Photoreceptor morphogenesis and retinal degeneration: lessons from Drosophila

Current Opinion in Neurobiology

Volumn 17, Issue 5, 2007, Pages 541-547

  Knust, Elisabeth ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTION; CELL TYPE; CYTOSKELETON; DROSOPHILA; ENERGY; ENVIRONMENTAL FACTOR; HUMAN; METAZOON; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MORPHOGENESIS; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PHOTOSENSITIVITY; PRIORITY JOURNAL; RETINA DEGENERATION; RETINA DYSTROPHY; REVIEW;

ANIMALS; DROSOPHILA; MODELS, BIOLOGICAL; MORPHOGENESIS; PHOTORECEPTORS, INVERTEBRATE; RETINAL DEGENERATION;

EID: 37549039118     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2007.08.001     Document Type: Review

References (40)

1. Kumar J.P. Signalling pathways in Drosophila and vertebrate retinal development. Nat Rev Genet 2 (2001) 846-857
2. Longley R.L.J., and Ready D.F. Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171 (1995) 415-433
3. Arikawa K., Hicks J.L., and Williams D.S. Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110 (1990) 1993-1998
4. Hong Y., Ackerman L., Jan L.Y., and Jan Y.-N. Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc Natl Acad Sci U S A 100 (2003) 12712-12717
5. Harris T.J.C., and Peifer M. The positioning and segregation of apical cues during eoithelial polarity establishment in Drosophila. J Cell Biol 170 (2005) 813-823
6. Benton R., and St. Johnston D. Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115 (2003) 691-704
7. Nam S.-C., Mukhopadhyay B., and Choi K.-W. Antagonistic functions of Par-1 kinase and protein phosphatase 2A are required for localisation of Bazooka and photoreceptor morphogenesis in Drosophila. Dev Biol 306 (2007) 624-635
8. von Stein W., Ramrath A., Grimm A., Muller-Borg M., and Wodarz A. Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132 (2005) 1675-1686
9. 3 at the apical and baso-lateral membrane, respectively, are required for proper epithelial polarity (see ref. [12]).
10. Funamoto S., Meili R., Lee S., Parry L., and Firtel R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109 (2002) 601-623
11. Iijima M., and Devreotes P.N. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Curr Biol 11 (2002) 559-610
12. Martin-Belmonte F., Gassama A., Datta A., Yu W., Rescher U., Gerke V., and Mostov K. PTEN-mediated apical segregation of phosphoinositides control epithelial morphogenesis through Cdc42. Cell 128 (2007) 383-397
13. Pellikka M., Tanentzapf G., Pinto M., Smith C., McGlade C.J., Ready D.F., and Tepass U. Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416 (2002) 143-149
14. Richard M., Grawe F., and Knust E. DPATJ plays a role in retinal morphogenesis and protects against light-dependent degeneration of photoreceptor cells in the Drosophila eye. Dev Dyn 235 (2006) 895-907
15. Berger S, Bulgakova NA, Grawe F, Knust E: Unravelling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics 2007, 176:2189-2200. The paper shows that Drosophila stardust, encoding a binding partner of Crumbs, and the fly orthologue of mammalian MPP5/Pals1 and zebrafish nagie oko is genetically complex. Some mutations only affect epithelial development in the embryo, while others also impair PRC morphogenesis and/or result in light-induced retinal degeneration. This complexity is the result of differential splicing, resulting in tissue-specific expression of different Stardust isoforms. They further suggest that Stardust may be engaged in cell-type specific protein complexes, which may have particular cell biological functions.
16. Laprise P., Beronja S., Silva-Gagliardi N.F., Pellikka M., Jensen A.M., McGlade C.J., and Tepass U. The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell 11 (2006) 363-374
17. Hsu Y.-C., Willoughby J.J., Christensen A.K., and Jensen A.M. Mosaic eyes is a novel component of the Crumbs complex and negatively regulates photoreceptor apical membrane. Development 133 (2006) 4849-4859. One important apical determinant of epithelial and photoreceptor cells in Drosophila, zebrafish, mouse and human is the transmembrane protein Crumbs. In all these cells, Crumbs is restricted to a subapical region, apical to the ZA. Here it organises a protein complex by recruiting the scaffolding protein Stardust/MPP5/Pals1 and DPATJ/PATJ/MUPP1. All Crumbs proteins contain a highly conserved FERM-binding domain. The two papers demonstrate that the Drosophila and the zebrafish FERM-protein Yurt/Mosaic Eyes negatively regulates the function of Crumbs. Yurt/Mosaic Eyes can directly bind to Crumbs, and its loss results in an enhanced activity of Crumbs. Drosophila yurt mutations can suppress the crumbs mutant phenotype in the embryo, but only in those crumbs mutants that still obtain some residual crumbs function, supporting the view that it mediates its function directly via Crumbs.
18. Omori Y., and Malicki J. oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryos. Curr Biol 16 (2006) 945-957
19. Izaddoost S., Nam S.-C., Bhat M.A., Bellen H.J., and Choi K.-W. Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416 (2002) 178-183
20. Johnson K., Grawe F., Grzeschik N., and Knust E. Drosophila Crumbs is required to inhibit light-induced photoreceptor degeneration. Curr Biol 12 (2002) 1675-1680
21. Nam S.-C., and Choi K.-W. Domain-specific early and late function of DPATJ in Drosophila photoreceptor cells. Dev Dynam 235 (2006) 1501-1507
22. Chang H.-Y., and Ready D.F. Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 290 (2000) 1978-1980
23. Kumar J.P., and Ready D.F. Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 121 (1995) 4359-4370
24. Karagiosis S.A., and Ready D.F. Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131 (2004) 725-732
25. Satoh A.K., O'Tousa J., Ozaki K., and Ready D.F. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132 (2005) 1487-1497
26. Li B.X., Satoh A.K., and Ready D.F. Myosin V, Rab11 and dRip11 direct apical secretion and cellular morphogenesis in Drosophila photoreceptor cells. J Cell Biol 177 (2007). The paper shows that Drosophila Rab 11 is engaged in the formation of a complex, containing Myosin V and Drip, similar as the corresponding proteins do in mammalian cells. This paper underlines the importance of MyoV in polarised membrane transport, which has already been shown for yeast and vertebrate cells.
27. Beronja S., Laprise P., Papoulas O., Pellikka M., Sisson J., and Tepass U. Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J Cell Biol 169 (2005) 635-646
28. Zelhof A.C., Hardy R.W., Becker A., and Zuker C.S. Transforming the architecture of compound eyes. Nature 443 (2006) 696-699
29. Husain N., Pellikka M., Hong H., Klimentova T., Choe K.-M., Clandinin T.R., and Tepass U. The Agrin/perlecan-related protein Eyes Shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell 11 (2006) 483-493. One of the characteristics of the Drosophila eye is the formation of an interrhabdomeral lumen to individualise the rhabdomeres. The two papers show that the secretion of Spacemaker/Eyes shut is required for this process, and that Prominin seems to be involved in binding to Spacemake. Interestingly, many insects have eyes with a closed rhabdom, in which the rhabdomeres remain fused and form a single, large photoreceptive structure, which increases the absolute sensitivity at the expense of spatial acuity. Strikingly, the house fly Musca domestica and the mosquito Toxorhynchites amboinensis, two other Diptera with an open rhabdom, express Spam, while the honeybee Apis mellifera and the beetle Tribolium castaneum, which develop a closed rhabdome, do not express Spam. In addition, expression of Spam in the Drosophila ocellar photoreceptors, which normally exhibit fused rhabdomeres, results in the formation of an interrhabdomeric lumen. This highlights how the expression of a single gene can influence the morphology of an organ.
30. den Hollander A.I., ten Brink J.B., de Kok Y.J., van Soest S., van den Born L.I., van Driel M.A., van de Pol D.J., Payne A.M., Bhattacharya S.S., Kellner U., et al. Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23 (1999) 217-221
31. den Hollander A.I., Heckenlively J.R., van den Born L.I., de Kok Y.J., van der Velde-Visser S.D., Kellner U., Jurklies B., van Schooneveld M.J., Blankenagel A., Rohrschneider K., et al. Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene. Am J Hum Genet 69 (2001) 198-203
32. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM, Young JA, Bechtold L, Haider NB, Tepass U, R. HJ et al.: CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet 2003, 12: 2179-2189.
33. van de Pavert S.A., Kantardzhieva A., Malysheva A., Meuleman J., Versteek I., Levelt C., Klooster J., geiger S., Seeliger M.W., Rashbass P., et al. Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci 117 (2004) 4169-4177
34. Bonilha V.L., Rayborn M.E., Saotome I., McClatchey A.I., and Hollyfield J.G. Microvilli defects in retinas of ezrin knockout mice. Exp Eye Res 82 (2006) 720-729
35. Maw M.A., Corbeil D., Koch J., Hellwig A., Wilson-Wheeler J.C., Bidges R.J., Kumaramanickavel G., John S., Nancarrow D., Röper K., et al. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9 (2000) 27-34
36. Jászai J., Fargeas C.A., Florek M., Huttner W.B., and Corbeil D. Focus on Molecules: Prominin-1 (CD133). Exp Eye Res (2006) 1-2
37. Wang T., and Montell C. Phototransduction and retinal degeneration in Drosophila. Pflügers Arch 454 (2007) 821-847. This review is an excellent, very detailed overview of the signal transduction mechanism in the Drosophila eye, the genes involved and their importance to prevent retinal degeneration.
38. Alloway P.G., Howard L., and Dolph P.J. The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28 (2000) 129-138
39. Kiselev A., Socolich M., Vinós J., Hardy R.W., Zuker C.S., and Ranganathan R. A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28 (2000) 139-152
40. Nichols R., and Pak W.L. Characterization of Drosophila melanogaster rhodopsin. J Biol Chem 260 (1985) 12670-12674