Gephyrin interacts with the glutamate receptor interacting protein 1 isoforms at GABAergic synapses

Journal of Neurochemistry

Volumn 105, Issue 6, 2008, Pages 2300-2314

  Yu, Wendou ^a   Charych, Erik I ^a   Serwanski, David R ^a   Li, Rong Wen ^a   Ali, Rashid ^a   Bahr, Ben A ^a   De Blas, Angel L ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Clustering; GABA synapse; GABAA receptor; Gephyrin; Glutamate receptor interacting protein 1; PDZ domain

Indexed keywords

4 AMINOBUTYRIC ACID; GEPHYRIN; NUCLEAR RECEPTOR COACTIVATOR 2;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; HIPPOCAMPUS; HUMAN; HUMAN CELL; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; RAT; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL LINE; CELLS, CULTURED; GAMMA-AMINOBUTYRIC ACID; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BINDING; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; TRANSFECTION;

RATTUS;

EID: 44649090640     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05311.x     Document Type: Article

References (67)

1. Ataman B., Ashley J., Gorczyca D., Gorczyca M., Mathew D., Wichmann C., Sigrist S. J. Budnik V. (2006) Nuclear trafficking of Drosophila frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl Acad. Sci. USA 103, 7841 7846.
2. Bladt F., Tafuri A., Gelkop S., Langille L. Pawson T. (2002) Epidermolysis bullosa and embryonic lethality in mice lacking the multi-PDZ domain protein GRIP1. Proc. Natl Acad. Sci. USA 99, 6816 6821.
3. Bohlhalter S., Mohler H. Fritschy J. M. (1994) Inhibitory neurotransmission in rat spinal cord: co-localization of glycine- and GABAA-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res. 642, 59 69.
4. Bruckner K., Pablo Labrador J., Scheiffele P., Herb A., Seeburg P. H. Klein R. (1999) EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22, 511 524.
5. Charych E. I., Yu W., Li R., Serwanski D. R., Miralles C. P., Li X., Yang B. Y., Pinal N., Walikonis R. De Blas A. L. (2004a) A four PDZ domain-containing splice variant form of GRIP1 is localized in GABAergic and glutamatergic synapses in the brain. J. Biol. Chem. 279, 38978 38990.
6. Charych E. I., Yu W., Miralles C. P., Serwanski D. R., Li X., Rubio M. De Blas A. L. (2004b) 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, 173 189.
7. Charych E. I., Li R., Serwanski D. R., Li X., Miralles C. P., Pinal N. De Blas A. L. (2006) Identification and characterization of two novel splice forms of GRIP1 in the rat brain. J. Neurochem. 97, 884 898.
8. Chen Z. W. Olsen R. W. (2007) GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J. Neurochem. 100, 279 294.
9. Christie S. B. De Blas A. L. (2003) GABAergic and glutamatergic axons innervate the axon initial segment and organize GABA(A) receptor clusters of cultured hippocampal pyramidal cells. J. Comp. Neurol. 456, 361 374.
10. Christie S. B., Li R. W., Miralles C. P., Riquelme R., Yang B. Y., Charych E., Yu W., Daniels S. B., Cantino M. E. De Blas A. L. (2002a) Synaptic and extrasynaptic GABAA receptor and gephyrin clusters. Prog. Brain Res. 136, 157 180.
11. Christie S. B., Miralles C. P. De Blas A. L. (2002b) GABAergic innervation organizes synaptic and extrasynaptic GABAA receptor clustering in cultured hippocampal neurons. J. Neurosci. 22, 684 697.
12. Christie S. B., Li R. W., Miralles C. P., Yang B. Y. De Blas A. L. (2006) Clustered and non-clustered GABAA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 31, 1 14.
13. DeSouza S., Fu J., States B. A. Ziff E. B. (2002) Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J. Neurosci. 22, 3493 3503.
14. Dong H., O'Brien R. J., Fung E. T., Lanahan A. A., Worley P. F. Huganir R. L. (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386, 279 284.
15. Dong H., Zhang P., Song I., Petralia R. S., Liao D. Huganir R. L. (1999) Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2. J. Neurosci. 19, 6930 6941.
16. Essrich C., Lorez M., Benson J. A., Fritschy J. M. Luscher B. (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat. Neurosci. 1, 563 571.
17. Feng G., Tintrup H., Kirsch J., Nichol M. C., Kuhse J., Betz H. Sanes J. R. (1998) Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282, 1321 1324.
18. Fernando L. P., Khan Z. U. De Blas A. L. (1995) Antibodies to the rat beta 3 subunit of the gamma-aminobutyric acid A receptors. Brain Res. Mol. Brain Res. 28, 94 100.
19. Fu J., deSouza S. Ziff E. B. (2003) Intracellular membrane targeting and suppression of Ser880 phosphorylation of glutamate receptor 2 by the linker I-set II domain of AMPA receptor-binding protein. J. Neurosci. 23, 7592 7601.
20. Gindhart J. G. (2006) Towards an understanding of kinesin-1 dependent transport pathways through the study of protein-protein interactions. Brief. Funct. Genomic. Proteomic. 5, 74 86.
21. Goslin K., Asmussen H. Banker G. (1998) Rat hippocampal neurons in low density culture, in Culturing Nerve Cells, 2nd edn Banker G. Goslin K., eds), pp. 339 370. MIT Press, Cambridge, MA.
22. Hirbec H., Francis J. C., Lauri S. E. et al. (2003) Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37, 625 638.
23. Hoogenraad C. C., Milstein A. D., Ethell I. M., Henkemeyer M. Sheng M. (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci. 8, 906 915.
24. Im Y. J., Park S. H., Rho S. H., Lee J. H., Kang G. B., Sheng M., Kim E. Eom S. H. (2003) Crystal structure of GRIP1 PDZ6-peptide complex reveals the structural basis for class II PDZ target recognition and PDZ domain-mediated multimerization. J. Biol. Chem. 278, 8501 8507.
25. Jacob T. C., Bogdanov Y. D., Magnus C., Saliba R. S., Kittler J. T., Haydon P. G. Moss S. J. (2005) Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 25, 10469 10478.
26. Kaufmann N., DeProto J., Ranjan R., Wan H. Van Vactor D. (2002) Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34, 27 38.
27. Kawasaki B. T., Hoffman K. B., Yamamoto R. S. Bahr B. A. (1997) Variants of the receptor/channel clustering molecule gephyrin in brain: distinct distribution patterns, developmental profiles, and proteolytic cleavage by calpain. J. Neurosci. Res. 49, 381 388.
28. Kim C. H., Chung H. J., Lee H. K. Huganir R. L. (2001) Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc. Natl Acad. Sci. USA 98, 11725 11730.
29. Kirsch J., Wolters I., Triller A. Betz H. (1993) Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366, 745 748.
30. Kittler J. T., Rostaing P., Schiavo G., Fritschy J. M., Olsen R., Triller A. Moss S. J. (2001) The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABA(A) receptors. Mol. Cell. Neurosci. 18, 13 25.
31. Kittler J. T., Arancibia-Carcamo I. L. Moss S. J. (2004) Association of GRIP1 with a GABA(A) receptor associated protein suggests a role for GRIP1 at inhibitory synapses. Biochem. Pharmacol. 68, 1649 1654.
32. Kneussel M., Brandstatter J. H., Laube B., Stahl S., Muller U. Betz H. (1999) Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J. Neurosci. 19, 9289 9297.
33. Kneussel M., Haverkamp S., Fuhrmann J. C., Wang H., Wassle H., Olsen R. W. Betz H. (2000) The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc. Natl Acad. Sci. USA 97, 8594 8599.
34. Kulangara K., Kropf M., Glauser L., Magnin S., Alberi S., Yersin A. Hirling H. (2007) Phosphorylation of glutamate receptor interacting protein 1 regulates surface expression of glutamate receptors. J. Biol. Chem. 282, 2395 2404.
35. Lardi-Studler B. Fritschy J. M. (2007) Matching of pre- and postsynaptic specializations during synaptogenesis. Neuroscientist 13, 115 126.
36. Leil T. A., Chen Z. W., Chang C. S. Olsen R. W. (2004) GABAA receptor-associated protein traffics GABAA receptors to the plasma membrane in neurons. J. Neurosci. 24, 11429 11438.
37. Levi S., Logan S. M., Tovar K. R. Craig A. M. (2004) Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 24, 207 217.
38. Li R. W., Serwanski D. R., Miralles C. P., Li X., Charych E., Riquelme R., Huganir R. L. de Blas A. L. (2005a) GRIP1 in GABAergic synapses. J. Comp. Neurol. 488, 11 27.
39. A receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J. Neurochem. 95, 756 770.
40. 2+ permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8, 768 775.
41. Luo J., Wang Y., Yasuda R. P., Dunah A. W. Wolfe B. W. (1997) The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol. Pharmacol. 51, 79 86.
42. Luscher B. Keller C. A. (2004) Regulation of GABA(A) receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol. Ther. 102, 195 221.
43. Maas C., Tagnaouti N., Loebrich S., Behrend B., Lappe-Siefke C. Kneussel M. (2006) Neuronal cotransport of glycine receptor and the scaffold protein gephyrin. J. Cell. Biol. 172, 441 451.
44. Meier J. Grantyn R. (2004) A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses. J. Neurosci. 24, 1398 1405.
45. Meyer G., Kirsch J., Betz H. Langosch D. (1995) Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron 15, 563 572.
46. Murai K. K. Pasquale E. B. (2004) Eph receptors, ephrins, and synaptic function. Neuroscientist 10, 304 314.
47. O'Sullivan G. A., Kneussel M., Elazar Z. Betz H. (2005) GABARAP is not essential for GABA receptor targeting to the synapse. Eur. J. Neurosci. 22, 2644 2648.
48. Osten P., Khatri L., Perez J. L., Kohr G., Giese G., Daly C., Schulz T. W., Wensky A., Lee L. M. Ziff E. B. (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27, 313 325.
49. Paarmann I., Schmitt B., Meyer B., Karas M. Betz H. (2006) Mass spectrometric analysis of glycine receptor-associated gephyrin splice variants. J. Biol. Chem. 281, 34918 34925.
50. Riquelme R., Miralles C. P. De Blas A. L. (2002) Bergmann glia GABA(A) receptors concentrate on the glial processes that wrap inhibitory synapses. J. Neurosci. 22, 10720 10730.
51. Sassoe-Pognetto M., Giustetto M., Panzanelli P., Cantino D., Kirsch J. Fritschy J. M. (1999) Postsynaptic colocalization of gephyrin and GABAA receptors. Ann. NY Acad. Sci. 868, 693 696.
52. Setou M., Seog D. H., Tanaka Y., Kanai Y., Takei Y., Kawagishi M. Hirokawa N. (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417, 83 87.
53. Srivastava S., Osten P., Vilim F. S. et al. (1998) Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron 21, 581 591.
54. Steiner P., Alberi S., Kulangara K. et al. (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J. 24, 2873 2884.
55. Swan L. E., Wichmann C., Prange U., Schmid A., Schmidt M., Schwarz T., Ponimaskin E., Madeo F., Vorbruggen G. Sigrist S. J. (2004) A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev. 18, 223 237.
56. Swan L. E., Schmidt M., Schwarz T., Ponimaskin E., Prange U., Boeckers T., Thomas U. Sigrist S. J. (2006) Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J. 25, 3640 3651.
57. Takamiya K., Kostourou V., Adams S., Jadeja S., Chalepakis G., Scambler P. J., Huganir R. L. Adams R. H. (2004) A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1. Nat. Genet. 36, 172 177.
58. Torres R., Firestein B. L., Dong H., Staudinger J., Olson E. N., Huganir R. L., Bredt D. S., Gale N. W. Yancopoulos G. D. (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21, 1453 1463.
59. Wang H., Bedford F. K., Brandon N. J., Moss S. J. Olsen R. W. (1999) GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397, 69 72.
60. Wyszynski M. Sheng M. (1999) Analysis of ion channel associated proteins. Methods Enzymol. 294, 371 385.
61. Wyszynski M., Valtschanoff J. G., Naisbitt S., Dunah A. W., Kim E., Standaert D. G., Weinberg R. Sheng M. (1999) Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J. Neurosci. 19, 6528 6537.
62. Wyszynski M., Kim E., Dunah A. W., Passafaro M., Valtschanoff J. G., Serra-Pages C., Streuli M., Weinberg R. J. Sheng M. (2002) Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron 34, 39 52.
63. Xia J., Chung H. J., Wihler C., Huganir R. L. Linden D. J. (2000) Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 28, 499 510.
64. Yamazaki M., Fukaya M., Abe M., Ikeno K., Kakizaki T., Watanabe M. Sakimura K. (2001) Differential palmitoylation of two mouse glutamate receptor interacting protein 1 forms with different N-terminal sequences. Neurosci. Lett. 304, 81 84.
65. Ye B., Liao D., Zhang X., Zhang P., Dong H. Huganir R. L. (2000) GRASP-1: a neuronal RasGEF associated with the AMPA receptor/GRIP complex. Neuron 26, 603 617.
66. Yu W. De Blas A. L. (2008) Gephyrin expression and clustering affects the size of glutamatergic synaptic contacts. J. Neurochem. 104, 830 845.
67. Yu W., Jiang M., Miralles C. P., Li R. W., Chen G. De Blas A. L. (2007) Gephyrin clustering is required for the stability of GABAergic synapses. Mol. Cell. Neurosci. 36, 484 500.