2pku › Citations

Clustering and synaptic targeting of PICK1 requires direct interaction between the PDZ domain and lipid membranes.

Pan L, Wu H, Shen C, Shi Y, Jin W, Xia J, Zhang M
EMBO J 26 4576-87 (2007)
Cited: 59 times
EuropePMC logo PMID: 17914463

Abstract

Protein interacting with c kinase 1 (PICK1) regulates the trafficking of receptors and ion-channels such as AMPA receptors. Traditionally, the PICK1 PDZ domain is regarded as an adaptor capable of binding to receptors trafficked by PICK1, and the lipid-binding BAR domain functions to tether PICK1 directly to membranes. Here, we show that the PICK1 PDZ domain can directly interact with lipid membranes. The PDZ domain and lipid membrane interaction is mediated by both a polybasic amino-acid cluster and a conserved 'Cys-Pro-Cys' motif located away from the peptide ligand-binding groove. Disruption of the PDZ and lipid membrane interaction totally abolished synaptic targeting of PICK1. Although mutation of the CPC motif did not affect the interaction between PICK1 and AMPA receptors, the mutant PICK1 was unable to cluster the GluR2 subunit of the receptor. In neurons, PICK1 containing the same mutation displayed dramatically compromised capacity in the trafficking of AMPA receptors. Taken together, our findings not only uncovered the novel lipid membrane-binding property of the PICK1 PDZ domain, but also provided direct evidence supporting the functional relevance of the PDZ-lipid interaction.

Reviews - 2pku mentioned but not cited (2)

  1. Plasticity of PDZ domains in ligand recognition and signaling. Ivarsson Y. FEBS Lett 586 2638-2647 (2012)
  2. Emerging Themes in PDZ Domain Signaling: Structure, Function, and Inhibition. Liu X, Fuentes EJ. Int Rev Cell Mol Biol 343 129-218 (2019)

Articles - 2pku mentioned but not cited (7)

  1. Clustering and synaptic targeting of PICK1 requires direct interaction between the PDZ domain and lipid membranes. Pan L, Wu H, Shen C, Shi Y, Jin W, Xia J, Zhang M. EMBO J 26 4576-4587 (2007)
  2. Interaction prediction and classification of PDZ domains. Kalyoncu S, Keskin O, Gursoy A. BMC Bioinformatics 11 357 (2010)
  3. Putting into practice domain-linear motif interaction predictions for exploration of protein networks. Luck K, Fournane S, Kieffer B, Masson M, Nominé Y, Travé G. PLoS One 6 e25376 (2011)
  4. Binding free energy landscape of domain-peptide interactions. Staneva I, Wallin S. PLoS Comput Biol 7 e1002131 (2011)
  5. Exploring Protein-Peptide Binding Specificity through Computational Peptide Screening. Bhattacherjee A, Wallin S. PLoS Comput Biol 9 e1003277 (2013)
  6. 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)
  7. Three Binding Conformations of BIO124 in the Pocket of the PICK1 PDZ Domain. Stevens AO, Luo S, He Y. Cells 11 2451 (2022)


Reviews citing this publication (18)

  1. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Feng W, Zhang M. Nat Rev Neurosci 10 87-99 (2009)
  2. Let's go bananas: revisiting the endocytic BAR code. Qualmann B, Koch D, Kessels MM. EMBO J 30 3501-3515 (2011)
  3. Structures and target recognition modes of PDZ domains: recurring themes and emerging pictures. Ye F, Zhang M. Biochem J 455 1-14 (2013)
  4. PICK1: a multi-talented modulator of AMPA receptor trafficking. Hanley JG. Pharmacol Ther 118 152-160 (2008)
  5. Metabolism of the neuromodulator D-serine. Pollegioni L, Sacchi S. Cell Mol Life Sci 67 2387-2404 (2010)
  6. Postmortem brain: an underutilized substrate for studying severe mental illness. McCullumsmith RE, Hammond JH, Shan D, Meador-Woodruff JH. Neuropsychopharmacology 39 65-87 (2014)
  7. BAR domain proteins-a linkage between cellular membranes, signaling pathways, and the actin cytoskeleton. Carman PJ, Dominguez R. Biophys Rev 10 1587-1604 (2018)
  8. PDZ Domains as Drug Targets. Christensen NR, Čalyševa J, Fernandes EFA, Lüchow S, Clemmensen LS, Haugaard-Kedström LM, Strømgaard K. Adv Ther (Weinh) 2 1800143 (2019)
  9. Ligand binding by PDZ domains. Chi CN, Bach A, Strømgaard K, Gianni S, Jemth P. Biofactors 38 338-348 (2012)
  10. Structural diversity of PDZ-lipid interactions. Gallardo R, Ivarsson Y, Schymkowitz J, Rousseau F, Zimmermann P. Chembiochem 11 456-467 (2010)
  11. Protein Amphipathic Helix Insertion: A Mechanism to Induce Membrane Fission. Zhukovsky MA, Filograna A, Luini A, Corda D, Valente C. Front Cell Dev Biol 7 291 (2019)
  12. Deciphering the BAR code of membrane modulators. Salzer U, Kostan J, Djinović-Carugo K. Cell Mol Life Sci 74 2413-2438 (2017)
  13. Mechanisms of AMPA Receptor Endosomal Sorting. Parkinson GT, Hanley JG. Front Mol Neurosci 11 440 (2018)
  14. D-amino acids in the brain: the biochemistry of brain serine racemase. Baumgart F, Rodríguez-Crespo I. FEBS J 275 3538-3545 (2008)
  15. Role of phosphoinositides at the neuronal synapse. Frere SG, Chang-Ileto B, Di Paolo G. Subcell Biochem 59 131-175 (2012)
  16. Membrane Binding and Modulation of the PDZ Domain of PICK1. Erlendsson S, Madsen KL. Membranes (Basel) 5 597-615 (2015)
  17. Protein interacting with C kinase and neurological disorders. Focant MC, Hermans E. Synapse 67 532-540 (2013)
  18. Synapse formation and remodeling. Luo Z. Sci China Life Sci 53 315-321 (2010)

Articles citing this publication (32)

  1. Structural basis for the regulated protease and chaperone function of DegP. Krojer T, Sawa J, Schäfer E, Saibil HR, Ehrmann M, Clausen T. Nature 453 885-890 (2008)
  2. TARP phosphorylation regulates synaptic AMPA receptors through lipid bilayers. Sumioka A, Yan D, Tomita S. Neuron 66 755-767 (2010)
  3. Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Sheng R, Chen Y, Yung Gee H, Stec E, Melowic HR, Blatner NR, Tun MP, Kim Y, Kim Y, Källberg M, Fujiwara TK, Hye Hong J, Pyo Kim K, Lu H, Kusumi A, Goo Lee M, Cho W. Nat Commun 3 1249 (2012)
  4. Par-3-mediated junctional localization of the lipid phosphatase PTEN is required for cell polarity establishment. Feng W, Wu H, Chan LN, Zhang M. J Biol Chem 283 23440-23449 (2008)
  5. The intellectual disability protein RAB39B selectively regulates GluA2 trafficking to determine synaptic AMPAR composition. Mignogna ML, Giannandrea M, Gurgone A, Fanelli F, Raimondi F, Mapelli L, Bassani S, Fang H, Van Anken E, Alessio M, Passafaro M, Gatti S, Esteban JA, Huganir R, D'Adamo P. Nat Commun 6 6504 (2015)
  6. Genome-wide functional annotation of dual-specificity protein- and lipid-binding modules that regulate protein interactions. Chen Y, Sheng R, Källberg M, Silkov A, Tun MP, Bhardwaj N, Kurilova S, Hall RA, Honig B, Lu H, Cho W. Mol Cell 46 226-237 (2012)
  7. Membrane localization is critical for activation of the PICK1 BAR domain. Madsen KL, Eriksen J, Milan-Lobo L, Han DS, Niv MY, Ammendrup-Johnsen I, Henriksen U, Bhatia VK, Stamou D, Sitte HH, McMahon HT, Weinstein H, Gether U. Traffic 9 1327-1343 (2008)
  8. Protein interacting with C kinase 1 (PICK1) reduces reinsertion rates of interaction partners sorted to Rab11-dependent slow recycling pathway. Madsen KL, Thorsen TS, Rahbek-Clemmensen T, Eriksen J, Gether U. J Biol Chem 287 12293-12308 (2012)
  9. Site-Specific Phosphorylation of PSD-95 PDZ Domains Reveals Fine-Tuned Regulation of Protein-Protein Interactions. Pedersen SW, Albertsen L, Moran GE, Levesque B, Pedersen SB, Bartels L, Wapenaar H, Ye F, Zhang M, Bowen ME, Strømgaard K. ACS Chem Biol 12 2313-2323 (2017)
  10. Frizzled 7 and PIP2 binding by syntenin PDZ2 domain supports Frizzled 7 trafficking and signalling. Egea-Jimenez AL, Gallardo R, Garcia-Pino A, Ivarsson Y, Wawrzyniak AM, Kashyap R, Loris R, Schymkowitz J, Rousseau F, Zimmermann P. Nat Commun 7 12101 (2016)
  11. PICK1 is implicated in organelle motility in an Arp2/3 complex-independent manner. Madasu Y, Yang C, Boczkowska M, Bethoney KA, Zwolak A, Rebowski G, Svitkina T, Dominguez R. Mol Biol Cell 26 1308-1322 (2015)
  12. Protein interacting with C-kinase 1 (PICK1) binding promiscuity relies on unconventional PSD-95/discs-large/ZO-1 homology (PDZ) binding modes for nonclass II PDZ ligands. Erlendsson S, Rathje M, Heidarsson PO, Poulsen FM, Madsen KL, Teilum K, Gether U. J Biol Chem 289 25327-25340 (2014)
  13. PICK1 regulates the trafficking of ASIC1a and acidotoxicity in a BAR domain lipid binding-dependent manner. Jin W, Shen C, Jing L, Zha XM, Xia J. Mol Brain 3 39 (2010)
  14. Structure of Dimeric and Tetrameric Complexes of the BAR Domain Protein PICK1 Determined by Small-Angle X-Ray Scattering. Karlsen ML, Thorsen TS, Johner N, Ammendrup-Johnsen I, Erlendsson S, Tian X, Simonsen JB, Høiberg-Nielsen R, Christensen NM, Khelashvili G, Streicher W, Teilum K, Vestergaard B, Weinstein H, Gether U, Arleth L, Madsen KL. Structure 23 1258-1270 (2015)
  15. The BAR Domain Superfamily Proteins from Subcellular Structures to Human Diseases. Safari F, Suetsugu S. Membranes (Basel) 2 91-117 (2012)
  16. Prevalence, specificity and determinants of lipid-interacting PDZ domains from an in-cell screen and in vitro binding experiments. Ivarsson Y, Wawrzyniak AM, Kashyap R, Polanowska J, Betzi S, Lembo F, Vermeiren E, Chiheb D, Lenfant N, Morelli X, Borg JP, Reboul J, Zimmermann P. PLoS One 8 e54581 (2013)
  17. The BAR domain protein PICK1 controls vesicle number and size in adrenal chromaffin cells. Pinheiro PS, Jansen AM, de Wit H, Tawfik B, Madsen KL, Verhage M, Gether U, Sørensen JB. J Neurosci 34 10688-10700 (2014)
  18. Biochemical and computational analysis of LNX1 interacting proteins. Wolting CD, Griffiths EK, Sarao R, Prevost BC, Wybenga-Groot LE, McGlade CJ. PLoS One 6 e26248 (2011)
  19. The PDZ protein MPP2 interacts with c-Src in epithelial cells. Baumgartner M, Weiss A, Fritzius T, Heinrich J, Moelling K. Exp Cell Res 315 2888-2898 (2009)
  20. Cooperative phosphoinositide and peptide binding by PSD-95/discs large/ZO-1 (PDZ) domain of polychaetoid, Drosophila zonulin. Ivarsson Y, Wawrzyniak AM, Wuytens G, Kosloff M, Vermeiren E, Raport M, Zimmermann P. J Biol Chem 286 44669-44678 (2011)
  21. The binding affinities of proteins interacting with the PDZ domain of PICK1. Bolia A, Gerek ZN, Keskin O, Banu Ozkan S, Dev KK. Proteins 80 1393-1408 (2012)
  22. Structural insights into the PIP2 recognition by syntenin-1 PDZ domain. Sugi T, Oyama T, Morikawa K, Jingami H. Biochem Biophys Res Commun 366 373-378 (2008)
  23. Serine 77 in the PDZ domain of PICK1 is a protein kinase Cα phosphorylation site regulated by lipid membrane binding. Ammendrup-Johnsen I, Thorsen TS, Gether U, Madsen KL. Biochemistry 51 586-596 (2012)
  24. Palmitoylated Proteins in Dendritic Spine Remodeling. Albanesi JP, Barylko B, DeMartino GN, Jameson DM. Front Synaptic Neurosci 12 22 (2020)
  25. Threonine 82 at the PDZ domain of PICK1 is critical for AMPA receptor interaction and localization. Shao X, Zhu L, Wang Y, Lu Y, Wang W, Zhu J, Shen Y, Xia J, Luo J. Neurochem Int 56 962-970 (2010)
  26. Zinc binding site in PICK1 is dominantly located at the CPC motif of its PDZ domain. Shi Y, Zhang L, Yuan J, Xiao H, Yang X, Niu L. J Neurochem 106 1027-1034 (2008)
  27. Lock and chop: A novel method for the generation of a PICK1 PDZ domain and piperidine-based inhibitor co-crystal structure. Marcotte DJ, Hus JC, Banos CC, Wildes C, Arduini R, Bergeron C, Hession CA, Baker DP, Lin E, Guckian KM, Dunah AW, Silvian LF. Protein Sci 27 672-680 (2018)
  28. Letter The Challenges of Polydisperse SAXS Data Analysis: Two SAXS Studies of PICK1 Produce Different Structural Models. Boczkowska M, Rebowski G, Dominguez R. Structure 23 1967-1968 (2015)
  29. Bcl-2/Bax expression levels tend to influence AMPAergic trafficking mechanisms during hibernation in Mesocricetus auratus. Mele M, Alò R, Avolio E, Canonaco M. J Mol Neurosci 55 374-384 (2015)
  30. In-silico structural and functional characterization of a V. cholerae O395 hypothetical protein containing a PDZ1 and an uncommon protease domain. Dutta A, Katarkar A, Chaudhuri K. PLoS One 8 e56725 (2013)
  31. Residue-Level Contact Reveals Modular Domain Interactions of PICK1 Are Driven by Both Electrostatic and Hydrophobic Forces. Stevens AO, He Y. Front Mol Biosci 7 616135 (2020)
  32. Unconventional PDZ Recognition Revealed in α7 nAChR-PICK1 Complexes. Bondarenko V, Chen Q, Tillman TS, Xu Y, Tang P. ACS Chem Neurosci 15 2070-2079 (2024)


Quick links