Crystal structure of the second PDZ domain of SAP97 in complex with a GluR-A C-terminal peptide

FEBS Journal

Volumn 273, Issue 22, 2006, Pages 5219-5229

  Von Ossowski, Ingemar ^a   Oksanen, Esko ^b   Von Ossowski, Lotta ^a   Cai, Chunlin ^a   Sundberg, Maria ^a   Goldman, Adrian ^a,b   Keinänen, Kari ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Crystal structure; GluR A; GluR1; PDZ domain; SAP97

Indexed keywords

GLUTAMATE RECEPTOR 1; PDZ PROTEIN; PROTEIN SAP97; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUTAMATE; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 33750535424     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05521.x     Document Type: Article

References (41)

1. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K & Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816.
2. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, et al. (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805-1811.
3. Lissin DV, Carroll RC, Nicoll RA, Malenka RC & von Zastrow M (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci 19, 1263-1272.
4. Bredt DS & Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40, 361-379.
5. Malinow R & Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25, 103-126.
6. Passafaro M, Piech V & Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4, 917-926.
7. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC & Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267.
8. Shi S, Hayashi Y, Esteban JA & Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343.
9. Piccini A & Malinow R (2002) Critical postsynaptic density 95/disc large/zonula occludens)1 interactions by glutamate receptor 1 (GluR1) and GluR2 required at different subcellular sites. J Neurosci 22, 5387-5392.
10. Kim CH, Takamiya K, Petralia RS, Sattler R, Yu S, Zhou W, Kalb R, Wenthold R & Huganir R (2005) Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat Neurosci 8, 985-987.
11. Leonard AS, Davare MA, Horne MC, Garner CC & Hell JW (1998) SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 273, 19518-19524.
12. Stricker NL & Huganir RL (2003) The PDZ domains of mLin-10 regulate its trans-Golgi network targeting and the surface expression of AMPA receptors. Neuropharmacology 45, 837-848.
13. Uchino S, Wada H, Honda S, Nakamura Y, Ondo Y, Uchiyama T, Tsutsumi M, Suzuki E, Hirasawa T & Kohsaka S (2006) Direct interaction of post-synaptic density-95/Dlg/ZO-1 domain-containing synaptic molecule Shank3 with GluR1 alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor. J Neurochem 97, 1203-1214.
14. Schulz TW, Nakagawa T, Licznerski P, Pawlak V, Kolleker A, Rozov A, Kim J, Dittgen T, Kohr G, Sheng M, et al. (2004) Actin/alpha-actinin-dependent transport of AMPA receptors in dendritic spines: role of the PDZ-LIM protein RIL. J Neurosci 24, 8584-8594.
15. Rumbaugh G, Sia GM, Garner CC & Huganir RL (2003) Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J Neurosci 23, 4567-4576.
16. Nakagawa T, Futai K, Lashuel HA, Lo I, Okamoto K, Walz T, Hayashi Y & Sheng M (2004) Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44, 453-467.
17. Wu H, Nash JE, Zamorano P & Garner CC (2002) Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking. J Biol Chem 277, 30928-30934.
18. Osterweil E, Wells DG & Mooseker MS (2005) A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J Cell Biol 168, 329-338.
19. von Ossowski L, Tossavainen H, von Ossowski I, Cai C, Aitio O, Fredriksson K, Permi P, Annila A & Keinänen K (2006) Peptide binding and NMR analysis of the interaction between SAP97 PDZ2 and GluR-A: potential involvement of a disulfide bond. Biochemistry 45, 5567-5575.
20. Cai C, Coleman SK, Niemi K & Keinänen K (2002) Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4- isoxazole propionate receptor subunit is determined by a novel sequence motif. J Biol Chem 277, 31484-31490.
21. Tochio H, Hung F, Li M, Bredt DS & Zhang M (2000) Solution structure and backbone dynamics of the second PDZ domain of postsynaptic density-95. J Mol Biol 295, 225-237.
22. Doyle DA, Lee A, Lewis J, Kim E, Sheng M & MacKinnon R (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85, 1067-1076.
23. Appleton BA, Zhang Y, Wu P, Yin JP, Hunziker W, Skelton NJ, Sidhu SS & Wiesmann C (2006) Comparative structural analysis of the Erbin PDZ domain and the first PDZ domain of ZO-1. Insights into determinants of PDZ domain specificity. J Biol Chem 281, 22312-22320.
24. Mehta S, Wu H, Garner CC & Marshall J (2001) Molecular mechanisms regulating the differential association of kainate receptor subunits with SAP90/PSD-95 and SAP97. J Biol Chem 276, 16092-16099.
25. Gardoni F, Mauceri D, Fiorentini C, Bellone C, Missale C, Cattabeni F & Di Luca M (2003) CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J Biol Chem 278, 44745-44752.
26. Lim IA, Hall DD & Hell JW (2002) Selectivity and promiscuity of the first and second PDZ domains of PSD-95 and synapse-associated protein 102. J Biol Chem 277, 21697-21711.
27. Morais Cabral JH, Petosa C, Sutcliffe MJ, Raza S, Byron O, Poy F, Marfatia SM, Chishti AH & Liddington RC (1996) Crystal structure of a PDZ domain. Nature 382, 649-652.
28. McGee AW, Dakoji SR, Olsen O, Bredt DS, Lim WA & Prehoda KE (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.
29. Tavares GA, Panepucci EH & Brunger AT (2001) Structural characterization of the intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. Mol Cell 8, 1313-1325.
30. Cai C, Li H, Rivera C & Keinänen K (2005) Interaction between SAP97 and PSD-95, two Maguk proteins involved in synaptic trafficking of AMPA receptors. J Biol Chem 281, 4267-4273.
31. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26, 795-800.
32. Long JF, Tochio H, Wang P, Fan JS, Sala C, Niethammer M, Sheng M & 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.
33. Vagin A & Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30, 1022-1025.
34. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Cryst D 50, 760-763.
35. Perrakis A, Morris R & Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6, 458-463.
36. Jones TA, Zou JY, Cowan SW & Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst A 47, 110-119.
37. Emsley P & Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Cryst D 60, 2126-2132.
38. Lovell SC, Davis IW, Arendall WB 3rd, de Bakker PI, Word JM, Prisant MG, Richardson JS & Richardson DC (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins 50, 437-450.
39. Krissinel E & Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Cryst D 60, 2256-2268.
40. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
41. Wallace AC, Laskowski RA & Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8, 127-134.