Q- and L-type calcium channels control the development of calbindin phenotype in hippocampal pyramidal neurons in vitro

European Journal of Neuroscience

Volumn 12, Issue 6, 2000, Pages 2068-2078

  Boukhaddaoui, Hassan ^a   Sieso, Victor ^a   Scamps, Frédérique ^a   Vigues, Stephan ^a   Roig, Anne ^a   Valmier, Jean ^a  

^a INSERM   (France)

Author keywords

Depolarization; High potassium; Intracellular calcium concentration; Phenotype differentiation; Rat

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALCIUM; CALCIUM CHANNEL; GLUTAMIC ACID; NEUROTRANSMITTER; POTASSIUM CHLORIDE;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CALCIUM TRANSPORT; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR CALCIUM; HIPPOCAMPUS; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, Q-TYPE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; HIPPOCAMPUS; NITRENDIPINE; OMEGA-AGATOXIN IVA; OMEGA-CONOTOXIN GVIA; PHENOTYPE; POTASSIUM CHLORIDE; PREGNANCY; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0034119758     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00105.x     Document Type: Article

References (50)

1. Airaksinen, M.S., Eilers, J., Garaschuk, O., Thoenen, H., Konnerth, A. & Meyer, M. (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Nutl Acad. Sci. USA, 94, 1488-1493.
2. Bading, H., Ginty, D.D. & Greenberg, M.E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science, 260, 181-186.
3. Baimbridge, K.G., Celio, M.R. & Rogers, J.H. (1992) Calcium-binding proteins in the nervous system. Trends Neurosci., 15, 303-308.
4. Ben-Ari, Y., Cherubini, E., Corradetti, R. & Gaiarsa, J.L. (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurons. J. Physiol. (Lond.), 416, 303-325.
5. Birnbaumer, L., Campbell, K.P., Catterall, W.A., Harpold, M.M., Hofmann, F., Horne, W.A., Mori, Y., Schwartz, A., Snutch, T.P., Tanabe, T. (1994) The naming of Voltage-gated calcium channels. Neuron, 13, 505-506.
6. Bourinet, E., Soong, T.W., Sutton, K., Slaymaker, S., Mathews, E., Monteil, A., Zamponi, G.W., Nargeot, J. & Snutch, T.P. (1999) Splicing of alpha 1A subunit gene generates phenotypic variants of P-and Q-type calcium channels. Nature Neurosci., 2, 407-415.
7. Caceres, A., Banker, G.A. & Binder, L. (1986) Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci., 6, 714-722.
8. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475.
9. Chameau, P., Lucas, P., Melliti, K., Bournaud, R. & Shimahara, T. (1999) Development of multiple calcium channel types in cultured mouse hippocampal neurons. Neuroscience, 90, 383-388.
10. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Bioehem., 162, 156-159.
11. Collazo, D., Takahashi, H. & McKay, R.D.G. (1992) Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron, 9, 643-656.
12. 2+ transients in developing hippocampai pyramidal cells. J. Neurobiol., 25, 243-251.
13. Dreyfus, C.F., Friedman, W.J., Markey, K.A. & Black, I.B. (1986) Depolarizing stimuli increase tyrosine hydroxylase in the mouse locus coeruleus in culture. Brain Res., 379, 216-222.
14. 2+ channels in mammalian central neurons. Trends Neurosci., 18, 89-98.
15. Enderlin, S., Norman, A.W. & Celio, M.R. (1987) Ontogeny of the calcium binding protein calbindin D-28k in the rat nervous system. Anat. Embryol. (Berl.), 177, 15-28.
16. Ghosh, A., Carnahan, J. & Greenberg, M.E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science, 263, 1618-1623.
17. Ghosh, A. & Greenberg, M.E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science, 268, 239-247.
18. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem., 260, 3440-3450.
19. 2+ transients. Nature, 375, 784-787.
20. Hillman, D., Chen, S., Aung, T.T., Cherksey, B., Sugimori, M. & Llinas, R.R. (1991) Localization of P-type calcium channels in the central nervous system. Proc. Natl Acad. Sci. USA, 88, 7076-7080.
21. Ip, N.Y., Li, Y., Yancopoulos, G.D. & Lindsay, R.M. (1993) Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci, 13, 3394-3405.
22. Katz, L.C. & Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133-1138.
23. Köhr, G. & Mody, I. (1991) Endogenous intracellular calcium buffering and the activation/inactivation of HVA calcium currents in rat dentate gyrus granule cells. J. Gen. Physiol., 98, 941-967.
24. Komuro, H. & Rakic, P. (1992) Selective role of N-type calcium channels in neuronal migration. Science, 257, 806-809.
25. Lee, S., Williamson, J., Lothman, E.W., Von Szele, F.G., Chesselet, M.F., Hagen, S., Sapolsky, R.M., Mattson, M.P. & Christakos, S. (1997) Early induction of mRNA for calbindin-D28k and BDNF but not NT-3 in rat hippocampus after kainic acid treatment. Brain Res. Mol. Brain Res., 47, 183-194.
26. Lledo, P.M., Somasundaram, B., Morton, A.J., Emson, P.C. & Mason, W.T. (1992) Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron, 9, 943-954.
27. Lowenstein, D.H., Miles, M.F., Hatam, F. & McCabe, T. (1991) Upregulation of calbindin-D28K mRNA in the rat hippocampus following focal stimulation of the perforant path. Neuron, 6, 627-633.
28. Luiten, P.C., Buwalda, B., Traber, J. & Nyakas, C. (1994) Induction of enhanced postnatal expression of immunoreactive calbindin-D28k in rat forebrain by the calcium antagonist nimodipine. Brain Res. Dev. Brain Res., 79, 10-18.
29. Malison, M.P. & Barger, S.W. (1993) Roles for calcium signaling in structural plasticity and pathology in the hippocampal system. Hippocampus, 3. 73-87.
30. Mattson, M.P., Rychlik, B., Chu, C. & Christakos, S. (1991) Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron, 6, 41-51.
31. Mintz, I.M., Venema, V.J., Swiderek, K.M., Lee, T.D., Bean, B.P. & Adams, M.E. (1992) P-type calcium channels blocked by the spider toxin ω-Aga-IVA. Nature, 355, 827-829.
32. Molinari, S., Battini, R., Ferrari, S., Pozzi, L., Killcross, A.S., Robbins, T.W., Jouvenceau, A., Billard, J.M., Dutar, P., Lamour, Y., Baker, W.A., Cox, H. & Emson, P.C. (1996) Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D28K expression. Proc. Natl Acad. Sci. USA, 93, 8028-8033.
33. Moody, W.J. (1998) Control of spontaneous activity during development. J. Neurobiol., 37, 97-109.
34. Ozawa, S., Tsuzuki, K., Iino, M., Ogura, A. & Kudo, Y. (1989) Three types of voltage-dependenl calcium current in cultured rat hippocampal neurons. Brain Res., 495, 329-336.
35. Perez-Reyes, E. (1998) Molecular characterization of a novel family of low voltage-aclivated, T-type, calcium channels. J. Bioener. Biomembr., 30, 313-318.
36. Perez-Reyes, E. & Schneider, T. (1994) Calcium channels: structure, function, and classification. Drug Dev. Res., 33, 295-318.
37. 2+ channel currents in rat cerebellar granule neurons. J. Neurosci., 15, 2995-3012.
38. Scamps, F., Valentin, S., Dayanithi, G. & Valmier, J. (1998) Calcium channel subtypes responsible for voltage-gated intracellular calcium elevations in embryonic rat motoneurons. Neuroscience, 87, 719-730.
39. Scholz, K. & Miller, R.J. (1995) Developmental changes in presynaptic calcium channels coupled to glutamate release in cultured rat hippocampal neurons. J. Neurosci., 15, 4612-4617.
40. Sheng, M., McFadden, G. & Greenberg, M.E. (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron, 4, 571-582.
41. 2+ channels in fetal rat hippocampal neurons: implications for neurite morphogenesis in vitro. J. Neurosci., 16, 6476-6489.
42. Spitzer, N.C. (1991) A developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation. J. Neurobiol., 22, 659-673.
43. 2+ spikes and waves in embryonic neurons: signaling systems for differentiation. Trends Neurosci., 17, 115-118.
44. Starr, T.V., Prystay, W. & Snutch, T.P. (1991) Primary structure of a calcium channel that is highly expressed in the rat cerebellum. Proc. Natl Acad. Sci. USA, 88, 5621-5625.
45. 2+-channels: four subtypes of alpha 1-and beta-subunits in developing and mature rat brain. Brain Res. Mol. Brain Res., 30, 1-16.
46. Verderio, C., Coco, S., Fumagalli, G. & Matteoli, M. (1995) Calcium-dependent glutamate release during neuronal development and synaptogenesis: different involvement of omega-agatoxin IVA-and omega-conotoxin GVIA-sensitive channels. Proc. Natl Acad. Sci. USA, 92, 6449-6453.
47. Vigues, S., Chabret, C., Valentin, S. & Valmier, J. (1998) Rat embryonic hippocampal neurons express a new class A calcium channel variant. Neurosci. Lett., 258, 37-40.
48. Wheeler, D.B., Randall, A., Sather, W.A. & Tsien, R.W. (1995) Neuronal calcium channels encoded by the alpha 1A subunit and their contribution to excitatory synaptic transmission in the CNS. Prog. Brain Res., 105, 65-78.
49. Yaari, Y., Hamon, B. & Lux, H.D. (1987) Development of two types of calcium channels in cultured mammalian hippocampal neurons. Science, 235, 680-682.
50. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H. & Lindholm, D. (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J., 9, 3545-3550.