Two-step selection of a single R8 photoreceptor: A bistable loop between senseless and rough locks in R8 fate

Development

Volumn 135, Issue 24, 2008, Pages 4071-4079

  Pepple, Kathryn L ^a   Atkins, Mardelle ^a   Venken, Koen ^a   Wellnitz, Karl ^a   Harding, Mark ^a   Frankfort, Benjamin ^a   Mardon, Graeme ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Drosophila; Eye; Lateral inhibition; Photoreceptor; Rough; Senseless

Indexed keywords

CELL PROTEIN; MUTANT PROTEIN; PROTEIN ROUGH; PROTEIN SENSELESS; RHO FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DROSOPHILA PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; ROD PROTEIN, DROSOPHILA; SENSELESS PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL SELECTION; CELL SPECIFICITY; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME INHIBITION; ENZYME REPRESSION; FEMALE; MALE; MOLECULAR MODEL; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN STABILITY; RETINA DEVELOPMENT; STEM CELL; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DNA PROBE; ENHANCER REGION; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR GENETICS; MORPHOGENESIS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BODY PATTERNING; CELL CYCLE PROTEINS; DNA PROBES; DROSOPHILA; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, NEUROLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PHOTORECEPTOR CELLS, INVERTEBRATE; TRANSCRIPTION FACTORS;

EID: 60849115616     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.028951     Document Type: Article

References (53)

1. Acar, M., Jafar-Nejad, H., Giagtzoglou, N., Yallampalli, S., David, G., He, Y., Delidakis, C. and Bellen, H. J. (2006). Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development 133, 1979-1989.
2. Baker, N. E. and Zitron, A. E. (1995). Drosophila eye development-notch and delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous. Mech. Dev. 49, 173-189.
3. Baker, N. E. and Yu, S. Y. (1997). Proneural function of neurogenic genes in the developing Drosophila eye. Curr. Biol. 7, 122-132.
4. Baker, N. E., Yu, S. and Han, D. (1996). Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr. Biol. 6, 1290-1301.
5. Barolo, S., Carver, L. A. and Posakony, J. W. (2000). GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29, 726; 728; 730; 732.
6. Bray, S. (2000). Specificity and promiscuity among proneural proteins. Neuron 25, 1-2.
7. Brown, N. L., Paddock, S. W., Sattler, C. A., Cronmiller, C., Thomas, B. J. and Carroll, S. B. (1996). daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. Dev. Biol. 179, 65-78.
8. Cagan, R. (1993). Cell fate specification in the developing Drosophila retina. Development Suppl. 19-28.
9. Cagan, R. and Ready, D. (1989). Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 8, 1099-1112.
10. Chanut, F., Luk, A. and Heberlein, U. (2000). A screen for dominant modifiers of ro(Dom), a mutation that disrupts morphogenetic furrow progression in Drosophila, identifies groucho and hairless as regulators of atonal expression. Genetics 156, 1203-1217.
11. D'Avino, P. P. and Thummel, C. S. (1999). Ectopic expression systems in Drosophila. Methods Enzymol. 306, 129-142.
12. Dokucu, M. E., Zipursky, S. L. and Cagan, R. L. (1996). Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina. Development 122, 4139-4147.
13. Domingos, P. M., Brown, S., Barrio, R., Ratnakumar, K., Frankfort, B. J., Mardon, G., Steller, H. and Mollereau, B. (2004). Regulation of R7 and R8 differentiation by the spalt genes. Dev. Biol. 273, 121-133.
14. Dominguez, M. (1999). Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126, 2345-2353.
15. Dominguez, M., Wasserman, J. D. and Freeman, M. (1998). Multiple functions of the EGF receptor in Drosophila eye development. Curr. Biol. 8, 1039-1048.
16. Ferrell, J. E. (2002). Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr. Opin. Cell Biol. 14, 140-148.
17. Frankfort, B. J. and Mardon, G. (2002). R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129, 1295-1306.
18. Frankfort, B. J., Nolo, R., Zhang, Z., Bellen, H. and Mardon, G. (2001). senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye. Neuron 32, 403-414.
19. 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.
20. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
21. Ghysen, A. and Dambly-Chaudiere, C. (1989). Genesis of the Drosophila peripheral nervous system. Trends Genet. 5, 251-255.
22. Heberlein, U., Mlodzik, M. and Rubin, G. M. (1991). Cell-fate determination in the developing Drosophila eye: role of the rough gene. Development 112, 703-712.
23. Heberlein, U., Wolff, T. and Rubin, G. M. (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.
24. Heberlein, U., Penton, A., Falsafi, S., Hackett, D. and Rubin, G. M. (1994). The C-terminus of the homeodomain is required for functional specificity of the Drosophila rough gene. Mech. Dev. 48, 35-49.
25. Hsiung, F. and Moses, K. (2002). Retinal development in Drosophila: specifying the first neuron. Hum. Mol. Genet. 11, 1207-1214.
26. Jafar-Nejad, H., Acar, M., Nolo, R., Lacin, H., Parkhurst, S. M. and Bellen, H. J. (2003). Senseless acts as a binary switch during sensory organ precursor selection. Genes Dev. 17, 2966-2978.
27. Jarman, A. P., Brand, M., Jan, L. Y. and Jan, Y. N. (1993a). The regulation and function of the helix-loop-helix gene, asense, in Drosophila neural precursors. Development 119, 19-29.
28. Jarman, A. P., Grau, Y., Jan, L. Y. and Jan, Y. N. (1993b). atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73, 1307-1321.
29. Jarman, A. P., Grell, E. H., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1994). Atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398-400.
30. Jarman, A. P., Sun, Y., Jan, L. Y. and Jan, Y. N. (1995). Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121, 2019-2030.
31. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
32. Lee, E. C., Hu, X., Yu, S. Y. and Baker, N. E. (1996). The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol. Cell. Biol. 16, 1179-1188.
33. Ma, C. Y., Zhou, Y., Beachy, P. A. and Moses, K. (1993). The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927-938.
34. Mikeladze-Dvali, T., Wernet, M. F., Pistillo, D., Mazzoni, E. O., Teleman, A. A., Chen, Y. W., Cohen, S. and 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.
35. Murre, C., McCaw, P. S. and Baltimore, D. (1989a). A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56, 777-783.
36. Murre, C., McCaw, P. S., Vaessin, H., Caudy, M., Jan, L. Y., Jan, Y. N., Cabrera, C. V., Buskin, J. N., Hauschka, S. D., Lassar, A. B. et al. (1989b). Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544.
37. Nolo, R., Abbot, L. A. and Bellen, H. J. (2000). Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102, 349-362.
38. Pepple, K. L., Anderson, A. E., Frankfort, B. J. and Mardon, G. (2007). A genetic screen in Drosophila for genes interacting with senseless during neuronal development identifies the importin moleskin. Genetics 175, 125-141.
39. Powell, L. M., Zur Lage, P. I., Prentice, D. R., Senthinathan, B. and Jarman, A. P. (2004). The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol. Cell. Biol. 24, 9517-9526.
40. Rawlins, E. L., White, N. M. and Jarman, A. P. (2003). Echinoid limits R8 photoreceptor specification by inhibiting inappropriate EGF receptor signalling within R8 equivalence groups. Development 130, 3715-3724.
41. Ready, D., Hanson, T. and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
42. Spencer, S. A. and Cagan, R. L. (2003). Echinoid is essential for regulation of Egfr signaling and R8 formation during Drosophila eye development. Development 130, 3725-3733.
43. Sprecher, S. G. and Desplan, C. (2008). Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons. Nature 454, 533-537.
44. Sukhanova, M. J., Deb, D. K., Gordon, G. M., Matakatsu, M. T. and Du, W. (2007). Proneural basic helix-loop-helix proteins and epidermal growth factor receptor signaling coordinately regulate cell type specification and cdk inhibitor expression during development. Mol. Cell. Biol. 27, 2987-2996.
45. Sun, Y., Jan, L. Y. and Jan, Y. N. (1998). Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development 125, 3731-3740.
46. Tio, M. and Moses, K. (1997). The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124, 343-351.
47. Tio, M., Ma, C. and 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.
48. Tomlinson, A. and Ready, D. F. (1987). Neuronal differentiation in the Drosophila ommatidium. Dev. Biol. 120, 366-376.
49. Venken, K. J. T., He, Y. C., Hoskins, R. A. and Bellen, H. J. (2006). P[acman]: A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751.
50. Voas, M. G. and Rebay, I. (2004). Signal integration during development: insights from the Drosophila eye. Dev. Dyn. 229, 162-175.
51. White, N. M. and Jarman, A. P. (2000). Drosophila atonal controls photoreceptor R8-specific properties and modulates both receptor tyrosine kinase and Hedgehog signalling. Development 127, 1681-1689.
52. Wolff, T. and Ready, D. F. (1991). The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113, 841-850.
53. Xie, B., Charlton-Perkins, M., McDonald, E., Gebelein, B. and Cook, T. (2007). Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134, 4243-4253.