Fluctuations in endogenous kynurenic acid control hippocampal glutamate and memory

Neuropsychopharmacology

Volumn 36, Issue 11, 2011, Pages 2357-2367

  Pocivavsek, Ana ^a   Wu, Hui Qiu ^a   Potter, Michelle C ^a,b   Elmer, Greg I ^a   Pellicciari, Roberto ^c   Schwarcz, Robert ^a  

^a MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Alzheimer's disease; astrocytes; cognition; kynurenine; schizophrenia; water maze

Indexed keywords

4 (ETHYLSULFONYL)BENZOYLALANINE; AMINOTRANSFERASE INHIBITOR; GLUTAMIC ACID; KYNURENIC ACID; KYNURENINE; KYNURENINE AMINOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL EXAMINATION; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIALYSIS; HIPPOCAMPUS; HYPOTHESIS; MALE; MEMORY; MENTAL DISEASE; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR DOWN REGULATION; UPREGULATION;

ANIMALS; EXTRACELLULAR FLUID; GLUTAMIC ACID; HIPPOCAMPUS; KYNURENIC ACID; MALE; MAZE LEARNING; MEMORY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80052710746     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.127     Document Type: Article

References (88)

1. Abbott A, Roberts BM, Turner L, Campbell DW, Schaffer CL, Campbell BM et al (2010). Inhibition of kynurenine amino-transferase II (KAT II) protects against ketamine-induced cognitive impairment and improves spatial working memory. Soc Neurosci Abstr 35: 472.18.
2. Ahlander M, Misane I, Schott PA, Ogren SO (1999). A behavioral analysis of the spatial learning deficit induced by the NMDA receptor antagonist MK-801 (dizocilpine) in the rat. Neuro-psychopharmacology 21: 414-426. (Pubitemid 29333080)
3. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009). Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89: 73-120.
4. Amori L, Wu HQ, Marinozzi M, Pellicciari R, Guidetti P, Schwarcz R (2009). Specific inhibition of kynurenate synthesis enhances extracellular dopamine levels in the rodent striatum. Neuroscience 159: 196-203.
5. Bannerman DM, Rawlins JN, Good MA (2006). The drugs don't work-or do they? Pharmacological and transgenic studies of the contribution of NMDA and GluR-A-containing AMPA receptors to hippocampal-dependent memory. Psychopharmacology (Berl) 188: 552-566. (Pubitemid 46758961)
6. Baran H, Jellinger K, Deecke L (1999). Kynurenine metabolism in Alzheimer's disease. J Neural Transm 106: 165-181. (Pubitemid 29137514)
7. Barik J, Wonnacott S (2006). Indirect modulation by alpha7 nicotinic acetylcholine receptors of noradrenaline release in rat hippocampal slices: interaction with glutamate and GABA systems and effect of nicotine withdrawal. Mol Pharmacol 69: 618-628. (Pubitemid 43121959)
8. Barnes J, Ourselin S, Fox NC (2009). Clinical application of measurement of hippocampal atrophy in degenerative dementias. Hippocampus 19: 510-516.
9. Boess FG, De Vry J, Erb C, Flessner T, Hendrix M, Luithle J et al (2007). The novel alpha7 nicotinic acetylcholine receptor agonist N-[(3R)-1- azabicyclo[2.2.2]oct-3-yl]-7-[2-(methoxy) phenyl]-1-benzofuran-2-carboxamide improves working and recognition memory in rodents. J Pharmacol Exp Ther 321: 716-725. (Pubitemid 46624485)
10. Carpenedo R, Chiarugi A, Russi P, Lombardi G, Carla V, Pellicciari R et al (1994). Inhibitors of kynurenine hydroxylase and kynureninase increase cerebral formation of kynurenate and have sedative and anticonvulsant activities. Neuroscience 61: 237-243.
11. Carpenedo R, Pittaluga A, Cozzi A, Attucci S, Galli A, Raiteri M et al (2001). Presynaptic kynurenate-sensitive receptors inhibit glutamate release. Eur J Neurosci 13: 2141-2147. (Pubitemid 32578800)
12. Chapin DS, Campbell B, Strick C, Kozak R (2010). The impact of a KATII inhibitor on performance in the rat sustained attentional task (SAT) and conditioned avoidance responding (CAR). Soc Neurosci Abstr 35: 472.16.
13. Chen Y, Meininger V, Guillemin GJ (2009). Recent advances in the treatment of amyotrophic lateral sclerosis. Emphasis on kynurenine pathway inhibitors. Cent Nerv Syst Agents Med Chem 9: 32-39.
14. Chess AC, Bucci DJ (2006). Increased concentration of cerebral kynurenic acid alters stimulus processing and conditioned responding. Behav Brain Res 170: 326-332. (Pubitemid 44255505)
15. Chess AC, Landers AM, Bucci DJ (2009). L-Kynurenine treatment alters contextual fear conditioning and context discrimination but not cue-specific fear conditioning. Behav Brain Res 201: 325-331.
16. Chess AC, Simoni MK, Alling TE, Bucci DJ (2007). Elevations of endogenous kynurenic acid produce spatial working memory deficits. Schizophr Bull 33: 797-804. (Pubitemid 47343705)
17. Clem RL, Celikel T, Barth AL (2008). Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319: 101-104.
18. Cosi C, Mannaioni G, Cozzi A, Carla V, Sili M, Cavone L et al (2010). G-protein coupled receptor 35 (GPR35) activation and inflammatory pain: studies on the antinociceptive effects of kynurenic acid and zaprinast. Neuropharmacology 60: 1227-1231.
19. Curatolo L, Caccia C, Speciale C, Raimondi L, Cini M, Marconi M et al (1996). Modulation of extracellular kynurenic acid content by excitatory amino acids in primary cultures of rat astrocytes. Adv Exp Med Biol 398: 273-276. (Pubitemid 126426240)
20. Curzon P, Anderson DJ, Nikkel AL, Fox GB, Gopalakrishnan M, Decker MW et al (2006). Antisense knockdown of the rat alpha7 nicotinic acetylcholine receptor produces spatial memory impairment. Neurosci Lett 410: 15-19. (Pubitemid 44667252)
21. Duffy S, Labrie V, Roder JC (2008). D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology 33: 1004-1018. (Pubitemid 351367543)
22. Erhardt S, Blennow K, Nordin C, Skogh E, Lindstrom LH, Engberg G (2001). Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci Lett 313: 96-98. (Pubitemid 32973903)
23. Erhardt S, Schwieler L, Emanuelsson C, Geyer M (2004). Endogenous kynurenic acid disrupts prepulse inhibition. Biol Psychiatry 56: 255-260. (Pubitemid 39092940)
24. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG et al (2001). Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21: 7993-8003. (Pubitemid 32952756)
25. Gramsbergen JB, Hodgkins PS, Rassoulpour A, Turski WA, Guidetti P, Schwarcz R (1997). Brain-specific modulation of kynurenic acid synthesis in the rat. J Neurochem 69: 290-298. (Pubitemid 27274184)
26. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716. (Pubitemid 26360646)
27. Guidetti P, Amori L, Sapko MT, Okuno E, Schwarcz R (2007a). Mitochondrial aspartate aminotransferase: a third kynurenate-producing enzyme in the mammalian brain. J Neurochem 102: 103-111. (Pubitemid 46906272)
28. Guidetti P, Hoffman GE, Melendez-Ferro M, Albuquerque EX, Schwarcz R (2007b). Astrocytic localization of kynurenine aminotransferase II in the rat brain visualized by immuno-cytochemistry. Glia 55: 78-92. (Pubitemid 44845511)
29. Guillemin GJ, Kerr SJ, Smythe GA, Smith DG, Kapoor V, Armati PJ et al (2001). Kynurenine pathway metabolism in human astrocytes: a paradox for neuronal protection. J Neurochem 78: 842-853. (Pubitemid 32777985)
30. Guillemin GJ, Smith DG, Kerr SJ, Smythe GA, Kapoor V, Armati PJ et al (2000). Characterisation of kynurenine pathway metabolism in human astrocytes and implications in neuropathogenesis. Redox Rep 5: 108-111. (Pubitemid 30488525)
31. Hamilton NB, Attwell D (2010). Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11: 227-238.
32. Han Q, Cai T, Tagle DA, Li J (2010). Structure, expression, and function of kynurenine aminotransferases in human and rodent brains. Cell Mol Life Sci 67: 353-368.
33. Hauber W, Schmidt WJ (1989). Effects of intrastriatal blockade of glutamatergic transmission on the acquisition of T-maze and radial maze tasks. J Neural Transm Gen Sect 78: 29-41. (Pubitemid 19183355)
34. Hertz L, Zielke HR (2004). Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27: 735-743. (Pubitemid 39488077)
35. Hilmas C, Pereira EF, Alkondon M, Rassoulpour A, Schwarcz R, Albuquerque EX (2001). The brain metabolite kynurenic acid inhibits alpha7 nicotinic receptor activity and increases non-alpha7 nicotinic receptor expression: physiopathological implications. J Neurosci 21: 7463-7473. (Pubitemid 32904945)
36. Jo YS, Park EH, Kim IH, Park SK, Kim H, Kim HT et al (2007). The medial prefrontal cortex is involved in spatial memory retrieval under partial-cue conditions. J Neurosci 27: 13567-13578. (Pubitemid 350255341)
37. Kalia LV, Kalia SK, Salter MW (2008). NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol 7: 742-755. (Pubitemid 351957932)
38. Kantrowitz JT, Javitt DC (2010). Thinking glutamatergically: changing concepts of schizophrenia based upon changing neuro-chemical models. Clin Schizophr Relat Psychoses 4: 189-200.
39. Karasawa J, Hashimoto K, Chaki S (2008). D-serine and a glycine transporter inhibitor improve MK-801-induced cognitive deficits in a novel object recognition test in rats. Behav Brain Res 186: 78-83. (Pubitemid 350100896)
40. Kessler M, Terramani T, Lynch G, Baudry M (1989). A glycine site associated with N-methyl-D-aspartic acid receptors: characterization and identification of a new class of antagonists. J Neurochem 52: 1319-1328. (Pubitemid 19085960)
41. Konradsson-Geuken A, Gash CR, Alexander K, Pomerleau F, Huettl P, Gerhardt GA et al (2009). Second-by-second analysis of alpha 7 nicotine receptor regulation of glutamate release in the prefrontal cortex of awake rats. Synapse 63: 1069-1082.
42. Lagostena L, Trocme-Thibierge C, Morain P, Cherubini E (2008). The partial alpha7 nicotine acetylcholine receptor agonist S 24795 enhances long-term potentiation at CA3-CA1 synapses in the adult mouse hippocampus. Neuropharmacology 54: 676-685.
43. Levin ED, McClernon FJ, Rezvani AH (2006). Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 184: 523-539. (Pubitemid 43255869)
44. Lynch G, Rex CS, Chen LY, Gall CM (2008). The substrates of memory: defects, treatments, and enhancement. Eur J Pharmacol 585: 2-13.
45. Martin LF, Freedman R (2007). Schizophrenia and the alpha7 nicotinic acetylcholine receptor. Int Rev Neurobiol 78: 225-246.
46. Meyer EM, Tay ET, Papke RL, Meyers C, Huang GL, de Fiebre CM (1997). 3-[2,4-Dimethoxybenzylidene]anabaseine (DMXB) selectively activates rat alpha7 receptors and improves memory-related behaviors in a mecamylamine-sensitive manner. Brain Res 768: 49-56. (Pubitemid 27433476)
47. Monaghan DT, Bridges RJ, Cotman CW (1989). The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol 29: 365-402. (Pubitemid 19107360)
48. Moroni F, Cozzi A, Carpendo R, Cipriani G, Veneroni O, Izzo E (2005). Kynurenine 3-mono-oxygenase inhibitors reduce gluta-mate concentration in the extracellular spaces of the basal ganglia but not in those of the cortex or hippocampus. Neuropharmacology 48: 788-795. (Pubitemid 40489036)
49. Moroni F, Russi P, Lombardi G, Beni M, Carla V (1988). Presence of kynurenic acid in the mammalian brain. J Neurochem 51: 177-180.
50. Morris R (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11: 47-60. (Pubitemid 14088970)
51. Morris RG (2006). Theories of hippocampal function. In: Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J (eds). The Hippocampus Book. Oxford University Press: New York. pp 581-713.
52. Mudo G, Belluardo N, Fuxe K (2007). Nicotinic receptor agonists as neuroprotective/neurotrophic drugs. Progress in molecular mechanisms. J Neural Transm 114: 135-147. (Pubitemid 46018681)
53. Nemeth H, Toldi J, Vécsei L (2005). Role of kynurenines in the central and peripheral nervous systems. Curr Neurovasc Res 2: 249-260. (Pubitemid 40980183)
54. O'Connor JC, Andre C, Wang Y, Lawson MA, Szegedi SS, Lestage J et al (2009). Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2, 3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin. J Neurosci 29: 4200-4209.
55. Parpura V, Zorec R (2010). Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63: 83-92.
56. Parsons CG, Danysz W, Quack G, Hartmann S, Lorenz B, Wollenburg C et al (1997). Novel systemically active antagonists of the glycine site of the N-methyl-D-aspartate receptor: electrophysiological, biochemical and behavioral characterization. J Pharmacol Exp Ther 283: 1264-1275. (Pubitemid 28016502)
57. Pellicciari R, Rizzo RC, Costantino G, Marinozzi M, Amori L, Guidetti P et al (2006). Modulators of the kynurenine pathway of tryptophan metabolism: synthesis and preliminary biological evaluation of (S)-4-(ethylsulfonyl) benzoylalanine, a potent and selective kynurenine aminotransferase II (KAT II) inhibitor. ChemMedChem 1: 528-531. (Pubitemid 43759763)
58. Pellicciari R, Venturoni F, Bellocchi D, Carotti A, Marinozzi M, Macchiarulo A et al (2008). Sequence variants in kynurenine aminotransferase II (KAT II) orthologs determine different potencies of the inhibitor S-ESBA. ChemMedChem 3: 1199-1202.
59. Pereira EF, Hilmas C, Santos MD, Alkondon M, Maelicke A, Albuquerque EX (2002). Unconventional ligands and modulators of nicotinic receptors. J Neurobiol 53: 479-500. (Pubitemid 35375580)
60. Perkins MN, Stone TW (1982). An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res 247: 184-187. (Pubitemid 12028646)
61. Potter MC, Elmer GI, Bergeron R, Albuquerque EX, Guidetti P, Wu HQ et al (2010). Reduction of endogenous kynurenic acid formation enhances extracellular glutamate, hippocampal plasticity, and cognitive behavior. Neuropsychopharmacology 35: 1734-1742.
62. Quarta D, Borycz J, Solinas M, Patkar K, Hockemeyer J, Ciruela F et al (2004). Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation. J Neurochem 91: 873-880. (Pubitemid 39507364)
63. Raison CL, Dantzer R, Kelley KW, Lawson MA, Woolwine BJ, Vogt G et al (2010). CSF concentrations of brain tryptophan and kynurenines during immune stimulation with IFN-alpha: relationship to CNS immune responses and depression. Mol Psychiatry 15: 393-403.
64. Rassoulpour A, Wu HQ, Ferré S, Schwarcz R (2005). Nanomolar concentrations of kynurenic acid reduce extracellular dopamine levels in the striatum. J Neurochem 93: 762-765. (Pubitemid 40617635)
65. Richter-Levin G, Canevari L, Bliss TV (1995). Long-term potentia-tion and glutamate release in the dentate gyrus: links to spatial learning. Behav Brain Res 66: 37-40.
66. Riekkinen M, Riekkinen Jr P. (1997). Nicotine and D-cycloserine enhance acquisition of water maze spatial navigation in aged rats. Neuroreport 8: 699-703. (Pubitemid 27128220)
67. Robbins TW, Murphy ER (2006). Behavioural pharmacology: 40+ years of progress, with a focus on glutamate receptors and cognition. Trends Pharmacol Sci 27: 141-148.
68. Russi P, Alesiani M, Lombardi G, Davolio P, Pellicciari R, Moroni F (1992). Nicotinylalanine increases the formation of kynurenic acid in the brain and antagonizes convulsions. J Neurochem 59: 2076-2080.
69. Scheff SW, Price DA (2006). Alzheimer's disease-related alterations in synaptic density: neocortex and hippocampus. J Alzheimers Dis 9: 101-115. (Pubitemid 44253303)
70. Schwarcz R, Du F, Schmidt W, Turski WA, Gramsbergen JB, Okuno E et al (1992). Kynurenic acid: a potential pathogen in brain disorders. Ann NY Acad Sci 648: 140-153.
71. Schwarcz R, Pellicciari R (2002). Manipulation of brain kynur-enines: glial targets, neuronal effects, and clinical opportunities. J Pharmacol Exp Ther 303: 1-10.
72. Schwarcz R, Rassoulpour A, Wu HQ, Medoff D, Tamminga CA, Roberts RC (2001). Increased cortical kynurenate content in schizophrenia. Biol Psychiatry 50: 521-530. (Pubitemid 32971883)
73. Shepard PD, Joy B, Clerkin L, Schwarcz R (2003). Micromolar brain levels of kynurenic acid are associated with a disruption of auditory sensory gating in the rat. Neuropsychopharmacology 28: 1454-1462. (Pubitemid 41070880)
74. Shibata K (1988). Fluorimetric micro-determination of kynurenic acid, an endogenous blocker of neurotoxicity, by high-performance liquid chromatography. J Chromatogr 430: 376-380.
75. Singer HS, Morris C, Grados M (2010). Glutamatergic modula-tory therapy for Tourette syndrome. Med Hypotheses 74: 862-867.
76. Speciale C, Wu HQ, Gramsbergen JB, Turski WA, Ungerstedt U, Schwarcz R (1990). Determination of extracellular kynurenic acid in the striatum of unanesthetized rats: effect of aminooxy-acetic acid. Neurosci Lett 116: 198-203. (Pubitemid 20237160)
77. Swartz KJ, During MJ, Freese A, Beal MF (1990). Cerebral synthesis and release of kynurenic acid: an endogenous antagonist of excitatory amino acid receptors. J Neurosci 10: 2965-2973.
78. Tamminga CA, Stan AD, Wagner AD (2010). The hippocampal formation in schizophrenia. Am J Psychiatry 167: 1178-1193.
79. Thomsen MS, Hansen HH, Timmerman DB, Mikkelsen JD (2010). Cognitive improvement by activation of alpha7 nicotinic acetylcholine receptors: from animal models to human patho-physiology. Curr Pharm Des 16: 323-343.
80. Timmermann DB, Gronlien JH, Kohlhaas KL, Nielsen EO, Dam E, Jorgensen TD et al (2007). An allosteric modulator of the alpha7 nicotinic acetylcholine receptor possessing cognition-enhancing properties in vivo. J Pharmacol Exp Ther 323: 294-307. (Pubitemid 47443280)
81. Turski WA, Nakamura M, Todd WP, Carpenter BK, Whetsell Jr WO., Schwarcz R (1988). Identification and quantification of kynurenic acid in human brain tissue. Brain Res 454: 164-169.
82. Varasi M, Della Torre A, Heidempergher F, Pevarello P, Speciale C, Guidetti P et al (1996). Derivatives of kynurenine as inhibitors of rat brain kynurenine aminotransferase. Eur J Med Chem 31: 11-21. (Pubitemid 26038832)
83. Venable N, Kelly PH (1990). Effects of NMDA receptor antagonists on passive avoidance learning and retrieval in rats and mice. Psychopharmacology (Berl) 100: 215-221. (Pubitemid 20038565)
84. Wallace TL, Callahan PM, Tehim A, Bertrand D, Tombaugh G, Wang S et al (2011). RG3487, a novel nicotinic alpha7 receptor partial agonist, improves cognition and sensorimotor gating in rodents. J Pharmacol Exp Ther 336: 242-253.
85. Wang J, Simonavicius N, Wu X, Swaminath G, Reagan J, Tian H et al (2006). Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J Biol Chem 281: 22021-22028. (Pubitemid 44181906)
86. Wu HQ, Pereira EF, Bruno JP, Pellicciari R, Albuquerque EX, Schwarcz R (2010). The astrocyte-derived alpha7 nicotinic receptor antagonist kynurenic acid controls extracellular glutamate levels in the prefrontal cortex. J Mol Neurosci 40: 204-210.
87. Wu HQ, Rassoulpour A, Schwarcz R (2007). Kynurenic acid leads, dopamine follows: a new case of volume transmission in the brain? J Neural Transm 114: 33-41. (Pubitemid 46018673)
88. Zmarowski A, Wu HQ, Brooks JM, Potter MC, Pellicciari R, Schwarcz R et al (2009). Astrocyte-derived kynurenic acid modulates basal and evoked cortical acetylcholine release. Eur J Neurosci 29: 529-538.