of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha: central monoamine, corticosterone, and behavioral variations. Neuropsy chopharmacology 22:566-580. CrossRef Medline
11. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924. CrossRef Medline
12. Chakravarty S, Herkenham M (2005) Toll-like receptor 4 on nonhemato poietic cells sustains CNS inflammation during endotoxemia, indepen dent of systemic cytokines. J Neurosci 25:1788-1796. CrossRef Medline
13. Cross-Mellor SK, Kavaliers M, Ossenkopp KP (2004) Comparing immune activation (lipopolysaccharide) and toxin (lithium chloride)-induced gustatory conditioning: lipopolysaccharide produces conditioned taste avoidance but not aversion. Behav Brain Res 148:11-19. CrossRef Medline
14. Cunningham C, Sanderson DJ (2008) Malaise in the water maze: untangling the effects of LPS and IL-1beta on learning and memory. Brain Behav Immun 22:1117-1127. CrossRef Medline
15. Danielson E, Zhang N, Metallo J, Kaleka K, Shin SM, Gerges N, Lee SH (2012) S-SCAM/MAGI-2 is an essential synaptic scaffolding molecule for the GluA2-containing maintenance pool of AMPA receptors. J Neurosci 32:6967-6980. CrossRef Medline
16. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46-56. CrossRef Medline
17. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758. CrossRef Medline
18. Färber K, Kettenmann H (2005) Physiology of microglial cells. Brain Res Brain Res Rev 48:133-143. CrossRef Medline
19. Ferrari D, Chiozzi P, Falzoni S, Dal Susino M, Melchiorri L, Baricordi OR, Di Virgilio F (1997) Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 159: 1451-1458. Medline
20. Ferreira G, Gutiérrez R, De La Cruz V, Bermúdez-Rattoni F (2002) Differential involvement of cortical muscarinic and NMDA receptors in short and long-term taste aversion memory. Eur J Neurosci 16:1139-1145.CrossRef Medline
21. Franklin AE, Engeland CG, Kavaliers M, Ossenkopp KP (2003) Lipopo-lysaccharide-induced hypoactivity and behavioral tolerance development are modulated by the light-dark cycle in male and female rats. Psychop harmacology (Berl) 170:399-408. CrossRef Medline
22. Franklin AE, Engeland CG, Kavaliers M, Ossenkopp KP (2007) The rate of behavioral tolerance development to repeated lipopolysaccharide treat-ments depends upon the time of injection during the light-dark cycle: a multivariable examination of locomotor activity. Behav Brain Res 180: 161-173. CrossRef Medline
23. Gal-Ben-Ari S, Rosenblum K (2011) Molecular mechanisms underlying memory consolidation of taste information in the cortex. Front Behav Neurosci 5:87. CrossRef Medline
24. Gonzalez PV, Schiöth HB, Lasaga M, Scimonelli TN (2009) Memory impairment induced by IL-1beta is reversed by alpha-MSH through central melanocortin-4 receptors. Brain Behav Immun 23:817-822. CrossRef Medline
25. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394. CrossRef Medline
26. Hanley JG, Khatri L, Hanson PI, Ziff EB (2002) NSF ATPase and alpha-/ beta-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34:53-67. CrossRef Medline
27. Haynes DR (2006) Emerging and future therapies for the treatment of bone loss associated with chronic inflammation. Inflammopharmacology 14: 193-197. CrossRef Medline
28. Joels G, Lamprecht R (2010) Interaction between N-ethylmaleimide sensitive factor and GluR2 is essential for fear memory formation in lateral amygdala. J Neurosci 30:15981-15986. CrossRef Medline
29. Kauer JA, Malenka RC (2006) LTP: AMPA receptors trading places. Nat Neurosci 9:593-594. CrossRef Medline
30. Lai AY, Swayze RD, El-Husseini A, Song C (2006) Interleukin-1 beta mod ulates AMPA receptor expression and phosphorylation in hippocampal neurons. J Neuroimmunol 175:97-106. CrossRef Medline
31. Lee SH, Liu L, Wang YT, Sheng M (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor traffick ing and hippocampal LTD. Neuron 36:661-674. CrossRef Medline
32. Lim W, Isaac JT (2005) ATP hydrolysis is required for the rapid regulation of AMPA receptors during basal synaptic transmission and long-term synaptic plasticity. Neuropharmacology 48:949-955. CrossRef Medline
33. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649-658. CrossRef Medline
34. Luthi A, Chittajallu R, Duprat F, Palmer MJ, Benke TA, Kidd FL, Henley JM, Isaac JT, Collingridge GL (1999) Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron 24: 389-399. CrossRef Medline
35. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126. CrossRef Medline
36. Matsumoto Y, Watanabe S, Suh YH, Yamamoto T (2002) Effects of intra hippocampal CT105, a carboxyl terminal fragment of beta-amyloid precursor protein, alone/with inflammatory cytokines on working memory in rats. J Neurochem 82:234-239. CrossRef Medline
37. Mehta VB, Hart J, Wewers MD (2001) ATP-stimulated release of interleukin (IL)-1beta and IL-18 requires priming by lipopolysaccharide and is indepen-dent of caspase-1 cleavage. J Biol Chem 276:3820-3826. CrossRef Medline
38. Migues PV, Hardt O, Finnie P, Wang YW, Nader K (2014) The maintenance of long-term memory in the hippocampus depends on the interaction between N-ethylmaleimide-sensitive factor and GluA2. Hippocampus 24:1112-1119. CrossRef Medline
39. Miranda MI, Ferreira G, Ramirez-Lugo L, Bermúdez-Rattoni F (2002) Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proc Natl Acad Sci U S A 99:11417-11422. CrossRef Medline
40. Miranda MI, Quirarte GL, Rodriguez-Garcia G, McGaugh JL, Roozendaal B (2008) Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learn Mem 15:468-476.CrossRef Medline
41. Nerad L, Ramírez-Amaya V, Ormsby CE, Bermúdez-Rattoni F (1996) Differential effects of anterior and posterior insular cortex lesions on the acquisition of conditioned taste aversion and spatial learning. Neurobiol Learn Mem 66:44-50. CrossRef Medline
42. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97. CrossRef Medline
43. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23: 365-376. CrossRef Medline
44. Ogoshi F, Yin HZ, Kuppumbatti Y, Song B, Amindari S, Weiss JH (2005) Tumor necrosis-factor-alpha (TNF-alpha) induces rapid insertion of Ca2 –permeable alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA)/ kainate (Ca-A/K) channels in a subset of hippocampal pyramidal neurons. Exp Neurol 193:384-393. CrossRef Medline
45. Pankratov Y, Lalo U, Krishtal O, Verkhratsky A (2002) Ionotropic P2X purinore-ceptors mediate synaptic transmission in rat pyramidal neurones of layer II/III of somato-sensory cortex. J Physiol 542:529-536. CrossRef Medline
46. Pankratov Y, Lalo U, Verkhratsky A, North RA (2007) Quantal release of ATP in mouse cortex. J Gen Physiol 129:257-265. CrossRef Medline
47. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A (2012) Microglia acti-vation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 109:E197-E205. CrossRef Medline
48. Perregaux D, Gabel CA (1994) Interleukin-1 beta maturation and release in response to ATP and nigericin: evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem 269:15195-15203. Medline
49. Pougnet JT, Toulme E, Martinez A, Choquet D, Hosy E, Boué-Grabot E (2014) ATP P2X receptors downregulate AMPA receptor trafficking and postsynaptic efficacy in hippocampal neurons. Neuron 83:417-430.CrossRef Medline
50. Pugh CR, Nguyen KT, Gonyea JL, Fleshner M, Wakins LR, Maier SF, Rudy JW (1999) Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav Brain Res 106:109-118.CrossRef Medline
51. Richard EM, Helbling JC, Tridon C, Desmedt A, Minni AM, Cador M, Pourtau L, Konsman JP, Mormède P, Moisan MP (2010) Plasma transcortin influences endocrine and behavioral stress responses in mice. Endocrinology 151:649-659. CrossRef Medline
52. Sewards TV, Sewards MA (2001) Cortical association areas in the gustatory system. Neurosci Biobehav Rev 25:395-407. CrossRef Medline
53. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21: 393-400. CrossRef Medline
54. Stehberg J, Moraga-Amaro R, Simon F (2011) The role of the insular cortex in taste function. Neurobiol Learn Mem 96:130-135. CrossRef Medline
55. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692-8700. Medline
56. Wang Y, Dong Q, Xu XF, Feng X, Xin J, Wang DD, Yu H, Tian T, Chen ZY (2013) Phosphorylation of cofilin regulates extinction of conditioned aversive memory via AMPAR trafficking. J Neurosci 33:6423-6433. CrossRef Medline
57. Windscheif U (1996) Purinoceptors: from history to recent progress. A review. J Pharm Pharmacol 48:993-1011. CrossRef Medline
58. Yang S, Liu ZW, Wen L, Qiao HF, Zhou WX, Zhang YX (2005) Interleukin 1beta enhances NMDA receptor-mediated current but inhibits excitatory synaptic transmission. Brain Res 1034:172-179. CrossRef Medline
59. Yirmiya R, Goshen I (2011) Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25:181-213.CrossRef Medline