BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2

Development

Volumn 130, Issue 7, 2003, Pages 1267-1280

  Aguado, Fernando ^a   Carmona, Maria A ^a   Pozas, Esther ^a   Aguiló, Agustín ^a   Martínez Guijarro, Francisco J ^b   Alcantara, Soledad ^a   Borrell, Victor ^a   Yuste, Rafael ^c   Ibañez, Carlos F ^d   Soriano, Eduardo ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

BDNF; Ca2+ oscillations; CNS; GABA; KCC2; Mouse; Spontaneous activity; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CHLORIDE ION; COTRANSPORTER; GLUTAMATE DECARBOXYLASE; IONOTROPIC RECEPTOR; NESTIN; NEUROTROPHIN; POTASSIUM CHLORIDE COTRANSPORTER; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BRAIN DEVELOPMENT; BRAIN SLICE; CELL ACTIVITY; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; GABAERGIC SYSTEM; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; HIPPOCAMPUS; HOMEOSTASIS; INTERNEURON; MOLECULAR CLONING; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL INHIBITION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SYNAPTOGENESIS; TRANSGENICS;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; ISOENZYMES; MICE; MICE, TRANSGENIC; RECEPTORS, NEUROTRANSMITTER; SYMPORTERS; SYNAPSES;

ANIMALIA;

EID: 0037383851     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00351     Document Type: Review

References (53)

1. Aguiló, A., Schwartz, T. H., Kumar, V. S., Peterlin, Z. A., Tsiola, A., Soriano, E. and Yuste, R. (1999). Involvement of Cajal-Retzius neurons in spontaneous correlated activity of embryonic and postnatal layer 1 from wild-type and reeler mice. J. Neurosci. 19, 10856-10868.
2. Alsina, B., Vu, T. and Cohen-Cory, S. (2001). Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4, 1093-1101.
3. Barallobre, M. J., del Rio, J. A., Alcántara, S., Borrell, V., Aguado, F., Ruiz, M., Carmona, M. A., Martin, M., Fabre, M. Yuste, R. et al. (2000). Aberrant development of hippocampal circuits and altered neuronal activity in netrin 1-deficient mice. Development 127, 4797-4810.
4. A, NMDA and AMPA receptors: a developmentally regulated 'ménage à trois'. Trends Neurosci. 20, 523-529.
5. Ben-Ari, Y. (2001). Developing networks play a similar melody. Trends Neurosci. 24, 353-360.
6. Berninger, B., Marty, S., Zafra, F., Berzaghi, M. P., Thoenen, H. and Lindholm, D. (1995). GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121, 2327-2335.
7. Blue, M. E. and Parnavelas, J. G. (1983). The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J. Neurocytol. 12, 599-616.
8. Bonhoeffer, T. (1996). Neurotrophins and activity-dependent development of the neocortex. Curr. Opin. Neurobiol. 6, 119-126.
9. Buonanno, A. and Fields, R. D. (1999). Gene regulation by patterned electrical activity during neural and skeletal muscle development. Curr. Opin. Neurobiol. 9, 110-120.
10. Cherubini, E., Gaiarsa, J. L. and Ben-Ari, Y. (1991). GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 14, 515-519.
11. Crespo, C., Blasco-Ibáñez, J. M., Briñón, J. G., Alonso, J. R., Domínguez, M. I. and Martínez-Guijarro, E. J. (2000). Subcellular localization of m2 muscarinic receptors in GABAergic interneurons of the olfactory bulb. Eur. J. Neurosci. 12, 3963-3974.
12. Diabira, D., Hennou, S., Chevassus-au-Louis, N., Ben-Ari, Y. and Gozlan, H. (1999). Late embryonic expression of AMPA receptor function in the CA1 region of the intact hippocampus in vitro. Eur. J. Neurosci. 11, 4015-4023.
13. Erlander, M. G., Tillakaratne, N. J., Feldblum, S., Patel, N. and Tobin, A. J. (1991). Two genes encode distinct glutamate decarboxylases. Neuron 7, 91-100.
14. Ernfors, P., Begzon, J., Kokaia, Z., Persson, H. and Lindvall, O. (1991). Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7, 165-176.
15. Feller, M. B. (1999). Spontaneous correlated activity in developing neural circuits. Neuron 22, 653-656.
16. Fiala, J. C., Feinberg, M., Popov, V. and Harris, M. (1998). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18, 8900-8911.
17. A-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci. 14, 5302-5324.
18. Ganguly, K., Schinder, A. F., Wong, S. T. and Poo, M. M. (2001). GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532.
19. Garaschuk, O., Hanse, E. and Konnerth, A. (1998). Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J. Physiol. 507, 219-236.
20. Gulyás, A. I., Sik, A., Payne, J. A., Kaila, K. and Freund, T. F. (2001). The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in rat hippocampus. Eur. J. Neurosci. 13, 2205-2217.
21. Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., Maffei, L. and Tonegawa, S. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739-755.
22. Huang, E. L. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
23. Hüber, C. A., Stein, V., Hermans-Borgmeyer, I., Meyer, T., Ballanyi, K. and Jentsch, T. (2001). Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30, 515-524.
24. Katz, L. C. and Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138.
25. Knüsel, B., Rabin, S. J., Hefti, F. and Kaplan, D. R. (1994). Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J. Neurosci. 14, 1542-1554.
26. Kohara, K., Kitamura, A., Morishima, M. and Tsumoto, T. (2001). Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291, 2419-2423.
27. 2+ fluctuations. J. Neurobiol. 37, 110-130.
28. Mao, B.-Q., Hamzei-Sichani, F., Aronov, D., Froemke, R. C. and Yuste, R. (2001). Dynamics of spontaneous activity in neocortical slices. Neuron 32, 883-898.
29. Martínez, A., Alcántara, S., Borrell, V., del Río, J. A., Blasi, J., Otal, R., Campos, N., Boronat, A., Barbacid, M., Silos-Santiago, I. et al. (1998). TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J. Neurosci. 18, 7336-7350.
30. Marty, S., Berzaghi, M. P. and Berninger, B. (1997). Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci. 20, 198-202.
31. McAllister, A. K., Katz, L. C. and Lo, D. C. (1999). Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22, 295-318.
32. O'Donovan, M. J. (1999). The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr. Opin. Neurobiol. 9, 94-104.
33. Owens, D. F., Boyce, L. H., Davis, M. B. E. and Kriegstein, A. R. (1996). Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16, 6414-6423.
34. Penn, A. A., Riquelme, P. A., Feller, M. B. and Shatz, C. J. (1998). Competition in retinogeniculate pattering driven by spontaneous activity. Science 279, 2108-2112.
35. Pozzo-Miller, L. D., Gottschalk, W., Zhang, L., McDermott, K., Du, J., Gopalakrishnan, R., Oho, C., Sheng, Z. H., Lu, B. (1999). Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 19, 4972-4983.
36. Ringstedt, T., Linnarsson, S., Wagner, J., Lendahl, U., Kokaia, Z., Arenas, E., Ernfors, P. and Ibañez, C. F. (1998). BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron 21, 305-315.
37. +/Cl- cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255.
38. Rosahl, T. W., Spillane, D., Missler, M., Herz, J., Selig, D. K., Wolff, J. R., Hammer, R. E., Malenka, R. C. and Südhof, T. C. (1995). Essential function of synapsins I and II in synaptic vesicle regulation. Nature 375, 488-493.
39. Schinder, A. F. and Poo, M. M. (2000). The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23, 639-645.
40. Schuman, E. M. (1999). Neurotrophin regulation of synaptic transmission. Curr. Opin. Neurobiol. 9, 105-109.
41. Schwartz, T., Rabinowtz, D., Unni, V., Kumar, V. S., Smetters, D. K., Tsiola, A. and Yuste, R. (1998). Networks of coactive neurons in developing layer 1. Neuron 20, 541-552.
42. Soriano, E., Cobas, A. and Fairen, A. (1989). Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: Regio superior and regio inferior. J. Comp. Neurol. 281, 586-602.
43. Soriano, E., del Río, J. A., Martínez, A. and Super, H. (1994). Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J. Comp. Neurol. 342, 571-595.
44. Spitzer, N. C., Lautermilch, N. J., Smith, R. D. and Gomez, T. M. (2000). Coding of neuronal differentiation by calcium transients. BioEssays 22, 811-817.
45. Stellwagen, D. and Shatz, C. J. (2002). An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33, 357-367.
46. Südhof, T. C. (2000). The synaptic vesicle cycle revisited. Neuron 28, 317-320.
47. Supèr, H. and Soriano, E. (1994). The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J. Comp. Neurol. 344, 101-120.
48. Supèr, H., Martinez, A., del Rio, J. A. and Soriano, E. (1998). Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J. Neurosci. 15, 4616-4626.
49. Vaughn, J. E. (1989). Review: Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3, 255-285.
50. Vicario-Abejón, C., Collin, C., McKay, R. D. and Segal, M. (1998). Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci. 18, 7256-7271.
51. Watanabe, M., Fukaya, M., Sakimura, K., Manabe, T., Mishina, M. and Inoue, Y. (1998). Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur. J. Neurosci. 10, 478-487.
52. Yuste, R., Peinado, A. and Katz, L. C. (1992). Neuronal domains in developing neocortex. Science 257, 665-669.
53. Yuste, R., Nelson, D. A., Rubin, W. W. and Katz, L. C. (1995). Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14, 7-17.