Kainate receptor post-translational modifications differentially regulate association with 4.1N to control activity-dependent receptor endocytosis

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 8952-8965

  Copits, Bryan A ^a   Swanson, Geoffrey T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY-DEPENDENT; CELLULAR MECHANISMS; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN ASSOCIATIONS; RECEPTOR ENDOCYTOSIS; SCAFFOLDING PROTEINS; SURFACE EXPRESSION; SYNAPTIC PLASTICITY;

ACYLATION; CELL MEMBRANES; MOLECULAR BIOLOGY; NEURONS; PROTEINS;

SCAFFOLDS (BIOLOGY);

GLU3 KAINATE RECEPTOR; GLUK1 KAINATE RECEPTOR; GLUK2 KAINATE RECEPTOR; GLUK2A KAINATE RECEPTOR; KAINIC ACID RECEPTOR; PROTEIN KINASE C; SYNAPSIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; CYTOSKELETON; ENDOCYTOSIS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; NEURONS; NEUROPEPTIDES; PALMITIC ACID; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84875980411     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.440719     Document Type: Article

References (56)

1. Contractor, A., Mulle, C., and Swanson, G. T. (2011) Kainate receptors coming of age. Milestones of two decades of research. Trends Neurosci. 34, 154-163
2. Kim, E., and Sheng, M. (2004) PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781
3. Elias, G. M., and Nicoll, R. A. (2007) Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol. 17, 343-352
4. Jackson, A. C., and Nicoll, R. A. (2011) The expanding social network of ionotropic glutamate receptors. TARPs and other transmembrane auxiliary subunits. Neuron 70, 178-199
5. Copits, B. A., and Swanson, G. T. (2012) Dancing partners at the synapse. Auxiliary subunits that shape kainate receptor function. Nat. Rev. Neurosci. 13, 675-686
6. Kennedy, M. J., and Ehlers, M. D. (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu. Rev. Neurosci. 29, 325-362
7. Shen, L., Liang, F., Walensky, L. D., and Huganir, R. L. (2000) Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1N-linked actin cytoskeletal association. J. Neurosci. 20, 7932-7940
8. Coleman, S. K., Cai, C., Mottershead, D. G., Haapalahti, J.-P., and Keinaänen, K. (2003) Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein. J. Neurosci. 23, 798-806
9. Lin, D.-T., Makino, Y., Sharma, K., Hayashi, T., Neve, R., Takamiya, K., and Huganir, R. L. (2009) Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat. Neurosci. 12, 879-887
10. Shepherd, J. D., and Huganir, R. L. (2007) The cell biology of synaptic plasticity. AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23, 613-643
11. Baines, A. J., Bennett, P. M., Carter, E. W., and Terracciano, C. (2009) Protein 4.1 and the control of ion channels. Blood Cell Mol. Dis. 42, 211-215
12. Bennett, V. (1989) The spectrin-actin junction of erythrocyte membrane skeletons. Biochim. Biophys. Acta 988, 107-121
13. 2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins. Biochemistry 45, 5725-5732
14. An, X.-L., Takakuwa, Y., Manno, S., Han, B.-G., Gascard, P., and Mohandas, N. (2001) Structural and functional characterization of protein 4.1Rphosphatidylserine interaction. Potential role in 4.1R sorting within cells. J. Biol. Chem. 276, 35778-35785
15. 2+-independent calmodulin binding sites in erythrocyte protein 4.1. Implications for regulation of protein 4.1 interactions with transmembrane proteins. J. Biol. Chem. 275, 6360-6367
16. Li, H., Khirug, S., Cai, C., Ludwig, A., Blaesse, P., Kolikova, J., Afzalov, R., Coleman, S. K., Lauri, S., Airaksinen, M. S., Keinänen, K., Khiroug, L., Saarma, M., Kaila, K., and Rivera, C. (2007) KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56, 1019-1033
17. Binda, A. V., Kabbani, N., Lin, R., and Levenson, R. (2002) D2 and D3 dopamine receptor cell surface localization mediated by interaction with protein 4.1N. Mol. Pharmacol. 62, 507-513
18. Pickering, D. S., Taverna, F. A., Salter, M. W., and Hampson, D. R. (1995) Palmitoylation of the GluR6 kainate receptor. Proc. Natl. Acad. Sci. U.S.A. 92, 12090-12094
19. Hirbec, H., Francis, J. C., Lauri, S. E., Braithwaite, S. P., Coussen, F., Mulle, C., Dev, K. K., Coutinho, V., Meyer, G., Isaac, J. T., Collingridge, G. L., and Henley, J. M. (2003) Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37, 625-638
20. Nasu-Nishimura, Y., Jaffe, H., Isaac, J. T., and Roche, K. W. (2010) Differential regulation of kainate receptor trafficking by phosphorylation of distinct sites on GluR6. J. Biol. Chem. 285, 2847-2856
21. Vivithanaporn, P., Lash, L. L., Marszalec, W., and Swanson, G. T. (2007) Critical roles for the M3-S2 transduction linker domain in kainate receptor assembly and postassembly trafficking. J Neurosci 27, 10423-10433
22. Copits, B. A., Robbins, J. S., Frausto, S., and Swanson, G. T. (2011) Synaptic targeting and functional modulation of GluK1 kainate receptors by the auxiliary neuropilin and tolloid-like (Neto) proteins. J. Neurosci. 31, 7334-7340
23. Shanks, N. F., Savas, J. N., Maruo, T., Cais, O., Hirao, A., Oe, S., Ghosh, A., Noda, Y., Greger, I. H., Yates, J. R., 3rd, and Nakagawa, T. (2012) Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L. Cell Rep. 1, 590-598
24. Lee, A. G. (2003) Lipid-protein interactions in biological membranes. A structural perspective. Biochim. Biophys. Acta 1612, 1-40
25. Yan, S., Sanders, J. M., Xu, J., Zhu, Y., Contractor, A., and Swanson, G. T. (2004) A C-terminal determinant of GluR6 kainate receptor trafficking. J. Neurosci. 24, 679-691
26. Jaskolski, F., Coussen, F., Nagarajan, N., Normand, E., Rosenmund, C., and Mulle, C. (2004) Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J. Neurosci. 24, 2506-2515
27. Parra, M., Gascard, P., Walensky, L. D., Gimm, J. A., Blackshaw, S., Chan, N., Takakuwa, Y., Berger, T., Lee, G., Chasis, J. A., Snyder, S. H., Mohandas, N., and Conboy, J. G. (2000) Molecular and functional characterization of protein 4.1B, a novel member of the protein 4.1 family with high level, focal expression in brain. J. Biol. Chem. 275, 3247-3255
28. Parra, M., Gascard, P., Walensky, L. D., Snyder, S. H., Mohandas, N., and Conboy, J. G. (1998) Cloning and characterization of 4.1G (EPB41L2), a new member of the skeletal protein 4.1 (EPB41) gene family. Genomics 49, 298-306
29. Puthenveedu, M. A., and von Zastrow, M. (2006) Cargo regulates clathrincoated pit dynamics. Cell 127, 113-124
30. Mondin, M., Carta, M., Normand, E., Mulle, C., and Coussen, F. (2010) Profilin II regulates the exocytosis of kainate glutamate receptors. J. Biol. Chem. 285, 40060-40071
31. Ehlers, M. D. (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28, 511-525
32. Martin, S., and Henley, J. M. (2004) Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways. EMBO J. 23, 4749-4759
33. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A., and Bredt, D. S. (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996
34. Park, Y., Jo, J., Isaac, J. T., and Cho, K. (2006) Long-term depression of kainate receptor-mediated synaptic transmission. Neuron 49, 95-106
35. Rivera, R., Rozas, J. L., and Lerma, J. (2007) PKC-dependent autoregulation of membrane kainate receptors. EMBO J. 26, 4359-4367
36. Selak, S., Paternain, A. V., Aller, M. I., Picó, E., Rivera, R., and Lerma, J. (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63, 357-371
37. Wozny, C., Breustedt, J., Wolk, F., Varoqueaux, F., Boretius, S., Zivkovic, A. R., Neeb, A., Frahm, J., Schmitz, D., Brose, N., and Ivanovic, A. (2009) The function of glutamatergic synapses is not perturbed by severe knockdown of 4.1N and 4.1G expression. J. Cell Sci. 122, 735-744
38. Pinheiro, P. S., Lanore, F., Veran, J., Artinian, J., Blanchet, C., Crépel, V., Perrais, D., and Mulle, C. (2013) Selective block of postsynaptic kainate receptors reveals their function at hippocampal mossy fiber synapses. Cereb. Cortex 23, 323-331
39. Kidd, F. L., and Isaac, J. T. (1999) Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400, 569-573
40. Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., and Ehlers, M. D. (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972-1975
41. Lu, J., Helton, T. D., Blanpied, T. A., Rácz, B., Newpher, T. M., Weinberg, R. J., and Ehlers, M. D. (2007) Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 55, 874-889
42. Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., and Dingledine, R. (2010) Glutamate receptor ion channels. Structure, regulation, and function. Pharmacol. Rev. 62, 405-496
43. Kessels, H. W., and Malinow, R. (2009) SynapticAMPAreceptor plasticity and behavior. Neuron 61, 340-350
44. Fukata, Y., and Fukata, M. (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat. Rev. Neurosci. 11, 161-175
45. Kang, R., Wan, J., Arstikaitis, P., Takahashi, H., Huang, K., Bailey, A. O., Thompson, J. X., Roth, A. F., Drisdel, R. C., Mastro, R., Green, W. N., Yates, J. R., 3rd, Davis, N. G., and El-Husseini, A. (2008) Neural palmitoylproteomics reveals dynamic synaptic palmitoylation. Nature 456, 904-909
46. Noritake, J., Fukata, Y., Iwanaga, T., Hosomi, N., Tsutsumi, R., Matsuda, N., Tani, H., Iwanari, H., Mochizuki, Y., Kodama, T., Matsuura, Y., Bredt, D. S., Hamakubo, T., and Fukata, M. (2009) Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95. J. Cell Biol. 186, 147-160
47. Martin, S., Nishimune, A., Mellor, J. R., and Henley, J. M. (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447, 321-325
48. Konopacki, F. A., Jaafari, N., Rocca, D. L., Wilkinson, K. A., Chamberlain, S., Rubin, P., Kantamneni, S., Mellor, J. R., and Henley, J. M. (2011) Agonist-induced PKC phosphorylation regulates GluK2 SUMOylation and kainate receptor endocytosis. Proc. Natl. Acad. Sci. U.S.A. 108, 19772-19777
49. Chamberlain, S. E., González-González, I. M., Wilkinson, K. A., Konopacki, F. A., Kantamneni, S., Henley, J. M., and Mellor, J. R. (2012) SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat. Neurosci. 15, 845-852
50. Horresh, I., Bar, V., Kissil, J. L., and Peles, E. (2010) Organization of myelinated axons by Caspr and Caspr2 requires the cytoskeletal adapter protein 4.1B. J. Neurosci. 30, 2480-2489
51. Buttermore, E. D., Dupree, J. L., Cheng, J., An, X., Tessarollo, L., and Bhat, M. A. (2011) The cytoskeletal adaptor protein band 4.1B is required for the maintenance of paranodal axoglial septate junctions in myelinated axons. J. Neurosci. 31, 8013-8024
52. Pinheiro, P. S., and Mulle, C. (2008) Presynaptic glutamate receptors. Physiological functions and mechanisms of action. Nat. Rev. Neurosci. 9, 423-436
53. Huyghe, D., Veran, J., Labrousse, V. F., Perrais, D., Mulle, C., and Coussen, F. (2011) Endocytosis of the glutamate receptor subunit GluK3 controls polarized trafficking. J. Neurosci. 31, 11645-11654
54. Garcia, E. P., Mehta, S., Blair, L. A., Wells, D. G., Shang, J., Fukushima, T., Fallon, J. R., Garner, C. C., and Marshall, J. (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21, 727-739
55. Heine, M., Groc, L., Frischknecht, R., Béïque, J.-C., Lounis, B., Rumbaugh, G., Huganir, R. L., Cognet, L., and Choquet, D. (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201-205
56. Petrini, E. M., Lu, J., Cognet, L., Lounis, B., Ehlers, M. D., and Choquet, D. (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92-105