Expression of NMDA receptors and Ca-impermeable AMPA receptors requires neuronal differentiation and allows discrimination between two different types of neural stem cells

Cellular Physiology and Biochemistry

Volumn 26, Issue 6, 2010, Pages 935-946

  Muth Köhne, Elke ^a   Pachernegg, Svenja ^a   Karus, Michael ^a   Faissner, Andreas ^a   Hollmann, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

AMPA receptor; Ionotropic glutamate receptors; NEPs; Neurogenesis; Neuronal differentiation; NMDA receptor; NSCs; Retinoic acid

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL CELL; ARTICLE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NEURAL STEM CELL; NEUROEPITHELIUM; NEUROTRANSMISSION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RECEPTOR UPREGULATION;

EID: 78651251370     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000324002     Document Type: Article

References (49)

1. Durand GM, Kovalchuk Y, Konnerth A: Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996;381:71-75. (Pubitemid 26130004)
2. Gasparini S, Saviane C, Voronin LL, Cherubini E: Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc Natl Acad Sci USA 2000;97:9741-9746.
3. Isaac JT, Crair MC, Nicoll RA, Malenka RC: Silent synapses during development of thalamocortical inputs. Neuron 1997;18:269-280.
4. Wu G, Malinow R, Cline HT: Maturation of a central glutamatergic synapse. Science 1996;274:972-976.
5. Ben-Ari Y: Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002;3:728-739. (Pubitemid 135706678)
6. Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL: GABAA, NMDA and AMPA receptors: a developmentally regulated 'menage a trois'. Trends Neurosci 1997;20:523-529.
7. Khazipov R, Ragozzino D, Bregestovski P: Kinetics and Mg2+ block of N-methyl-D-aspartate receptor channels during postnatal development of hippocampal CA3 pyramidal neurons. Neuroscience 1995;69:1057-1065.
8. Pickard L, Noel J, Henley JM, Collingridge GL, Molnar E: Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci 2000;20:7922-7931.
9. Hagimura N, Tsuzuki K, Iino M, Takatsuru Y, Yoshida Y, Kishi S, Ozawa S: Predominant expression of GluR2 among the AMPA receptor subunits in neuronal progenitor cells of the rat hippocampus. Brain Res Dev Brain Res 2004;152:213-223.
10. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR: GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995;15:1287-1298.
11. Maric D, Liu QY, Grant GM, Andreadis JD, Hu Q, Chang YH, Barker JL, Joseph J, Stenger DA, Ma W: Functional ionotropic glutamate receptors emerge during terminal cell division and early neuronal differentiation of rat neuroepithelial cells. J Neurosci Res 2000;61:652-662.
12. Sah DW, Ray J, Gage FH: Regulation of voltage- and ligand-gated currents in rat hippocampal progenitor cells in vitro. J Neurobiol 1997;32:95-110.
13. Rumpel S, Hatt H, Gottmann K: Silent synapses in the developing rat visual cortex: evidence for postsynaptic expression of synaptic plasticity. J Neurosci 1998;18:8863-8874.
14. Liao D, Scannevin RH, Huganir R: Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J Neurosci 2001;21:6008-6017.
15. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL: Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 1999;2:37-43.
16. Groc L, Gustafsson B, Hanse E: AMPA signalling in nascent glutamatergic synapses: there and not there! Trends Neurosci 2006;29:132-139.
17. Ying QL, Stavridis M, Griffiths D, Li M, Smith A: Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 2003;21:183-186.
18. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A: Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005;3:e283.
19. Haubensak W, Attardo A, Denk W, Huttner WB: Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 2004;101:3196-3201.
20. Miyata T, Kawaguchi A, Okano H, Ogawa M: Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001;31:727-741.
21. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR: Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001;409:714-720.
22. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR: Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004;7:136-144.
23. Muth-Kohne E, Terhag J, Pahl S, Werner M, Joshi I, Hollmann M: Functional excitatory GABAA receptors precede ionotropic glutamate receptors in radial glia-like neural stem cells. Mol Cell Neurosci 2010;43:209-221.
24. Aubert J, Stavridis MP, Tweedie S, O'Reilly M, Vierlinger K, Li M, Ghazal P, Pratt T, Mason JO, Roy D, Smith A: Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc Natl Acad Sci USA 2003;100:11836-11841.
25. Stavridis MP, Smith AG: Neural differentiation of mouse embryonic stem cells. Biochem Soc Trans 2003;31:45-49.
26. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
27. Rougon G, Dubois C, Buckley N, Magnani JL, Zollinger W: A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J Cell Biol 1986;103:2429-2437.
28. Takahashi J, Palmer TD, Gage FH: Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol 1999;38:65-81.
29. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N: Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 1994;347:150-160.
30. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH: Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994;12:529-540.
31. Douyard J, Shen L, Huganir RL, Rubio ME: Differential neuronal and glial expression of GluR1 AMPA receptor subunit and the scaffolding proteins SAP97 and 4.1N during rat cerebellar development. J Comp Neurol 2007;502:141-156.
32. Riquelme R, Miralles CP, De Blas AL: Bergmann glia GABA(A) receptors concentrate on the glial processes that wrap inhibitory synapses. J Neurosci 2002;22:10720-10730.
33. Ripellino JA, Neve RL, Howe JR: Expression and heteromeric interactions of non-N-methyl-D-aspartate glutamate receptor subunits in the developing and adult cerebellum. Neuroscience 1998;82:485-497.
34. Hall BJ, Ghosh A: Regulation of AMPA receptor recruitment at developing synapses. Trends Neurosci 2008;31:82-89.
35. Zhu JJ, Esteban JA, Hayashi Y, Malinow R: Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci 2000;3:1098-1106.
36. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A: Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716.
37. Gotz M: Glial cells generate neurons- master control within CNS regions: developmental perspectives on neural stem cells. Neuroscientist 2003;9:379-397.
38. Hartfuss E, Galli R, Heins N, Gotz M: Characterization of CNS precursor subtypes and radial glia. Dev Biol 2001;229:15-30.
39. Umesono K, Giguere V, Glass CK, Rosenfeld MG, Evans RM: Retinoic acid and thyroid hormone induce gene expression through a common responsive element. Nature 1988;336:262-265.
40. Gleeson JG, Lin PT, Flanagan LA, Walsh CA: Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999;23:257-271.
41. Doetsch F: The glial identity of neural stem cells. Nat Neurosci 2003;6:1127-1134. (Pubitemid 37346029)
42. Steindler DA, Laywell ED: Astrocytes as stem cells: nomenclature, phenotype, and translation. Glia 2003;43:62-69.
43. Bear MF, Malenka RC: Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 1994;4:389-399.
44. Bliss TV, Collingridge GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993;361:31-39.
45. Stevens CF, Sullivan J: Synaptic plasticity. Curr Biol 1998;8:R151-153.
46. Tovar KR, Westbrook GL: The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 1999;19:4180-4188.
47. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA: Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 2009;62:254-268.
48. Seeburg PH, Higuchi M, Sprengel R: RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res Brain Res Rev 1998;26:217-229.
49. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.