Absence of aryl hydrocarbon receptors increases endogenous kynurenic acid levels and protects mouse brain against excitotoxic insult and oxidative stress

Journal of Neuroscience Research

Volumn 93, Issue 9, 2015, Pages 1423-1433

  García Lara, Lucia ^a   Pérez Severiano, Francisca ^b   González Esquivel, Dinora ^b   Elizondo, Guillermo ^a   Segovia, José ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

Author keywords

Aryl hydrocarbon receptor; Excitotoxicity; neuroprotection; Kynurenic acid; Kynurenine

Indexed keywords

4 AMINOBUTYRIC ACID; AROMATIC HYDROCARBON RECEPTOR; KYNURENIC ACID; QUINOLINIC ACID; REACTIVE OXYGEN METABOLITE; ACYLTRANSFERASE; AHR PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; TRYPTOPHAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOMORPHINE TEST; ARTICLE; BRAIN; BRAIN TISSUE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS STRIATUM; EXCITOTOXICITY; HUNTINGTON CHOREA; KNOCKOUT MOUSE; LIPID ANALYSIS; MALE; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ROTAROD TEST; WILD TYPE; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES;

ACETYLTRANSFERASES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; KYNURENIC ACID; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES; OXIDATIVE STRESS; QUINOLINIC ACID; RECEPTORS, ARYL HYDROCARBON; TRYPTOPHAN;

EID: 84948064003     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23595     Document Type: Article

References (66)

1. Abedi Mukutenga P, Taghzouti K, Bengelloun WA. 2012. Effects of bilateral electrolytic lesions of the dorsomedial striatum on motor behavior and instrumental learning in rats. Basic Clin Neurosci 3:52-59.
2. Alexander KS, Pocivavsek A, Wu HQ, Pershing ML, Schwarcz R, Bruno JP. 2013. Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine. Neuroscience 238:19-28.
3. Amaral M, Outeiro TF, Scrutton NS, Giorgini F. 2013. The causative role and therapeutic potential of the kynurenine pathway in neurodegenerative disease. J Mol Med 91:705-713.
4. Arregui L, Segovia J. 2004. Molecular strategies for the treatment of Huntington's disease. Curr Pharmacogenomics 2:299-311.
5. Arregui L, Benitez JA, Razgado LF, Vergara P, Segovia J. 2011. Adenoviral astrocyte-specific expression of BDNF in the striata of mice transgenic for Huntington's disease delays the onset of the motor phenotype. Cell Mol Neurobiol 31:1229-1243.
6. Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng PF, Kavalali ET, Monteggia LM. 2011. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475:91-95.
7. Ballard ED, Ionescu DF, Vande Voort JL, Niciu MJ, Richards EM, Luckenbaugh DA, Brutsche NE, Ameli R, Furey ML, Zarate CA Jr. 2014. Improvement in suicidal ideation after ketamine infusion: relationship to reductions in depression and anxiety. J Psychiatr Res 58:161-166.
8. Beal MF, Matson WR, Swartz KJ, Gamache PH, Bird ED. 1990. Kynurenine pathway measurements in Huntington's disease striatum: evidence for reduced formation of kynurenic acid. J Neurochem 55:1327-1339.
9. Beal MF, Matson WR, Storey E, Milbury P, Ryan EA, Ogawa T, Bird ED. 1992. Kynurenic acid concentrations are reduced in Huntington's disease cerebral cortex. J Neurol Sci 108:80-87.
10. 2+ transients and contributes to the kynurenic acid-dependent reduction of synaptic activity at CA3-CA1 synapses. PLoS One 8:e82180.
11. Cao Y, Gu ZL, Lin F, Han R, Qin ZH. 2005. Caspase-1 inhibitor Ac-YVAD-CHO attenuates quinolinic acid-induced increases in p53 and apoptosis in rat striatum. Acta Pharmacol Sin 26:150-154.
12. Carpenedo R, Pittaluga A, Cozzi A, Attucci S, Galli A, Raiteri M, Moroni F. 2001. Presynaptic kynurenate-sensitive receptors inhibit glutamate release. Eur J Neurosci 13:2141-2147.
13. Cepeda C, Ariano MA, Calvert CR, Flores-Hernandez J, Chandler SH, Leavitt BR, Hayden MR, Levine MS. 2001. NMDA receptor function in mouse models of Huntington disease. J Neurosci Res 66:525-539.
14. 3H]kynurenine in the developing rat brain in vivo: effect of intrastriatal ibotenate injections. Brain Res Dev Brain Res 100:73-81.
15. Diaz-Barriga F, Carrizales L, Yanez L, Hernandez JM, Dominguez Robles MC, Palmer E, Saborio JL. 1989. Interaction of cadmium with actin microfilaments in vitro. Toxicol In Vitro 3:277-284.
16. DiNatale BC, Murray IA, Schroeder JC, Flaveny CA, Lahoti TS, Laurenzana EM, Omiecinski CJ, Perdew GH. 2010. Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicol Sci 115:89-97.
17. Erhardt S, Schwieler L, Nilsson L, Linderholm K, Engberg G. 2007. The kynurenic acid hypothesis of schizophrenia. Physiol Behav 92:203-209.
18. Estrada-Sanchez AM, Montiel T, Segovia J, Massieu L. 2009. Glutamate toxicity in the striatum of the R6/2 Huntington's disease transgenic mice is age-dependent and correlates with decreased levels of glutamate transporters. Neurobiol Dis 34:78-86.
19. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, Kimura S, Nebert DW, Rudikoff S, Ward JM, Gonzalez FJ. 1995. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268:722-726.
20. Filbrandt CR, Wu Z, Zlokovic B, Opanashuk L, Gasiewicz TA. 2004. Presence and functional activity of the aryl hydrocarbon receptor in isolated murine cerebral vascular endothelial cells and astrocytes. Neurotoxicology 25:605-616.
21. Gal EM, Sherman AD. 1978. Synthesis and metabolism of L-kynurenine in rat brain. J Neurochem 30:607-613.
22. Garcia-Tovar CG, Luna J, Mena R, Soto-Zarate CI, Cortes R, Perez A, Leon-Avila G, Mornet D, Rendon A, Hernandez JM. 2002. Dystrophin isoform Dp7l is present in lamellipodia and focal complexes in human astrocytoma cells U-373 MG. Acta Histochem 104:245-254.
23. 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.
24. Guidetti P, Okuno E, Schwarcz R. 1997. Characterization of rat brain kynurenine aminotransferases I and II. J Neurosci Res 50:457-465.
25. Guidetti P, Reddy PH, Tagle DA, Schwarcz R. 2000. Early kynurenergic impairment in Huntington's disease and in a transgenic animal model. Neurosci Lett 283:233-235.
26. Guidetti P, Bates GP, Graham RK, Hayden MR, Leavitt BR, MacDonald ME, Slow EJ, Wheeler VC, Woodman B, Schwarcz R. 2006. Elevated brain 3-hydroxykynurenine and quinolinate levels in Huntington disease mice. Neurobiol Dis 23:190-197.
27. 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.
28. Hardeland R, Zsizsik BK, Poeggeler B, Fuhrberg B, Holst S, Coto-Montes A. 1999. Indole-3-pyruvic and -propionic acids, kynurenic acid, and related metabolites as luminophores and free-radical scavengers. Adv Exp Med Biol 467:389-395.
29. Herve C, Beyne P, Jamault H, Delacoux E. 1996. Determination of tryptophan and its kynurenine pathway metabolites in human serum by high-performance liquid chromatography with simultaneous ultraviolet and fluorimetric detection. J Chromatogr B Biomed Appl 675:157-161.
30. Hilgier W, Kocki T, Obara-Michlewska M, Turski WA, Oja SS, Saransaari P, Albrecht J. 2014. Modulation by kynurenine of extracellular kynurenate and glutamate in cerebral cortex of rats with acute liver failure. Pharmacol Rep 66:466-470.
31. Jauch D, Urbanska EM, Guidetti P, Bird ED, Vonsattel JP, Whetsell WO Jr, Schwarcz R. 1995. Dysfunction of brain kynurenic acid metabolism in Huntington's disease: focus on kynurenine aminotransferases. J Neurol Sci 130:39-47.
32. Lalonde R, Bensoula AN, Filali M. 1995. Rotorod sensorimotor learning in cerebellar mutant mice. Neurosci Res 22:423-426.
33. Leipnitz G, Schumacher C, Scussiato K, Dalcin KB, Wannmacher CM, Wyse AT, Dutra-Filho CS, Wajner M, Latini A. 2005. Quinolinic acid reduces the antioxidant defenses in cerebral cortex of young rats. Int J Dev Neurosci 23:695-701.
34. Li L, Fan M, Icton CD, Chen N, Leavitt BR, Hayden MR, Murphy TH, Raymond LA. 2003. Role of NR2B-type NMDA receptors in selective neurodegeneration in Huntington disease. Neurobiol Aging 24:1113-1121.
35. Lievens JC, Woodman B, Mahal A, Spasic-Boscovic O, Samuel D, Kerkerian-Le Goff L, Bates GP. 2001. Impaired glutamate uptake in the R6 Huntington's disease transgenic mice. Neurobiol Dis 8:807-821.
36. Lin CH, Chen CC, Chou CM, Wang CY, Hung CC, Chen JY, Chang HW, Chen YC, Yeh GC, Lee YH. 2009. Knockdown of the aryl hydrocarbon receptor attenuates excitotoxicity and enhances NMDA-induced BDNF expression in cortical neurons. J Neurochem 111:777-789.
37. Luthi-Carter R, Apostol BL, Dunah AW, DeJohn MM, Farrell LA, Bates GP, Young AB, Standaert DG, Thompson LM, Cha JH. 2003. Complex alteration of NMDA receptors in transgenic Huntington's disease mouse brain: analysis of mRNA and protein expression, plasma membrane association, interacting proteins, and phosphorylation. Neurobiol Dis 14:624-636.
38. Mishra J, Kumar A. 2014. Improvement of mitochondrial function by paliperidone attenuates quinolinic acid-induced behavioural and neurochemical alterations in rats: implications in Huntington's disease. Neurotox Res 26:363-81.
39. Moroni F, Cozzi A, Sili M, Mannaioni G. 2012. Kynurenic acid: a metabolite with multiple actions and multiple targets in brain and periphery. J Neural Transm 119:133-139.
40. Nebert DW, Dalton TP, Okey AB, Gonzalez FJ. 2004. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279:23847-23850.
41. Nozaki K, Beal MF. 1992. Neuroprotective effects of L-kynurenine on hypoxia-ischemia and NMDA lesions in neonatal rats. J Cereb Blood Flow Metab 12:400-407.
42. Obara-Michlewska M, Tuszynska P, Albrecht J. 2013. Ammonia upregulates kynurenine aminotransferase II mRNA expression in rat brain: a role for astrocytic NMDA receptors? Metab Brain Dis 28:161-165.
43. Ogura T, Ogata M, Akita H, Jitsuki S, Akiba L, Noda K, Hoka S, Saji M. 2005. Impaired acquisition of skilled behavior in rotarod task by moderate depletion of striatal dopamine in a presymptomatic stage model of Parkinson's disease. Neurosci Res 51:299-308.
44. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, Schumacher T, Jestaedt L, Schrenk D, Weller M, Jugold M, Guillemin GJ, Miller CL, Lutz C, Radlwimmer B, Lehmann I, von Deimling A, Wick W, Platten M. 2011. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478:197-203.
45. Paxinos G, Franklin KBJ. 2008. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
46. Perez-Neri I, Montes S, Boll MC, Ramirez-Bermudez J, Rios C. 2004. Liquid chromatographic-fluorimetric method for the estimation of nitric oxide biosynthesis in the central nervous system. J Chromatogr B Anal Technol Biomed Life Sci 806:133-139.
47. Perez-Severiano F, Escalante B, Rios C. 1998. Nitric oxide synthase inhibition prevents acute quinolinate-induced striatal neurotoxicity. Neurochem Res 23:1297-1302.
48. Perez-Severiano F, Rios C, Segovia J. 2000. Striatal oxidative damage parallels the expression of a neurological phenotype in mice transgenic for the mutation of Huntington's disease. Brain Res 862:234-237.
49. Perez-Severiano F, Montes S, Geronimo-Olvera C, Segovia J. 2013. Study of oxidative damage and antioxidant systems in two Huntington's disease rodent models. Methods Mol Biol 1010:177-200.
50. Petersen SL, Curran MA, Marconi SA, Carpenter CD, Lubbers LS, McAbee MD. 2000. Distribution of mRNAs encoding the arylhydrocarbon receptor, arylhydrocarbon receptor nuclear translocator, and arylhydrocarbon receptor nuclear translocator-2 in the rat brain and brainstem. J Comp Neurol 427:428-439.
51. Pineda-Farias JB, Perez-Severiano F, Gonzalez-Esquivel DF, Barragan-Iglesias P, Bravo-Hernandez M, Cervantes-Duran C, Aguilera P, Rios C, Granados-Soto V. 2013. The L-kynurenine-probenecid combination reduces neuropathic pain in rats. Eur J Pain 17:1365-1373.
52. Rodriguez-Sosa M, Elizondo G, Lopez-Duran RM, Rivera I, Gonzalez FJ, Vega L. 2005. Over production of IFN-gamma and IL-12 in AhR-null mice. FEBS Lett 579:6403-6410.
53. Salvati P, Ukmar G, Dho L, Rosa B, Cini M, Marconi M, Molinari A, Post C. 1999. Brain concentrations of kynurenic acid after a systemic neuroprotective dose in the gerbil model of global ischemia. Prog Neuropsychopharmacol Biol Psychiatry 23:741-752.
54. Santamaria A, Rios C. 1993. MK-801, an N-methyl-D-aspartate receptor antagonist, blocks quinolinic acid-induced lipid peroxidation in rat corpus striatum. Neurosci Lett 159:51-54.
55. Saran T, Hilgier W, Urbanska EM, Turski WA, Albrecht J. 2004. Kynurenic acid synthesis in cerebral cortical slices of rats with progressing symptoms of thioacetamide-induced hepatic encephalopathy. J Neurosci Res 75:436-440.
56. Schwarcz R, Whetsell WO Jr, Mangano RM. 1983. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science 219:316-318.
57. Schwarcz R, Okuno E, White RJ, Bird ED, Whetsell WO Jr. 1988. 3-Hydroxyanthranilate oxygenase activity is increased in the brains of Huntington disease victims. Proc Natl Acad Sci U S A 85:4079-4081.
58. Schwarcz R, Bruno JP, Muchowski PJ, Wu HQ. 2012. Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 13:465-477.
59. Sherrard RM. 2011. Cerebellar control of fine motor function. Animal models of movement disorders. New York: Humana Press. p 263-279.
60. Shibata K. 1988. Fluorimetric microdetermination of kynurenic acid, an endogenous blocker of neurotoxicity, by high-performance liquid chromatography. J Chromatogr 430:376-380.
61. Speciale C, Schwarcz R. 1990. Uptake of kynurenine into rat brain slices. J Neurochem 54:156-163.
62. Stoy N, Mackay GM, Forrest CM, Christofides J, Egerton M, Stone TW, Darlington LG. 2005. Tryptophan metabolism and oxidative stress in patients with Huntington's disease. J Neurochem 93:611-623.
63. Tavares RG, Tasca CI, Santos CE, Alves LB, Porciuncula LO, Emanuelli T, Souza DO. 2002. Quinolinic acid stimulates synaptosomal glutamate release and inhibits glutamate uptake into astrocytes. Neurochem Int 40:621-627.
64. 2+ injection. J Neurochem 42:976-980.
65. Zadori D, Nyiri G, Szonyi A, Szatmari I, Fulop F, Toldi J, Freund TF, Vecsei L, Klivenyi P. 2011. Neuroprotective effects of a novel kynurenic acid analogue in a transgenic mouse model of Huntington's disease. J Neural Transm 118:865-875.
66. Zeron MM, Hansson O, Chen N, Wellington CL, Leavitt BR, Brundin P, Hayden MR, Raymond LA. 2002. Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33:849-860.