Gephyrin clustering is required for the stability of GABAergic synapses

Molecular and Cellular Neuroscience

Volumn 36, Issue 4, 2007, Pages 484-500

  Yu, Wendou ^a   Jiang, Min ^b   Miralles, Celia P ^a   Li, Rong wen ^a   Chen, Gong ^b   de Blas, Angel L ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GEPHYRIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GABAERGIC SYSTEM; HIPPOCAMPUS; HUMAN; HUMAN CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; DOWN-REGULATION; GAMMA-AMINOBUTYRIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; MEMBRANE PROTEINS; NEURAL INHIBITION; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR AGGREGATION; RECEPTORS, GABA-A; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 35449002711     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.08.008     Document Type: Article

References (57)

1. Alvarez V.A., Ridenour D.A., and Sabatini B.L. Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J. Neurosci. 26 (2006) 7820-7825
2. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., and Sudhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48 (2005) 229-236
3. Bruckner K., Pablo Labrador J., Scheiffele P., Herb A., Seeburg P.H., and Klein R. EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22 (1999) 511-524
4. Chandra D., Korpi E.R., Miralles C.P., De Blas AL., and Homanics G.E. GABAA receptor gamma 2 subunit knockdown mice have enhanced anxiety-like behavior but unaltered hypnotic response to benzodiazepines. BMC Neurosci. 6 (2005) 30
5. Charrier C., Ehrensperger M.V., Dahan M., Levi S., and Triller A. Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. J. Neurosci. 26 (2006) 8502-8511
6. Charych E.I., Yu W., Miralles C.P., Serwanski D.R., Li X., Rubio M., and De Blas AL. The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J. Neurochem. 90 (2004) 173-189
7. Charych E.I., Yu W., Li R., Serwanski D.R., Miralles C.P., Li X., Yang B.Y., Pinal N., Walikonis R., and De Blas A.L. A four PDZ domain-containing splice variant form of GRIP1 is localized in GABAergic and glutamatergic synapses in the brain. J. Biol. Chem. 279 (2004) 38978-38990
8. Charych E.I., Li R., Serwanski D.R., Li X., Miralles C.P., Pinal N., and De Blas A.L. Identification and characterization of two novel splice forms of GRIP1 in the rat brain. J. Neurochem. 97 (2006) 884-898
9. Chen Y., Deng L., Maeno-Hikichi Y., Lai M., Chang S., Chen G., and Zhang J.F. Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell 115 (2003) 37-48
10. Chih B., Engelman H., and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307 (2005) 1324-1328
11. Chih B., Gollan L., and Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51 (2006) 171-178
12. Christie S.B., and De Blas A.L. GABAergic and glutamatergic axons innervate the axon initial segment and organize GABA(A) receptor clusters of cultured hippocampal pyramidal cells. J. Comp. Neurol. 456 (2003) 361-374
13. Christie S.B., Li R.W., Miralles C.P., Riquelme R., Yang B.Y., Charych E., Yu W., Daniels S.B., Cantino M.E., and De Blas A.L. Synaptic and extrasynaptic GABAA receptor and gephyrin clusters. Prog. Brain Res. 136 (2002) 157-180
14. Christie S.B., Miralles C.P., and De Blas A.L. GABAergic innervation organizes synaptic and extrasynaptic GABAA receptor clustering in cultured hippocampal neurons. J. Neurosci. 22 (2002) 684-697
15. Christie S.B., Li R.W., Miralles C.P., Yang B.Y., and De Blas A.L. Clustered and non-clustered GABAA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 31 (2006) 1-14
16. Contractor A., Rogers C., Maron C., Henkemeyer M., Swanson G.T., and Heinemann S.F. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296 (2002) 1864-1869
17. Craig A.M., Banker G., Chang W., McGrath M.E., and Serpinskaya A.S. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 16 (1996) 3166-3177
18. Dean C., and Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 29 (2006) 21-29
19. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6 (2003) 708-716
20. De Blas A.L., Vitorica J., and Friedrich P. Localization of the GABAA receptor in the rat brain with a monoclonal antibody to the 57,000 Mr peptide of the GABAA receptor/benzodiazepine receptor/Cl-channel complex. J. Neurosci. 8 (1988) 602-614
21. Dong N., Qi J., and Chen G. Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABA(A) receptors. Mol. Cell. Neurosci. 35 (2007) 14-23
22. Dykxhoorn D.M., Novina C.D., and Sharp P.A. Killing the messenger: short RNAs that silence gene expression. Nat. Rev., Mol. Cell Biol. 4 (2003) 457-467
23. Essrich C., Lorez M., Benson J.A., Fritschy J.M., and Luscher B. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat. Neurosci. 1 (1998) 563-571
24. Ewert M., De Blas A.L., Mohler H., and Seeburg P.H. A prominent epitope on GABAA receptors is recognized by two different monoclonal antibodies. Brain Res. 569 (1992) 57-62
25. Fang C., Deng L., Keller C.A., Fukata M., Fukata Y., Chen G., and Luscher B. GODZ-mediated palmitoylation of GABA-A receptors is required for normal assembly and function of GABAergic inhibitory synapses. J. Neurosci. 26 (2006) 12758-12768
26. Feng G., Tintrup H., Kirsch J., Nichol M.C., Kuhse J., Betz H., and Sanes J.R. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282 (1998) 1321-1324
27. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
28. Graf E.R., Kang Y., Hauner A.M., and Craig A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 26 (2006) 4256-4265
29. Goslin K., Asmussen H., and Banker G. Rat hippocampal neurons in low density culture. In: Banker G., and Goslin K. (Eds). Culturing Nerve Cells. 2nd ed. (1998), MIT Press, Cambridge, MA 339-370
30. Homanics G.E., Harrison N.L., Quinlan J.J., Krasowski M.D., Rick C.E., De Blas A.L., Mehta A.K., Kist F., Mihalek R.M., Aul J.J., and Firestone L.L. Normal electrophysiological and behavioral responses to ethanol in mice lacking the long splice variant of the gamma2 subunit of the gamma-aminobutyrate type A receptor. Neuropharmacology 38 (1999) 253-265
31. Jacob T.C., Bogdanov Y.D., Magnus C., Saliba R.S., Kittler J.T., Haydon P.G., and Moss S.J. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 25 (2005) 10469-10478
32. Jiang M., and Chen G. High Ca(2+)-phosphate transfection efficiency in low-density neuronal cultures. Nat. Protoc. 1 (2006) 695-700
33. Kim E.Y., Schrader N., Smolinsky B., Bedet C., Vannier C., Schwarz G., and Schindelin H. Deciphering the structural framework of glycine receptor anchoring by gephyrin. EMBO J. 25 (2006) 1385-1395
34. Kittler J.T., Arancibia-Carcamo I.L., and Moss S.J. Association of GRIP1 with a GABA(A) receptor associated protein suggests a role for GRIP1 at inhibitory synapses. Biochem. Pharmacol. 68 (2004) 1649-1654
35. Kneussel M., and Betz H. Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J. Physiol. 525 (2000) 1-9
36. Kneussel M., Brandstatter J.H., Laube B., Stahl S., Muller U., and Betz H. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J. Neurosci. 19 (1999) 9289-9297
37. Kneussel M., Brandstatter J.H., Gasnier B., Feng G., Sanes J.R., and Betz H. Gephyrin-independent clustering of postsynaptic GABA(A) receptor subtypes. Mol. Cell. Neurosci. 17 (2001) 973-982
38. Levi S., Logan S.M., Tovar K.R., and Craig A.M. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 24 (2004) 207-217
39. Levinson J.N., Chery N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., and El-Husseini A. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J. Biol. Chem. 280 (2005) 17312-17319
40. Li R.W., Serwanski D.R., Miralles C.P., Li X., Charych E., Riquelme R., Huganir R.L., and De Blas A.L. GRIP1 in GABAergic synapses. J. Comp. Neurol. 488 (2005) 11-27
41. A receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J. Neurochem. 95 (2005) 756-770
42. Meier J., and Grantyn R. A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses. J. Neurosci. 24 (2004) 1398-1405
43. Meier J., Vannier C., Serge A., Triller A., and Choquet D. Fast and reversible trapping of surface glycine receptors by gephyrin. Nat. Neurosci. 4 (2001) 253-260
44. Miralles C.P., Li M., Mehta A.K., Khan Z.U., and De Blas A.L. Immunocytochemical localization of the beta(3) subunit of the gamma-aminobutyric acid(A) receptor in the rat brain. J. Comp. Neurol. 413 (1999) 535-548
45. Prange O., Wong T.P., Gerrow K., Wang Y.T., and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc. Natl. Acad. Sci. 101 (2004) 13915-13920
46. Riquelme R., Miralles C.P., and De Blas A.L. Bergmann glia GABA(A) receptors concentrate on the glial processes that wrap inhibitory synapses. J. Neurosci. 22 (2002) 10720-10730
47. Scheiffele P., Fan J., Choih J., Fetter R., and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101 (2000) 657-669
48. Serwanski D.R., Miralles C.P., Christie S.B., Mehta A.K., Li X., and De Blas A.L. Synaptic and nonsynaptic localization of GABAA receptors containing the alpha5 subunit in the rat brain. J. Comp. Neurol. 499 (2006) 458-470
49. Song J.Y., Ichtchenko K., Sudhof T.C., and Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. 96 (1999) 1100-1105
50. Taniguchi H., Gollan L., Scholl F.G., Mahadomrongkul V., Dobler E., Limthong N., Peck M., Aoki C., and Scheiffele P. Silencing of neuroligin function by postsynaptic neurexins. J. Neurosci. 27 (2007) 2815-2824
51. Varoqueaux F., Jamain S., and Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83 (2004) 449-456
52. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., and Brose N. Neuroligins determine synapse maturation and function. Neuron 51 (2006) 741-754
53. - channel complex. J. Neurosci. 8 (1988) 615-622
54. Yang F., Moss L.G., and Phillips Jr. G.N. The molecular structure of green fluorescent protein. Nat. Biotechnol. 14 (1996) 1246-1251
55. Yao J., Qi J., and Chen G. Actin-dependent activation of presynaptic silent synapses contributes to long-term synaptic plasticity in developing hippocampal neurons. J. Neurosci. 26 (2006) 8137-8147
56. Yu J.Y., DeRuiter S.L., and Turner D.L. RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells. Proc. Natl. Acad. Sci. 99 (2002) 6047-6052
57. Zeringue H.C., and Constantine-Paton M. Post-transcriptional gene silencing in neurons. Curr. Opin. Neurobiol. 14 (2004) 654-659