NMDA receptors increase the size of GABAergic terminals and enhance GABA release

Journal of Neuroscience

Volumn 25, Issue 8, 2005, Pages 2024-2031

  Fiszman, Mónica L ^a,b   Barberis, Andrea ^a   Lu, Congyi ^a   Fu, Zhanyan ^a   Erdélyi, Ferenc ^c   Szabó, Gábor ^c   Vicini, Stefano ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

BDNF; Cerebellum; GFP; Interneuron; Patch clamp; Synapses

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE 65; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; CEREBELLUM; CONDUCTANCE; CONTROLLED STUDY; GABAERGIC SYSTEM; GRANULE CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE ENDING; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; STELLATE CELL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CEREBELLUM; DENDRITES; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GENES, REPORTER; INTERNEURONS; MICE; MICE, TRANSGENIC; N-METHYLASPARTATE; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 14244262988     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4980-04.2005     Document Type: Article

References (41)

1. Balázs R, Hack N, Jorgensen OS, Cotman CW (1989) N-methyl-D-aspartate promotes the survival of cerebellar granule cells: pharmacological characterization. Neurosci Lett 101:241-246.
2. Bhave SV, Ghoda L, Hoffman PL (1999) Brain-derived neurotrophic factor mediates the anti-apoptotic effect of NMDA in cerebellar granule neurons: signal transduction cascades and site of ethanol action. J Neurosci 19:3277-3286.
3. 2+ calmodulin-dependent protein kinase II and mitogen-activated protein kinase kinase to neural activity-induced neurite outgrowth and survival of cerebellar granule cells. J Neurochem 80:1062-1070.
4. Brager DH, Luther PW, Erdelyi F, Szabo G, Alger BE (2003) Regulation of exocytosis from single visualized GABAergic boutons in hippocampal slices. J Neurosci 23:10475-10486.
5. Bureau I, Mulle C (1998) Potentiation of GABAergic synaptic transmission by AMPA receptors in mouse cerebellar stellate cells: changes during development. J Physiol (Lond) 509:817-831.
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. Chang S, De Camilli P (2001) Glutamate regulates actin-based motility in axonal filopodia. Nat Neurosci 4:787-793.
8. Clark BA, Cull-Candy SG (2002) Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22:4428-4436.
9. Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
10. De Camilli P, Benfenatti F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6:443-450.
11. Duguid IC, Smart TG (2004) Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7:525-533.
12. Eccles JC, Ito M, Szentágothai J (1967) The cerebellum as a neuronal machine. New York: Springer.
13. Fernandez-Alfonso T, Ryan TA (2004) The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41:943-953.
14. Galarreta M, Erdélyi F, Szabó G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 24:9770-9778.
15. Gallo V, Kingsbury A, Balázs R, Jorgensen OS (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7:2203-2213.
16. Gao WQ, Zheng JL, Karihaloo M (1995) Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J Neurosci 15:2656-2667.
17. Glitsch M, Marty A (1999) Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19:511-519.
18. 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.
19. Huang H, Bordey A (2004) Glial glutamate transporters limit spillover activation of presynaptic NMDA receptors and influence synaptic inhibition of Purkinje neurons. J Neurosci 24:5659-5669.
20. Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, Floor E, Hsu CC, Kopke RD, Wu JY (2003) Demonstration of functional coupling between gamma-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA 100:4293-4298.
21. Krueger SR, Kolar A, Fitzsimonds M (2003) The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40:945-957.
22. Lopez-Benedito G, Sugress K, Erdélyi F, Szabó G, Molnár Z, Poulsen O (2004) Preferential origin and layer destination of GAD65-eGFP cortical interneurons. Cereb Cortex 14:1122-1133.
23. Ma L, Zablow L, Kandel ER, Siegelbaum SA (1999) Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures. Nat Neurosci 2:24-30.
24. Marini AM, Rabin SJ, Lipsky RH, Mocchetti I (1998) Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. J Biol Chem 273:29394-29399.
25. A receptor α6 subunit gene. J Neurosci 18:2822-2833.
26. Murase K, Ryu PD, Randic M (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56-63.
27. A receptor regulates inhibitory synaptic strength. J Neurophysiol 92:1718-1727.
28. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization New York: Springer.
29. Petralia RS, Wang YX, Wenthold RJ (1994) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
30. Pouzat C, Hestrin S (1997) Developmental regulation of basket/stellate cell-Purkinje cell synapses in the cerebellum. J Neurosci 17:9104-9112.
31. Resink A, Villa M, Benke D, Hidaka H, Mohler H, Balázs R (1996) Characterization of agonist-induced down-regulation of NMDA receptors in cerebellar granule cell cultures. J Neurochem 66:369-377.
32. Southan AP, Robertson BJ (1998) Patch-clamp recordings from cerebellar basket cell bodies and their presynaptic terminals reveal an asymmetric distribution of voltage-gated potassium channels. J Neurosci 18:948-955.
33. Spatkowski G, Schilling K (2003) Postnatal dendritic morphogenesis of cerebellar basket and stellate cells in vitro. J Neurosci Res 72:317-326.
34. Studler B, Fritschy JM, Brunig I (2002) GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro. Neuroscience 114:123-133.
35. Tashiro A, Dunaevsky A, Blazeski R, Mason CA, Yuste R (2003) Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors: a two-step model of synaptogenesis. Neuron 38:773-784.
36. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS, Raman IM (2004) Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41:113-126.
37. Ueno S, Zempel JM, Steinbach JH (1996) Differences in the expression of GABA(A) receptors between functionally innervated and non-innervated granule neurons in neonatal rat cerebellar cultures. Brain Res 714:49-56.
38. A receptor α1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21:3009-3016.
39. Virginio C, Martina M, Cherubini E (1995) Spontaneous GABA-mediated synaptic currents in cerebellar granule cells in culture. NeuroReport 6:1285-1289.
40. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759-772.
41. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci USA 101:7158-7163.