Inhibition of NMDA Receptors Induces Delayed Neuronal Maturation and Sustained Proliferation of Progenitor Cells during Neocortical Development

Journal of Neuroscience Research

Volumn 74, Issue 5, 2003, Pages 676-687

  Hirasawa, Takae ^a   Wada, Hidenori ^a   Kohsaka, Shinichi ^a   Uchino, Shigeo ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

BrdU; D APV; Neocortex; NMDA receptor; Notch signaling

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; BROXURIDINE; CALCIUM; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN DERIVATIVE; PROTEIN HES5; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; BRAIN VENTRICLE; CELL COUNT; CELL LABELING; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; IMAGING; LONG TERM EXPOSURE; NEOCORTEX; NERVE CELL; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; RECEPTOR BLOCKING; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIVISION; CELL MOVEMENT; CELLS, CULTURED; EMBRYO; EXCITATORY AMINO ACID ANTAGONISTS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEOCORTEX; NEURONS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS;

EID: 0344862095     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10795     Document Type: Article

References (42)

1. Artavanis-Tsakonas S, Rand MD, Lake RJ. 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770-776.
2. Ascher P, Nowak L. 1986. Calcium permeability of the channels activated by N-methyl-D-aspartate (NMDA) in isolated mouse central neurons. J Physiol 377:35.
3. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL. 1999. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449-4461.
4. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
5. Brooks WJ, Petit TL, LeBoutillier JC. 1997. Effect of chronic administration of NMDA antagonists on synaptic development. Synapse 26:104-113.
6. Burgoyne RD, Graham ME, Cambray-Deakin M. 1993. Neurotrophic effects of NMDA receptor activation on developing cerebellar granule cells. J Neurocytol 22:689-695.
7. Cameron HA, McEwen BS, Gould E. 1995. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-4692.
8. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
9. Carter C, Rivy JP, Scatton B. 1989. Ifenprodil and SL82.0715 are antagonists at the polyamine site of the N-methyl-D-aspartate (NMDA) receptor. Eur J Pharmacol 164:611-612.
10. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA. 1995. Cloning and characterization of χ-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15:6498-6508.
11. Gould E, Cameron HA, McEwen BS. 1994. Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J Comp Neurol 340:551-565.
12. Haydar TF, Wang F, Schwartz ML, Rakic P. 2000. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20:5764-5774.
13. Hirai H, Launey T. 2000. The regulatory connection between the activity of granule cell NMDA receptors and dendritic differentiation of cerebellar Purkinje cells. J Neurosci 20:5217-5224.
14. Hirasawa T, Nakamura K, Mizushima A, Morita M, Ezawa I, Miyakawa H, Kudo Y. 2000. Adverse effects of an active fragment of parathyroid hormone on rat hippocampal organotypic cultures. Br J Pharmacol 129: 21-28.
15. Hoffmann H, Gremme T, Hatt H, Gottmann K. 2000. Synaptic activity-dependent developmental regulation of NMDA receptor subunit expression in cultured neocortical neurons. J Neurochem 75: 1590-1599.
16. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
17. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vöckler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW. 1999. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283:70-74.
18. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
19. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
20. Li JH, Wang YH, Wolfe BB, Krueger KE, Corsi L, Stocca G, Vicini S. 1998. Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur J Neurosci 10:1704-1715.
21. Lipton SA, Kater SB. 1989. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 12:265-270.
22. LoTurco JJ, Owens DF, Heath MJS, Davis MBE, Kriegstein AR. 1995. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
23. Malenka RC, Nicoll RA. 1993. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trend Neurosci 16:521-527.
24. Maric D, Liu, QY, Grant GM, Andereadis JD, Hu Q, Chang YH, Barker JL, Pancrazio JJ, Stenger DA, Ma W. 2000. Functional ionotropic glutamate receptors emerge during terminal cell division and early neuronal differentiation of rat neuroepithelial cells. J Neurosci Res 61:652-662.
25. Marret S, Gressens P, Evrard P. 1996. Arrest of neuronal migration by excitatory amino acids in hamster developing brain. Proc Natl Acad Sci USA 93:15463-15468.
26. 2+ of NMDA responses in spinal cord neurons. Nature 309:261-263.
27. McKinney RA, Lüthi A, Bandtlow CE, Gähwiler BH, Thompson SM. 1999. Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures. Proc Natl Acad Sci USA 96:11631-11636.
28. Monti B, Contestabile A. 2000. Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur J Neurosci 12:3117-3123.
29. Monyer H, Burnashev N, Laurie D, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
30. Mori H, Mishina M. 1995. Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219-1237.
31. Nacher J, Rosell DR, Alonso-Llosa G, McEwen BS. 2001. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 13:512-520.
32. Nadarajah B, Parnavelas JG. 2002. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432.
33. Nishi M, Hinds H, Lu HP, Kawata M, Hayashi Y. 2001. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 21: RC185.
34. 2+ after exposure to glutamate receptor agonists. Exp Brain Res 73:447-458.
35. Ohtsuka T, Sakamoto M, Guillemot F, Kageyama R. 2001. Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J Biol Chem 276:30467-30474.
36. Rossi DJ, Slater NT. 1993. The developmental onset of NMDA receptor-channel activity during neuronal migration. Neuropharmacology 32:1239-1248.
37. Sugiura N, Patel RG, Corriveau RA. 2001. N-methyl-D-aspartate receptors regulate a group of transiently expressed genes in the developing brain. J Biol Chem 276:14257-14263.
38. Vallano ML. 1998. Developmental aspects of NMDA receptor function. Neurobiology 12:177-204.
39. Watanabe M, Inoue Y, Sakimura K, Mishina M. 1992. Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3:1138-1140.
40. Weinmaster G. 1997. The ins and outs of Notch signaling. Mol Cell Neurosci 9:91-102.
41. Williams K, Russell SL, Shen YM, Molinoff PB. 1993. Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
42. Wu G-Y, Malinow R, Cline HT. 1996. Maturation of a central glutamatergic synapse. Science 274:972-976.