Effect of systemic kynurenine on cortical spreading depression and its modulation by sex hormones in rat

Experimental Neurology

Volumn 236, Issue 2, 2012, Pages 207-214

  Chauvel, Virginie ^a   Vamos, Eniko ^b   Pardutz, Arpad ^b   Vecsei, Laszlo ^b   Schoenen, Jean ^a   Multon, Sylvie ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Cortical spreading depression; Kynurenine; Migraine; Sex hormones

Indexed keywords

AMINO ACID; KYNURENIC ACID; KYNURENINE; POTASSIUM CHLORIDE; PROBENECID; SEX HORMONE; SODIUM CHLORIDE;

AMINO ACID BRAIN LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; ESTRUS CYCLE; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; OCCIPITAL CORTEX; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SPRAGUE DAWLEY RAT; SPREADING CORTICAL DEPRESSION; VAGINA SMEAR;

ANIMALS; CEREBRAL CORTEX; CORTICAL SPREADING DEPRESSION; FEMALE; GONADAL STEROID HORMONES; INJECTIONS, INTRAPERITONEAL; KYNURENINE; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS;

EID: 84861722895     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.05.002     Document Type: Article

References (104)

1. Addae J.I., Ali N., Stone T.W. Effects of AMPA and clomethiazole on spreading depression cycles in the rat neocortex in vivo. Eur. J. Pharmacol. 2011, 653:41-46.
2. Atlas A., Gisslen M., Nordin C., Lindstrom L., Schwieler L. Acute psychotic symptoms in HIV-1 infected patients are associated with increased levels of kynurenic acid in cerebrospinal fluid. Brain Behav. Immun. 2007, 21:86-91.
3. Ayata C. Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29:1095-1114.
4. Ayata C., Moskowitz M.A. Cortical spreading depression confounds concentration-dependent pial arteriolar dilation during N-methyl-D-aspartate superfusion. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:1837-1841.
5. Ayata C., Jin H., Kudo C., Moskowitz M.A. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol. 2006, 54:652-661.
6. Bergerot A., Holland P.R., Akerman S., Bartsch T., Ahn A.H., Maassen Van Den Brink A., Reuter U., Schoenen J., Mitsikostas D.D., van den Maagdenberg A.M., Goasby P.J. Animal models of migraine: looking at the component parts of a complex disorder. Eur. J. Neurosci. 2006, 24:1517-1534.
7. Bethea C.L., Reddy A.P., Tokuyama Y., Henderson J.A., Lima F.B. Protective actions of ovarian hormones in the serotonin system of macaques. Front. Neuroendocrinol. 2009, 30:212-238.
8. Bogdanov V.B., Multon S., Chauvel V., Bogdanova O.V., Prodanov D., Makarchuk M.Y., Shoenen J. Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol. Dis. 2011, 41:430-435.
9. Bolay H., Reuter U., Dunn A.K., Huang Z., Boas D.A., Moskowitz M.A. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med. 2002, 8:136-142.
10. Brennan K.C., Romero Reyes M., Lopez Valdes H.E., Arnold A.P., Charles A.C. Reduced threshold for cortical spreading depression in female mice. Ann. Neurol. 2007, 61:603-606.
11. Brinton R.D., Proffitt P., Tran J., Luu R. Equilin, a principal component of the estrogen replacement therapy premarin, increases the growth of cortical neurons via an NMDA receptor-dependent mechanism. Exp. Neurol. 1997, 147:211-220.
12. Brown R.R., Thornton M.J., Price J.M. The effect of vitamin supplementation on the urinary excretion of tryptophan metabolites by pregnant women. J. Clin. Invest. 1961, 40:617-623.
13. Carpenedo R., Pittaluga A., Cozzi A., Attucci S., Galli A., Raiteri M., Moroni F. Presynaptic kynurenate-sensitive receptors inhibit glutamate release. Eur. J. Neurosci. 2001, 13:2141-2147.
14. Chiarugi A., Carpenedo R., Molina M.T., Mattoli L., Pellicciari R., Moroni F. Comparison of the neurochemical and behavioral effects resulting from the inhibition of kynurenine hydroxylase and/or kynureninase. J. Neurochem. 1995, 65:1176-1183.
15. Cunningham R.F., Israili Z.H., Dayton P.G. Clinical pharmacokinetics of probenecid. Clin. Pharmacokinet. 1981, 6:135-151.
16. Cyr M., Ghribi O., Di Paolo T. Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain. J. Neuroendocrinol. 2000, 12:445-452.
17. Dominguez R., Liu R., Baudry M. 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J. Neurochem. 2007, 101:232-240.
18. Eikermann-Haerter K., Dilekoz E., Kudo C., Savitz S.I., Waeber C., Baum M.J., van den Maagdenberg A.M., Moskowitz M.A., Ayata C. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J. Clin. Invest. 2009, 119:99-109.
19. Eliot A.C., Kirsch J.F. Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations. Annu. Rev. Biochem. 2004, 73:383-415.
20. Fabricius M., Jensen L.H., Lauritzen M. Microdialysis of interstitial amino acids during spreading depression and anoxic depolarization in rat neocortex. Brain Res. 1993, 612:61-69.
21. Fejes A., Párdutz A., Toldi J., Vécsei L. Kynurenine metabolites and migraine: experimental studies and therapeutic perspectives. Curr. Neuropharmacol. 2011, 9:376-387.
22. Freeman M.E. Neuroendocrine control of the ovarian cycle of the rat. Knobil and Neill's Physiology of Reproduction 2006, 2327-2388. Elsevier Academic Press. J.D. Neill (Ed.).
23. Frye C.A. Effects and mechanisms of progestogens and androgens in ictal activity. Epilepsia 2010, 3:135-140.
24. Frye C.A., Rhodes M.E. Female sex steroids and neuronal excitability. Encyclopedia of Basic Epilepsy Research 2009, Volume 1:477-484. Academic Press, Oxford.
25. Fukui S., Schwarcz R., Rapoport S.I., Takada Y., Smith Q.R. Blood-brain barrier transport of kynurenines: implications for brain synthesis and metabolism. J. Neurochem. 1991, 56:2007-2017.
26. Fumal A., Schoenen J. Current migraine management-patient acceptability and future approaches. Neuropsychiatr. Dis. Treat. 2008, 4:1043-1057.
27. Gazzaley A.H., Weiland N.G., McEwen B.S., Morrison J.H. Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J. Neurosci. 1996, 16:6830-6838.
28. Granella F., Sances G., Pucci E., Nappi R.E., Ghiotto N., Napp G. Migraine with aura and reproductive life events: a case control study. Cephalalgia 2000, 20:701-707.
29. Grilli M., Raiteri L., Patti L., Parodi M., Robino F., Raiteri M., Marchi M. Modulation of the function of presynaptic alpha7 and non-alpha7 nicotinic receptors by the tryptophan metabolites, 5-hydroxyindole and kynurenate in mouse brain. Br. J. Pharmacol. 2006, 149:724-732.
30. Guedes R.C., de Oliveira J.A., Amancio-Dos-Santos A., Garcia-Cairasco N. Sexual differentiation of cortical spreading depression propagation after acute and kindled audiogenic seizures in the Wistar audiogenic rat (WAR). Epilepsy Res. 2009, 83:207-214.
31. Guillemin G.J., Cullen K.M., Lim C.K., Smythe G.A., Garner B., Kapoor V., Takikawa O., Brew B.J. Characterization of the kynurenine pathway in human neurons. J. Neurosci. 2007, 27:12884-12892.
32. Guo S., Vecsei L., Ashina M. The L-kynurenine signalling pathway in trigeminal pain processing: a potential therapeutic target in migraine?. Cephalalgia 2011, 31:1029-1038.
33. Hadjikhani N., Sanchez Del Rio M., Wu O., Schwartz D., Bakker D., Fischi B., Kwong K.K., Cutrer F.M., Rosen B.R., Tootell R.B., Sorensen A.G., Moskowitz M.A. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4687-4692.
34. Haghir H., Kovac S., Speckmann E.J., Zilles K., Gorji A. Patterns of neurotransmitter receptor distributions following cortical spreading depression. Neuroscience 2009, 163:1340-1352.
35. Hilmas C., Pereira E.F., Alkondon M., Rassoulpour A., Schwarcz R., Albuquerque E.X. The brain metabolite kynurenic acid inhibits alpha7 nicotinic receptor activity and increases non-alpha7 nicotinic receptor expression: physiopathological implications. J. Neurosci. 2001, 21:7463-7473.
36. Ilzecka J., Kocki T., Stelmasiak Z., Turski W.A. Endogenous protectant kynurenic acid in amyotrophic lateral sclerosis. Acta Neurol. Scand. 2003, 107:412-418.
37. Kaube H., Herzog J., Kaufer T., Dichgans M., Diener H.C. Aura in some patients with familial hemiplegic migraine can be stopped by intranasal ketamine. Neurology 2000, 55:139-141.
38. Kessler M., Terramani T., Lynch G., Baudry M. A glycine site associated with N-methyl-D-aspartic acid receptors: characterization and identification of a new class of antagonists. J. Neurochem. 1989, 52:1319-1328.
39. Knyihar-Csillik E., Toldi J., Krisztin-Peva B., Chadaide Z., Nemeth H., Fenyo R., Vecsei L. Prevention of electrical stimulation-induced increase of c-fos immunoreaction in the caudal trigeminal nucleus by kynurenine combined with probenecid. Neurosci. Lett. 2007, 418:122-126.
40. Konradsson-Geuken A., Wu H.Q., Gash C.R., Alexander K.S., Campbell A., Sozeri Y., Pellicciari R., Schwarcz R., Bruno J.P. Cortical kynurenic acid bi-directionally modulates prefrontal glutamate levels as assessed by microdialysis and rapid electrochemistry. Neuroscience 2010, 169:1848-1859.
41. Koylu E., Demirgoren S., London E.D., Pogun S. Sex difference in up-regulation of nicotinic acetylcholine receptors in rat brain. Life Sci. 1997, 61:185-190.
42. Kravzov J., Santamaria A., Rios C., Flores A., Altagracia M. Protective effect of probenecid on circling behavior of rats with unilateral quinollinic acid induced striatal lesions. Proc. West. Pharmacol. Soc. 1993, 36:255-257.
43. Lambert J.J., Belelli D., Peden D.R., Vardy A.W., Peters J.A. Neurosteroid modulation of GABAA receptors. Prog. Neurobiol. 2003, 71:67-80.
44. Lauritzen M., Hansen A.J. The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J. Cereb. Blood Flow Metab. 1992, 12:223-229.
45. Lauritzen M., Olesen J. Regional cerebral blood flow during migraine attacks by Xenon-133 inhalation and emission tomography. Brain 1984, 107:447-461.
46. Lauritzen M., Rice M.E., Okada Y., Nicholson C. Quisqualate, kainate and NMDA can initiate spreading depression in the turtle cerebellum. Brain Res. 1988, 475:317-327.
47. Leao A. Spreading depression of activity in cerebral cortex. J. Neurophysiol. 1944, 7:159-390.
48. Leo L., Gherardini L., Barone V., De Fusco M., Pietrobon D., Pizzorusso T., Casari G. Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet. 2011, 7:e1002129.
49. Maggioni F., Alessi C., Maggino T., Zanchin G. Headache during pregnancy. Cephalalgia 1997, 17:765-769.
50. Magis D., Schoenen J. Treatment of migraine: update on new therapies. Curr. Opin. Neurol. 2011, 24:203-210.
51. Marcus D.A. Interrelationships of neurochemicals, estrogen, and recurring headache. Pain 1995, 62:129-139.
52. Marrannes R., Willems R., De Prins E., Wauquier A. Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res. 1988, 457:226-240.
53. Maurice T., Grégoire C., Espallergues J. Neuro(active)steroids actions at the neuromodulatory sigma1 (sigma1) receptor: biochemical and physiological evidences, consequences in neuroprotection. Pharmacol. Biochem. Behav. 2006, 84:581-597.
54. Michael A.F., Drummond K.N., Doeden D., Anderson J.A., Good R.A. Tryptophan metabolism in man. J. Clin. Invest. 1964, 43:1730-1746.
55. Milner P.M. Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalogr. Clin. Neurophysiol. 1958, 10:705.
56. Miranda A.F., Boegman R.J., Beninger R.J., Jhamandas K. Protection against quinolinic acid-mediated excitotoxicity in nigrostriatal dopaminergic neurons by endogenous kynurenic acid. Neuroscience 1997, 78:967-975.
57. Mochizuki T., Villemagne V.L., Scheffel U., Dannals R.F., Finley P., Zhan Y., Wagner H.N., Musachio J.L. Nicotine induced up-regulation of nicotinic receptors in CD-1 mice demonstrated with an in vivo radiotracer: gender differences. Synapse 1998, 30:116-118.
58. Monte-Guedes C.K., Alves E.V., Viana-da-Silva E., Guedes R.C. Chronic treatment with ascorbic acid enhances cortical spreading depression in developing well-nourished and malnourished rats. Neurosci. Lett. 2011, 496:191-194.
59. Moroni F., Carpenedo R., Cozzi A., Meli E., Chiarugi A., Pellegrini-Giampietro D.E. Studies on the neuroprotective action of kynurenine mono-oxygenase inhibitors in post-ischemic brain damage. Adv. Exp. Med. Biol. 2003, 527:127-136.
60. Moskowitz M.A. The neurobiology of vascular head pain. Ann. Neurol. 1984, 16:157-168.
61. Moskowitz M.A., Nozaki K., Kraig R.P. Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci. 1993, 13:1167-1177.
62. Nellgard B., Wieloch T. NMDA-receptor blockers but not NBQX, an AMPA-receptor antagonist, inhibit spreading depression in the rat brain. Acta Physiol. Scand. 1992, 146:497-503.
63. Nemeth H., Robotka H., Kis Z., Rozsa E., Janaky T., Somlai T., Marosi M., Farkas T., Toldi J., Vescei L. Kynurenine administered together with probenecid markedly inhibits pentylenetetrazol-induced seizures. An electrophysiological and behavioural study. Neuropharmacology 2004, 47:916-925.
64. Nilsson L.K., Nordin C., Jonsson E.G., Engberg G., Linderholm K.R., Erhardt S. Cerebrospinal fluid kynurenic acid in male and female controls-correlation with monoamine metabolites and influences of confounding factors. J. Psychiatr. Res. 2007, 41:144-151.
65. Oxenkrug G.F. Genetic and hormonal regulation of tryptophan kynurenine metabolism: implications for vascular cognitive impairment, major depressive disorder, and aging. Ann. N. Y. Acad. Sci. 2007, 1122:35-49.
66. Párdutz A., Fejes A., Bohár Z., Tar L., Toldi J., Vécsei L. Kynurenines and headache. J. Neural Transm. 2012, 119:285-296.
67. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elsevier Academic Press. sixth ed.
68. Perkins M.N., Stone T.W. An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res. 1982, 247:184-187.
69. Pertovaara M., Raitala A., Uusitalo H., Pukander J., Helin H., Oja S.S., Hurme M. Mechanisms dependent on tryptophan catabolism regulate immune responses in primary Sjogren's syndrome. Clin. Exp. Immunol. 2005, 142:155-161.
70. Rasmussen B.K., Olesen J. Migraine with aura and migraine without aura: an epidemiological study. Cephalalgia 1992, 12:221-228.
71. Rasmussen B.K., Jensen R., Schroll M., Olesen J. Epidemiology of headache in a general population-a prevalence study. J. Clin. Epidemiol. 1991, 44:1147-1157.
72. Redecker C., Wang W., Fritschy J.M., Witte O.W. Widespread and long-lasting alterations in GABA(A)-receptor subtypes after focal cortical infarcts in rats: mediation by NMDA-dependent processes. J. Cereb. Blood Flow Metab. 2002, 22:1463-1475.
73. Rose D.P. The influence of oestrogens on tryptophan metabolism in man. Clin. Sci. 1966, 31:265-272.
74. Rose D.P., Braidman I.P. Excretion of tryptophan metabolites as affected by pregnancy, contraceptive steroids, and steroid hormones. Am. J. Clin. Nutr. 1971, 24:673-683.
75. Rossi F., Valentina C., Garavaglia S., Sathyasaikumar K.V., Schwarcz R., Kojima S., Okuwaki K., Ono S., Kajii Y., Rizzi M. Crystal structure-based selective targeting of the pyridoxal 5'-phosphate dependent enzyme kynurenine aminotransferase II for cognitive enhancement. J. Med. Chem. 2010, 53:5684-5689.
76. Russell M.B., Olesen J. Migrainous disorder and its relation to migraine without aura and migraine with aura. A genetic epidemiological study. Cephalalgia 1996, 16:431-435.
77. Saad A.A., Abdel-Tawab G.A., El-Zoghby S.M., Mostafa M.H., Moursi G.E. Relationship between pyridoxal phosphate and some synthetic oestrogens in their effect on kynurenine hydrolase and kynurenine aminotransferase enzymes of normal mouse liver. Biochem. Pharmacol. 1974, 23:999-1013.
78. Sachs M., Pape H.C., Speckmann E.J., Gorji A. The effect of estrogen and progesterone on spreading depression in rat neocortical tissues. Neurobiol. Dis. 2007, 25:27-34.
79. Santamaria A., Rios C., Solis-Hernandez F., Ordaz-Moreno J., Gonzalez-Reynoso L., Altagracia M., Kravkov J. Systemic DL-kynurenine and probenecid pretreatment attenuates quinolinic acid-induced neurotoxicity in rats. Neuropharmacology 1996, 35:23-28.
80. Schwarcz R., Pellicciari R. Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J. Pharmacol. Exp. Ther. 2002, 303:1-10.
81. Silberstein S.D. Preventive migraine treatment. Neurol. Clin. 2009, 27:429-443.
82. Silva-Adaya D., Perez-De La Cruz V., Villeda-Hernandez J., Carrillo-Mora P., Gonzalez-Herrera I.G., Garcia E., Colin-Barenque L., Santamaria A. Protective effect of l-kynurenine and probenecid on 6-hydroxydopamine-induced striatal toxicity in rats: implications of modulating kynurenate as a protective strategy. Neurotoxicol. Teratol. 2011, 33:303-312.
83. Silverman W., Locovei S., Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 2008, 295:C761-C767.
84. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 2001, 81:1065-1096.
85. Sone K., Yamamoto-Sawamura T., Kuwahara S., Nishijima K., Ohno T., Aoyama H., Tanaka S. Changes of estrous cycles with aging in female F344/n rats. Exp. Anim. 2007, 56:139-148.
86. Stone T.W., Forrest C.M., Mackay G.M., Stoy N., Darlington L.G. Tryptophan, adenosine, neurodegeneration and neuroprotection. Metab. Brain Dis. 2007, 22:337-352.
87. Tang B., Ji Y., Traub R.J. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain 2008, 137:540-549.
88. Taylor D.L., Urenjak J., Zilkha E., Obrenovitch T.P. Effects of probenecid on the elicitation of spreading depression in the rat striatum. Brain Res. 1997, 764:117-125.
89. Tottene A., Conti R., Fabbro A., Vecchia D., Shapovalova M., Santello M., van den Maagdenberg A.M., Ferrari M.D., Pietrobon D. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009, 61:762-773.
90. Urenjak J., Obrenovitch T.P., Zilkha E. Effect of probenecid on depolarizations evoked by N-methyl-D-aspartate (NMDA) in the rat striatum. Naunyn Schmiedebergs Arch. Pharmacol. 1997, 355:36-42.
91. Vamos E., Pardutz A., Fejes A., Tajti J., Toldi J., Vecsei L. Modulatory effects of probenecid on the nitroglycerin-induced changes in the rat caudal trigeminal nucleus. Eur. J. Pharmacol. 2009, 621:33-37.
92. Vamos E., Pardutz A., Klivenyi P., Toldi J., Vecsei L. The role of kynurenines in disorders of the central nervous system: possibilities for neuroprotection. J. Neurol. Sci. 2009, 283:21-27.
93. Vamos E., Pardutz A., Varga H., Bohar Z., Tajti J., Fulop F., Vesei L. l-kynurenine combined with probenecid and the novel synthetic kynurenic acid derivative attenuate nitroglycerin-induced nNOS in the rat caudal trigeminal nucleus. Neuropharmacology 2009, 57:425-429.
94. Vamos E., Voros K., Zadori D., Vecsei L., Klivenyi P. Neuroprotective effects of probenecid in a transgenic animal model of Huntington's disease. J. Neural Transm. 2009, 116:1079-1086.
95. van den Maagdenberg A.M., Pietrobon D., Pizzorusso T., Kaja S., Broos L.A., Cesetti T., van de Ven R.C., Tottene A., van der Kaa J., Plomp J., Ferrari M.D. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710.
96. Vecsei L., Miller J., MacGarvey U., Beal M.F. Kynurenine and probenecid inhibit pentylenetetrazol- and NMDLA-induced seizures and increase kynurenic acid concentrations in the brain. Brain Res. Bull. 1992, 28:233-238.
97. Világi I., Klapka N., Luhmann H.J. Optical recording of spreading depression in rat neocortical slices. Brain Res. 2001, 898:288-296.
98. Widner B., Sepp N., Kowald E., Ortner U., Wirleitner B., Fritsch P., Baier-Bitterlich G. Enhanced tryptophan degradation in systemic lupus erythematosus. Immunobiology 2000, 201:621-630.
99. Wolf H., Walter S., Brown R.R., Arend R.A. Effect of natural oestrogens on tryptophan metabolism: evidence for interference of oestrogens with kynureninase. Scand. J. Clin. Lab. Invest. 1980, 40:15-22.
100. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 1992, 12:2549-2554.
101. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336:293-306.
102. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J. Neurosci. 1994, 14:7680-7687.
103. Zadori D., Klivenyi P., Vamos E., Fulop F., Toldi J., Vecsei L. Kynurenines in chronic neurodegenerative disorders: future therapeutic strategies. J. Neural Transm. 2009, 116:1403-1409.
104. Zhu W.H., Lu C.Z., Huang Y.M., Link H., Xiao B.G. A putative mechanism on remission of multiple sclerosis during pregnancy: estrogen-induced indoleamine 2,3-dioxygenase by dendritic cells. Mult. Scler. 2007, 13:33-40.