Home LiteratureArticle Details
PMID: 10629226 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering.

The Journal of cell biology ·Vol. 148 ·No. 1 ·2000-01-10 ·Pages 159-72

El-Husseini AE, Craven SE, Chetkovich DM, Firestein BL, Schnell E, Aoki C, Bredt DS

Abstract

Postsynaptic density-95 (PSD-95/SAP-90) is a palmitoylated peripheral membrane protein that scaffolds ion channels at excitatory synapses. To elucidate mechanisms for postsynaptic ion channel clustering, we analyzed the cellular trafficking of PSD-95. We find that PSD-95 transiently associates with a perinuclear membranous compartment and traffics with vesiculotubular structures, which migrate in a microtubule-dependent manner. Trafficking of PSD-95 with these vesiculotubular structures requires dual palmitoylation, which is specified by five consecutive hydrophobic residues at the NH(2) terminus. Mutations that disrupt dual palmitoylation of PSD-95 block both ion channel clustering by PSD-95 and its synaptic targeting. Replacing the palmitoylated NH(2) terminus of PSD-95 with alternative palmitoylation motifs at either the NH(2) or COOH termini restores ion channel clustering also induces postsynaptic targeting, respectively. In brain, we find that PSD-95 occurs not only at PSDs but also in association with intracellular smooth tubular structures in dendrites and spines. These data imply that PSD-95 is an itinerant vesicular protein; initial targeting of PSD-95 to an intracellular membrane compartment may participate in postsynaptic ion channel clustering by PSD-95.

MeSH Terms
Animals Biological Transport Brefeldin A/pharmacology Cell Line Cell Nucleus/metabolism Cell Polarity Cerebral Cortex/cytology Consensus Sequence Disks Large Homolog 4 Protein Dogs Epithelial Cells/metabolism Green Fluorescent Proteins Guanylate Kinases Humans Intracellular Signaling Peptides and Proteins Kv1.4 Potassium Channel Luminescent Proteins/genetics,metabolism Membrane Proteins Nerve Tissue Proteins/genetics,metabolism Neurons/metabolism Nocodazole/pharmacology Nucleoside-Phosphate Kinase/metabolism Palmitic Acids/metabolism Potassium Channels/metabolism Potassium Channels, Voltage-Gated Rats Recombinant Fusion Proteins/genetics,metabolism SAP90-PSD95 Associated Proteins Synapses
Chemicals
Disks Large Homolog 4 Protein Dlg4 protein, rat Intracellular Signaling Peptides and Proteins KCNA4 protein, human Kcna4 protein, rat Kv1.4 Potassium Channel Luminescent Proteins Membrane Proteins Nerve Tissue Proteins Palmitic Acids Potassium Channels Potassium Channels, Voltage-Gated Recombinant Fusion Proteins SAP90-PSD95 Associated Proteins postsynaptic density proteins Green Fluorescent Proteins Brefeldin A Nucleoside-Phosphate Kinase Guanylate Kinases Nocodazole
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
El-Husseini A E
Department of Physiology, University of California at San Francisco, San Francisco, California 94143, USA.
Craven S E
Chetkovich D M
Firestein B L
Schnell E
Aoki C
Bredt D S
References (35)
35 references, click to expand
  1. PDZ proteins organize synaptic signaling pathways.
    Cell. 1998 May 15;93(4):495-8 PMID: 9604925
  2. N-terminal palmitoylation of PSD-95 regulates association with cell membranes and interaction with K+ channel Kv1.4.
    Neuron. 1998 Jan;20(1):125-34 PMID: 9459448
  3. Signal transduction molecules at the glutamatergic postsynaptic membrane.
    Brain Res Brain Res Rev. 1998 May;26(2-3):243-57 PMID: 9651538
  4. Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane.
    J Cell Sci. 1998 Aug;111 ( Pt 16):2365-76 PMID: 9683631
  5. LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia.
    Cell. 1998 Sep 18;94(6):751-9 PMID: 9753322
  6. Paralemmin, a prenyl-palmitoyl-anchored phosphoprotein abundant in neurons and implicated in plasma membrane dynamics and cell process formation.
    J Cell Biol. 1998 Nov 2;143(3):795-813 PMID: 9813098
  7. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein.
    Nature. 1998 Dec 3;396(6710):433-9 PMID: 9853749
  8. The subcellular distribution of nitric oxide synthase relative to the NR1 subunit of NMDA receptors in the cerebral cortex.
    Prog Brain Res. 1998;118:83-97 PMID: 9932436
  9. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1.
    Neuron. 1999 Jan;22(1):179-87 PMID: 10027300
  10. Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs.
    Neuron. 1999 Mar;22(3):497-509 PMID: 10197530
  11. Expression of NR2 receptor subunit in rat somatic sensory cortex: synaptic distribution and colocalization with NR1 and PSD-95.
    J Comp Neurol. 1999 Aug 9;410(4):599-611 PMID: 10398051
  12. Molecular determinants for subcellular localization of PSD-95 with an interacting K+ channel.
    Neuron. 1999 May;23(1):149-57 PMID: 10402201
  13. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein.
    Neuron. 1992 Nov;9(5):929-42 PMID: 1419001
  14. SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A.
    J Biol Chem. 1993 Mar 5;268(7):4580-3 PMID: 7680343
  15. Analysis of the palmitoylation and membrane targeting domain of neuromodulin (GAP-43) by site-specific mutagenesis.
    Biochemistry. 1993 Oct 12;32(40):10714-9 PMID: 8399217
  16. Signal-dependent membrane protein trafficking in the endocytic pathway.
    Annu Rev Cell Biol. 1993;9:129-61 PMID: 8280459
  17. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95.
    Science. 1995 Sep 22;269(5231):1737-40 PMID: 7569905
  18. Interaction of tyrosine-based sorting signals with clathrin-associated proteins.
    Science. 1995 Sep 29;269(5232):1872-5 PMID: 7569928
  19. Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases.
    Nature. 1995 Nov 2;378(6552):85-8 PMID: 7477295
  20. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains.
    Cell. 1996 Mar 8;84(5):757-67 PMID: 8625413
  21. PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses.
    J Neurosci. 1996 Feb 15;16(4):1380-8 PMID: 8778289
  22. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites.
    Mol Biol Cell. 1996 Apr;7(4):631-50 PMID: 8730104
  23. Cloning and characterization of postsynaptic density 93, a nitric oxide synthase interacting protein.
    J Neurosci. 1996 Dec 1;16(23):7407-15 PMID: 8922396
  24. Use of electron microscopy in the detection of adrenergic receptors.
    Methods Mol Biol. 2000;126:535-63 PMID: 10685434
  25. The mannose 6-phosphate receptor and the biogenesis of lysosomes.
    Cell. 1988 Feb 12;52(3):329-41 PMID: 2964276
  26. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture.
    Cell. 1990 Jul 13;62(1):63-72 PMID: 2163770
  27. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding.
    J Neurosci Methods. 1990 Aug;33(2-3):113-27 PMID: 1977960
  28. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic.
    Cell. 1991 Nov 1;67(3):601-16 PMID: 1682055
  29. Essential role for dlg in synaptic clustering of Shaker K+ channels in vivo.
    J Neurosci. 1997 Jan 1;17(1):152-9 PMID: 8987744
  30. Disulfide-linked head-to-head multimerization in the mechanism of ion channel clustering by PSD-95.
    Neuron. 1997 May;18(5):803-14 PMID: 9182804
  31. Interaction of ion channels and receptors with PDZ domain proteins.
    Curr Opin Neurobiol. 1997 Jun;7(3):368-73 PMID: 9232802
  32. Ion channel targeting in neurons.
    Bioessays. 1997 Oct;19(10):847-53 PMID: 9363678
  33. Golgi tubule traffic and the effects of brefeldin A visualized in living cells.
    J Cell Biol. 1997 Dec 1;139(5):1137-55 PMID: 9382862
  34. Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg.
    Neuron. 1997 Nov;19(5):1007-16 PMID: 9390515
  35. The polarized sorting of membrane proteins expressed in cultured hippocampal neurons using viral vectors.
    Neuron. 1998 May;20(5):855-67 PMID: 9620691
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2000-01-10
Pages
159-72
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2156213
Subset
IM
Grants
NEI NIH HHS · R01-EY08055 · United States
NINDS NIH HHS · R01-NS36017 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com