Mechanisms of homomeric α1 glycine receptor endocytosis

Biochemistry

Volumn 46, Issue 41, 2007, Pages 11484-11493

  Huang, Renqi ^a   He, Shaoqing ^a   Chen, Zhenglan ^a   Dillon, Glenn H ^a   Leidenheimer, Nancy J ^b  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC; ENDOCYTOSIS; GLYCINE RECEPTOR ENDOCYTOSIS; IMMUNOFLUORESCENCE;

BIOACTIVITY; CELLS; ENZYME INHIBITION; GENE EXPRESSION; IMMUNOLOGY; PEPTIDES;

AMINO ACIDS;

AMINO ACID; DYNAMIN; GLYCINE; GLYCINE RECEPTOR; GLYCINE RECEPTOR ALPHA1; LEUCINE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ARTICLE; CHLORIDE CURRENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; CELL LINE; KINETICS; METABOLISM; PHYSIOLOGY;

CELL LINE; DYNAMINS; ENDOCYTOSIS; HUMANS; KINETICS; MICROSCOPY, CONFOCAL; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; RECEPTORS, GLYCINE; TETRADECANOYLPHORBOL ACETATE;

EID: 35348916130     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701093j     Document Type: Article

References (57)

1. Lynch, J. W. (2004) Molecular structure and function of the glycine receptor chloride channel, Physiol. Rev. 84, 1051-1095.
2. Breitinger, H. G., and Becker, C. M. (2002) The inhibitory glycine receptor-simple views of a complicated channel, ChemBioChem 3, 1042-1052.
3. Karlin, A. (2002) Emerging structure of the nicotinic acetylcholine receptors, Nat. Rev. Neurosci. 3, 102-114.
4. Laube, B., Maksay, G., Schemm, R., and Betz, H. (2002) Modulation of glycine receptor function: a novel approach for therapeutic intervention at inhibitory synapses, Trends Pharmacol. Sci. 23, 519-527.
5. Rosenberg, M., Meier, J., Triller, A., and Vannier, C. (2001) Dynamics of glycine receptor insertion in the neuronal plasma membrane, J. Neurosci. 21, 5036-5044.
6. Meier, J., Vannier, C., Serge, A., Triller, A., and Choquet, D. (2001) Fast and reversible trapping of surface glycine receptors by gephyrin, Nat. Neurosci. 4, 253-260.
7. Dahan, M., Levi, S., Luccardini, C., Rostaing, P., Riveau, B., and Triller, A. (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking, Science 302, 442-445.
8. Levi, S., Logan, S. M., Tovar, K. R., and 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.
9. Meier, J., and Grantyn, R. (2004) A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses, J. Neurosci. 24, 1398-1405.
10. Hanus, C., Vannier, C., and Triller, A. (2004) Intracellular association of glycine receptor with gephyrin increases its plasma membrane accumulation rate, J. Neurosci. 24, 1119-1128.
11. Rasmussen, H., Rasmussen, T., Triller, A., and Vannie, C. (2002) Strychnine-blocked glycine receptor is removed from synapses by a shift in insertion/degradation equilibrium, Mol. Cell Neurosci. 19, 201-215.
12. Buttner, C., Sadtler, S., Leyendecker, A., Laube, B., Griffon, N., Betz, H., and Schmalzing, G. (2001) Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors, J. Biol. Chem. 276, 42978-42985.
13. Huang, R. Q., and Dillon, G. H. (1999) Effect of extracellular pH on GABA-activated current in rat recombinant receptors and thin hypothalamic slices, J. Neurophysiol. 82, 1233-1243.
14. Herring, D., Huang, R., Singh, M., Robinson, L. C., Dillon, G. H., and Leidenheimer, N. J. (2003) Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor, J. Biol. Chem. 278, 24046-24052.
15. Herring, D., Huang, R., Singh, M., Dillon, G. H., and Leidenheimer, N. J. (2005) PKC modulation of GABAA receptor endocytosis and function is inhibited by mutation of a dileucine motif within the receptor beta 2 subunit, Neuropharmacology 48, 181-194.
16. Schmid, S. L., McNiven, M. A., and De Camilli, P. (1998) Dynamin and its partners: a progress report, Curr. Opin. Cell Biol. 10, 504-512.
17. Marks, B., and McMahon, H. T. (1998) Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals, Curr. Biol. 8, 740-749.
18. Wigge, P., and McMahon, H. T. (1998) The amphiphysin family of proteins and their role in endocytosis at the synapse, Trends Neurosci. 21, 339-344.
19. Bonifacino, J. S., and Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes, Annu. Rev. Biochem. 72, 395-447.
20. Brose, N., and Rosenmund, C. (2002) Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters, J. Cell Sci. 115, 4399-4411.
21. Ruiz-Gomez, A., Vaello, M. L., Valdivieso, F., and Mayor, F., Jr. (1991) Phosphorylation of the 48-kDa subunit of the glycine receptor by protein kinase C, J. Biol. Chem. 266, 559-566.
22. Kittler, J. T., Delmas, P., Jovanovic, J. N., Brown, D. A., Smart, T. G., and Moss, S. J. (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons, J. Neurosci. 20, 7972-7977.
23. Carroll, R. C., Beattie, E. C., Xia, H., Luscher, C., Altschuler, Y., Nicoll, R. A., Malenka, R. C., and von Zastrow, M. (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors, Proc. Natl. Acad. Sci. U.S.A. 96, 14112-14117.
24. Nong, Y., Huang, Y. Q., Ju, W., Kalia, L. V., Anmadian, G., Wang, Y. T., and Salter, M. W. (2003) Glycine binding primes NMDA receptor internalization, Nature 422, 302-307.
25. Montgomery, J. M., Selcher, J. C., Hanson, J. E., and Madison, D. V. (2005) Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state, BMC Neurosci. 6, 48.
26. Morishita, W., Marie, H., and Malenka, R. C. (2005) Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses, Nat. Neurosci. 8, 1043-1050.
27. Le Borgne, R., and Hoflack, B. (1998) Mechanisms of protein sorting and coat assembly: insights from the clathrin-coated vesicle pathway, Curr. Opin. Cell Biol. 10, 499-503.
28. Lee, S. H., Liu, L., Wang, Y. T., and Sheng, M. (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD, Neuron 36, 661-674.
29. Diviani, D., Lattion, A. L., Abuin, L., Staub, O., and Cotecchia, S. (2003) The adaptor complex 2 directly interacts with the alpha 1b-adrenergic receptor and plays a role in receptor endocytosis, J. Biol. Chem. 278, 19331-19340.
30. Wojcikiewicz, R. J. (2004) Regulated ubiquitination of proteins in GPCR-initiated signaling pathways, Trends Pharmacol. Sci. 25, 35-41.
31. van Kerkhof, P., Sachse, M., Klumperman, J., and Strous, G. J. (2001) Growth hormone receptor ubiquitination coincides with recruitment to clathrin-coated membrane domains, J. Biol. Chem. 276, 3778-3784.
32. Nishizaki, T., and Ikeuchi, Y. (1995) Activation of endogenous protein kinase C enhances currents through alpha 1 and alpha 2 glycine receptor channels, Brain Res. 687, 214-216.
33. Tao, L., and Ye, J. H. (2002) Protein kinase C modulation of ethanol inhibition of glycine-activated current in dissociated neurons of rat ventral tegmental area, J. Pharmacol. Exp. Ther. 300, 967-975.
34. Tapia, J. C., Espinoza, F., and Aguayo, L. G. (1997) Differential intracellular regulation of cortical GABA(A) and spinal glycine receptors in cultured neurons, Brain Res. 769, 203-210.
35. Vaello, M. L., Ruiz-Gomez, A., Lerma, J., and Mayor, F., Jr. (1994) Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase, J. Biol. Chem. 269, 2002-2008.
36. Machu, T., Dillon, G. H., Huang, R., Lovinger, D. M., and Leidenheimer, N. J. (2006) Temperature: An important experimental in studying PKC modulation of ligand-gated ion channels, Mol. Brain Res. 1086, 1-8.
37. Tomoda, H., Kishimoto, Y., and Lee, Y. C. (1989) Temperature effect on endocytosis and exocytosis by rabbit alveolar macrophages, J. Biol. Chem. 264, 15445-15450.
38. Seddiki, T., and Ollivier-Bousquet, M. (1991) Temperature dependence of prolactin endocytosis and casein exocytosis in epithelial mammary cells, Eur. J. Cell Biol. 55, 60-70.
39. Gu, Y., and Huang, L. Y. (1998) Cross-modulation of glycine-activated Cl-channels by protein kinase C and cAMP-dependent protein kinase in the rat, J. Physiol. 506, 331-339.
40. Schonrock, B., and Bormann, J. (1995) Modulation of hippocampal glycine receptor channels by protein kinase C, Neuroreport 6, 301-304.
41. Xu, T. L., Nabekura, J., and Akaike, N. (1996) Protein kinase C-mediated enhancement of glycine response in rat sacral dorsal commissural neurones by serotonin, J. Physiol. 496 (Pt 2), 491-501.
42. Chapell, R., Bueno, O. F., Alvarez-Hernandez, X., Robinson, L. C., and Leidenheimer, N. J. (1998) Activation of protein kinase C induces gamma-aminobutyric acid type A receptor internalization in Xenopus oocytes, J. Biol. Chem. 273, 32595-32601.
43. Connolly, C. N., Kittler, J. T., Thomas, P., Uren, J. M., Brandon, N. J., Smart, T. G., and Moss, S. J. (1999) Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition, J. Biol. Chem. 274, 36565-36572.
44. Liu, J. P., Powell, K. A., Sudhof, T. C., and Robinson, P. J. (1994) Dynamin I is a Ca(2+)-sensitive phospholipid-binding protein with very high affinity for protein kinase C, J. Biol. Chem. 269, 21043-21050.
45. Robinson, P. J., Sontag, J. M., Liu, J. P., Fykse, E. M., Slaughter, C., McMahon, H., and Sudhof, T. C. (1993) Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals, Nature 365, 163-166.
46. Cinar, H., and Barnes, E. M., Jr. (2001) Clathrin-independent endocytosis of GABA(A) receptors in HEK 293 cells, Biochemistry 40, 14030-14036.
47. Filippova, N., Dudley, R., and Weiss, D. S. (1999) Evidence for phosphorylation-dependent internalization of recombinant human rho1 GABAC receptors, J. Physiol. 518, 385-399.
48. Chung, H. J., Xia, J., Scannevin, R. H., Zhang, X., and Huganir, R. L. (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins, J. Neurosci. 20, 7258-7267.
49. Chattipakorn, S. C., and McMahon, L. L. (2003) Strychnine-sensitive glycine receptors depress hyperexcitability in rat dentate gyrus, J. Neurophysiol. 89, 1339-1342.
50. Jaeken, J. (2002) Genetic disorders of gamma-aminobutyric acid, glycine, and serine as causes of epilepsy, J. Child Neurol. 17, 3S84-87; discussion 83S88.
51. 2+ in combined rat entorhinal cortex-hippocampal slices, Epilepsia 44, 1145-1152.
52. Harvey, R. J., Depner, U. B., Wassle, H., Ahmadi, S., Heindl, C., Reinold, H., Smart, T. G., Harvey, K., Schutz, B., and Abo-Salem, O. M., et al. (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization, Science 304, 884-887.
53. Zeilhofer, H. U. (2005) The glycinergic control of spinal pain processing, Cell Mol. Life Sci. 62 (18), 2027-2035.
54. Zhou, L., Chillag, K. L., and Nigro, M. A. (2002) Hyperekplexia: a treatable neurogenetic disease, Brain Dev. 24, 669-674.
55. Humeny, A., Bonk, T., Becker, K., Jafari-Boroujerdi, M., Stephani, U., Reuter, K., and Becker, C. M. (2002) A novel recessive hyperekplexia allele GLRA1 (S231R): genotyping by MALDITOF mass spectrometry and functional characterisation as a determinant of cellular glycine receptor trafficking, Eur. J. Hum. Genet. 10, 188-196.
56. Castaldo, P., Stefanoni, P., Miceli, F., Coppola, G., Del, Giudice, E. M., Bellini, G., Pascotto, A., Trudell, J. R., Harrison, N. L., Annunziato, L., and Taglialatela, M. (2004) A novel hyperekplexia-causing mutation in the pre-transmembrane segment 1 of the human glycine receptor alpha1 subunit reduces membrane expression and impairs gating by agonists, J. Biol. Chem. 279, 25598-25604.
57. Hirata, H., Saint-Amant, L., Downes, G. B., Cui, W. W., Zhou, W., Granato, M., and Kuwada, J. Y. (2005) Zebrafish bandoneon mutants display behavioral defects due to a mutation in the glycine receptor beta-subunit, Proc. Natl. Acad. Sci. U.S.A. 102, 8345-8350.