The neuronal transcription factor erect wing regulates specification and maintenance of Drosophila R8 photoreceptor subtypes

Developmental Biology

Volumn 381, Issue 2, 2013, Pages 482-490

  Hsiao, Hui Yi ^a   Jukam, David ^a   Johnston, Robert ^a   Desplan, Claude ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Drosophila; Ewg; Hippo pathway; Photoreceptors; R8; Retina; Rhodopsin

Indexed keywords

RHODOPSIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC CODE; IMAGO; INSECT GENETICS; MALE; NONHUMAN; NUCLEAR RESPIRATORY FACTOR 1 GENE; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; PUPATION; REGULATOR GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84882846115     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.07.001     Document Type: Article

References (45)

1. Barrio R., de Celis J.F., Bolshakov S., Kafatos F.C. Identification of regulatory regions driving the expression of the Drosophila spalt complex at different developmental stages. Dev. Biol. 1999, 215:33-47.
2. Benchabane H., Xin N., Tian A., Hafler B.P., Nguyen K., Ahmed A., Ahmed Y. Jerky/Earthbound facilitates cell-specific Wnt/Wingless signalling by modulating beta-catenin-TCF activity. EMBO J. 2011, 30:1444-1458.
3. Calzone F.J., Hoog C., Teplow D.B., Cutting A.E., Zeller R.W., Britten R.J., Davidson E.H. Gene regulatory factors of the sea urchin embryo. I. Purification by affinity chromatography and cloning of P3A2, a novel DNA-binding protein. Development 1991, 112:335-350.
4. Chou W.H., Hall K.J., Wilson D.B., Wideman C.L., Townson S.M., Chadwell L.V., Britt S.G. Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 1996, 17:1101-1115.
5. Chou W.H., Huber A., Bentrop J., Schulz S., Schwab K., Chadwell L.V., Paulsen R., Britt S.G. Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 1999, 126:607-616.
6. Cook T., Pichaud F., Sonneville R., Papatsenko D., Desplan C. Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev. Cell 2003, 4:853-864.
7. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
8. Efiok B.J., Chiorini J.A., Safer B. A key transcription factor for eukaryotic initiation factor-2 alpha is strongly homologous to developmental transcription factors and may link metabolic genes to cellular growth and development. J. Biol. Chem. 1994, 269:18921-18930.
9. Emoto K., Parrish J.Z., Jan L.Y., Jan Y.N. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 2006, 443:210-213.
10. Evans M.J., Scarpulla R.C. Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. J. Biol. Chem. 1989, 264:14361-14368.
11. Fazio I.K., Bolger T.A., Gill G. Conserved regions of the Drosophila erect wing protein contribute both positively and negatively to transcriptional activity. J. Biol. Chem. 2001, 276:18710-18716.
12. Fortini M.E., Rubin G.M. Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev. 1990, 4:444-463.
13. Franceschini N., Kirschfeld K., Minke B. Fluorescence of photoreceptor cells observed in vivo. Science 1981, 213:1264-1267.
14. Furukawa T., Morrow E.M., Cepko C.L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 1997, 91:531-541.
15. Halder G., Johnson R.L. Hippo signaling: growth control and beyond. Development 2011, 138:9-22.
16. Hardie R. Functional organization of the fly retina. Progress in Sensory Physiology 1985, 5:1-79. Springer.
17. Harvey K., Tapon N. The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network. Nature reviews. Cancer 2007, 7:182-191.
18. Haussmann I.U., Soller M. Differential activity of EWG transcription factor isoforms identifies a subset of differentially regulated genes important for synaptic growth regulation. Dev. Biol. 2010, 348:224-230.
19. Haussmann I.U., White K., Soller M. Erect wing regulates synaptic growth in Drosophila by integration of multiple signaling pathways. Genome Biol. 2008, 9:R73.
20. Hough-Evans B.R., Franks R.R., Zeller R.W., Britten R.J., Davidson E.H. Negative spatial regulation of the lineage specific CyIIIa actin gene in the sea urchin embryo. Development 1990, 110:41-50.
21. Hsiao H.Y., Johnston R.J., Jukam D., Vasiliauskas D., Desplan C., Rister J. Dissection and immunohistochemistry of larval, pupal and adult Drosophila retinas. J Vis Exp. 2005, 69:e43471-5.
22. Huang J., Wu S., Barrera J., Matthews K., Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 2005, 122:421-434.
23. Johnston R.J., Otake Y., Sood P., Vogt N., Behnia R., Vasiliauskas D., McDonald E., Xie B., Koenig S., Wolf R., Cook T., Gebelein B., Kussell E., Nakagoshi H., Desplan C. Interlocked feedforward loops control cell-type-specific Rhodopsin expression in the Drosophila eye. Cell 2011, 145:956-968.
24. Jukam D., Desplan C. Binary regulation of Hippo pathway by Merlin/NF2, Kibra, Lgl, and Melted specifies and maintains postmitotic neuronal fate. Dev. Cell 2011, 21:874-887.
25. Jukam, D., Xie, B., Rister, J., Terrell, D., Charlton-Perkins, M, Pistillo, D. Gebelein, B., Desplan, C., Cook, T. Opposite network-level feedback in the Hippo pathway for growth control and neural fate. Science, in press.
26. LaJeunesse D.R., McCartney B.M., Fehon R.G. Structural analysis of Drosophila merlin reveals functional domains important for growth control and subcellular localization. J. Cell Biol. 1998, 141:1589-1599.
27. Mikeladze-Dvali T., Wernet M.F., Pistillo D., Mazzoni E.O., Teleman A.A., Chen Y.W., Cohen S., Desplan C. The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 2005, 122:775-787.
28. Mollereau B., Dominguez M., Webel R., Colley N.J., Keung B., de Celis J.F., Desplan C. Two-step process for photoreceptor formation in Drosophila. Nature 2001, 412:911-913.
29. Pan D. The hippo signaling pathway in development and cancer. Dev. Cell 2010, 19:491-505.
30. Papatsenko D., Sheng G., Desplan C. A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 1997, 124:1665-1673.
31. Pepple K.L., Atkins M., Venken K., Wellnitz K., Harding M., Frankfort B., Mardon G. Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate. Development 2008, 135:4071-4079.
32. Pichaud F., Briscoe A., Desplan C. Evolution of color vision. Curr. Opin. Neurobiol. 1999, 9:622-627.
33. Pichaud F., Desplan C. A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia. Development 2001, 128:815-826.
34. Polesello C., Tapon N. Salvador-Warts-Hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr. Biol.: CB 2007, 17:1864-1870.
35. Rister J., Desplan C. The retinal mosaics of opsin expression in invertebrates and vertebrates. Dev. Neurobiol. 2011, 71:1212-1226.
36. Rister J., Desplan C., Vasiliauskas D. Establishing and maintaining gene expression patterns: insights from sensory receptor patterning. Development 2013, 140:493-503.
37. Tahayato A., Sonneville R., Pichaud F., Wernet M.F., Papatsenko D., Beaufils P., Cook T., Desplan C. Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev. Cell 2003, 5:391-402.
38. Thanawala S.U., Rister J., Goldberg G.W., Zuskov A., Olesnicky E.C., Flowers J.M., Jukam D., Purugganan M.D., Gavis E.R., Desplan C., Johnston R.J. Regional modulation of a stochastically expressed factor determines photoreceptor subtypes in the Drosophila retina. Dev. Cell 2013, 25:93-105.
39. Vasiliauskas D., Mazzoni E.O., Sprecher S.G., Brodetskiy K., Johnston R.J., Lidder P., Vogt N., Celik A., Desplan C. Feedback from rhodopsin controls rhodopsin exclusion in Drosophila photoreceptors. Nature 2011, 479:108-112.
40. Wernet M.F., Labhart T., Baumann F., Mazzoni E.O., Pichaud F., Desplan C. Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors. Cell 2003, 115:267-279.
41. Wernet M.F., Mazzoni E.O., Celik A., Duncan D.M., Duncan I., Desplan C. Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 2006, 440:174-180.
42. Xin N., Benchabane H., Tian A., Nguyen K., Klofas L., Ahmed Y. Erect Wing facilitates context-dependent Wnt/Wingless signaling by recruiting the cell-specific Armadillo-TCF adapter Earthbound to chromatin. Development 2011, 138:4955-4967.
43. Xu T., Wang W., Zhang S., Stewart R.A., Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 1995, 121:1053-1063.
44. Yamaguchi S., Desplan C., Heisenberg M. Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc. Natl. Acad. Sci. USA 2010, 107:5634-5639.
45. Zhao B., Tumaneng K., Guan K.L. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 2011, 13:877-883.