Dynorphin up-regulation in the dentate granule cell mossy fiber pathway following chronic inhibition of GluN2B-containing NMDAR is associated with increased CREB (Ser 133) phosphorylation, but is independent of BDNF/TrkB signaling pathways

Molecular and Cellular Neuroscience

Volumn 60, Issue , 2014, Pages 63-71

  Rittase, W Bradley ^a   Dong, Yu ^a   Barksdale, DaRel ^a   Galdzicki, Zygmunt ^a   Bausch, Suzanne B ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Hippocampus; Ifenprodil; Memantine; N methyl d aspartate; Neuropeptide Y

Indexed keywords

4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DYNORPHIN; IFENPRODIL; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPEPTIDE Y; 2 AMINO 5 PHOSPHONOVALERIC ACID; NR2B NMDA RECEPTOR; PHENOL DERIVATIVE; PIPERIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GRANULE CELL; LONG TERM EXPOSURE; MOSSY FIBER; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SEIZURE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HIPPOCAMPAL MOSSY FIBER; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; SPRAGUE DAWLEY RAT;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DYNORPHINS; MEMANTINE; MOSSY FIBERS, HIPPOCAMPAL; NEUROPEPTIDE Y; PHENOLS; PHOSPHORYLATION; PIPERIDINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84900036827     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.04.002     Document Type: Article

References (101)

1. Aguirre C.C., Baudry M. Progesterone reverses 17β-estradiol-mediated neuroprotection and BDNF induction in cultured hippocampal slices. Eur. J. Neurosci. 2009, 29:447-454.
2. Andersson G., Påhlman S., Parrow V., Johansson I., Hammerling U. Activation of the human NPY gene during neuroblastoma cell differentiation: induced transcriptional activities of AP-1 and AP-2. Cell Growth Differ. 1994, 5:27-36.
3. Bannister A.J., Kouzarides T. The CBP co-activator is a histone acetyltransferase. Nature 1996, 384:641-643.
4. Baraban S.C. Neuropeptide Y and epilepsy: recent progress, prospects and controversies. Neuropeptides 2004, 38:261-265.
5. Barksdale D.M., Dong Y., Galdzicki Z., Bausch S.B. Differential effects of NR2B selective versus general NMDAR antagonists on CREB phosphorylation and downstream expression of neuropeptides. Soc. Neurosci. Abstr. Program 2004, 49:10.
6. Barria A., Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 2005, 48:289-301.
7. Bausch S.B., Patterson T.A., Appleyard S.M., Chavkin C. Immunocytochemical localization of delta opioid receptors in mouse brain. J. Chem. Neuroanat. 1995, 8:175-189.
8. Bausch S.B., Esteb T.M., Terman G.W., Chavkin C. Administered and endogenously released kappa opioids decrease pilocarpine-induced seizures and seizure-induced histopathology. J. Pharmacol. Exp. Ther. 1998, 284:1147-1155.
9. Binder D.K., Routbort M.J., Ryan T.E., Yancopoulos G.D., McNamara J.O. Selective inhibition of kindling development by intraventricular administration of TrkB receptor body. J. Neurosci. 1999, 19:1424-1436.
10. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy: too much of a good thing?. Trends Neurosci. 2001, 24:47-53.
11. Carlezon W.A., Thome J., Olson V.G., Lane-Ladd S.B., Brodkin E.S., Hiroi N., Duman R.S., Neve R.L., Nestler E.J. Regulation of cocaine reward by CREB. Science 1998, 282:2272-2275.
12. Carlezon W.A., Duman R.S., Nestler E.J. The many faces of CREB. Trends Neurosci. 2005, 28:436-445.
13. Chance W.T., Sheriff S., Peng F., Ambikaipakan B. Antagonism of NPY-induced feeding by pretreatment with cyclic AMP response element binding protein antisense oligonucleotide. Neuropeptides 2000, 34:167-172.
14. Chazot P.L., Lawrence S., Thompson C.L. Studies on the subtype selectivity of CP-101,606: evidence for two classes of NR2B-selective NMDA receptor antagonists. Neuropharmacology 2002, 42:319-324.
15. Chen L., Huang L. Dynorphin block of N-methyl-d-aspartate channels increases with peptide length. J. Pharmacol. Exp. Ther. 1998, 284:826-831.
16. Chen L., Gu Y., Huang L. The mechanism of action for the block of NMDA receptor channels by the opioid peptide dynorphin. J. Neurosci. 1995, 15:4602-4611.
17. 2+-responsive transcription in neurons. J. Neurosci. 2003, 23:2572-2581.
18. Chen M., Lu T.J., Chen X.J., Zhou Y., Chen Q., Feng X.Y., Xu L., Duan W.H., Xiong Z.Q. Differential roles of NMDA receptor subtypes in ischemic neuronal cell death and ischemic tolerance. Stroke 2008, 39:3042-3048.
19. Chenard B.L., Shalaby I.A., Koe B.K., Ronau R.T., Butler T.W., Prochniak M.A., Schmidt A.W., Fox C.B. Separation of alpha 1 adrenergic and N-methyl-d-aspartate antagonist activity in a series of ifenprodil compounds. J. Med. Chem. 1991, 34:3085-3090.
20. Chrivia J.C., Kwok R.P., Lamb N., Hagiwara M., Montminy M.R., Goodman R.H. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 1993, 365:855-859.
21. 2+ channels in rat and mouse cultured hippocampal pyramidal neurones: comparison with N-methyl-d-aspartate receptor antagonist actions. Br. J. Pharmacol. 1994, 113:499-507.
22. Cole R.L., Konradi C., Douglass J., Hyman S.E. Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 1995, 14:813-823.
23. Colmers W.F., Lukowiak K., Pittman Q.J. Presynaptic action of neuropeptide Y in area CA1 of the rat hippocampus. J. Physiol. 1987, 383:285-299.
24. Colmers W.F., Lukowiak K., Pittman Q.J. Neuropeptide Y action in the rat hippocampal slice: site and mechanism of presynaptic inhibition. J. Neurosci. 1988, 8:3827-3837.
25. Croll S.D., Wiegand S.J., Anderson K.D., Lindsay R.M., Nawa H. Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF. Eur. J. Neurosci. 1994, 6:1343-1353.
26. Croll S.D., Chesnutt C.R., Greene N.A., Linday R.M., Wiegand S.J. Peptide immunoreactivity in aged rat cortex and hippocampus as a function of memory and BDNF infusion. Pharmacol. Biochem. Behav. 1999, 64:625-635.
27. 2+/calmodulin-as well as cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:5061-5065.
28. Dong Y., Pi X., Rosenberg H.C. Seizure induced calcineurin activation and long-lasting reduction of CREB phosphorylation. Soc. Neurosci. Abstr. Program 2002, 791:3.
29. Douglass J., McKinzie A.A., Pollock K.M. Identification of multiple DNA elements regulating basal and protein kinase A-induced transcriptional expression of the rat prodynorphin gene. Mol. Endocrinol. 1994, 8:333-344.
30. Drake C.T., Terman G.W., Simmons M.L., Milner T.A., Kunkel D.D., Schwartzkroin P.A., Chavkin C. Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. J. Neurosci. 1994, 14:3736-3750.
31. Finkbeiner S., Tavazoie S.F., Maloratsky A., Jacobs K.M., Harris K.M., Greenberg M.E. CREB: a major mediator of neuronal neurotrophin responses. Neuron 1997, 19:1031-1047.
32. Flint A.C., Maisch U.S., Weishaupt J.H., Kriegstein A.R., Monyer H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci. 1997, 17:2469-2476.
33. Foulkes N.S., Borrelli E., Sassone-Corsi P. CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 1991, 64:739-749.
34. Gill R., Chang P.K., Prenosil G.A., Deane E.C., McKinney R.A. Blocking brain-derived neurotrophic factor inhibits injury-induced hyperexcitability of hippocampal CA3 neurons. Eur. J. Neurosci. 2013, 38:3554-3566.
35. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
36. Gray J.A., Shi Y., Usui H., During M.J., Sakimura K., Nicoll R.A. Distinct modes of AMPA receptor suppression at developing synapses by GluN2A and GluN2B: single-cell NMDA receptor subunit deletion in vivo. Neuron 2011, 71:1085-1101.
37. Groc L., Heine M., Cousins S.L., Stephenson F.A., Lounis B., Cognet L., Choquet D. NMDA receptor surface mobility depends on NR2A-2B subunits. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18769-18774.
38. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002, 5:405-414.
39. Harris A.Z., Pettit D.L. Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices. J. Physiol. 2007, 584:509-519.
40. Hatton C.J., Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 2005, 46:261-274.
41. He X.P., Kotloski R., Nef S., Luikart B.W., Parada L.F., McNamara J.O. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 2004, 43:31-42.
42. He S., Shao L.R., Wang Y., Bausch S.B. Synaptic and extrasynaptic plasticity in glutamatergic circuits involving dentate granule cells following chronic N-methyl-d-aspartate receptor inhibition. J. Neurophysiol. 2013, 109:1535-1547.
43. Higuchi H., Yang H.Y., Sabol S.L. Rat neuropeptide Y precursor gene expression. mRNA structure, tissue distribution, and regulation by glucocorticoids, cyclic AMP, and phorbol ester. J. Biol. Chem. 1988, 263:6288-6295.
44. 2+/calmodulin-dependent transcriptional activation of neuropeptide Y gene induced by membrane depolarization: determination of Ca(2+)- and cyclic AMP/phorbol 12-myristate 13-acetate-responsive elements. J. Neurochem. 1996, 66:1802-1809.
45. Hsu S.-M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 1981, 29:577-580.
46. Jiang Y., Jakovcevski M., Bharadwaj R., Connor C., Schroeder F.A., Lin C.L., Straubhaar J., Martin G., Akbarian S. Setdb1 histone methyltransferase regulates mood-related behaviors and expression of the NMDA receptor subunit NR2B. J. Neurosci. 2010, 30:7152-7167.
47. Kaynard A.H., McMurray C.T., Douglass J., Curry T.E., Melner M.H. Regulation of prodynorphin gene expression in the ovary: distal DNA regulatory elements confer gonadotropin regulation of promoter activity. Mol. Endocrinol. 1992, 6:2244-2256.
48. Klapstein G.J., Colmers W.F. Neuropeptide Y suppresses epileptiform activity in rat hippocampus in vitro. J. Neurophysiol. 1997, 78:1651-1661.
49. Kokaia M., Ernfors P., Kokaia Z., Elmer E., Jaenisch R., Lindvall O. Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol. 1995, 133:215-224.
50. Koyama R., Yamada M.K., Fujisawa S., Katoh-Semba R., Matsuki N., Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. J. Neurosci. 2004, 24:7215-7224.
51. Lauterborn J.C., Pineda E., Chen L.Y., Ramirez E.A., Lynch G., Gall C.M. Ampakines cause sustained increases in brain-derived neurotrophic factor signaling at excitatory synapses without changes in AMPA receptor subunit expression. Neuroscience 2009, 159:283-295.
52. Lavezzari G., McCallum J., Dewey C.M., Roche K.W. Subunit-specific regulation of NMDA receptor endocytosis. J. Neurosci. 2004, 24:6383-6391.
53. Liu X.-B., Murray K.D., Jones E.G. Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci. 2004, 24:8885-8895.
54. Liu Y., Wong T.P., Aarts M., Rooyakkers A., Liu L., Lai T.W., Wu D.C., Lu J., Tymianski M., Craig A.M., Wang Y.T. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 2007, 27:2846-2857.
55. Lonze B.E., Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002, 35:605-623.
56. Malmber A.B., Chen C., Tonegawa S., Basbaum A.I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCγ. Science 1997, 278:279-283.
57. McCool B.A., Lovinger D.M. Ifenprodil inhibition of the 5-hydroxytryptamine3 receptor. Neuropharmacology 1995, 34:621-629.
58. McGinty J.F., Bohler W.T., Patterson T.A., Chavkin C. Kappa receptor immunoreactivity is present in cells and fibers of the rat forebrain. Regul. Pept. 1994, 54:185-186.
59. Minth C.D., Dixon J.E. Expression of the human neuropeptide Y gene. J. Biol. Chem. 1990, 265:12933-12939.
60. Montminy M.R., Sevarino K.A., Wagner J.A., Mandel G., Goodman R.H. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:6682-6686.
61. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994, 12:529-540.
62. Nawa H., Bessho Y., Carnahan J., Nakanishi S., Mizuno K. Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor. J. Neurochem. 1993, 60:772-775.
63. Patrylo P.R., van den Pol A.N., Spencer D.D., Williamson A. NPY inhibits glutamatergic excitation in the epileptic human dentate gyrus. J. Neurophysiol. 1999, 82:478-483.
64. Pickel V.M., Chan J., Sesack S.R. Cellular substrates for interactions between dynorphin terminals and dopamine dendrites in rat ventral tegmental area and substantia nigra. Brain Res. 1993, 602:275-289.
65. Pierce J.P., Kurucz O.S., Milner T.A. Morphometry of a peptidergic transmitter system: dynorphin B-like immunoreactivity in the rat hippocampal mossy fiber pathway before and after seizures. Hippocampus 1999, 9:255-276.
66. Pizzorusso T., Ratto G.M., Putignano E., Maffei L. Brain-derived neurotrophic factor causes cAMP response element-binding protein phosphorylation in absence of calcium increases in slices and cultured neurons from rat visual cortex. J. Neurosci. 2000, 20:2809-2816.
67. 2+ signals evoked by coincident EPSPs and back-propagating action potentials in CA1 pyramidal neurons. Brain Res. 2006, 1104:45-54.
68. Rauner C., Köhr G. Triheteromeric NR1/NR2A/NR2B receptors constitute the major N-methyl-d-aspartate receptor population in adult hippocampal synapses. J. Biol. Chem. 2011, 286:7558-7566.
69. Rex C.S., Lauterborn J.C., Lin C.Y., Kramár E.A., Rogers G.A., Gall C.M., Lynch G. Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J. Neurophysiol. 2006, 96:677-685.
70. Rex C.S., Lin C.Y., Kramár E.A., Chen L.Y., Gall C.M., Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J. Neurosci. 2007, 27:3017-3029.
71. Richichi C., Lin E.-J.D., Stefanin D., Colella D., Ravizza T., Grignaschi G., Veglianese P., Sperk G., During M.J., Vezzani A. Anticonvulsant and antiepileptogenic effects mediated by adeno-associated virus vector neuropeptide Y expression in the rat hippocampus. J. Neurosci. 2004, 24:3051-3059.
72. Rittase W.B., Barksdale D.M., Bausch S.B. Up-regulation of dynorphin in the dentate granule cell mossy fiber pathway following chronic treatment with NR2B-selective NMDAR antagonists is not dependent on BDNF. Soc. Neurosci. Abstr. Program 2008, 129:20.
73. Sato K., Akaishi T., Matsuki N., Ohno Y., Nakazawa K. β-Estradiol induces synaptogenesis in the hippocampus by enhancing brain-derived neurotrophic factor release from dentate gyrus granule cells. Brain Res. 2007, 1150:108-120.
74. Sheng M., Thompson M.A., Greenberg M.E. Creba Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 1991, 252:1427-1430.
75. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994, 368:144-147.
76. Shieh P.B., Hu S.C., Bobb K., Timmusk T., Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 1998, 20:727-740.
77. Shirayama Y., Muneoka K.T., Iwata M., Ishida H., Hazama G., Kawahara R. Pregnenolone and dehydroepiandrosterone administration in neonatal rats alters the immunoreactivity of hippocampal synapsin I, neuropeptide Y and glial fibrillary acidic protein at post-puberty. Neuroscience 2005, 133:147-157.
78. Shukla V.K., Lemaire S. Non-opioid effects of dynorphins: possible role of the NMDA receptor. Trends Pharmacol. Sci. 1994, 15:420-424.
79. Simmons M.L., Chavkin C. κ-Opioid receptor activation of a dendrotoxin-sensitive potassium channel mediates presynaptic inhibition of mossy fiber neurotransmitter release. Mol. Pharmacol. 1996, 50:80-85.
80. Simmons M.L., Chavkin C. Endogenous opioid regulation of hippocampal function. Int. Rev. Neurobiol. 1996, 39:146-197.
81. Simonato M., Romualdi P. Dynorphin and epilepsy. Prog. Neurobiol. 1996, 50:557-583.
82. Stoppini L., Buchs P.-A., Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 1991, 37:173-182.
83. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 1994, 8:2527-2539.
84. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998, 20:709-726.
85. Tao X., West A.E., Chen W.G., Corfas G., Greenberg M.E. A calcium-responsive transcription factor, CaRF, that regulates neuronal activity-dependent expression of BDNF. Neuron 2002, 33:383-395.
86. Terasaki Y., Sasaki T., Yagita Y., Okazaki S., Sugiyama Y., Oyama N., Omura-Matsuoka E., Sakoda S., Kitagawa K. Activation of NR2A receptors induces ischemic tolerance through CREB signaling. J. Cereb. Blood Flow Metab. 2010, 8:1441-1449.
87. Terman G.W., Drake C.T., Simmons M.L., Milner T.A., Chavkin C. Opioid modulation of recurrent excitation in the hippocampal dentate gyrus. J. Neurosci. 2000, 20:4379-4388.
88. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M., Persson H. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 1993, 10:475-489.
89. Tortella F.C. Endogenous opioid peptides and epilepsy: quieting the seizing brain. Trends Pharmacol. Sci. 1988, 9:366-372.
90. Tovar K.R., Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 1999, 19:4180-4188.
91. Tyler W.J., Pozzo-Miller L.D. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 2001, 21:4249-4258.
92. Vicini S., Wang J.F., Li J.H., Zhu W.J., Wang Y.H., Luo J.H., Wolfe B.B., Grayson D.R. Functional and pharmacological differences between recombinant N-methyl-d-aspartate receptors. J. Neurophysiol. 1998, 79:555-566.
93. Wagner J.J., Caudle R.M., Chavkin C. Kappa-opioids decrease excitatory transmission in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 1992, 12:132-141.
94. Wagner J.J., Terman G.W., Chavkin C. Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 1993, 363:451-454.
95. Wang X.-M., Bausch S.B. Effects of distinct classes of N-methyl-d-aspartate receptor antagonists on seizures, axonal sprouting and neuronal loss in vitro: suppression by NR2B-selective antagonists. Neuropharmacology 2004, 47:1008-1020.
96. Wang Y., Bausch S.B. In contrast to NR2B-selective antagonists, chronic treatment with NR2A-selective or non-subunit selective antagonists reduced interneuron survival and GAD65/67 expression. Soc. Neurosci. Abstr. Program 2006, 278:16.
97. Weisskopf M.G., Zalutsky R.A., Nicoll R.A. The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 1993, 362:423-427.
98. Wyllie D.J., Livesey M.R., Hardingham G.E. Influence of GluN2 subunit identity on NMDA receptor function. Neuropharmacology 2013, 74:4-17.
99. Xapelli S., Bernardino L., Ferreira R., Grade S., Silva A.P., Salgado J.R., Cavadas C., Grouzmann E., Poulsen F.R., Jakobsen B., Oliveira C.R., Zimmer J., Malva J.O. Interaction between neuropeptide Y (NPY) and brain-derived neurotrophic factor in NPY-mediated neuroprotection against excitotoxicity: a role for microglia. Eur. J. Neurosci. 2008, 27:2089-2102.
100. Yamakura T., Shimoji K. Subunit- and site-specific pharmacology of the NMDA receptor channel. Prog. Neurobiol. 1999, 59:279-298.
101. Zhou Q., Sheng M. NMDA receptors in nervous system diseases. Neuropharmacology 2013, 74:69-75.