Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro

Journal of Neuroscience

Volumn 25, Issue 26, 2005, Pages 6127-6136

  Sinagra, Mélanie ^a   Verrier, Danièle ^a   Frankova, Daniela ^b   Korwek, Kimberly M ^c   Blahos, Jaroslav ^b   Weeber, Edwin J ^c   Manzoni, Olivier J ^a   Chavis, Pascale ^a  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ApoER2; Hippocampus; Maturation; NMDA receptor; Reelin; VLDLR

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; APOLIPOPROTEIN E2; LOW DENSITY LIPOPROTEIN RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; REELIN; SCLEROPROTEIN; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MATURATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO DEVELOPMENT; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MOUSE; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL CULTURE TECHNIQUES; CULTURE MEDIA; EXTRACELLULAR MATRIX PROTEINS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTEGRINS; MICE; NERVE TISSUE PROTEINS; NEURONS; RECEPTORS, LDL; RECEPTORS, LIPOPROTEIN; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE ENDOPEPTIDASES;

EID: 21544442844     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1757-05.2005     Document Type: Article

References (43)

1. Alcantara S, Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779-7799.
2. Ali DW, Salter MW (2001) NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11:336-342.
3. Arnaud L, Ballif BA, Forster E, Cooper JA (2003) Fyn tyrosine kinase is a critical regulator of Disabled-1 during brain development. Curr Biol 13:9-17.
4. Audinat E, Lambolez B, Rossier J, Crepel F (1994) Activity-dependent regulation of N-methyl-D-aspartate receptor subunit expression in rat cerebellar granule cells. Eur J Neurosci 6:1792-1800.
5. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353.
6. Beffert U, Stolt PC, Herz J (2004) Functions of lipoprotein receptors in neurons. J Lipid Res 45:403-409.
7. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Sudhof TC (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531.
8. Bock HH, Herz J (2003) Reelin activates SRC family tyrosine kinases in neurons. Curr Biol 13:18-26.
9. Chavis P, Westbrook G (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411:317-321.
10. Chun D, Gall CM, Bi X, Lynch G (2001) Evidence that integrins contribute to multiple stages in the consolidation of long-term potentiation in rat hippocampus. Neuroscience 105:815-829.
11. D'Arcangelo G, Curran T (1998) Reeler: new tales on an old mutant mouse. BioEssays 20:235-244.
12. D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T (1997) Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 17:23-31.
13. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.
14. Dityatev A, Schachner M (2003) Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4:456-468.
15. Drakew A, Deller T, Heimrich B, Gebhardt C, Del Turco D, Tielsch A, Forster E, Herz J, Frotscher M (2002) Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp Neurol 176:12-24.
16. Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds α3β1 integrin and inhibits neuronal migration. Neuron 27:33-44.
17. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695-701.
18. Herz J, Goldstein JL, Strickland DK, Ho YK, Brown MS (1991) 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J Biol Chem 266:21232-21238.
19. Heynen AJ, Quinlan EM, Bae DC, Bear MF (2000) Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28:527-536.
20. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of Disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.
21. 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.
22. Jossin Y, Ogawa M, Metin C, Tissir F, Goffinet AM (2003) Inhibition of SRC family kinases and nonclassical protein kinases C induce a reeler-like malformation of cortical plate development. J Neurosci 23:9953-9959.
23. Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert de Rouvroit C, Goffinet AM (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 24:514-521.
24. Lacor PN, Grayson DR, Auta J, Sugaya I, Costa E, Guidotti A (2000) Reelin secretion from glutamatergic neurons in culture is independent from neurotransmitter regulation. Proc Natl Acad Sci USA 97:3556-3561.
25. Lambert de Rouvrait C, de Bergeyck V, Cortvrindt C, Bar I, Eeckhout Y, Goffinet AM (1999) Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp Neurol 156:214-217.
26. Legendre P, Rosenmund C, Westbrook GL (1993) Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13:674-684.
27. Miyata T, Nakajima K, Mikoshiba K, Ogawa M (1997) Regulation of Purkinje cell alignment by Reelin as revealed with CR-50 antibody. J Neurosci 17:3599-3609.
28. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
29. Nakajima K, Mikoshiba K, Miyata T, Kudo C, Ogawa M (1997) Disruption of hippocampal development in vivo by CR-50 mAb against Reelin. Proc Natl Acad Sci USA 94:8196-8201.
30. Niu S, Renfro A, Quattrocchi CC, Sheldon M, D'Arcangelo G (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ ApoER2-Dab1 pathway. Neuron 41:71-84.
31. Quinlan EM, Lebel D, Brash I, Barkai E (2004) A molecular mechanism for stabilization of learning-induced synaptic modifications. Neuron 41:185-192.
32. Scotti AL, Herrmann G (2002) Reelin immunoreactivity in dissociated cultures of the postnatal hippocampus. Brain Res 924:209-218.
33. Senzaki K, Ogawa M, Yagi T (1999) Proteins of the CNR family are multiple receptors for Reelin. Cell 99:635-647.
34. Thibault G (2000) Sodium dodecyl sulfate-stable complexes of echistatin and RGD-dependent integrins: a novel approach to study integrins. Mol Pharmacol 58:1137-1145.
35. Triller A, Choquet D (2005) Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28:133-139.
36. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689-701.
37. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR (1998) Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79:555-566.
38. Weeber EJ, Beffert U, Jones C, Christian JM, Forster E, Sweatt JD, Herz J (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277:39944-39952.
39. Wenthold RJ, Prybylowski K, Standley S, Sans N, Petralia RS (2003) Trafficking of NMDA receptors. Annu Rev Pharmacol Toxicol 43:335-358.
40. Wenzel A, Fritschy JM, Mohler H, Benke D (1997) NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469-478.
41. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44:851-859.
42. 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.
43. Yu XM, Askalan R, Keil II GJ, Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.