Small-angle X-ray scattering and NMR studies of the conformation of the PDZ region of SAP97 and its interactions with Kir2.1

Biochemistry

Volumn 46, Issue 49, 2007, Pages 14117-14128

  Goult, Benjamin T ^a   Rapley, Jonathan D ^b,c   Dart, Caroline ^d   Kitmitto, Ashraf ^e   Grossmann, J Günter ^f   Leyland, Mark L ^a   Lian, Lu Yun ^d  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f SCIENCE AND TECHNOLOGY FACILITIES COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL DYNAMICS; CYTOPLASMIC DOMAIN; INTERDOMAIN CONTACTS;

CONFORMATIONS; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; X RAY SCATTERING;

PROTEINS;

GUANYLATE CYCLASE; MEMBRANE PROTEIN; PROTEIN SAP97; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; ISOTOPE LABELING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; RADIATION SCATTERING; RAT; SPECTROSCOPY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; MEMBRANE PROTEINS; MICE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PDZ DOMAINS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN CONFORMATION; RATS; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

EID: 37049001482     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701257z     Document Type: Article

References (48)

1. Lahey, T., Gorczyca, M., Jia, X. X., and Budnik, V. (1994) The Drosophila tumor suppressor gene Dlg is required for normal synaptic bouton structure, Neuron 13, 823-835.
2. Mitic, L. L., and Anderson, J. M. (1998) Molecular architecture of tight junction, Annu. Rev. Physiol. 60, 121-142.
3. Rafael, J. A., Hutchinson, T. L., Lumeng, C. N., Marfatia, S. M., Chishti, A. H., and Chamberlain, J. S. (1998) Localization of Dlg at the mammalian neuromuscular junction, Neuroreport 9, 2121-2125.
4. Boekers, T. M. (2006) The postsynaptic density, Cell Tissue Res. 326, 409-422.
5. Muller, B. M., Kistner, U., Veh, R. W., Cases-Langhoff, C., Becker, B., Gungelfinger, E. D., and Garner, C. C. (1995) Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein, J. Neurosci. 15, 2354-2366.
6. Hata, Y., Nakanishi, H., and Takai, Y. (1998) Synaptic PDZ domain-containing protein, Neurosci. Res. 32, 1-7.
7. Feng, W., Long, J. F., Fan, J. S., Suetake, T., and Zhang, M. (2004) The tetrameric L27 domain complex as an organizational platform for supramolecular assemblies, Nat. Struct. Mol. Biol. 11, 475-480.
8. Wang, L., Piserchio, A., and Mierke, D. F. (2005) Structural characterization of the intermolecular interactions of synapse-associated protein-97 with the NR2B subunit of N-methyl-D-aspartate receptors, J. Biol. Chem. 280, 26992-26996.
9. von Ossowski, I., Oksanen, E., von Ossowski, L., Cai, C., Sundberg, M., Goldman, A., and Keinänen, K. (2006) Crystal structure of the second PDZ domain of SAP97 in complex with a GluR-A C-terminal peptide, FEBS J. 273, 5219-5229.
10. Cabrai, J. H. M., Petosa, C., Sutcliffe, M. J., Raza, S., Byron, O., Poy, F., Marfatia, S. M., Chishti, A. H., and Liddington, R. C. (1996) Crystal structure of a PDZ domain, Nature (London, U.K.) 382, 649-652.
11. Zhang, Y., Dasgupta, J., Ma, R. L. Z., Banks, L., Thomas, M., and Chen, X. J. S. (2007) Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: Mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein, J. Virol. 81, 3618-3626.
12. McGee, A. W., Dakoji, S. R., Olsen, O., Bredt, D. S., Lim, W. A., and Prehoda K. A. (2001) Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins, Mol. Cell 8, 1291-1301.
13. Tavares, G. A., Panepucci, E. H., and Brunger, A. T. (2001) Structural characterization of the intramolecular interaction between SH3 and guanylate kinase domains of PSD-95, Mol. Cell 8, 1313-1325.
14. Nakagawa, T., Futai, K., Okamota, K., Walz, T., Hayashi, Y., and Sheng, M. (2004) Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions, Neuron 44, 453-467.
15. Wu, H. J., Reissner, C., Kuhlendahl, S., Coblentz, B., Reuver, S., Kindler, S., Gundelfinger, E. D., and Garner, C. C. (2000) Intramolecular interactions regulate SAP97 binding to GKAP, EMBO J. 19, 5740-5751.
16. Qian, Y., and Prehoda, K. E. (2006) Interdomain interactions in the tumor suppressor discs large regulate binding to the synaptic protein GukHolder, J. Biol. Chem. 281, 35757-35763.
17. Stanfield, P. R., Nakajima, S., and Nakajima, Y. (2002) Constitutively active and G-protein coupled inward rectifier K+ channels: Kir2.0 and Kir3.0, Rev. Physiol. Biochem. Pharmacol. 145, 47-179.
18. Nichols, C. G., and Lopatin, A. N. (1997) Inward rectifier potassium channels, Annu. Rev. Physiol. 59, 171-191.
19. Isomoto, S., Kondo, C., and Kurachi, Y. (1997) Inwardly rectifying potassium channels: Their molecular heterogeneity and function, Jpn. J. Physiol. 47, 11-39.
20. Cohen, N. A., Brenman, J. E., Snyder, S. H., and Bredt, D. S. (1996) Binding of the inward rectifier K+ channel Kir2.3 to PSD-95 is regulated by protein kinase A phosphorylation, Neuron 17, 759-767.
21. Nehring, R. B., Wischmeyer, E., Doring, F., Veh, R. W., Sheng, M., and Karschin, A. (2000) Neuronal inwardly rectifying K+ channels differentially couple to PDZ proteins of the PSD-95/SAP90 family, J. Neurosci. 20, 156-162.
22. Olsen, O., Liu, H., Wade, J. B., Merot, J., and Welling, P. A. (2002) Basolateral membrane expression of the Kir2.3 channel is coordinated by PDZ interaction with Lin-7/CASK complex, Am. J. Physiol. Cell Physiol. 282, 183-195.
23. Inanobe, A., Fujita, A., Ito, M., Tomoike, H., Inageda, K., and Kurachi, Y. (2002) Inward Rectifier K+ Channel Kir2.3 is localized at the postsynaptic membrane of excitatory synapses, Am. J. Physiol. Cell Physiol. 282, 1396-1403.
24. Leonoudakis, D., Mailliard, W. S., Wingerd, K. L., Clegg, D. O., and Vandenberg, C. A. (2001) Inward rectifier potassium channel Kir2.2 is associated with synapse-associated protein SAP97, J. Cell Sci. 114, 987-998.
25. Leonoudakis, D., Conti, L. R., Anderson, S., Radeke, C. M., McGuire, L. M. M., Adams, M. E., Froehner, S. C., Yates, J. R., and Vandenberg, C. A. (2004) Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins, J. Biol. Chem. 279, 22331-22346.
26. Leonoudakis, D., Conti, L. R., Radeke, C. M., McGuire, L. M. M., and Vandenberg, C. A. (2004) A multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels, J. Biol. Chem. 279, 19051-19063.
27. Nishida, M., and MacKinnon, R. (2002) Structural basis of inward rectification: Cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8 Å resolution, Cell 111, 957-965.
28. Kuo, A. L., Gulbis, J. M., Antcliff, J. F., Rahman, T., Lowe, E. D., Zimmer, J., Cuthbertson, J., Ashcroft, F. M., Ezaki, T., and Doyle, D. A. (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state, Science (Washington, DC, U.S.) 300, 1922-1926.
29. Pegan, S., Arrabit, C., Zhou, W., Kwiatkowski, W., Collins, A., Slesinger, P. A., and Choe, S. (2005) Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification, Nat. Neurosci. 8, 279-287.
30. Pegan, S., Tan, J., Huang, A., Slesinger, P. A., Riek, R., and Choe, S. (2007) NMR studies of interactions between C-terminal tail of Kir2.1 channel and PDZ12 domains of PSD-95, Biochemistry 46, 5315-5322.
31. Gardoni, F., Mauceri, D., Fiorentini, C., Bellone, C., Missale, C., Cattabeni, F., and Di Luca, M. (2002) CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction, J. Biol. Chem. 45, 44745-44752.
32. Peiretti, F., Deprez-Beauclair, P., Bonardo, B., Aubert, H., Juhan-Vague, I., and Nalbone, G. (2003) Identification of SAP97 as an intracellular binding partner of TACE, J. Cell. Sci. 116, 1949-1957.
33. Sabio, G., Arthur, J. S. C., Kuma, Y., Peggie, M., Carr, J., Murray-Tait, V., Centeno, F., Goedert, M., Morrice, N. A., and Cuenda, A. (2005) p38γ regulates the localization of SAP97 in the cytoskeleton by modulating its interaction with GKAP, EMBO J. 24, 1134-1145.
34. Folco, E. J., Liu, G. X., and Koren, G. (2004) Caveolin-3 and SAP97 form a scaffolding protein complex that regulates the voltage-gated potassium channel Kv 1.5, Am. J. Physiol.: Heart Circ. Physiol. 287, 681-690.
35. Lee, S. S., Weiss, R. S., and Javier, R. T. (1997) Binding of human virus oncoproteins to hDlgySAP97, a mammalian homologue of the Drosophila discs large tumor suppressor protein, Proc. Natl. Acad. Sci. U.S.A. 94, 6670-6675.
36. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) Nmrpipe: A multidimensional spectral processing system based on unix pipes, J. Biomol. NMR 6, 277-293.
37. Johnson, B. A., and Blevins, R. A. (1994) NMR View: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
38. Wishart, D. S., and Sykes, B. D. (1994) The C-13 chemical shift index: A simple method for the identification of protein secondary structure using C-13 chemical shift data, J. Biomol. NMR 4, 171-180.
39. Orekhov, V. Y., Nolde, D. E., Golovanov, A. P., Korzhnev, D. M., and Arseniev, A. S. (1995) Processing of heteronuclear NMR relaxation data with the new software DASHA, Appl. Magn. Reson. 9, 581-588.
40. Towns-Andrews, E., Berry, A., Bordas, J., Mant, P. K., Murray, K., Roberts, K., Sumner, I., Worgan, J. S., and Lewis, R. (1989) Time-resolved X-ray diffraction station: X-ray optics, detectors, and data acquisition, Rev. Sci. Instrum. 60, 2346-2349.
41. Lewis, R. (1994) Multiwire gas proportional counters: Decrepit antiques or classic performers, J. Synchrotron Radiat. 1, 43-53.
42. Grossmann, J. G., Hall, J. F., Kanbi, L. D., and Hasnain, S. S. (2002) The N-terminal extension of rusticyanin is not responsible for its acid stability, Biochemistry 41, 3613-3619.
43. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. J. (2001) Restoring low-resolution structure of biological macromolecules from solution scattering using simulated annealing, Biophys. J. 80, 2946-2953.
44. Petoukhov, M. V., and Svergun, D. I. (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data, Biophys. J. 89, 1237-1250.
45. Wu, S., and Zhang, Y. (2007) LOMETS: A local meta-threading-server for protein structure prediction, Nucleic Acids Res. 35, 3375-3382.
46. Long, J. F., Tochio, H., Wang, P., Fan, J. S., Sala, C., Niethammer, M., Sheng, M., and Zhang, M. (2003) Supramodular structure and synergistic target binding of the N-terminal tandem PDZ domains of PSD-95, J. Mol. Biol. 327, 203-214.
47. Battiste, J. L., and Wagner, G. (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear Overhauser effect data, Biochemistry 39, 5355-5365.
48. Grossmann, J. G. (2007) Biological solution scattering: Recent achievements and future challenges, J. Appl. Crystallogr. 40, 217-222.