Rhomboid mediates specification of blue- and greensensitive R8 photoreceptor cells in Drosophila

Journal of Neuroscience

Volumn 29, Issue 9, 2009, Pages 2666-2675

  Birkholz, Denise A ^a   Chou, Wen Hai ^b,c   Phistry, Meridee M ^a   Britt, Steven G ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; RHO FACTOR;

ARTICLE; BLUE LIGHT; CELL DIFFERENTIATION; CELL STRAIN; COLOR DISCRIMINATION; CONTROLLED STUDY; DROSOPHILA; GENE; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA;

ALGORITHMS; ANIMALS; CELL DIFFERENTIATION; COMPOUND EYE, ARTHROPOD; DROSOPHILA; DROSOPHILA PROTEINS; GENOTYPE; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, SCANNING; PHOTORECEPTOR CELLS, INVERTEBRATE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHO-ASSOCIATED KINASES; RHODOPSIN;

EID: 63849216852     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5988-08.2009     Document Type: Article

References (54)

1. Bang AG, Kintner C (2000) Rhomboid and Star facilitate presentation and processing of the Drosophila TGF-alpha homolog Spitz. Genes Dev 14:177-186.
2. Bell ML, Earl JB, Britt SG (2007) Two types of Drosophila R7 photoreceptor cells are arranged randomly: a model for stochastic cell-fate determination. J Comp Neurol 502:75-85.
3. Cagan RL, Ready DF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099-1112.
4. Carthew RW, Rubin GM (1990) seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63:561-577.
5. Chou WH, Hall KJ, Wilson DB, Wideman CL, Townson SM, Chadwell LV, Britt SG (1996) Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17:1101-1115.
6. Chou WH, Huber A, Bentrop J, Schulz S, Schwab K, Chadwell LV, Paulsen R, Britt SG (1999) Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126:607-616.
7. Cook T, Pichaud F, Sonneville R, Papatsenko D, Desplan C (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4:853-864.
8. Cooper MT, Bray SJ (2000) R7 photoreceptor specification requires Notch activity. Curr Biol 10:1507-1510.
9. Domínguez M, Wasserman JD, Freeman M (1998) Multiple functions of the EGF receptor in Drosophila eye development. Curr Biol 8:1039-1048.
10. Earl JB, Britt SG (2006) Expression of Drosophila rhodopsins during photo-receptor cell differentiation: insights into R7 and R8 cell subtype commitment. Gene Expr Patterns 6:687-694.
11. Fleiss JL, Levin BA, Paik MC (2003) Statistical methods for rates and proportions, Ed 3. Hoboken, NJ: Wiley-Interscience.
12. Fortini ME, Rubin GM (1991) The optic lobe projection pattern of polarization-sensitive photoreceptor cells in Drosophila melanogaster. Cell Tissue Res 265:185-191.
13. Fortini ME, Simon MA, Rubin GM (1992) Signalling by the sevenless protein tyrosine kinase is mimicked by Ras 1 activation. Nature 355:559-561.
14. Franceschini N, Kirschfeld K, Minke B (1981) Fluorescence of photoreceptor cells observed in vivo. Science 213:1264-1267.
15. Freeman M ( 1994) The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. Mech Dev 48:25-33.
16. Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651-660.
17. Freeman M (2008) Rhomboid proteases and their biological functions. Annu Rev Genet 42:191-210.
18. Freeman M, Kimmel BE, Rubin GM (1992) Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development 116:335-346.
19. Fuse N, Matakatsu H, Taniguchi M, Hayashi S (1999) Snail-type zinc finger proteins prevent neurogenesis in Scutoid and transgenic animals of Drosophila. Dev Genes Evol 209:573-580.
20. Hardie RC (1979) Electrophysiological analysis of fly retina. I: comparative properties of R 1-6 and R 7 and 8. J Comp Physiol 129:19-33.
21. Hardie RC (1985) Functional organization of the fly retina. In: Progress in sensory physiology (Autrum H, Ottoson D, Perl ER, Schmidt RF, Shimazu H, Willis WD, eds), pp 1-79. Berlin: Springer.
22. Heberlein U, Wolff T, Rubin GM (1993) The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75:913-926.
23. Kirschfeld K, Feiler R, Franceschini N (1978) A photostable pigment within the rhabdomeres of fly photoreceptors no. 7. J Comp Physiol 125:275-284.
24. Kumar JP, Tio M, Hsiung F, Akopyan S, Gabay L, Seger R, Shilo BZ, Moses K (1998) Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125:3875-3885.
25. Lee JR, Urban S, Garvey CF, Freeman M (2001) Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107:161-171.
26. Lesokhin AM, Yu SY, Katz J, Baker NE (1999) Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev Biol 205:129-144.
27. Mazzoni EO, Celik A, Wernet MF, Vasiliauskas D, Johnston RJ, Cook TA, Pichaud F, Desplan C (2008) Iroquois complex genes induce coexpression of rhodopsins in Drosophila. PLoS Biol 6:e97.
28. Mikeladze-Dvali T, Wernet MF, Pistillo D, Mazzoni EO, Teleman AA, Chen YW, Cohen S, Desplan C (2005) The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122:775-787.
29. Mollereau B, Dominguez M, Webel R, Colley NJ, Keung B, de Celis JF, Desplan C (2001) Two-step process for photoreceptor formation in Drosophila. Nature 412:911-913.
30. Newsome TP, Asling B, Dickson BJ (2000) Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127:851-860.
31. Papatsenko D, Sheng G, Desplan C (1997) A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 124:1665-1673.
32. Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 71:708-712.
33. Rutledge BJ, Zhang K, Bier E, Jan YN, Perrimon N (1992) The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsalventral axis formation and neurogenesis. Genes Dev 6:1503-1517.
34. Schweitzer R, Shaharabany M, Seger R, Shilo BZ (1995) Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev 9:1518-1529.
35. Shilo BZ (2003) Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res 284:140-149.
36. Spatz HC, Emanns A, Reichert H (1974) Associative learning of Drosophila melanogaster. Nature 248:359-361.
37. Stenkamp DL, Cameron DA (2002) Cellular pattern formation in the retina: retinal regeneration as a model system. Mol Vis 8:280-293.
38. Tahayato A, Sonneville R, Pichaud F, Wernet MF, Papatsenko D, Beaufils P, Cook T, Desplan C (2003) Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev Cell 5:391-402.
39. Tang S, Guo A (2001) Choice behavior of Drosophila facing contradictory visual cues. Science 294:1543-1547.
40. Tio M, Moses K (1997) The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124:343-351.
41. Tio M, Ma C, Moses K (1994) spitz, a Drosophila homolog of transforming growth factor-alpha, is required in the founding photoreceptor cells of the compound eye facets. Mech Dev 48:13-23.
42. Tomlinson A (2003) Patterning the peripheral retina of the fly: decoding a gradient. Dev Cell 5:799-809.
43. Tomlinson A, Struhl G (2001) Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol Cell 7:487-495.
44. Tsruya R, Schlesinger A, Reich A, Gabay L, Sapir A, Shilo BZ (2002) Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev 16:222-234.
45. Tsruya R, Wojtalla A, Carmon S, Yogev S, Reich A, Bibi E, Merdes G, Schejter E, Shilo BZ (2007) Rhomboid cleaves Star to regulate the levels of secreted Spitz. EMBO J 26:1211-1220.
46. Urban S, Lee JR, Freeman M (2001) Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107:173-182.
47. Urban S, Lee JR, Freeman M (2002) A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J 21:4277-4286.
48. Wasserman JD, Urban S, Freeman M (2000) A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling. Genes Dev 14:1651-1663.
49. Wernet MF, Labhart T, Baumann F, Mazzoni EO, Pichaud F, Desplan C (2003) Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors. Cell 115:267-279.
50. Wernet MF, Mazzoni EO, Celik A, Duncan DM, Duncan I, Desplan C (2006) Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 440:174-180.
51. Xu T, Rubin GM (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117:1223-1237.
52. Yang L, Baker NE (2001 ) Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina. Development 128:1183-1191.
53. Yogev S, Schejter ED, Shilo BZ (2008) Drosophila EGFR signalling is modulated by differential compartmentalization of Rhomboid intramembrane proteases. EMBO J 27:1219-1230.
54. Zipursky SL, Rubin GM (1994) Determination of neuronal cell fate: lessons from the R7 neuron oí Drosophila. Annu Rev Neurosci 17:373-397.