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

von Ossowski I, Oksanen E, von Ossowski L, Cai C, Sundberg M, Goldman A, Keinänen K
FEBS J 273 5219-29 (2006)
Related entries: 2awu, 2aww, 2awx

Cited: 26 times
EuropePMC logo PMID: 17069616

Abstract

Synaptic targeting of GluR-A subunit-containing glutamate receptors involves an interaction with synapse-associated protein 97 (SAP97). The C-terminus of GluR-A, which contains a class I PDZ ligand motif (-x-Ser/Thr-x-phi-COOH where phi is an aliphatic amino acid) associates preferentially with the second PDZ domain of SAP97 (SAP97(PDZ2)). To understand the structural basis of this interaction, we have determined the crystal structures of wild-type and a SAP97(PDZ2) variant in complex with an 18-mer C-terminal peptide (residues 890-907) of GluR-A and of two variant PDZ2 domains in unliganded state at 1.8-2.44 A resolutions. SAP97(PDZ2) folds to a compact globular domain comprising six beta-strands and two alpha-helices, a typical architecture for PDZ domains. In the structure of the peptide complex, only the last four C-terminal residues of the GluR-A are visible, and align as an antiparallel beta-strand in the binding groove of SAP97(PDZ2). The free carboxylate group and the aliphatic side chain of the C-terminal leucine (Leu907), and the hydroxyl group of Thr905 of the GluR-A peptide are engaged in essential class I PDZ interactions. Comparison between the free and complexed structures reveals conformational changes which take place upon peptide binding. The betaAlpha-betaBeta loop moves away from the C-terminal end of alphaB leading to a slight opening of the binding groove, which may better accommodate the peptide ligand. The two conformational states are stabilized by alternative hydrogen bond and coulombic interactions of Lys324 in betaAlpha-betaBeta loop with Asp396 or Thr394 in betaBeta. Results of in vitro binding and immunoprecipitation experiments using a PDZ motif-destroying L907A mutation as well as the insertion of an extra alanine residue between the C-terminal Leu907 and the stop codon are also consistent with a 'classical' type I PDZ interaction between SAP97 and GluR-A C-terminus.

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  1. The plastic energy landscape of protein folding: a triangular folding mechanism with an equilibrium intermediate for a small protein domain. Haq SR, Jürgens MC, Chi CN, Koh CS, Elfström L, Selmer M, Gianni S, Jemth P. J Biol Chem 285 18051-18059 (2010)
  2. SAP97 controls the trafficking and resensitization of the beta-1-adrenergic receptor through its PDZ2 and I3 domains. Nooh MM, Naren AP, Kim SJ, Xiang YK, Bahouth SW. PLoS One 8 e63379 (2013)
  3. Structural characterization and computational analysis of PDZ domains in Monosiga brevicollis. Gao M, Mackley IGP, Mesbahi-Vasey S, Bamonte HA, Struyvenberg SA, Landolt L, Pederson NJ, Williams LI, Bahl CD, Brooks L, Amacher JF. Protein Sci 29 2226-2244 (2020)
  4. Schizophrenia-associated SAP97 mutations increase glutamatergic synapse strength in the dentate gyrus and impair contextual episodic memory in rats. Kay Y, Tsan L, Davis EA, Tian C, Décarie-Spain L, Sadybekov A, Pushkin AN, Katritch V, Kanoski SE, Herring BE. Nat Commun 13 798 (2022)


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  1. Ligand binding by PDZ domains. Chi CN, Bach A, Strømgaard K, Gianni S, Jemth P. Biofactors 38 338-348 (2012)
  2. Modulation of behavior by scaffolding proteins of the post-synaptic density. Gao C, Tronson NC, Radulovic J. Neurobiol Learn Mem 105 3-12 (2013)
  3. Allosterism in the PDZ Family. Stevens AO, He Y. Int J Mol Sci 23 1454 (2022)
  4. Peptide Targeting of PDZ-Dependent Interactions as Pharmacological Intervention in Immune-Related Diseases. Gutiérrez-González LH, Rivas-Fuentes S, Guzmán-Beltrán S, Flores-Flores A, Rosas-García J, Santos-Mendoza T. Molecules 26 6367 (2021)

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  1. Synaptic SAP97 isoforms regulate AMPA receptor dynamics and access to presynaptic glutamate. Waites CL, Specht CG, Härtel K, Leal-Ortiz S, Genoux D, Li D, Drisdel RC, Jeyifous O, Cheyne JE, Green WN, Montgomery JM, Garner CC. J Neurosci 29 4332-4345 (2009)
  2. Mechanism underlying selective regulation of G protein-gated inwardly rectifying potassium channels by the psychostimulant-sensitive sorting nexin 27. Balana B, Maslennikov I, Kwiatkowski W, Stern KM, Bahima L, Choe S, Slesinger PA. Proc Natl Acad Sci U S A 108 5831-5836 (2011)
  3. Crystallographic and nuclear magnetic resonance evaluation of the impact of peptide binding to the second PDZ domain of protein tyrosine phosphatase 1E. Zhang J, Sapienza PJ, Ke H, Chang A, Hengel SR, Wang H, Phillips GN, Lee AL. Biochemistry 49 9280-9291 (2010)
  4. Resequencing and Association Analysis of Six PSD-95-Related Genes as Possible Susceptibility Genes for Schizophrenia and Autism Spectrum Disorders. Xing J, Kimura H, Wang C, Ishizuka K, Kushima I, Arioka Y, Yoshimi A, Nakamura Y, Shiino T, Oya-Ito T, Takasaki Y, Uno Y, Okada T, Iidaka T, Aleksic B, Mori D, Ozaki N. Sci Rep 6 27491 (2016)
  5. Evolutionary expansion and specialization of the PDZ domains. Sakarya O, Conaco C, Egecioglu O, Solla SA, Oakley TH, Kosik KS. Mol Biol Evol 27 1058-1069 (2010)
  6. Structural basis of beta-catenin recognition by Tax-interacting protein-1. Zhang J, Yan X, Shi C, Yang X, Guo Y, Tian C, Long J, Shen Y. J Mol Biol 384 255-263 (2008)
  7. Molecular mechanism of inward rectifier potassium channel 2.3 regulation by tax-interacting protein-1. Yan X, Zhou H, Zhang J, Shi C, Xie X, Wu Y, Tian C, Shen Y, Long J. J Mol Biol 392 967-976 (2009)
  8. Interaction of the RhoA exchange factor Net1 with discs large homolog 1 protects it from proteasome-mediated degradation and potentiates Net1 activity. Carr HS, Cai C, Keinänen K, Frost JA. J Biol Chem 284 24269-24280 (2009)
  9. In vitro and in vivo analysis of the binding of the C terminus of the HDL receptor scavenger receptor class B, type I (SR-BI), to the PDZ1 domain of its adaptor protein PDZK1. Kocher O, Birrane G, Tsukamoto K, Fenske S, Yesilaltay A, Pal R, Daniels K, Ladias JA, Krieger M. J Biol Chem 285 34999-35010 (2010)
  10. Molecular basis for the recognition of adenomatous polyposis coli by the Discs Large 1 protein. Zhang Z, Li H, Chen L, Lu X, Zhang J, Xu P, Lin K, Wu G. PLoS One 6 e23507 (2011)
  11. A physical model for PDZ-domain/peptide interactions. Kaufmann K, Shen N, Mizoue L, Meiler J. J Mol Model 17 315-324 (2011)
  12. Sorting of β1-adrenergic receptors is mediated by pathways that are either dependent on or independent of type I PDZ, protein kinase A (PKA), and SAP97. Nooh MM, Chumpia MM, Hamilton TB, Bahouth SW. J Biol Chem 289 2277-2294 (2014)
  13. Conformational change upon ligand binding and dynamics of the PDZ domain from leukemia-associated Rho guanine nucleotide exchange factor. Liu J, Zhang J, Yang Y, Huang H, Shen W, Hu Q, Wang X, Wu J, Shi Y. Protein Sci 17 1003-1014 (2008)
  14. Identification of the PDZ3 domain of the adaptor protein PDZK1 as a second, physiologically functional binding site for the C terminus of the high density lipoprotein receptor scavenger receptor class B type I. Kocher O, Birrane G, Yesilaltay A, Shechter S, Pal R, Daniels K, Krieger M. J Biol Chem 286 25171-25186 (2011)
  15. Corticotropin-Releasing Hormone Receptor Type 1 (CRHR1) Clustering with MAGUKs Is Mediated via Its C-Terminal PDZ Binding Motif. Bender J, Engeholm M, Ederer MS, Breu J, Møller TC, Michalakis S, Rasko T, Wanker EE, Biel M, Martinez KL, Wurst W, Deussing JM. PLoS One 10 e0136768 (2015)
  16. Cysteine 893 is a target of regulatory thiol modifications of GluA1 AMPA receptors. von Ossowski L, Li LL, Möykkynen T, Coleman SK, Courtney MJ, Keinänen K. PLoS One 12 e0171489 (2017)
  17. Molecular analysis of the prostacyclin receptor's interaction with the PDZ1 domain of its adaptor protein PDZK1. Birrane G, Mulvaney EP, Pal R, Kinsella BT, Kocher O. PLoS One 8 e53819 (2013)
  18. Investigating the allosteric response of the PICK1 PDZ domain to different ligands with all-atom simulations. Stevens AO, Kazan IC, Ozkan B, He Y. Protein Sci 31 e4474 (2022)


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