DLG differentially localizes Shaker K+-channels in the central nervous system and retina of Drosophila

Journal of Neurochemistry

Volumn 82, Issue 6, 2002, Pages 1490-1501

  Ruiz Canada C ^a,b   Koh, Y H ^b   Budnik, V ^b   Tejedor, F J ^a,c  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c INSTITUTO DE NEUROCIENCIAS   (Spain)

Author keywords

DLG; Ion channel clustering; Ion channel localization; MAGUK; Potassium channels; Shaker

Indexed keywords

GUANYLATE KINASE; ION CHANNEL; POTASSIUM CHANNEL; PROTEIN; PROTEIN DLG; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; DROSOPHILA; IMMUNOCYTOCHEMISTRY; NERVE TRACT; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RETINA; SIGNAL TRANSDUCTION; SOLUBILIZATION;

ANIMALS; CENTRAL NERVOUS SYSTEM; DETERGENTS; DROSOPHILA; DROSOPHILA PROTEINS; INSECT PROTEINS; LARVA; MUTATION; ORGAN SPECIFICITY; PHOTORECEPTORS, INVERTEBRATE; POTASSIUM CHANNELS; PROTEIN STRUCTURE, TERTIARY; RETINA; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SUBCELLULAR FRACTIONS; SYNAPSES; TUMOR SUPPRESSOR PROTEINS;

INSECTA;

EID: 0036736261     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2002.01092.x     Document Type: Article

References (81)

1. + channel. Neuron 23, 149-157.
2. A channel transcript with homology to vertebrate Na+ channel. EMBO J. 6, 3419-3429.
3. Becker M. N., Brenner R. and Atkinson N. S. (1995) Tissue-specific expression of a Drosophila calcium-activated potassium channel. J. Neurosci. 15, 6250-6259.
4. Breer H. and Knipper M. (1985) Neurochemical Studies in Insect Research. Springer-Verlag, Berlin, pp. 125-155.
5. Brenman J. E., Topinka J. R., Cooper E. C., McGee A. W., Rosen J., Milroy T., Ralston H. J. and Bredt D. S. (1998) Localization of postsynaptic density-93 to dendritic microtubules and interaction with microtubule-associated protein 1A. J. Neurosci. 18, 8805-8813.
6. Butler A., Wei A., Baker K. and Salkoff L. (1989) A family of putative potassium channel genes in Drosophila. Science 243, 943-947.
7. Chevesich J., Kreuz A. J. and Montell C. (1997) Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron 18, 95-105.
8. Cho K. O., Hunt C. A. and Kennedy M. B. (1992) The rat brain post-synaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
9. + channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17, 759-767.
10. Craven S. E., El-Husseini A. E. and Bredt D. S. (1999) Synaptic targeting of the post-synaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 22, 497-509.
11. Deguchi M., Hata Y., Takeuchi M., Ide N., Hirao K., Yao I., Irie M., Toyoda A. and Takai Y. (1998) BEGAIN (brain-enriched guanylate kinase-associated protein), a novel neuronal PSD-95/SAP90-binding protein. J. Biol. Chem. 273, 26269-26272.
12. El-Husseini A. E., Craven S. E., Chetkovich D. M., Firestein B. L., Schnell E., Aoki C. and Bredt D. S. (2000) Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, post-synaptic targeting, and ion channel clustering. J Cell Biol. 148, 159-172.
13. Fanning A. S. and Anderson J. M. (1999) Protein modules as organizers of membrane structure. Curr. Opin. Cell Biol. 11, 432-439.
14. Fernandez-Larrea J., Merlos-Suarez A., Urena J. M., Baselga J. and Arribas J. (1999) A role for a PDZ protein in the early secretory pathway for the targeting of proTGF-α to the cell surface. Mol. Cell. 3, 423-433.
15. Ferrus A., Llamazares S., de la Pompa J. L., Tanouye M. A. and Pongs O. (1990) Genetic analysis of the Shaker gene complex of Drosophila melanogaster. Genetics 125, 383-398.
16. Fischbach K. F. and Ditrich A. P. M. (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258, 441-475.
17. Garcia E. P., Mehta S., Blair L. A., Wells D. G., Shang J., Fukushima T., Fallon J. R., Garner C. C. and Marshall J. (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21, 727-739.
18. Garner C. and Kindler S. (1996) Synaptic proteins and the assambly of synaptic junctions. Trends Cell Biol. 6, 429-433.
19. Garner C. C., Nash J. and Huganir R. L. (2000) PDZ domains in synapse assembly and signalling. Trends Cell Biol. 10, 274-280.
20. Gisselmann G., Sewing S., Madsen B. W., Mallart A., Angaut-Petit D., Müller-. Holtkamp F., Ferr£S. A. and Pongs O. (1989) The interference of truncated with normal potassium channels leads to abnormal bahaviour in transgenic Drosophila melanogaster. EMBO J. 8, 2359-2364.
21. Gomperts S. N. (1996) Clustering membrane proteins: It's all coming together with the PSD-95/SAP90 protein family. Cell 84, 659-662.
22. Gramates L. S. and Budnik V. (1999) Assembly and maturation of the Drosophila larval neuromuscular junction. Int. Rev. Neurobiol. 43, 93-117.
23. Hanada T., Lin L., Tibaldi E. V., Reinherz E. L. and Chishti A. H. (2000) GAKIN, a novel kinesin-like protein associates with the human homologue of the Drosophila discs large tumor suppressor in T lymphocytes. J. Biol. Chem. 275, 28774-28784.
24. Haugland F. N. and Wu C. F. (1990) A voltage-clamp analysis of genedosage effects of the Shaker locus on larval muscle potassium currents in Drosophila. J. Neurosci. 10, 1357-1371.
25. Hille B. (1992) Ionic channels of excitable membranes. Sinauer, Sunderland, MA.
26. Horio Y., Hibino H., Inanobe A., Yamada M., Ishii M., Tada Y., Satoh E., Hata Y., Takai Y. and Kurachi Y. (1997) Clustering and enhanced activity of an inwardly rectifying potassium channel, Kir4.1, by an anchoring protein, PSD-95/SAP90. J Biol. Chem. 272, 12885-12888.
27. Hough C. D., Woods D. F., Park S. and Bryant P. J. (1997) Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK discs-large. Genes Dev. 11, 3242-3253.
28. Hsueh Y.-P., Kim E. and Sheng M. (1997) Disulfide-linked head-to-head multimerization in the mechanism of ion channel clustering by PSD-95. Neuron 18, 803-814.
29. + channels of the Shab subfamily. J. Neurosci. 13, 1569-1576.
30. Jan L. Y. and Jan Y. N. (1992) Tracing the roots of ion channels. Cell 69, 715-718.
31. Jugloff D. G., Khanna R., Schlichter L. C. and Jones O. T. (2000) Internalization of the Kv1.4 potassium channel is suppressed by clustering interactions with PSD-95. J. Biol. Chem. 275, 1357-1364.
32. Kamb and Tanouye M. (1988) Multiple products of the Drosophila Shaker gene may contribute to potassium channel diversity. Neuron 1, 421-430.
33. + channels by interaction with a family of membrane-associated guanylat kinases. Nature 378, 85-88.
34. Kim E., Cho K. O., Rothschild A. and Sheng M. (1996) Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins. Neuron 17, 103-113.
35. Kim E., Naisbit S., Hsueh Y.-P., Rao A., Rothschild A., Craig A. M. and Sheng M. (1997) GKAP, a novel synaotic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J. Cell Biol. 136, 669-678.
36. Kistner U., Wenzel B. M., Veh R. W., Cases-Langhoff C., Garner A. M., Appeltauer U., Voss B., Gundelfinger E. D. and Garner C. C. (1993) SAP90, a rat pre-synaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J. Biol. Chem 268, 4580-4583.
37. Kornau H.-C., Schenker L. T., Kennedy M. B. and Seeburg P. H. (1995) Domain interaction between NMDA receptor subunits postsynaptic density protein PSD-95. Science 269, 1737-1740.
38. Kornau H.-C., Seeburg P. H. and Kennedy M. B. (1997) Interaction of ion channels and receptors with PDZ domain proteins. Curr. Opin. Neurobiol. 7, 368-373.
39. Lichtinghagen R., Stocker M., Wittka R., Boheim G., Stuhmer W., Ferrus A. and Pongs O. (1990) Molecular basis of altered excitability in Shaker mutants of Drosophila melanogaster. EMBO J. 9, 4399-4407.
40. Lindsley D. L. and Zimm C. C. (1992) The Genome of Drosophila Melanogaster Academic Press, New York.
41. McGee A. W. and Bredt D. S. (1999) Identification of an intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. J. Biol. Chem. 274, 17431-17436.
42. + channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J. Neurosci. 15, 3840-3851.
43. Mi H., Deerinck T. J., Ellisman M. H. and Schwarz T. L. (1995) Differential distribution of closely related potassium channels in rat Schwann cells. J. Neurosci. 15, 3761-3774.
44. Müller B. M., Kistner U., Kindler S., Chung W. J., Kuhlendahl S., Fenster S. D., Lau L. F., Veh R. W., Huganir R. L., Gundelfinger E. D. and Garner C. C. (1996) SAP102, a novel post-synaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17, 255-265.
45. Naisbitt S., Kim E., Weinberg R. J., Rao A., Yang F. C., Craig A. M. and Sheng M. (1997) Characterization of guanylate kinase-associated protein, a post-synaptic density protein at excitatory synapses that interacts directly with postsynaptic density-95/synapse-associated protein 90. J. Neurosci. 17, 5687-5696.
46. Nehring R. B., Wischmeyer E., Doring F., Veh R. W., Sheng M. and Karschin A. (2000) Neuronal inwardly rectifying K(+) channels differentially couple to PDZ proteins of the PSD-95/SAP90 family. J. Neurosci. 20, 156-162.
47. Niethammer M., Kim E. and Sheng M. (1996) Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16, 2157-2163.
48. Nix S. L., Chishti A. H., Anderson J. M. and Walther Z. (2000) hCASK and hDlg associate in epithelia, and their src homology 3 and guanylate kinase domains participate in both intramolecular and intermolecular interactions. J. Biol. Chem. 275, 41192-41200.
49. Pak D. T., Yang S., Rudolph-Correia S., Kim E. and Sheng M. (2001) Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31, 289-303.
50. Pongs O. (1992) Molecular biology of voltage-dependent potassium channels. Physiol. Rev. 72, S69-S88.
51. Pongs O., Kecskemethy N., Müller R., Krah-Jentgens I., Baumann A., Kiltz H.-H., Canal I., Llamazares S., Ferrus A. (1988) Shaker encodes a family of putative potassium channels in the nervous system of Drosophila. EMBO J. 7, 1087-1096.
52. Ramon y Cajal S. and Sanchez D. (1915) Contribucion al conocimiento d elos centros nerviosos de los insectos. Trab. Lab. Invest. Biol. 13, 1-164.
53. Rogero O. and Tejedor F. J. (1995) Immunochemical characterization and developmental expression of Shaker potassium channels from the nervous system of Drosophila. J. Biol. Chem. 270, 25746-25751.
54. Rogero O., Hammerle B. and Teledor F. J. (1997) Diverse expression and distribution of Shaker potassium channels during the development of the Drosophila nervous system. J Neurosci. 17, 5108-5118.
55. Rudy B. (1988) Diversity and ubiquity of K-channels. Neuroscience 25, 729-749.
56. Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N. and Jan L. Y. (1988) Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature 331, 137-142.
57. +-channel components from the Shaker locus and differential distribution of splicing variants in Drosophila. Neuron 2, 119-127.
58. + channel assembly. Neuron 11, 67-76.
59. Sheng M. (1996) PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron 17, 575-578.
60. Sheng M. and Sala C. (2001) PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24, 1-29.
61. Sheng M. and Wyszynski M. (1997) Ion channel targeting in neurons. Bioessays. 19, 847-853.
62. + channels detected in vivo. Nature. 365, 72-75.
63. Shin H., Hsueh Y. P., Yang F. C., Kim E. and Sheng M. (2000) An Intramolecular interaction between src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J. Neurosci. 20, 3580-3587.
64. Standley S., Roche K. W., McCallum J., Sans N. and Wenthold R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887-898.
65. Strausfeld N. J. (1976) Atlas of an Insect Brain. Springer, Berlin.
66. Takeuchi M., Hata Y., Hirao K., Toyoda A., Irie M. and Takai Y. (1997) SAPAPs a family of PSD-95/SAP90-associated proteins localized at post-synaptic density. J. Biol. Chem. 272, 11943-11951.
67. Tanouye M. A. and Ferrus A. (1985) Action potentials in normal and Shaker mutant in Drosophila. J. Neurogenet. 2, 253-271.
68. +-channels in vivo. J. Neurosci. 17, 152-159.
69. Thomas U., Kim E., Kuhlendahl S., Koh Y. H., Gundelfinger E. D., Sheng M., Garner C. C. and Budnik V. (1997) Synaptic clustering of the cell adhesion molecule fasciclin. II: Discs-large, its role regulation pre-synaptic structure. Neuron 19, 787-799.
70. Thomas U., Ebitsch S., Gorczyca M., Koh D. S., Hough C. D., Woods D. F., Gundelfinger E. D. and Budnik V. (2000) Synaptic targeting and localization of disc-large is a stepwise process controlled by different domains of the protein. Curr. Biol. 10, 1108-1117.
71. + channel surface expression and clustering. J. Cell Biol. 148, 147-158.
72. Vahnick I., Trimmer J. S., Schwarz T. L., Levinson S. R., Risal D. and Shrager P. (1999) Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J. Neurosci. 19, 747-758.
73. Veh R. W., Lichtinghagen R., Sewing S., Wunder F., Grumbach I. M. and Pongs O. (1995) Immunohistochemical localization of five members of the Kv1 channel subunits: contrasting subcellular locations and neuron-specific co-localizations in rat brain. Eur. J. Neurosci. 7, 2189-2205.
74. Wang H., Kunkel D. D., Schwartzkroin P. A. and Tempel B. L. (1994) Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J. Neurosci. 14, 4588-4599.
75. + current diversity is produced by an extended gene family conserved in Drosophila and mouse. Science 248, 598-603.
76. Weiser M., Bueno E., Sekimjak C., Martone M. E., Baker H., Hillman D., Chen S., Thornhill W., Ellisman M. and Rudy B. (1995) The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J. Neurosci. 15, 4298-4314.
77. Woods D. F. and Bryant P. J. (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate homolog localized at septate junctions. Cell 66, 451-464.
78. Woods D. F., Hough C., Callaini G. and Bryant P. J. (1996) Dlg protein is required for junction structure, cell polarity, proliferation control Drosophila epithelia. J. Cell Biol. 134, 1469-1482.
79. Wu C. F. and Haugland F. N. (1985) voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants. J. Neurosci. 5, 2626-2640.
80. Wu H., Reissner C., Kuhlendahl S., Coblentz B., Reuver S., Kindler S., Gundelfinger E. D. and Garner C. C. (2000) Intramolecular interactions regulate SAP97 binding to GKAP. EMBO J. 19, 5740-575.
81. Zito K., Fetter R. D., Goodman C. S. and Isacoff E. Y. (1997) Synaptic clustering of fasciclin II and Shaker: essential targeting sequences role for dlg. Neuron 19, 1007-1016.