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

Journal of Cell Biology

Volumn 148, Issue 1, 2000, Pages 159-171

  El Husseini, Alaa E ^a   Craven, Sarah E ^a   Chetkovich, Dane M ^a   Firestein, Bonnie L ^a   Schnell, Eric ^a   Aoki, Chiye ^b   Bredt, David S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Clustering; MAGUK; Palmitoylation; PSD; Trafficking

Indexed keywords

ION CHANNEL; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL SELECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROTUBULE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SYNAPSE;

ANIMALS; BIOLOGICAL TRANSPORT; BREFELDIN A; CELL LINE; CELL NUCLEUS; CELL POLARITY; CEREBRAL CORTEX; CONSENSUS SEQUENCE; DOGS; EPITHELIAL CELLS; GREEN FLUORESCENT PROTEINS; GUANYLATE KINASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KV1.4 POTASSIUM CHANNEL; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NOCODAZOLE; NUCLEOSIDE-PHOSPHATE KINASE; PALMITIC ACIDS; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RECOMBINANT FUSION PROTEINS; SYNAPSES;

ANIMALIA;

EID: 0034627757     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.148.1.159     Document Type: Article

References (36)

1. Aoki, C., D.S. Bredt, S. Fenstemaker, and M. Lubin. 1998. The subcellular distribution of nitric oxide synthase relative to the NR1 subunit of NMDA receptors in the cerebral cortex. Prog. Brain Research. 118:83-97.
2. Aoki, C., H. Oviedo, L. Alexandre, and D.S. Bredt. 1999a. Synaptic membranous and cytoplasmic localization of PSD-95: EM-immunocytochemical detection with intact developing cortical neuropil. Soc. Neurosci. Abstr. 510.8: 1277.
3. Aoki, C., S. Rodrigues, and H. Kurose. 1999b. Use of electron microscopy in the detection of adrenergic receptors, in Methods in Molecular Biology: Adrenergic Receptor Protocols. C.M. Machinda, editor. Humana Press. 535-563.
4. Arnold, D.B., and D.E. Clapham. 1999. Molecular determinants for subcellular localization of PSD-95 with an interacting K+ channel. Neuron. 23:149-157.
5. Brenman, J.E., D.S. Chao, S.H. Gee, A.W. McGee, S.E. Craven, D.R. Santillano, F. Huang, H. Xia, M.F. Peters, S.C. Froehner, and D.S. Bredt. 1996a. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α-1 syntrophin mediated by PDZ motifs. Cell. 84:757-767.
6. Brenman, J.E., K.S. Christopherson, S.E. Craven, A.W. McGee, and D.S. Bredt. 1996b. Cloning and characterization of postsynaptic density 93 (PSD-93), a nitric oxide synthase interacting protein. J. Neurosci. 16:7407-7415.
7. Chan, J., C. Aoki, and V.M. Pickel. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods. 33:113-127.
8. Cho, K.O., C.A. Hunt, and M.B. Kennedy. 1992. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron. 9:929-942.
9. Cole, N.B., N. Sciaky, A. Marotta, J. Song, and J. Lippincott-Schwartz. 1996. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:631-650.
10. Craven, S.E., and D.S. Bredt. 1998. PDZ proteins organize synaptic signaling pathways. Cell. 93:495-498.
11. Craven, S.E., A.E. El-Husseini, and D.S. Bredt. 1999. Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron. 22:497-509.
12. Dotti, C.G., and K. Simons. 1990. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell. 62:63-72.
13. Griffiths, G., B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52: 329-341.
14. Hsueh, Y.P., E. Kim, and M. Sheng. 1997. Disulfide-linked head-to-head multimerization in the mechanism of ion channel clustering by PSD-95. Neuron. 18:803-814.
15. Hunt, A.C., L.J. Schenker, and M.B. Kennedy. 1996. PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J. Neurosci. 16:1380-1388.
16. Jareb, M., and G. Banker. 1998. The polarized sorting of membrane proteins expressed in cultured hippocampal neurons using viral vectors. Neuron. 20: 855-867.
17. Kennedy, M.B. 1998. Signal transduction molecules at the glutamatergic postsynaptic membrane, Brain Res. Rev. 26:243-257.
18. Kim, E., M. Niethammer, A. Rothschild, Y.N. Jan, and M. Sheng. 1995. Clustering of Shaker-type K+ channels by direct interaction with the PSD-95/ SAP90 family of membrane-associated guanylate kinases. Nature. 378:85-88.
19. Kistner, U., B.M. Wenzel, R. W. Veh, C. Cases-Langhoff, A.M. Garner, U. Appeltauer, B. Voss, E.D. Gundelfinger, and C.C. Garner. 1993. SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J. Biol Chem. 268:4580-4583.
20. Kornau, H.-C., L.T. Schenker, M.B. Kennedy, and P.H. Seeburg. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science. 269:1737-1740.
21. Kornau, H.-C., P.H. Seeburg, and M.B. Kennedy. 1997. Interaction of ion channels and receptors with PDZ domains. Curr. Opin. Neurobiol. 7:368-373.
22. Kutzleb, C., G. Sanders, R. Yamamoto, X. Wang, B. Lichte, E. Petrasch-Parwez, and M.W. Kilimann. 1998. Paralemmin, a prenyl-palmitoyl-anchored phosphoprotein abundant in neurons and implicated in plasma membrane dynamics and cell process formation. J. Cell Biol. 143:795-813.
23. Lippincott-Schwartz, J., L. Yuan, C. Tipper, M. Amherdt, L. Orci, and R.D. Klausner. 1991. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 67:601-616.
24. Liu, Y., D.A. Fisher, and D.R. Storm. 1993. Analysis of the palmitoylation and membrane targeting domain of neuromodulin (GAP-43) by site-specific mutagenesis. Biochemistry. 32:10714-10719.
25. Migaud, M., P. Charlesworth, M. Dempster, L.C. Webster, A.M. Watabe, M. Makhinson, Y. He, M.F. Ramsay, R.G. Morris. J.H. Morrison, T.J. O'Dell, and S.G. Grant. 1998. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:433-439.
26. Ohno, H., J. Stewart, M.C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J.S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science, 269: 1872-1875.
27. Rongo, C., C.W. Whitfield, A. Rodal, S.K. Kim, and J.M. Kaplan. 1998. LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell. 94:751-759.
28. Sciaky, N., J. Presley, C. Smith, K.J. Zaal, N. Cole, J.E. Moreira, M. Terasaki, E. Siggia, and J. Lippincott-Schwartz. 1997. Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139:1137-1155.
29. Sheng, M., and M. Wyszynski. 1997. Ion channel targeting in neurons. Bioessays. 19:847-853.
30. Tejedor, F.J., A. Bokhari, O. Rogero, M. Gorczyca, J. Zhang, E. Kim, M. Sheng, and V. Budnik. 1997. Essential role for dlg in synaptic clustering of Shaker K+ channels in vivo. J. Neurosci. 17:152-159.
31. Topinka, J.R., and D.S. Bredt. 1998. N-terminal palmitoylation of PSD-95 regulates association with cell membranes and interaction with K+ channel, Kv1.4. Neuron. 20:125-134.
32. Trowbridge, I.S., J.F. Collawn, and C.R. Hopkins. 1993 Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9:129-161.
33. Valtschanoff, J.G., A. Burette, R.J. Wenthold, and R.J. Weinberg. 1999. Expression of NR2 receptor subunit in rat somatic sensory cortex: synaptic distribution and colocalization with NR1 and PSD-95. J. Comp. Neurol. 410: 599-611.
34. Wu, H., S.M. Reuver, S. Kuhlendahl, W.J. Chung, and C.C. Garner. 1998. Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane. J. Cell Sci. 111:2365-2376.
35. Xia, J., X. Zhang, J. Staudinger, and R.L. Huganir. 1999. Clustering of AMPA Receptors by the synaptic PDZ domain-containing protein PICK1. Neuron. 22:179-187.
36. Zito, K., R.D. Fetter, C.S. Goodman, and E.Y. Isacoff. 1997. Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron. 19:1007-1016.