Vol. 15, No. 4, 2006/2007
Issue release date: June 2007
Neurosignals 2006–07;15:190–201
(DOI:10.1159/000098482)
Review
Add to my selection

Structure and Function of PICK1

Xu J. · Xia J.
Department of Biochemistry, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, SAR, China
email Corresponding Author


 goto top of outline Key Words

  • PICK1
  • PDZ domain
  • BAR domain
  • Protein trafficking
  • AMPA receptor
  • Long-term potentiation
  • Long-term depression
  • Synaptic plasticity
  • Lipid binding
  • Phosphoinositides

 goto top of outline Abstract

PICK1 is a peripheral membrane protein conserved from Caenorhabditis elegans to the human. It is expressed in many tissues with high levels in brain and testis. Inside cells, PICK1 is localized at the perinuclear region as well as specialized structures such as synapses of neurons. PICK1 contains a PDZ domain and a BAR domain. The PDZ domain of PICK1 binds to a large number of membrane proteins, especially proteins with C-terminal type II PDZ-binding motifs. The BAR domain of PICK1 binds to lipid molecules, mainly phosphoinositides. While the PDZ domain and the linker region of PICK1 enhance BAR domain’s lipid binding, the C-terminal region of PICK1 inhibits its lipid binding. PICK1 regulates the subcellular localization and surface expression of its PDZ-binding partners. Lipid binding of PICK1’s BAR domain is important for this regulation. With its PDZ domain interacting with membrane proteins and its BAR domain binding to lipids, the unique structure of PICK1 enables it to couple membrane proteins to protein-trafficking machinery.

Copyright © 2007 S. Karger AG, Basel


 goto top of outline References
  1. Staudinger J, Zhou J, Burgess R, Elledge SJ, Olson EN: PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J Cell Biol 1995;128:263–271.
  2. Gardner SM, Takamiya K, Xia J, et al: Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 2005;45:903–915.
  3. Steinberg JP, Takamiya K, Shen Y, et al: Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 2006;49:845–860.
  4. Xia J, Zhang X, Staudinger J, Huganir RL: Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 1999;22:179–187.
  5. Perez JL, Khatri L, Chang C, Srivastava S, Osten P, Ziff EB: PICK1 targets activated protein kinase Cα to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J Neurosci 2001;21:5417–5428.
  6. Torres GE, Yao WD, Mohn AR, et al: Functional interaction between monoamine plasma membrane transporters and the synaptic PDZ domain-containing protein PICK1. Neuron 2001;30:121–134.
  7. Torres R, Firestein BL, Dong H, et al: PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 1998;21:1453–1463.
  8. Jaulin-Bastard F, Saito H, Le Bivic A, et al: The ERBB2/HER2 receptor differentially interacts with ERBIN and PICK1 PSD-95/DLG/ZO-1 domain proteins. J Biol Chem 2001;276:15256–15263.
  9. McInvale AC, Staudinger J, Harlan RE, Garcia MM: Immunolocalization of PICK1 in the ascending auditory pathways of the adult rat. J Comp Neurol 2002;450:382–394.
  10. Wang WL, Yeh SF, Chang YI, et al: PICK1, an anchoring protein that specifically targets protein kinase Cα to mitochondria selectively upon serum stimulation in NIH 3T3 cells. J Biol Chem 2003;278:37705–37712.
  11. Sheng M, Sala C: PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 2001;24:1–29.
  12. Brenman JE, Chao DS, Gee SH, et al: Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 1996;84:757–767.
  13. Zimmermann P, Meerschaert K, Reekmans G, et al: PIP2-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol Cell 2002;9:1215–1225.
  14. Stricker NL, Christopherson KS, Yi BA, et al: PDZ domain of neuronal nitric oxide synthase recognizes novel C-terminal peptide sequences. Nat Biotechnol 1997;15:336–342.
  15. Tochio H, Zhang Q, Mandal P, Li M, Zhang M: Solution structure of the extended neuronal nitric oxide synthase PDZ domain complexed with an associated peptide. Nat Struct Biol 1999;6:417–421.
  16. Sheng M: Molecular organization of the postsynaptic specialization. Proc Natl Acad Sci USA 2001;98:7058–7061.
  17. Tsunoda S, Sierralta J, Sun Y, et al: A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 1997;388:243–249.
  18. Staudinger J, Lu J, Olson EN: Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-α. J Biol Chem 1997;272:32019–32024.
  19. Boudin H, Craig AM: Molecular determinants for PICK1 synaptic aggregation and mGluR7a receptor coclustering: role of the PDZ, coiled-coil, and acidic domains. J Biol Chem 2001;276:30270–30276.
  20. Madsen KL, Beuming T, Niv MY, et al: Molecular determinants for the complex binding specificity of the PDZ domain in PICK1. J Biol Chem 2005;280:20539–20548.
  21. Wigge P, McMahon HT: The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci 1998;21:339–344.
  22. Slepnev VI, De Camilli P: Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 2000;1:161–172.
  23. Takei K, Slepnev VI, Haucke V, De Camilli P: Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1999;1:33–39.
  24. Peter BJ, Kent HM, Mills IG, et al: BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004;303:495–499.
  25. Tarricone C, Xiao B, Justin N, et al: The structural basis of arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 2001;411:215–219.
  26. Jin W, Ge WP, Xu J, et al: Lipid binding regulates synaptic targeting of PICK1, AMPA receptor trafficking, and synaptic plasticity. J Neurosci 2006;26:2380–2390.
  27. Takeya R, Takeshige K, Sumimoto H: Interaction of the PDZ domain of human PICK1 with class I ADP- ribosylation factors. Biochem Biophys Res Commun 2000;267:149–155.
  28. Hanley JG, Khatri L, Hanson PI, Ziff EB: NSF ATPase and α-/β-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 2002;34:53–67.
  29. Dong H, Zhang P, Song I, Petralia RS, Liao D, Huganir RL: Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2. J Neurosci 1999;19:6930–6941.
  30. Lu W, Ziff EB: PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 2005;47:407–421.
  31. Yawata S, Tsuchida H, Kengaku M, Hirano T: Membrane-proximal region of glutamate receptor δ2 subunit is critical for long-term depression and interaction with protein interacting with C kinase 1 in a cerebellar Purkinje neuron. J Neurosci 2006;26:3626–3633.
  32. Hanley JG, Henley JM: PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J 2005;24:3266–3278.
  33. Williams ME, Wu SC, McKenna WL, Hinck L: Surface expression of the netrin receptor UNC5H1 is regulated through a protein kinase C-interacting protein/protein kinase-dependent mechanism. J Neurosci 2003;23:11279–11288.
  34. Bartoe JL, McKenna WL, Quan TK, et al: Protein interacting with C-kinase 1/protein kinase Cα-mediated endocytosis converts netrin-1-mediated repulsion to attraction. J Neurosci 2006;26:3192–3205.
  35. Dev KK, Nishimune A, Henley JM, Nakanishi S: The protein kinase C-α binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharmacology 1999;38:635–644.
  36. Terashima A, Cotton L, Dev KK, et al: Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J Neurosci 2004;24:5381–5390.
  37. Bliss TV, Collingridge GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993;361:31–39.
  38. Malinow R, Malenka RC: AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002;25:103–126.
  39. Matsuda S, Launey T, Mikawa S, Hirai H: Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 2000;19:2765–2774.
  40. Xia J, Chung HJ, Wihler C, Huganir RL, Linden DJ: Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 2000;28:499–510.
  41. Kim CH, Chung HJ, Lee HK, Huganir RL: Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci USA 2001;98:11725–11730.
  42. Matsuda S, Mikawa S, Hirai H: Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J Neurochem 1999;73:1765–1768.
  43. Chung HJ, Xia J, Scannevin RH, Zhang X, Huganir RL: Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci 2000;20:7258–7267.
  44. Chung HJ, Steinberg JP, Huganir RL, Linden DJ: Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 2003;300:1751–1755.
  45. Seidenman KJ, Steinberg JP, Huganir R, Malinow R: Glutamate receptor subunit 2 serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J Neurosci 2003;23:9220–9228.
  46. Liu SQ, Cull-Candy SG: Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 2000;405:454–858.
  47. Liu SJ, Cull-Candy SG: Subunit interaction with PICK and GRIP controls Ca2+ permeability of AMPARs at cerebellar synapses. Nat Neurosci 2005;8:768–775.
  48. Pulver AE, Karayiorgou M, Lasseter VK, et al: Follow-up of a report of a potential linkage for schizophrenia on chromosome 22q12-q13.1. Part 2. Am J Med Genet 1994;54:44–50.
  49. Pulver AE, Karayiorgou M, Wolyniec PS, et al: Sequential strategy to identify a susceptibility gene for schizophrenia: report of potential linkage on chromosome 22q12-q13.1. Part 1. Am J Med Genet 1994;54:36–43.
  50. Coon H, Holik J, Hoff M, et al: Analysis of chromosome 22 markers in nine schizophrenia pedigrees. Am J Med Genet 1994;54:72–79.
  51. Schwab SG, Lerer B, Albus M, et al: Potential linkage for schizophrenia on chromosome 22q12-q13: a replication study. Am J Med Genet 1995;60:436–443.
  52. DeLisi LE, Shaw SH, Crow TJ, et al: A genome-wide scan for linkage to chromosomal regions in 382 sibling pairs with schizophrenia or schizoaffective disorder. Am J Psychiatry 2002;159:803–812.
  53. Berrettini WH: Susceptibility loci for bipolar disorder: overlap with inherited vulnerability to schizophrenia. Biol Psychiatry 2000;47:245–251.
  54. Fujii K, Maeda K, Hikida T, et al: Serine racemase binds to PICK1: potential relevance to schizophrenia. Mol Psychiatry 2006;11:150–147.
  55. Hong CJ, Liao DL, Shih HL, Tsai SJ: Association study of PICK1 rs3952 polymorphism and schizophrenia. Neuroreport 2004;15:1965–1967.
  56. Beneyto M, Meador-Woodruff JH: Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia. Synapse 2006;60:585–598.
  57. Dracheva S, McGurk SR, Haroutunian V: mRNA expression of AMPA receptors and AMPA receptor binding proteins in the cerebral cortex of elderly schizophrenics. J Neurosci Res 2005;79:868–878.
  58. Cowan CA, Yokoyama N, Bianchi LM, Henkemeyer M, Fritzsch B: EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron 2000;26:417–430.
  59. Excoffon KJ, Hruska-Hageman A, Klotz M, Traver GL, Zabner J: A role for the PDZ-binding domain of the coxsackie B virus and adenovirus receptor (CAR) in cell adhesion and growth. J Cell Sci 2004;117:4401–4409.
  60. Hirbec H, Francis JC, Lauri SE, et al: Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 2003;37:625–638.
  61. Penzes P, Johnson RC, Sattler R, et al: The neuronal Rho-GEF kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 2001;29:229–242.
  62. El Far O, Airas J, Wischmeyer E, Nehring RB, Karschin A, Betz H: Interaction of the C-terminal tail region of the metabotropic glutamate receptor 7 with the protein kinase C substrate PICK1. Eur J Neurosci 2000;12:4215–4221.
  63. Meyer G, Varoqueaux F, Neeb A, Oschlies M, Brose N: The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 2004;47:724–733.
  64. Hruska-Hageman AM, Wemmie JA, Price MP, Welsh MJ: Interaction of the synaptic protein PICK1 (protein interacting with C kinase 1) with the non-voltage gated sodium channels BNC1 (brain Na+ channel 1) and ASIC (acid-sensing ion channel). Biochem J 2002;361:443–450.
  65. Duggan A, Garcia-Anoveros J, Corey DP: The PDZ domain protein PICK1 and the sodium channel BNaC1 interact and localize at mechanosensory terminals of dorsal root ganglion neurons and dendrites of central neurons. J Biol Chem 2002;277:5203–5208.
  66. Leonard AS, Yermolaieva O, Hruska-Hageman A, et al: cAMP-dependent protein kinase phosphorylation of the acid-sensing ion channel-1 regulates its binding to the protein interacting with C-kinase-1. Proc Natl Acad Sci USA 2003;100:2029–2034.
  67. Reymond N, Garrido-Urbani S, Borg JP, Dubreuil P, Lopez M: PICK-1: a scaffold protein that interacts with nectins and JAMs at cell junctions. FEBS Lett 2005;579:2243–2249.
  68. Boudin H, Doan A, Xia J, et al: Presynaptic clustering of mGluR7a requires the PICK1 PDZ domain binding site. Neuron 2000;28:485–497.
  69. Dev KK, Nakajima Y, Kitano J, Braithwaite SP, Henley JM, Nakanishi S: PICK1 interacts with and regulates PKC phosphorylation of mGLUR7. J Neurosci 2000;20:7252–7257.
  70. Enz R, Croci C: Different binding motifs in metabotropic glutamate receptor type 7b for filamin A, protein phosphatase 1C, protein interacting with protein kinase C (PICK) 1 and syntenin allow the formation of multimeric protein complexes. Biochem J 2003;372:183–191.
  71. Perroy J, El Far O, Bertaso F, et al: PICK1 is required for the control of synaptic transmission by the metabotropic glutamate receptor 7. EMBO J 2002;21:2990–2999.
  72. Lin SH, Arai AC, Wang Z, Nothacker HP, Civelli O: The carboxyl terminus of the prolactin-releasing peptide receptor interacts with PDZ domain proteins involved in α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor clustering. Mol Pharmacol 2001;60:916–923.
  73. Lin WJ, Chang YF, Wang WL, Huang CY: Mitogen-stimulated TIS21 protein interacts with a protein-kinase-Cα- binding protein rPICK1. Biochem J 2001;354:635–643.

 goto top of outline Author Contacts

Dr. Jun Xia
Department of Biochemistry
The Hong Kong University of Science and Technology
Kowloon, Hong Kong, SAR (China)
Tel. +852 2358 7274, Fax +852 2358 1552, E-Mail jxia@ust.hk


 goto top of outline Article Information

Received: September 2, 2006
Accepted after revision: October 11, 2006
Published online: January 11, 2007
Number of Print Pages : 12
Number of Figures : 4, Number of Tables : 1, Number of References : 73


 goto top of outline Publication Details

Neurosignals

Vol. 15, No. 4, Year 2006/2007 (Cover Date: June 2007)

Journal Editor: Ip, N.Y. (Hong Kong)
ISSN: 1424–862X (print), 1424–8638 (Online)

For additional information: http://www.karger.com/NSG


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.