Antagonistic functions of two stardust isoforms in Drosophila photoreceptor cells

Molecular Biology of the Cell

Volumn 21, Issue 22, 2010, Pages 3915-3925

  Bulgakova, Natalia A ^a,b   Rentsch, Michaela ^a   Knust, Elisabeth ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA; FEMALE; HOMEOSTASIS; MALE; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GUANYLATE KINASE; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PHOTORECEPTOR CELLS, INVERTEBRATE; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN KINASE C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78649673026     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E09-10-0917     Document Type: Article

References (57)

1. Bachmann, A., Grawe, F., Johnson, K., and Knust, E. (2008). Drosophila Lin-7 is a component of the Crumbs complex in epithelia and photoreceptor cells and prevents light-induced retinal degeneration. Eur. J. Cell Biol. 87, 123-136.
2. Bachmann, A., Kobler, O., Kittel, R. J., Wichmann, C., Sierralta, J., Sigrist, S. J., Gundelfinger, E. D., Knust, E., and Thomas, U. (2010). A perisynaptic ménage à trois between Dlg, DLin-7, and Metro controls proper organization of Drosophila synaptic junctions. J. Neurosci. 30, 5811-5824.
3. Bachmann, A., Schneider, M., Grawe, F., Theilenberg, E., and Knust, E. (2001). Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity. Nature 414, 638-643.
4. Bachmann, A., Timmer, M., Sierralta, J., Pietrini, G., Gundelfinger, E. D., Knust, E., and Thomas, U. (2004). Cell type-specific recruitment of Drosophila Lin-7 to distinct MAGUK-based protein complexes defines novel roles for Sdt and Dlg-S97. J. Cell Sci. 117, 1899-1909.
5. Berger, S., Bulgakova, N. A., Grawe, F., Johnson, K., and Knust, E. (2007). Unravelling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics 176, 2189-2200.
6. Bit-Avragim, N., Hellwig, N., Rudolph, F., Munson, C., Stainier, D.Y.S., and Abdelilah-Seyfried, S. (2008). Divergent polarization mechanisms during vertebrate epithelial development mediated by the Crumbs complex protein Nagie oko. J. Cell Sci. 121, 2503-2510.
7. Blonska, M., Pappu, B. P., Matsumoto, R., Li, H., Su, B., Wang, D., and Lin, X. (2007). The CARMA1-Bcl10 signaling complex selectively regulates JNK2 kinase in the T cell receptor-signaling pathway. Immunity 26, 55-66.
8. Bulgakova, N. A., Kempkens, Ö., and Knust, E. (2008). Multiple domains of Drosophila Stardust differentially mediate localisation of the Crumbs/Stardust complex during photoreceptor development. J. Cell Sci. 121, 2018-2026.
9. Bulgakova, N. A., and Knust, E. (2009). The Crumbs complex. J. Cell Sci. 122, 2587-2596.
10. Cho, K. O., Hunt, C. A., and Kennedy, M. B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
11. Dimitratos, S. D., Woods, D. F., Stathakis, D. G., and Bryant, P. J. (1999). Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays 21, 912-921.
12. Funke, L., Dakoji, S., and Bredt, D. S. (2005). Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem. 74, 219-245.
13. Gavarini, S., Bécamel, C., Altier, C., Lory, P., Poncet, J., Wijnholds, J., Bockaert, J., and Marin, P. (2006). Opposite effects of PSD-95 and MPP3 PDZ proteins on serotonin 5-hydroxytryptamine2C receptor desensitization and membrane stability. Mol. Biol. Cell 17, 4619-4631.
14. González-Mariscal, L., Betanzos, A., and Avila-Flores, A. (2000). MAGUK proteins: structure and role in the tight junction. Semin. Cell Dev. Biol. 11, 315-324.
15. Gosens, I., Sessa, A., I., den Hollander, A. I., Letteboer, S. J., Belloni, V., Arends, M. L., Le Bivic, A., Cremers, F. P., Broccoli, V., and Roepman, R. (2007a). FERM protein EPB41L5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp. Cell Res. 313, 3959-3970.
16. Gosens, I., et al. (2007b). MPP1 links the Usher protein network and the Crumbs protein complex in the retina. Hum. Mol. Genet. 16, 1993-2003.
17. Hay, B. A., Wolff, T., and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
18. Hong, Y., Ackerman, L., Jan, L. Y., and Jan, Y.-N. (2003). Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc. Natl. Acad. Sci. USA 100, 12712-12717.
19. Hong, Y., Stronach, B., Perrimon, N., Jan, L. Y., and Jan, Y. N. (2001). Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts. Nature 414, 634-638.
20. Horne-Badovinac, S., and Bilder, D. (2008). Dynein regulates epithelial polarity and the apical localization of stardust A mRNA. PLoS Genet. 4, e8.
21. Hsu, Y.-C., Willoughby, J. J., Christensen, A. K., and Jensen, A. M. (2006). Mosaic eyes is a novel component of the Crumbs complex and negatively regulates photoreceptor apical membrane. Development 133, 4849-4859.
22. Izaddoost, S., Nam, S.-C., Bhat, M. A., Bellen, H. J., and Choi, K.-W. (2002). Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416, 178-183.
23. Johnson, K., Grawe, F., Grzeschik, N., and Knust, E. (2002). Drosophila Crumbs is required to inhibit light-induced photoreceptor degeneration. Curr. Biol. 12, 1675-1680.
24. Kantardzhieva, A., et al. (2005). MPP5 recruits MPP4 to the CRB1 complex in photoreceptors. Invest. Ophtalmol. Vis. Sci. 46, 2192-2201.
25. Kempkens, Ö., Médina, E., Fernandez-Ballester, G., Özüyaman, S., Le Bivic, A., Serrano, L., and Knust, E. (2006). Computer modelling in combination with in vitro studies reveals similar binding affinities of Drosophila Crumbs for the PDZ domains of Stardust and DmPar-6. Eur. J. Cell Biol. 85, 753-767. (Pubitemid 44070573)
26. Kim, S., et al. (2010). The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66, 69-84.
27. Kumar, J. P., and Ready, D. F. (1995). Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 121, 4359-4370.
28. Laprise, P., Beronja, S., Silva-Gagliardi, N. F., Pellikka, M., Jensen, A. M., McGlade, C. J., and Tepass, U. (2006). The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev. Cell 11, 363-374. (Pubitemid 44283938)
29. Lee, S. J., and Montell, C. (2004). Suppression of constant-light-induced blindness but not retinal degeneration by inhibition of the rhodopsin degradation pathway. Curr. Biol. 14, 2076-2085.
30. Lee, T., and Luo, L. (2001). Mosaic analysis with a repressable cell marker (MARCM) for Drosophila development. Trends Neurosci. 24, 251-254.
31. Li, Z., Wang, L., Hays, T. S., and Cai, Y. (2008). Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity. J. Cell Biol. 180, 31-38.
32. Ling, C., Zheng, Y., Yin, F., Yu, J., Huang, J., Hong, Y., Wu, S., and Pan, D. (2010). The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc. Natl. Acad. Sci. USA. 107, 10532-10537.
33. Longley, R.L.J., and Ready, D. F. (1995). Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev. Biol. 171, 415-433.
34. Mendoza, C., Olguín, P., Lafferte, G., Thomas, U., Ebitsch, S., Gundelfinger, E. D., Kukuljan, M., and Sierralta, J. (2003). Novel isoforms of Dlg are fundamental for neuronal development in Drosophila. J. Neurosci. 23, 2073-2101.
35. Müller, B. M., Kistner, U., Veh, R. W., Cases-Langhoff, C., Becker, B., Gundelfinger, E. D., and Garner, C. C. (1995). Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J. Neurosci. 15, 2354-2366.
36. Nam, S.-C., and Choi, K.-W. (2003). Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development 130, 4363-4372.
37. Nam, S.-C., and Choi, K.-W. (2006). Domain-specific early and late function of Dpatj in Drosophila photoreceptor cells. Dev. Dyn. 235, 1501-1507.
38. Newsome, T. P., Asling, B., and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
39. Pellikka, M., Tanentzapf, G., Pinto, M., Smith, C., McGlade, C. J., Ready, D. F., and Tepass, U. (2002). Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416, 143-149.
40. Perrin, L., Bloyer, S., Ferraz, C., Agrawal, N., Sinha, P., and Dura, J. M. (2003). The leucine zipper motif of the Drosophila AF10 homologue can inhibit PRE-mediated repression: implications for leukemogenic activity of human MLLAF10 fusions. Mol. Cell Biol. 23, 119-130.
41. Peterson, R. E., Hoffman, S., and Kern, M. J. (2005). Opposing roles of two isoforms of the Prx1 homeobox gene in chondrogenesis. Dev. Dyn. 233, 811-821.
42. Richard, M., Grawe, F., and Knust, E. (2006). DPATJ plays a role in retinal morphogenesis and protects against light-dependent degeneration of photoreceptor cells in the Drosophila eye. Dev. Dyn. 235, 895-907.
43. Richard, M., Muschalik, N., Grawe, F., Ozüyaman, S., and Knust, E. (2009). A role for the extracellular domain of Crumbs in morphogenesis of Drosophila photoreceptor cells. Eur. J. Cell Biol. 88, 765-777.
44. Robinson, B. S., Huang, J., Hong, Y., and Moberg, K. H. (2010). Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein expanded. Curr. Biol. 20, 582-590.
45. Round, J. L., Humphries, L. A., Tomassian, T., Mittelstadt, P., Zhang, M., and Miceli, M. C. (2007). Scaffold protein Dlgh1 coordinates alternative p38 kinase activation, directing T cell receptor signals toward NFAT but not NF-kappaB transcription factors. Nat. Immunol. 8, 154-161.
46. Schlüter, O. M., Xu, W., and Malenka, R. C. (2006). Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51, 99-111.
47. Sheng, G., Thouvenot, E., Schmucker, D., Wilson, D. S., and Desplan, C. (1997). Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. Genes Dev. 11, 1122-1131.
48. Sierralta, J., and Mendoza, C. (2004). PDZ-containing proteins: alternative splicing as a source of functional diversity. Brain Res. Brain Res. Rev. 47, 105-115.
49. Stöhr, H., Molday, L. L., Molday, R. S., Weber, B. H., Biedermann, B., Reichenbach, A., and Kramer, F. (2005). Membrane-associated guanylate kinase proteins MPP4 and MPP5 associate with Veli3 at distinct intercellular junctions of the neurosensory retina. J. Comp. Neurol. 481, 31-41.
50. Stucke, V. M., Timmerman, E., Vandekerckhove, J., Gevaert, K., and Hall, A. (2007). The MAGUK protein MPP7 binds to the polarity protein hDlg1 and facilitates epithelial tight junction formation. Mol. Biol. Cell 18, 1744-1755.
51. Tanentzapf, G., Smith, C., McGlade, J., and Tepass, U. (2000). Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J. Cell Biol. 151, 891-904.
52. Tejedor, F. J., Bokhari, A., Rogero, O., Gorczyca, M., Zhang, J., Kim, E., Sheng, M., and Budnik, V. (1997). Essential role for dlg in synaptic clustering of Shaker K+ channels in vivo. J. Neurosci. 17, 152-159. (Pubitemid 27008858)
53. Tepass, U., and Knust, E. (1993). crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev. Biol. 159, 311-326. (Pubitemid 23287244)
54. 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 by discs-large and its role in the regulation of presynaptic structure. Neuron 19, 787-799.
55. van Rossum, A. G., Aartsen, W. M., Meuleman, J., Klooster, J., Malysheva, A., Versteeg, I., Arsanto, J. P., Le Bivic, A., and Wijnholds, J. (2006). Pals1/Mpp5 is required for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum. Mol. Genet. 15, 2659-2672.
56. Wang, Q., Hurd, T. W., and Margolis, B. (2004). Tight junction protein Par6 interacts with an evolutionarily conserved region in the amino terminus of PALS1/Stardust. J. Biol. Chem. 279, 30715-30721.
57. Wei, X., and Ellis, H. M. (2001). Localisation of the Drosophila MAGUK protein Polychaetoid is controlled by alternative splicing. Mech. Dev. 100, 217-231.