Changes in synaptic transmission and protein expression in the brains of adult offspring after prenatal inhibition of the kynurenine pathway

Neuroscience

Volumn 254, Issue , 2013, Pages 241-259

  Forrest, C M ^a   Khalil, O S ^a   Pisar, M ^a   McNair, K ^a   Kornisiuk, E ^b   Snitcofsky, M ^b   Gonzalez, N ^b   Jerusalinsky, D ^b   Darlington, L G ^c   Stone, T W ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c EPSOM GENERAL HOSPITAL   (United Kingdom)

Author keywords

Doublecortin; Hedgehog; Kynurenic acid; Kynurenines; Neurodevelopment; Tryptophan

Indexed keywords

COMPLEMENTARY DNA; DOUBLECORTIN; KYNURENIC ACID; KYNURENINE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SONIC HEDGEHOG PROTEIN; TRYPTOPHAN; N-METHYL D-ASPARTATE RECEPTOR SUBTYPE 2A; RO 61-8048; SULFONAMIDE; THIAZOLE DERIVATIVE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; IMMUNOBLOTTING; LOCOMOTION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; AGE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN; DOWN REGULATION; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PREGNANCY; SIGNAL TRANSDUCTION; WISTAR RAT;

AGE FACTORS; ANIMALS; BRAIN; DOWN-REGULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; KYNURENINE; MALE; NEUROGENESIS; ORGAN CULTURE TECHNIQUES; PREGNANCY; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SULFONAMIDES; SYNAPTIC TRANSMISSION; THIAZOLES;

EID: 84886943694     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.09.034     Document Type: Article

References (135)

1. Ahn S., Joyner A.L. In vivo analysis of quiescent adult neural stem cells responding to sonic hedgehog. Nature 2005, 437:894-897.
2. Alberati-Giani D., Ricciardi-Castiglioni P., Kohler C., Cesura A.M. Regulation of the kynurenine metabolic pathway by interferon-gamma in murine cloned macrophages and microglial cells. J Neurochem 1996, 66:996-1004.
3. Alexander K.S., Pocivavsek A., Wu H.-Q., Pershing M.L., Schwarcz R., Bruno J.P. Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine. Neuroscience 2013, 234:19-28.
4. Alexander K.S., Wu H.-Q., Schwarcz R., Bruno J.P. Acute elevations of brain kynurenic acid impair cognitive flexibility: normalization by the alpha7 positive modulator galantamine. Psychopharmacology 2012, 220:627-637.
5. Al-Hayani A., Davies S.N. Effect of cannabinoids on synaptic transmission in the rat hippocampal slice is temperature-dependent. Eur J Pharmacol 2002, 442:47-54.
6. Alvarez V.A., Ridenour D.A., Sabatini B.L. Distinct structural and ionotropic roles of NMDA receptors in controlling spine and synapse stability. J Neurosci 2007, 27:7365-7376.
7. Angot E., Loulier K., Nguyen-Ba-Charvet K.T., Gadeau A.-P., Ruat M., Traiffort E. Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 2008, 26:2311-2320.
8. Baez M.V., Oberholzer M.V., Cercato M.C., Snitcofsky M., Aguirre A.I., Jerusalinsky D.A. NMDA receptor subunits in the adult rat hippocampus undergo similar changes after 5minutes in an open field and after LTP induction. PLOS One 2013, 8:e55244.
9. Banerjee T., Duhadaway J.B., Gaspari P., Sutanto-Ward E., Munn D.H., Mellor A.L., Malachowski W.P., Prendergast G.C., Muller A.J. A key in vivo antitumor mechanism of action of natural product-based brassinins is inhibition of indoleamine 2,3-dioxygenase. Oncogene 2008, 27:2851-2857.
10. Beal M.F., Swartz K.J., Isacson O. Developmental changes in brain kynurenic acid concentrations. Dev Brain Res 1992, 68:136-139.
11. Breton J., Avanzini S., Covini N., Magistrelli G., Cozzi L., Isacchi A. Functional characterisation and mechanism of action of recombinant human kynurenine-3-hydroxylase. Eur J Biochem 2000, 267:1092-1099.
12. Broadstock M., Austin P.J., Betts M.J., Duty S. Antiparkinsonian potential of targeting group III metabotropic glutamate receptor subtypes in the rodent substantia nigra pars reticulate. Br J Pharmacol 2012, 165:1034-1045.
13. Brown A.S. Prenatal infection as a risk factor in schizophrenia. Schizophren Bull 2006, 32:200-202.
14. Brown A.S. The environment and susceptibility to schizophrenia. Prog Neurobiol 2011, 93:23-58.
15. Cai Y., Xiong K., Chu Y., Luo D.-W., Luo X.-G., Yuan X.-Y., Struble R.G., Clough R.W., Spencer D.D., Williamson A., Kordower J.H., Patrylo P.R., Yan X.X. Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol 2009, 216:342-356.
16. Charytoniuk D., Traiffort E., Hantraye P., Hermel J.M., Galdes A., Ruat M. Intrastriatal sonic hedgehog injection increases patched transcript levels in the adult rat subventricular zone. Eur J Pharmacol 2002, 16:2351-2357.
17. Chess A.C., Simoni M.K., Alling T.E., Bucci D.J. Elevations of endogenous kynurenic acid produce spatial working memory deficits. Schizophren Bull 2007, 33:797-804.
18. Chess A.C., Bucci D.J. Increased concentration of cerebral kynurenic acid alters stimulus processing and conditioned responding. Behav Brain Res 2006, 170:326-332.
19. Chess A.C., Landers A.M., Bucci D.J. L-Kynurenine treatment alters contextual fear conditioning and context discrimination but not cue-specific fear conditioning. Behav Brain Res 2009, 201:325-331.
20. Chiarugi A., Moroni F. Quinolinic acid formation in immune-activated mice: studies with (m-nitrobenzoyl)-alanine (mNBA) and 3,4-dimethoxy-[-N-4-(-3-nitrophenyl)thiazol-2yl]-benzenesulfonamide (Ro 61-8048), two potent and selective inhibitors of kynurenine hydroxylase. Neuropharmacology 1999, 38:1225-1233.
21. Clark C.J., Mackay G.M., Smythe G.A., Bustamante S., Stone T.W., Phillips S.R. Prolonged survival of a murine model of cerebral malaria by kynurenine synthesis inhibition. Infect Immun 2005, 73:5249-5251.
22. Colonnese M.T., Zhao J.P., Constantine-Paton M. NMDA receptor currents suppress synapse formation on sproutin axons in vivo. J Neurosci 2005, 25:1291-1303.
23. Copeland C.S., Neale S.A., Salt T.E. Actions of xanthurenic acid, a putative endogenous group II metabotropic glutamate receptor agonist, on sensory transmission in the thalamus. Neuropharmacology 2013, 66:133-142.
24. Corbo J.C., Deuel T.A., Long J.M., LaPorte P., Tsai E., Wynshaw-Boris A., Walsh C.A. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 2002, 22:7548-7557.
25. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 2005, 21:1-14.
26. Cozzi A., Carpenedo R., Moroni F. Kynurenine hydroxylase inhibitors reduce ischemic brain damage: studies with (m-nitrobenzoyl)-alanine (mNBA) and 3,4-dimethoxy-[-N-4-(nitrophenyl)thiazol-2YL]-benzenesulfonamide (Ro61-8048) in models of focal or global brain ischaemia. J Cereb Blood Flow Metab 1999, 19:771-777.
27. Cuppini R., Sartini S., Ambrogini P., Falcieri E., Maltarello M.C., Gallo G. Control of neuron outgrowth by NMDA receptors. J Submicrosc Cytol Pathol 1999, 31:31-40.
28. Dave R.K., Ellis T., Toumpas M.C., Robson J.P., Julian E., Adolphe C., Bartlett P.F., Cooper H.M., Reynolds B.A., Wainwright B.J. Sonic hedgehog and notch signaling can cooperate to regulate neurogenic divisions of neocortical progenitors. PLOS One 2011, 6(2). Article e14680.
29. Dellovade T., Romer J.T., Curran T., Rubin L.L. The hedgehog pathway and neurological disorders. Ann Rev Neurosci 2006, 29:539-563.
30. Dikranian K., Ishimaru M.J., Tenkova T., Labruyere J., Qin Y.Q., Ikonomidou C., Olney J.W. Apoptosis in the in vivo mammalian forebrain. Neurobiol Dis 2001, 8:359-379.
31. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
32. Dobelis P., Staley K.J., Cooper D.C. Lack of modulation of nicotinic acetylcholine alpha-7 receptor currents by kynurenic acid in adult hippocampal interneurons. PLoS One 2012, 7. Article e41108.
33. Drian M.J., Bardoul M., Konig N. Blockade of AMPA/kainate receptors can either decrease or increase the survival of cultured neocortical cells depending on the stage of maturation. Neurochem Int 2001, 38:509-517.
34. du Bois T.M., Huang X.F. Early brain development disruption from NMDA receptor hypofunction: relevance to schizophrenia. Brain Res Rev 2007, 53:260-270.
35. Dykens J.A., Sullivan S.G., Stern A. Oxidative reactivity of the tryptophan metabolites 3-hydroxyanthranilate, cinnabarinate, quinolinate and picolinate. Biochem Pharmacol 1987, 36:211-217.
36. English J.A., Pennington K., Dunn M.J., Cotter D.R. The neuroproteomics of schizophrenia. Biol Psychiatry 2011, 69:163-172.
37. Erhardt S., Schwieler L., Emanuelsson C., Geyer M. Endogenous kynurenic acid disrupts prepulse inhibition. Biol Psychiatry 2004, 56:255-260.
38. Ernst A.F., Jurney W.M., McLoon S.C. Mechanisms involved in development of retinotectal connections: roles of Eph receptor tyrosine kinases NMDA receptors and nitric oxide. Prog Brain Res 1998, 118:115-131.
39. Fagiolini M., Katagiri H., Miyamoto H., Mori H., Grant S.G.N., Mishina M., Hensch T.K. Separable features of visual cortical plasticity revealed by N-methyl-d-aspartate receptor 2A signaling. Proc Natl Acad Sci USA 2003, 100:2854-2859.
40. Fatemi S.H., Pearce D.A., Brooks A.I., Sidwell R.W. Prenatal viral infection in mouse causes differential expression of genes in brains of mouse progeny: a potential animal model for schizophrenia and autism. Synapse 2005, 57:91-99.
41. Fazio F., Lionetto L., Molinaro G., Bertrand H.O., Acher F., Ngomba R.T., Notartomaso S., Curini M., Rosati O., Scarselli P., Di Marco R., Battaglia G., Bruno V., Simmaco M., Pin J.P., Nicoletti F., Goudet C. Cinnabarinic acid, an endogenous metabolite of the kynurenine pathway, activates type 4 metabotropic glutamate receptors. Mol Pharmacol 2012, 81:643-656.
42. Forrest C.M., Khalil O.S., Pisar M., Darlington L.G., Stone T.W. Prenatal inhibition of the tryptophan-kynurenine pathway alters synaptic plasticity and protein expression in the rat hippocampus. Brain Res 2013, 1504:1-15.
43. Forsythe I.D., Clements J.D. Presynaptic glutamate receptors depress excitatory monosynaptic transmission between mouse hippocampal-neurons. J Physiol (Lond) 1990, 429:1-16.
44. Friocourt G., Liu J.S., Antypa M., Rakic S., Walsh C.A., Parnavelas J.G. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 2007, 27:3875-3883.
45. Gleeson J.G., Minnerath S.R., Fox J.W., Allen K.M., Luo R.F., Hong S.E., Berg M.J., Kuzniecky R., Reitnauer P.J., Borgatti R., Mira A.P., Guerrini R., Holmes G.L., Rooney C.M., Berkovic S., Scheffer I., Cooper E.C., Ricci S., Cusmai R., Crawford T.O., Leroy R., Andermann E., Wheless J.W., Dobyns W.B., Ross M.E., Walsh C.A. Characterization of mutations in the gene doublecortin in patients with double cortex syndrome. Ann Neurol 1999, 45:146-153.
46. Gobaille S., Kemmel V., Brumaru D., Dugave C., Aunis D., Maitre M., Gobaille S. Xanthurenic acid distribution, transport, accumulation and release in the rat brain. J Neurochem 2008, 105:982-993.
47. Goncalves J., Queiroz G. Presynaptic adenosine and P2Y receptors. Handb Exp Pharmacol 2008, 184:339-372.
48. Guidetti P., Hoffman G.E., Melendez-Ferro M., Albuquerque E.X., Schwarcz R. Astrocytic localization of kynurenine aminotransferase II in the rat brain visualized by immunocytochemistry. Glia 2007, 55:78-92.
49. Guillemin G.J., Smythe G., Takikawa O., Brew B.J. Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia 2005, 49:15-23.
50. Guillemin G.J., Kerr S.J., Smythe G.A., Smith D.G., Kapoor V., Armati P.J., Croitoru J., Brew B.J. Kynurenine pathway metabolism in human astrocytes: a paradox for neuronal protection. J Neurochem 2001, 78:842-853.
51. Gurdon J.B., Bourillot P.Y. Morphogen gradient interpretation. Nature 2001, 413:797-803.
52. Harris L.W., Sharp T., Gartlon J., Jones D.N.C., Harrison P.J. Long-term behavioural molecular and morphological effects of neonatal NMDA receptor antagonism. Eur J Neurosci 2003, 18:1706-1710.
53. 1 receptors and enhances consolidation of step-down avoidance. Behav Brain Res 2012, 234:184-191.
54. Heng J.E., Zurakowski D., Vorwerk C.K., Grosskreutz C.L., Dreyer E.B. Cation channel control of neurite morphology. Dev Brain Res 1999, 113:67-73.
55. Higgins M.J., Stone T.W. Bicuculline-resistant paired-pulse inhibition in the rat hippocampal slice. Eur J Pharmacol 1993, 317:215-223.
56. Higgins M.J., Stone T.W. The contribution of adenosine to paired-pulse inhibition in the normal and disinhibited hippocampal slice. Br J Pharmacol 1996, 109:1164-1168.
57. Hilmas C., Pereira E.F.R., Alkondon M., Rassoulpour A., Schwarcz R., Albuquerque E.X. The brain metabolite kynurenic acid inhibits alpha 7 nicotinic receptor activity and increases non-alpha 7 nicotinic receptor expression: physiopathological implications. J Neurosci 2001, 21:7463-7473.
58. Hiramatsu R., Hara T., Akimoto H., Takikawa O., Kawabe T., Isobe K., Nagase F. Cinnabarinic acid generated from 3-hydroxyanthranilic acid strongly induces apoptosis in thymocytes through the generation of reactive oxygen species and the induction of caspase. J Cell Biochem 2008, 103:42-53.
59. Hoffman K.B., Murray B.A., Lynch G., Munirathinam S., Bahr B.A. Delayed and isoform-specific effect of NMDA exposure on neural cell adhesion molecules in hippocampus. Neurosci Res 2001, 39:167-173.
60. Holtze M., Saetre P., Engberg G., Schwieler L., Werge T., Andreassen O.A., Hall H., Terenius L., Agartz I., Jonsson E.G., Schalling M., Erhardt S. Kynurenine 3-monooxygenase polymorphisms: relevance for kynurenic acid synthesis in patients with schizophrenia and healthy controls. J Psychiatry Neurosci 2012, 37:53-57.
61. Hor C.H.H., Tang B.L. Sonic hedgehog as a chemoattractant for adult NPCs. Cell Adhes Migr 2010, 4:1-3.
62. Hornig M., Weissenbock H., Horscroft N., Lipkin W.I. An infection-based model of neurodevelopmental damage. Proc Natl Acad Sci U S A 1999, 96:12102-12107.
63. Huang F.-S., Meng K., Tang J.-S. Properties of paired-pulse firing thresholds and the relationship with paired-pulse plasticity in hippocampal CA3-CA1 synapses. Eur J Neurosci 2007, 25:3253-3263.
64. Hynes M., Porter J.A., Chiang C., Chang D., Tessierlavigne M., Beachy P.A., Rosenthal A. Induction of midbrain dopaminergic-neurons by sonic hedgehog. Neuron 1995, 15:35-44.
65. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T.I., Stefovska V., Turski L., Olney J.W. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999, 283:70-74.
66. Iwasato T., Datwani A., Wolf A.M., Nishiyama H., Taguchi Y., Tonegawa S., Knopfel T., Erzurumlu R.S., Itohara S. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 2000, 406:726-731.
67. Jin K., Wang X., Xie L., Mao X.O., Greenberg D.A. Transgenic ablation of doublecortin-expressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc Natl Acad Sci U S A 2010, 107:7993-7998.
68. Kappeler C., Saillour Y., Baudoin J.P., Tuy F.P.D., Alvarez C., Houbron C., Gaspar P., Hamard G., Chelly J., Metin C., Francis F. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 2006, 15:1387-1400.
69. Kemp N., Bashir Z.I. Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors. Neuropharmacology 1999, 38:495-504.
70. Kerjan G., Koizumi H., Han E.B., Dube C.M., Djakovic S.N., Patrick G.N., Baram T.Z., Heinemann S.F., Gleeson J.G. Mice lacking doublecortin and doublecortin-like kinase 2 display altered hippocampal neuronal maturation and spontaneous seizures. Proc Natl Acad Sci U S A 2009, 106:6766-6771.
71. Larson J., Wong D.L., Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 1986, 368:347-350.
72. Leung L.S., Fu X.-W. Factors affecting paired-pulse facilitation in hippocampal CA1 neurons in vitro. Brain Res 1994, 650:75-84.
73. Martel G., Jaffard R., Guillou J.-L. Identification of hippocampus-dependent and hippocampus independent memory components in step-down inhibitory avoidance tasks. Behav Brain Res 2010, 207:138-143.
74. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol 2010, 90:285-326.
75. Miller C.L., Llenos I.C., Dulay J.R., Weis S. Upregulation of the initiating step of the kynurenine pathway in postmortem anterior cingulate cortex from individuals with schizophrenia and bipolar disorder. Brain Res 2006, 1073:25-37.
76. Mok M.H.S., Fricker A.C., Weil A., Kew J.N.C. Electrophysiological characterisation of the actions of kynurenic acid at ligand-gated ion channels. Neuropharmacology 2009, 57:242-249.
77. Munn D.H. Indoleamine 2,3-dioxygenase, Tregs and cancer. Curr Med Chem 2011, 18:2240-2246.
78. Myers W.A., Churchill J.D., Muja N., Garraghty P.E. Role of NMDA receptors in adult primate cortical somatosensory plasticity. J Comp Neurol 2000, 418:373-382.
79. Nacher J., Crespo C., McEwen B.S. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 2001, 14:629-644.
80. Nathan T., Jensen M.S., Lambert J.D.C. GABA-B receptors play a major role in paired-pulse facilitation in area CA1 of the rat hippocampus. Brain Res 1990, 531:55-65.
81. Neale S.A., Copeland C.S., Uebele V.N., Thomson F.J., Salt T.E. Modulation of hippocampal synaptic transmission by the kynurenine pathway member xanthurenic acid and other VGLUT inhibitors. Neuropsychopharmacology 2013, 38:1060-1067.
82. Neher E., Sakaba T. Estimating transmitter release rates from postsynaptic current fluctuations. J Neurosci 2001, 21:9638-9654.
83. Nilsson L.K., Linderholm K.R., Erhardt S. Subchronic treatment with kynurenine and probenecid: effects on prepulse inhibition and firing of midbrain dopamine neurons. J Neural Transm 2006, 113:557-571.
84. Niswender C.M., Johnson K.A., Weaver C.D., Jones C.K., Xiang Z., Luo Q.W., Rodriguez A.L., Marlo J.E., de Paulis T., Thompson A., Days E.L., Nalywajko T., Austin C.A., Williams M.B., Ayala J.E., Williams R., Lindsley C.W., Conn P.J. Discovery, characterization and antiparkinsonian effect of novel positive allosteric modulators of metabotropic glutamate receptor 4. Mol Pharmacol 2008, 74:1345-1358.
85. O'Kane E.M., Stone T.W., Morris B.J. Activation of Rho GTPases by synaptic transmission in the hippocampus. J Neurochem 2003, 87:1309-1312.
86. Okuda S., Nishiyama N., Saito H., Katsuki H. 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem 1998, 70:299-307.
87. Otis T.S., Wu Y.C., Trussell L.O. Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 1996, 16:1634-1644.
88. Ozaki M., Tohyama K., Kishida H., Buonanno A., Yano R., Hashikawa T. Roles of neuregulin in synaptogenesis between mossy fibers and cerebellar granule cells. J Neurosci Res 2000, 59:612-623.
89. Palma V., Lim D.A., Dahmane N., Sanchez P., Brlonne T.C., Herzberg C.D., Gitton Y., Carleton A., Alvarez-Buylla A., Altaba A.R.I. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005, 132:335-344.
90. Parish C.L., Castelo-Branco G., Rawal N., Tonnesen J., Sorensen A.T., Salto C., Kokaia M., Lindvall O., Arenas E. Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement therapy in parkinsonian mice. J Clin Invest 2008, 118:149-160.
91. Pena F., Bargas J., Tapia R. Paired-pulse facilitation is turned into paired-pulse depression in hippocampal slices after epilepsy induced by 4-aminopyridine in vivo. Neuropharmacology 2002, 42:807-812.
92. Perkins M.N., Stone T.W. An iontophoretic investigation of the action of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res 1982, 247:184-187.
93. Pfaffl M.W., Horan G.W., Dempfle L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
94. Pocivavsek A., Wu H.-Q., Elmer G.I., Bruno J.P., Schwarcz R. Pre- and postnatal exposure to kynurenine causes cognitive deficits in adulthood. Eur J Neurosci 2012, 35:1605-1612.
95. Potter M.C., Elmer G.I., Bergeron R., Albuquerque E.X., Guidetti P., Wu H.-Q., Schwarcz R. Reduction of endogenous kynurenic acid formation enhances extracellular glutamate, hippocampal plasticity and cognitive behaviour. Neuropsychopharmacology 2010, 35:1734-1742.
96. Prajerova I., Honsa P., Chvatal A., Anderova M. Distinct effects of sonic hedgehog and Wnt-7a on differentiation of neonatal neural stem/progenitor cells in vitro. Neuroscience 2010, 171:693-711.
97. Rajan I., Cline H.T. Glutamate receptor activity is required for normal development of tectal cells dendrites in vivo. J Neurosci 1998, 18:7836-7846.
98. Ramakers C., Ruijter J.M., Deprez R.H.L., Moorman A.F.M. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 2003, 339:62-66.
99. Ramoa A.S., Mower A.F., Liao D., Safri S.I.A. Suppression of cortical NMDA receptor function prevents development of orientation selectivity in the primary visual cortex. J Neurosci 2001, 21:4299-4309.
100. Rodgers J., Stone T.W., Barratt M.P., Bradley B., Kennedy P.G. Kynurenine pathway inhibition reduces CNS inflammation in a model of human African trypanosomiasis. Brain 2009, 132:1259-1267.
101. Rosenmund C., Stevens C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 1996, 16:1197-1207.
102. Röver S., Cesura A.M., Huguenin P., Kettler R., Szente A. Synthesis and biochemical evaluation of N-(4-phenylthiazol-2-yl)benzenesulfonamides as high-affinity inhibitors of kynurenine 3-hydroxylase. J Med Chem 1997, 40:4378-4385.
103. Saito K., Nowak T.S., Suyama K., Quearry B.J., Saito M., Crowley J.S., Markey S.P., Heyes M.P. Kynurenine pathway enzymes in brain - responses to ischemic brain injury versus systemic immune activation. J Neurochem 1993, 61:2061-2070.
104. Saviane C., Savtchenko L.P., Raffaelli G., Voronin L.L., Cherubini E. Frequency-dependent shift from paired-pulse facilitation to paired-pulse depression at unitary CA3-CA3 synapses in the rat hippocampus. J Physiol (Lond) 2002, 544:469-476.
105. Schwarcz R., Pellicciari R. Manipulation of brain kynurenines: glial targets neuronal effects and clinical opportunities. J Pharmacol Exp Therap 2002, 303:1-10.
106. Schwarcz R., Bruno J.P., Muchowski P.J., Wu H.Q. Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 2012, 13:465-477.
107. Shin M., Yamada O., Sano Km Umezawa C. Effect of branched-chain α-keto acids on kynurenine-3-hydroxylase from rat liver. J Nutr Sci Vitaminol 1982, 28:203-207.
108. Simon D.K., Prusky G.T., Oleary D.D.M., Constantine-Paton M. NMDA receptor antagonists disrupt the formation of a mammalian neural map. Proc Natl Acad Sci U S A 1992, 89:10593-10597.
109. Sims J.R., Lee S.W., Topalkara K., Qiu J., Xu J., Zhou Z., Moskowitz M.A. Sonic hedgehog regulates ischemia/hypoxia-induced neural progenitor proliferation. Stroke 2009, 40:3618-3626.
110. Spassky N., Han Y.-G., Aguilar A., Strehl L., Besse L., Laclef C., Ros M.R., Garcia-Verdugo J.M., Alvarez-Buylla A. Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 2008, 317:246-259.
111. Stone T.W., Darlington L.G. Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 2002, 1:609-620.
112. Stone T.W., Darlington L.G. The kynurenine pathway as a therapeutic target in cognitive and neurodegenerative disorders. Br J Pharmacol 2013, 169:1211-1277.
113. Stone T.W., Perkins M.N. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol 1981, 72:411-412.
114. Stone T.W., Ceruti S., Abbracchio M. Adenosine receptors and neurological disease: neuroprotection and neurodegeneration. Handb Exp Pharmacol 2009, 193:535-587.
115. Stone T.W., Stoy N., Darlington L.G. An expanding range of targets for kynurenine metabolites of tryptophan. Trends Pharmacol Sci 2013, 34:136-143.
116. Stringer J.L., Lothman E.W. Repetitive seizures cause an increase in paired-pulse inhibition in the dentate gyrus. Neurosci Lett 1989, 105:91-95.
117. Taleb O., Maammar M., Brumaru D., Bourguignon J.J., Schmitt M., Klein C., Kemmel V., Maitre M., Mensah-Nyagan A.G. Xanthurenic acid binds to neuronal G-protein-coupled receptors that secondarily activate cationic channels in the cell line NCB-20. PLoS One 2012, 7:e48553.
118. Tang M., Villaescusa J.C., Luo S.X., Guitarte C., Lei S., Miyamoto Y., Taketo M.M., Arenas E., Huang E.J. Interactions of wnt/beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci 2010, 30:9280-9291.
119. Traiffort E., Charytoniuk D.A., Faure H., Ruat M. Regional distribution of sonic hedgehog patched and smoothened mRNA in the adult rat brain. J Neurochem 1998, 70:1327-1330.
120. Traiffort E., Moya K.L., Faure H., Hassig R., Ruat M. High expression and anterograde axonal transport of aminoterminal sonic hedgehog in the adult hamster brain. Eur J Neurosci 2001, 14:839-850.
121. Traiffort E., Angot E., Ruat M. Sonic hedgehog in the mammalian brain. J Neurochem 2010, 113:576-590.
122. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure regulation and function. Pharmacol Rev 2010, 62:405-496.
123. Udin S.B., Grant S. Plasticity in the tectum of Xenopus laevis: binocular maps. Prog Neurobiol 1999, 59:81-106.
124. Ultanir S.K., Kim J.E., Hall B.J., Deerinck T., Ellisman M., Ghosh A. Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Natl Acad Sci U S A 2007, 104:19553-19558.
125. Vaillant C., Monard D. SHH pathway and cerebellar development. Cerebellum 2009, 8:291-301.
126. Vincent A., Kessler J.P., Baude A., Dipasquale E., Tell F. N-methyl-d-aspartate receptor activation exerts a dual control on postnatal development of nucleus tractus solitarii neurons in vivo. Neuroscience 2004, 126:185-194.
127. Waldeck R.F., Pereda A., Faber D.S. Properties and plasticity of paired-pulse depression at a central synapse. J Neurosci 2000, 20:5312-5320.
128. Walker D.W., Curtis B., Lacey B., Nitsos I. Kynurenic acid in brain and cerebrospinal fluid of fetal newborn and adult sheep and effects of placental embolization. Pediatr Res 1999, 45:820-826.
129. Wang M.Z., Jin P., Bumcrot D.A., Marigo V., McMahon A.P., Wang E.A., Woolf T., Pang K. Induction of dopaminergic neuron phenotype in the midbrain by sonic hedgehog protein. Nat Med 1995, 1:1184-1188.
130. Wang L.Y., Kaczmarek L.K. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 1998, 394:384-388.
131. Wierońska J.M., Stachowicz K., Pałucha-Poniewiera A., Acher F., Brański P., Pilc A. Metabotropic glutamate receptor 4 novel agonist LSP1-2111 with anxiolytic, but not antidepressant-like activity, mediated by serotonergic and GABAergic systems. Neuropharmacology 2010, 59:627-634.
132. Wu S.M., Tan K.S., Chen H., Beh T.T., Yeo H.C., Ng S.K.-L., Wei S., Lee D.-Y., Choo A.B.-H., Chan K.K.-K. Enhanced production of neuroprogenitors dopaminergic neurons and identification of target genes by overexpression of sonic hedgehog in human embryonic stem cells. Stem Cells Dev 2012, 21:729-741.
133. Xiong K., Luo D.-W., Patrylo P.R., Luo X.-G., Struble R.G., Clough R.W., Yan X.-X. Doublecortin-expressing cells are present in layer II across the adult guinea pig cerebral cortex: partial colocalization with mature interneuron markers. Exp Neurol 2008, 211:271-282.
134. Zucker R.S., Delaney K.R., Mulkey R., Tank D.W. Presynaptic calcium in transmitter release and posttetanic potentiation. Ann N Y Acad Sci 1991, 635:191-207.
135. Zuckerman L., Weiner I. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J Psychiatry Res 2005, 39:311-323.