The transmembrane domain C of AMPA receptors is critically involved in receptor function and modulation

Frontiers in Molecular Neuroscience

Volumn 3, Issue DEC, 2010, Pages

  Terhag, Jan ^a   Gottschling, Kevin ^a   Hollmann, Michael ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

AMPA receptor; Desensitization; Domain transplantation; Gating; TARP; Transmembrane domain

Indexed keywords

EID: 81155142109     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2010.00117     Document Type: Article

References (40)

1. Armstrong, D. J., and Roman, A. (1992). Mutagenesis of human papillomavirus types 6 and 16 E7 open reading frames alters the electrophoretic mobility of the expressed proteins. J. Gen. Virol. 73(Pt 5), 1275-1279.
2. Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., and Nicoll, R. A. (2000). Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943.
3. Collingridge, G. L., Isaac, J. T. R., and Wang, Y. T. (2004). Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952-962.
4. Collingridge, G. L., Olsen, R., Peters, J. A., and Spedding, M. (2009). Ligand gated ion channels. Neuropharmacology 56, 1.
5. Dunker, A. K., and Rueckert, R. R. (1969). Observations on molecular weight determinations on polyacrylamide gel. J. Biol. Chem. 244, 5074-5080.
6. Fasano, O., Aldrich, T., Tamanoi, F., Taparowsky, E., Furth, M., and Wigler, M. (1984). Analysis of the transforming potential of the human H-ras gene by random mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 81, 4008-4012.
7. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., and Malinow, R. (2000). Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267.
8. Hoffmann, J., Gorodetskaia, A., and Hollmann, M. (2006a). Ion pore properties of ionotropic glutamate receptors are modulated by a transplanted potassium channel selectivity filter. Mol. Cell Neurosci. 33, 335-343.
9. Hoffmann, J., Villmann, C., Werner, M., and Hollmann, M. (2006b). Investigation via ion pore transplantation of the putative relationship between glutamate receptors and K+ channels. Mol. Cell Neurosci. 33, 358-370.
10. Hollmann, M. (1999). "Structure of ionotropic glutamate receptors," in Handbook of Experimental Pharmacology, Vol. 141, eds P. Jonas and H. Monyer (Berlin: Springer-Verlag), 3-98.
11. Hollmann, M., Boulter, J., Maron, C., and Heinemann, S. (1994). Molecular biology of glutamate receptors. Potentiation of N-methyl-D-aspartate receptor splice variants by zinc. Ren. Physiol. Biochem. 17, 182-183.
12. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
13. Horak, M., Chang, K., and Wenthold, R. J. (2008). Masking of the endoplasmic reticulum retention signals during assembly of the NMDA receptor. J. Neurosci. 28, 3500-3509.
14. Jang, M.-K., Mierke, D. F., Russek, S. J., and Farb, D. H. (2004). A steroid modulatory domain on NR2B controls N-methyl-D-aspartate receptor proton sensitivity. Proc. Natl. Acad. Sci. U.S.A. 101, 8198-8203.
15. Javadpour, M. M., Eilers, M., Groesbeek, M., and Smith, S. O. (1999). Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys. J. 77, 1609-1618.
16. Kott, S., Werner, M., Körber, C., and Hollmann, M. (2007). Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J. Neurosci. 27, 3780-3789.
17. Kuner, T., Seeburg, P. H., and Guy, H. R. (2003). A common architecture for K+ channels and ionotropic glutamate receptors? Trends Neurosci. 26, 27-32.
18. Kuryatov, A., Laube, B., Betz, H., and Kuhse, J. (1994). Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 12, 1291-1300.
19. Lerma, J. (2003). Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481-495.
20. McBain, C. J., and Mayer, M. L. (1994). N-methyl-D-aspartic acid receptor structure and function. Physiol. Rev. 74, 723-760.
21. O'Hara, P. J., Sheppard, P. O., Thøgersen, H., Venezia, D., Haldeman, B. A., McGrane, V., Houamed, K. M., Thomsen, C., Gilbert, T. L., and Mulvihill, E. R. (1993). The ligandbinding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11, 41-52.
22. Priel, A., Kolleker, A., Ayalon, G., Gillor, M., Osten, P., and Stern-Bach, Y. (2005). Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25, 2682-2686.
23. Ren, H., Honse, Y., Karp, B. J., Lipsky, R. H., and Peoples, R. W. (2003a). A site in the fourth membrane-associated domain of the N-methyl-D-aspartate receptor regulates desensitization and ion channel gating. J. Biol. Chem. 278, 276-283.
24. Ren, H., Honse, Y., and Peoples, R. W. (2003b). A site of alcohol action in the fourth membrane-associated domain of the N-methyl-D-aspartate receptor. J. Biol. Chem. 278, 48815-48820.
25. Rosenmund, C., Stern-Bach, Y., and Stevens, C. F. (1998). The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599.
26. Rozas, J. L., Paternain, A. V., and Lerma, J. (2003). Noncanonical signaling by ionotropic kainate receptors. Neuron 39, 543-553.
27. Schmid, S. M., Kott, S., Sager, C., Huelsken, T., and Hollmann, M. (2009). The glutamate receptor subunit delta2 is capable of gating its intrinsic ion channel as revealed by ligand binding domain transplantation. Proc. Natl. Acad. Sci. U.S.A. 106, 10320-10325.
28. Schmidt, C., Werner, M., and Hollmann, M. (2006). Revisiting the postulated "unitary glutamate receptor": electrophysiological and pharmacological analysis in two heterologous expression systems fails to detect evidence for its existence. Mol. Pharmacol. 69, 119-129.
29. Seeburg, P. H., Higuchi, M., and Sprengel, R. (1998). RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res. Brain Res. Rev. 26, 217-229.
30. Sheng, M., and Lee, S. H. (2001). AMPA receptor trafficking and the control of synaptic transmission. Cell 105, 825-828.
31. Sobolevsky, A. I., Rosconi, M. P., and Gouaux, E. (2009). X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756.
32. Sommer, B., Keinänen, K., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Köhler, M., Takagi, T., Sakmann, B., and Seeburg, P. H. (1990). Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580-1585.
33. Strutz-Seebohm, N., Werner, M., Madsen, D. M., Seebohm, G., Zheng, Y., Walker, C. S., Maricq, A. V., and Hollmann, M. (2003). Functional analysis of Caenorhabditis elegans glutamate receptor subunits by domain transplantation. J. Biol. Chem. 278, 44691-44701.
34. Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., and Gouaux, E. (2002). Mechanism of glutamate receptor desensitization. Nature 417, 245-253.
35. Tapken, D., and Hollmann, M. (2008). Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. J. Mol. Biol. 383, 36-48.
36. Turetsky, D., Garringer, E., and Patneau, D. K. (2005). Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J. Neurosci. 25, 7438-7448.
37. Vandenberghe, W., Nicoll, R. A., and Bredt, D. S. (2005). Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. J. Neurosci. 25, 1095-1102.
38. Villmann, C., Hoffmann, J., Werner, M., Kott, S., Strutz-Seebohm, N., Nilsson, T., and Hollmann, M. (2008). Different structural requirements for functional ion pore transplantation suggest different gating mechanisms of NMDA and kainate receptors. J. Neurochem. 107, 453-465.
39. Villmann, C., Strutz, N., Morth, T., and Hollmann, M. (1999). Investigation by ion channel domain transplantation of rat glutamate receptor subunits, orphan receptors and a putative NMDA receptor subunit. Eur. J. Neurosci. 11, 1765-1778.
40. Wenthold, R. J., Petralia, R. S., Blahos, J. II., and Niedzielski, A. S. (1996). Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989.