Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Jun;155(2):733–752. doi: 10.1093/genetics/155.2.733

A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ.

S Abdelilah-Seyfried 1, Y M Chan 1, C Zeng 1, N J Justice 1, S Younger-Shepherd 1, L E Sharp 1, S Barbel 1, S A Meadows 1, L Y Jan 1, Y N Jan 1
PMCID: PMC1461115  PMID: 10835395

Abstract

The Drosophila adult external sensory organ, comprising a neuron and its support cells, is derived from a single precursor cell via several asymmetric cell divisions. To identify molecules involved in sensory organ development, we conducted a tissue-specific gain-of-function screen. We screened 2293 independent P-element lines established by P. Rorth and identified 105 lines, carrying insertions at 78 distinct loci, that produced misexpression phenotypes with changes in number, fate, or morphology of cells of the adult external sensory organ. On the basis of the gain-of-function phenotypes of both internal and external support cells, we subdivided the candidate lines into three classes. The first class (52 lines, 40 loci) exhibits partial or complete loss of adult external sensory organs. The second class (38 lines, 28 loci) is associated with increased numbers of entire adult external sensory organs or subsets of sensory organ cells. The third class (15 lines, 10 loci) results in potential cell fate transformations. Genetic and molecular characterization of these candidate lines reveals that some loci identified in this screen correspond to genes known to function in the formation of the peripheral nervous system, such as big brain, extra macrochaetae, and numb. Also emerging from the screen are a large group of previously uncharacterized genes and several known genes that have not yet been implicated in the development of the peripheral nervous system.

Full Text

The Full Text of this article is available as a PDF (350.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alphey L., Jimenez J., White-Cooper H., Dawson I., Nurse P., Glover D. M. twine, a cdc25 homolog that functions in the male and female germline of Drosophila. Cell. 1992 Jun 12;69(6):977–988. doi: 10.1016/0092-8674(92)90616-k. [DOI] [PubMed] [Google Scholar]
  2. Artavanis-Tsakonas S., Rand M. D., Lake R. J. Notch signaling: cell fate control and signal integration in development. Science. 1999 Apr 30;284(5415):770–776. doi: 10.1126/science.284.5415.770. [DOI] [PubMed] [Google Scholar]
  3. Auld V. J., Fetter R. D., Broadie K., Goodman C. S. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell. 1995 Jun 2;81(5):757–767. doi: 10.1016/0092-8674(95)90537-5. [DOI] [PubMed] [Google Scholar]
  4. Bailey A. M., Posakony J. W. Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev. 1995 Nov 1;9(21):2609–2622. doi: 10.1101/gad.9.21.2609. [DOI] [PubMed] [Google Scholar]
  5. Bang A. G., Bailey A. M., Posakony J. W. Hairless promotes stable commitment to the sensory organ precursor cell fate by negatively regulating the activity of the Notch signaling pathway. Dev Biol. 1995 Dec;172(2):479–494. doi: 10.1006/dbio.1995.8033. [DOI] [PubMed] [Google Scholar]
  6. Bang A. G., Posakony J. W. The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development. Genes Dev. 1992 Sep;6(9):1752–1769. doi: 10.1101/gad.6.9.1752. [DOI] [PubMed] [Google Scholar]
  7. Blochlinger K., Jan L. Y., Jan Y. N. Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development. 1993 Feb;117(2):441–450. doi: 10.1242/dev.117.2.441. [DOI] [PubMed] [Google Scholar]
  8. Brand A. H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993 Jun;118(2):401–415. doi: 10.1242/dev.118.2.401. [DOI] [PubMed] [Google Scholar]
  9. Broadus J., Doe C. Q. Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr Biol. 1997 Nov 1;7(11):827–835. doi: 10.1016/s0960-9822(06)00370-8. [DOI] [PubMed] [Google Scholar]
  10. Brou C., Logeat F., Lecourtois M., Vandekerckhove J., Kourilsky P., Schweisguth F., Israël A. Inhibition of the DNA-binding activity of Drosophila suppressor of hairless and of its human homolog, KBF2/RBP-J kappa, by direct protein-protein interaction with Drosophila hairless. Genes Dev. 1994 Oct 15;8(20):2491–2503. doi: 10.1101/gad.8.20.2491. [DOI] [PubMed] [Google Scholar]
  11. Cant K., Knowles B. A., Mooseker M. S., Cooley L. Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J Cell Biol. 1994 Apr;125(2):369–380. doi: 10.1083/jcb.125.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Carmena A., Murugasu-Oei B., Menon D., Jiménez F., Chia W. Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 1998 Feb 1;12(3):304–315. doi: 10.1101/gad.12.3.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Courtot C., Fankhauser C., Simanis V., Lehner C. F. The Drosophila cdc25 homolog twine is required for meiosis. Development. 1992 Oct;116(2):405–416. doi: 10.1242/dev.116.2.405. [DOI] [PubMed] [Google Scholar]
  14. Cui X., Doe C. Q. The role of the cell cycle and cytokinesis in regulating neuroblast sublineage gene expression in the Drosophila CNS. Development. 1995 Oct;121(10):3233–3243. doi: 10.1242/dev.121.10.3233. [DOI] [PubMed] [Google Scholar]
  15. Doe C. Q., Chu-LaGraff Q., Wright D. M., Scott M. P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell. 1991 May 3;65(3):451–464. doi: 10.1016/0092-8674(91)90463-9. [DOI] [PubMed] [Google Scholar]
  16. Doherty D., Jan L. Y., Jan Y. N. The Drosophila neurogenic gene big brain, which encodes a membrane-associated protein, acts cell autonomously and can act synergistically with Notch and Delta. Development. 1997 Oct;124(19):3881–3893. doi: 10.1242/dev.124.19.3881. [DOI] [PubMed] [Google Scholar]
  17. Dye C. A., Lee J. K., Atkinson R. C., Brewster R., Han P. L., Bellen H. J. The Drosophila sanpodo gene controls sibling cell fate and encodes a tropomodulin homolog, an actin/tropomyosin-associated protein. Development. 1998 May;125(10):1845–1856. doi: 10.1242/dev.125.10.1845. [DOI] [PubMed] [Google Scholar]
  18. Edgar B. A., Datar S. A. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev. 1996 Aug 1;10(15):1966–1977. doi: 10.1101/gad.10.15.1966. [DOI] [PubMed] [Google Scholar]
  19. Edgar B. A., O'Farrell P. H. Genetic control of cell division patterns in the Drosophila embryo. Cell. 1989 Apr 7;57(1):177–187. doi: 10.1016/0092-8674(89)90183-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ellis H. M., Spann D. R., Posakony J. W. extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell. 1990 Apr 6;61(1):27–38. doi: 10.1016/0092-8674(90)90212-w. [DOI] [PubMed] [Google Scholar]
  21. Fischer-Vize J. A., Rubin G. M., Lehmann R. The fat facets gene is required for Drosophila eye and embryo development. Development. 1992 Dec;116(4):985–1000. doi: 10.1242/dev.116.4.985. [DOI] [PubMed] [Google Scholar]
  22. Foe V. E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development. 1989 Sep;107(1):1–22. [PubMed] [Google Scholar]
  23. Fogarty P., Campbell S. D., Abu-Shumays R., Phalle B. S., Yu K. R., Uy G. L., Goldberg M. L., Sullivan W. The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr Biol. 1997 Jun 1;7(6):418–426. doi: 10.1016/s0960-9822(06)00189-8. [DOI] [PubMed] [Google Scholar]
  24. Frise E., Knoblich J. A., Younger-Shepherd S., Jan L. Y., Jan Y. N. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11925–11932. doi: 10.1073/pnas.93.21.11925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fuse N., Hirose S., Hayashi S. Diploidy of Drosophila imaginal cells is maintained by a transcriptional repressor encoded by escargot. Genes Dev. 1994 Oct 1;8(19):2270–2281. doi: 10.1101/gad.8.19.2270. [DOI] [PubMed] [Google Scholar]
  26. Garrell J., Modolell J. The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell. 1990 Apr 6;61(1):39–48. doi: 10.1016/0092-8674(90)90213-x. [DOI] [PubMed] [Google Scholar]
  27. Gellon G., Harding K. W., McGinnis N., Martin M. M., McGinnis W. A genetic screen for modifiers of Deformed homeotic function identifies novel genes required for head development. Development. 1997 Sep;124(17):3321–3331. doi: 10.1242/dev.124.17.3321. [DOI] [PubMed] [Google Scholar]
  28. Gho M., Bellaïche Y., Schweisguth F. Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development. 1999 Aug;126(16):3573–3584. doi: 10.1242/dev.126.16.3573. [DOI] [PubMed] [Google Scholar]
  29. Ghysen A., Dambly-Chaudiere C. Genesis of the Drosophila peripheral nervous system. Trends Genet. 1989 Aug;5(8):251–255. doi: 10.1016/0168-9525(89)90097-8. [DOI] [PubMed] [Google Scholar]
  30. Giniger E., Tietje K., Jan L. Y., Jan Y. N. lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development. 1994 Jun;120(6):1385–1398. doi: 10.1242/dev.120.6.1385. [DOI] [PubMed] [Google Scholar]
  31. Gomes R., Karess R. E., Ohkura H., Glover D. M., Sunkel C. E. Abnormal anaphase resolution (aar): a locus required for progression through mitosis in Drosophila. J Cell Sci. 1993 Feb;104(Pt 2):583–593. doi: 10.1242/jcs.104.2.583. [DOI] [PubMed] [Google Scholar]
  32. Guo M., Bier E., Jan L. Y., Jan Y. N. tramtrack acts downstream of numb to specify distinct daughter cell fates during asymmetric cell divisions in the Drosophila PNS. Neuron. 1995 May;14(5):913–925. doi: 10.1016/0896-6273(95)90330-5. [DOI] [PubMed] [Google Scholar]
  33. Gómez-Skarmeta J. L., Modolell J. araucan and caupolican provide a link between compartment subdivisions and patterning of sensory organs and veins in the Drosophila wing. Genes Dev. 1996 Nov 15;10(22):2935–2945. doi: 10.1101/gad.10.22.2935. [DOI] [PubMed] [Google Scholar]
  34. Hammond L. E., Rudner D. Z., Kanaar R., Rio D. C. Mutations in the hrp48 gene, which encodes a Drosophila heterogeneous nuclear ribonucleoprotein particle protein, cause lethality and developmental defects and affect P-element third-intron splicing in vivo. Mol Cell Biol. 1997 Dec;17(12):7260–7267. doi: 10.1128/mcb.17.12.7260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hartenstein V., Posakony J. W. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development. 1989 Oct;107(2):389–405. doi: 10.1242/dev.107.2.389. [DOI] [PubMed] [Google Scholar]
  36. Hassan B. A., Prokopenko S. N., Breuer S., Zhang B., Paululat A., Bellen H. J. skittles, a Drosophila phosphatidylinositol 4-phosphate 5-kinase, is required for cell viability, germline development and bristle morphology, but not for neurotransmitter release. Genetics. 1998 Dec;150(4):1527–1537. doi: 10.1093/genetics/150.4.1527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hayashi S. A Cdc2 dependent checkpoint maintains diploidy in Drosophila. Development. 1996 Apr;122(4):1051–1058. doi: 10.1242/dev.122.4.1051. [DOI] [PubMed] [Google Scholar]
  38. Hayashi S., Hirose S., Metcalfe T., Shirras A. D. Control of imaginal cell development by the escargot gene of Drosophila. Development. 1993 May;118(1):105–115. doi: 10.1242/dev.118.1.105. [DOI] [PubMed] [Google Scholar]
  39. Heberlein U., Wolff T., Rubin G. M. The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell. 1993 Dec 3;75(5):913–926. doi: 10.1016/0092-8674(93)90535-x. [DOI] [PubMed] [Google Scholar]
  40. Hirata J., Nakagoshi H., Nabeshima Y., Matsuzaki F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature. 1995 Oct 19;377(6550):627–630. doi: 10.1038/377627a0. [DOI] [PubMed] [Google Scholar]
  41. Huang Y., Baker R. T., Fischer-Vize J. A. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science. 1995 Dec 15;270(5243):1828–1831. doi: 10.1126/science.270.5243.1828. [DOI] [PubMed] [Google Scholar]
  42. Ikeshima-Kataoka H., Skeath J. B., Nabeshima Y., Doe C. Q., Matsuzaki F. Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature. 1997 Dec 11;390(6660):625–629. doi: 10.1038/37641. [DOI] [PubMed] [Google Scholar]
  43. Jarriault S., Brou C., Logeat F., Schroeter E. H., Kopan R., Israel A. Signalling downstream of activated mammalian Notch. Nature. 1995 Sep 28;377(6547):355–358. doi: 10.1038/377355a0. [DOI] [PubMed] [Google Scholar]
  44. Kania A., Salzberg A., Bhat M., D'Evelyn D., He Y., Kiss I., Bellen H. J. P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics. 1995 Apr;139(4):1663–1678. doi: 10.1093/genetics/139.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kavaler J., Fu W., Duan H., Noll M., Posakony J. W. An essential role for the Drosophila Pax2 homolog in the differentiation of adult sensory organs. Development. 1999 May;126(10):2261–2272. doi: 10.1242/dev.126.10.2261. [DOI] [PubMed] [Google Scholar]
  46. Knoblich J. A., Jan L. Y., Jan Y. N. Asymmetric segregation of Numb and Prospero during cell division. Nature. 1995 Oct 19;377(6550):624–627. doi: 10.1038/377624a0. [DOI] [PubMed] [Google Scholar]
  47. Knoblich J. A., Jan L. Y., Jan Y. N. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13005–13010. doi: 10.1073/pnas.94.24.13005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kraut R., Chia W., Jan L. Y., Jan Y. N., Knoblich J. A. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature. 1996 Sep 5;383(6595):50–55. doi: 10.1038/383050a0. [DOI] [PubMed] [Google Scholar]
  49. Lane M. E., Sauer K., Wallace K., Jan Y. N., Lehner C. F., Vaessin H. Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell. 1996 Dec 27;87(7):1225–1235. doi: 10.1016/s0092-8674(00)81818-8. [DOI] [PubMed] [Google Scholar]
  50. Lecourtois M., Schweisguth F. The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev. 1995 Nov 1;9(21):2598–2608. doi: 10.1101/gad.9.21.2598. [DOI] [PubMed] [Google Scholar]
  51. Lieber T., Kidd S., Alcamo E., Corbin V., Young M. W. Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev. 1993 Oct;7(10):1949–1965. doi: 10.1101/gad.7.10.1949. [DOI] [PubMed] [Google Scholar]
  52. Lin X., Perrimon N. Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signalling. Nature. 1999 Jul 15;400(6741):281–284. doi: 10.1038/22343. [DOI] [PubMed] [Google Scholar]
  53. Lu B., Ackerman L., Jan L. Y., Jan Y. N. Modes of protein movement that lead to the asymmetric localization of partner of Numb during Drosophila neuroblast division. Mol Cell. 1999 Dec;4(6):883–891. doi: 10.1016/s1097-2765(00)80218-x. [DOI] [PubMed] [Google Scholar]
  54. Lu B., Rothenberg M., Jan L. Y., Jan Y. N. Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell. 1998 Oct 16;95(2):225–235. doi: 10.1016/s0092-8674(00)81753-5. [DOI] [PubMed] [Google Scholar]
  55. Ma C., Zhou Y., Beachy P. A., Moses K. The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell. 1993 Dec 3;75(5):927–938. doi: 10.1016/0092-8674(93)90536-y. [DOI] [PubMed] [Google Scholar]
  56. Miklos G. L., Rubin G. M. The role of the genome project in determining gene function: insights from model organisms. Cell. 1996 Aug 23;86(4):521–529. doi: 10.1016/s0092-8674(00)80126-9. [DOI] [PubMed] [Google Scholar]
  57. Milán M., Diaz-Benjumea F. J., Cohen S. M. Beadex encodes an LMO protein that regulates Apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev. 1998 Sep 15;12(18):2912–2920. doi: 10.1101/gad.12.18.2912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Mullor J. L., Calleja M., Capdevila J., Guerrero I. Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning. Development. 1997 Mar;124(6):1227–1237. doi: 10.1242/dev.124.6.1227. [DOI] [PubMed] [Google Scholar]
  59. Nakao K., Campos-Ortega J. A. Persistent expression of genes of the enhancer of split complex suppresses neural development in Drosophila. Neuron. 1996 Feb;16(2):275–286. doi: 10.1016/s0896-6273(00)80046-x. [DOI] [PubMed] [Google Scholar]
  60. Nakato H., Futch T. A., Selleck S. B. The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. Development. 1995 Nov;121(11):3687–3702. doi: 10.1242/dev.121.11.3687. [DOI] [PubMed] [Google Scholar]
  61. O'Neill E. M., Rebay I., Tjian R., Rubin G. M. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell. 1994 Jul 15;78(1):137–147. doi: 10.1016/0092-8674(94)90580-0. [DOI] [PubMed] [Google Scholar]
  62. Phillips R. G., Whittle J. R. wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development. Development. 1993 Jun;118(2):427–438. doi: 10.1242/dev.118.2.427. [DOI] [PubMed] [Google Scholar]
  63. Posakony J. W. Nature versus nurture: asymmetric cell divisions in Drosophila bristle development. Cell. 1994 Feb 11;76(3):415–418. doi: 10.1016/0092-8674(94)90105-8. [DOI] [PubMed] [Google Scholar]
  64. Rao Y., Bodmer R., Jan L. Y., Jan Y. N. The big brain gene of Drosophila functions to control the number of neuronal precursors in the peripheral nervous system. Development. 1992 Sep;116(1):31–40. doi: 10.1242/dev.116.1.31. [DOI] [PubMed] [Google Scholar]
  65. Rao Y., Jan L. Y., Jan Y. N. Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature. 1990 May 10;345(6271):163–167. doi: 10.1038/345163a0. [DOI] [PubMed] [Google Scholar]
  66. Rhyu M. S., Jan L. Y., Jan Y. N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 1994 Feb 11;76(3):477–491. doi: 10.1016/0092-8674(94)90112-0. [DOI] [PubMed] [Google Scholar]
  67. Rørth P., Szabo K., Bailey A., Laverty T., Rehm J., Rubin G. M., Weigmann K., Milán M., Benes V., Ansorge W. Systematic gain-of-function genetics in Drosophila. Development. 1998 Mar;125(6):1049–1057. doi: 10.1242/dev.125.6.1049. [DOI] [PubMed] [Google Scholar]
  68. Salzberg A., D'Evelyn D., Schulze K. L., Lee J. K., Strumpf D., Tsai L., Bellen H. J. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron. 1994 Aug;13(2):269–287. doi: 10.1016/0896-6273(94)90346-8. [DOI] [PubMed] [Google Scholar]
  69. Schuldt A. J., Adams J. H., Davidson C. M., Micklem D. R., Haseloff J., St Johnston D., Brand A. H. Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 1998 Jun 15;12(12):1847–1857. doi: 10.1101/gad.12.12.1847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Schweisguth F., Posakony J. W. Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development. 1994 Jun;120(6):1433–1441. doi: 10.1242/dev.120.6.1433. [DOI] [PubMed] [Google Scholar]
  71. Schweisguth F., Posakony J. W. Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell. 1992 Jun 26;69(7):1199–1212. doi: 10.1016/0092-8674(92)90641-o. [DOI] [PubMed] [Google Scholar]
  72. Shiomi K., Takeichi M., Nishida Y., Nishi Y., Uemura T. Alternative cell fate choice induced by low-level expression of a regulator of protein phosphatase 2A in the Drosophila peripheral nervous system. Development. 1994 Jun;120(6):1591–1599. doi: 10.1242/dev.120.6.1591. [DOI] [PubMed] [Google Scholar]
  73. Shoresh M., Orgad S., Shmueli O., Werczberger R., Gelbaum D., Abiri S., Segal D. Overexpression Beadex mutations and loss-of-function heldup-a mutations in Drosophila affect the 3' regulatory and coding components, respectively, of the Dlmo gene. Genetics. 1998 Sep;150(1):283–299. doi: 10.1093/genetics/150.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  75. Simpson P., Woehl R., Usui K. The development and evolution of bristle patterns in Diptera. Development. 1999 Apr;126(7):1349–1364. doi: 10.1242/dev.126.7.1349. [DOI] [PubMed] [Google Scholar]
  76. Skeath J. B., Carroll S. B. Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 1991 Jun;5(6):984–995. doi: 10.1101/gad.5.6.984. [DOI] [PubMed] [Google Scholar]
  77. Skeath J. B., Doe C. Q. Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development. 1998 May;125(10):1857–1865. doi: 10.1242/dev.125.10.1857. [DOI] [PubMed] [Google Scholar]
  78. Spana E. P., Doe C. Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development. 1995 Oct;121(10):3187–3195. doi: 10.1242/dev.121.10.3187. [DOI] [PubMed] [Google Scholar]
  79. Su M. T., Venkatesh T. V., Wu X., Golden K., Bodmer R. The pioneer gene, apontic, is required for morphogenesis and function of the Drosophila heart. Mech Dev. 1999 Feb;80(2):125–132. doi: 10.1016/s0925-4773(98)00197-x. [DOI] [PubMed] [Google Scholar]
  80. Sullivan W., Fogarty P., Theurkauf W. Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development. 1993 Aug;118(4):1245–1254. doi: 10.1242/dev.118.4.1245. [DOI] [PubMed] [Google Scholar]
  81. Tilney L. G., Connelly P., Smith S., Guild G. M. F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J Cell Biol. 1996 Dec;135(5):1291–1308. doi: 10.1083/jcb.135.5.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Tilney L. G., Tilney M. S., Guild G. M. F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J Cell Biol. 1995 Aug;130(3):629–638. doi: 10.1083/jcb.130.3.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Tsuda M., Kamimura K., Nakato H., Archer M., Staatz W., Fox B., Humphrey M., Olson S., Futch T., Kaluza V. The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature. 1999 Jul 15;400(6741):276–280. doi: 10.1038/22336. [DOI] [PubMed] [Google Scholar]
  84. Turner C. M., Adler P. N. Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila. Mech Dev. 1998 Jan;70(1-2):181–192. doi: 10.1016/s0925-4773(97)00194-9. [DOI] [PubMed] [Google Scholar]
  85. Uemura T., Shepherd S., Ackerman L., Jan L. Y., Jan Y. N. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell. 1989 Jul 28;58(2):349–360. doi: 10.1016/0092-8674(89)90849-0. [DOI] [PubMed] [Google Scholar]
  86. Uemura T., Shiomi K., Togashi S., Takeichi M. Mutation of twins encoding a regulator of protein phosphatase 2A leads to pattern duplication in Drosophila imaginal discs. Genes Dev. 1993 Mar;7(3):429–440. doi: 10.1101/gad.7.3.429. [DOI] [PubMed] [Google Scholar]
  87. Vaessin H., Grell E., Wolff E., Bier E., Jan L. Y., Jan Y. N. prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell. 1991 Nov 29;67(5):941–953. doi: 10.1016/0092-8674(91)90367-8. [DOI] [PubMed] [Google Scholar]
  88. Wang S., Younger-Shepherd S., Jan L. Y., Jan Y. N. Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless. Development. 1997 Nov;124(22):4435–4446. doi: 10.1242/dev.124.22.4435. [DOI] [PubMed] [Google Scholar]
  89. Weigmann K., Lehner C. F. Cell fate specification by even-skipped expression in the Drosophila nervous system is coupled to cell cycle progression. Development. 1995 Nov;121(11):3713–3721. doi: 10.1242/dev.121.11.3713. [DOI] [PubMed] [Google Scholar]
  90. Whiteley M., Noguchi P. D., Sensabaugh S. M., Odenwald W. F., Kassis J. A. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech Dev. 1992 Feb;36(3):117–127. doi: 10.1016/0925-4773(92)90063-p. [DOI] [PubMed] [Google Scholar]
  91. Wiellette E. L., Harding K. W., Mace K. A., Ronshaugen M. R., Wang F. Y., McGinnis W. spen encodes an RNP motif protein that interacts with Hox pathways to repress the development of head-like sclerites in the Drosophila trunk. Development. 1999 Dec;126(23):5373–5385. doi: 10.1242/dev.126.23.5373. [DOI] [PubMed] [Google Scholar]
  92. Xiong W. C., Montell C. tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev. 1993 Jun;7(6):1085–1096. doi: 10.1101/gad.7.6.1085. [DOI] [PubMed] [Google Scholar]
  93. Xu T., Rubin G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 1993 Apr;117(4):1223–1237. doi: 10.1242/dev.117.4.1223. [DOI] [PubMed] [Google Scholar]
  94. Zeng C., Justice N. J., Abdelilah S., Chan Y. M., Jan L. Y., Jan Y. N. The Drosophila LIM-only gene, dLMO, is mutated in Beadex alleles and might represent an evolutionarily conserved function in appendage development. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10637–10642. doi: 10.1073/pnas.95.18.10637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Zeng C., Younger-Shepherd S., Jan L. Y., Jan Y. N. Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 1998 Apr 15;12(8):1086–1091. doi: 10.1101/gad.12.8.1086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. de Nooij J. C., Letendre M. A., Hariharan I. K. A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell. 1996 Dec 27;87(7):1237–1247. doi: 10.1016/s0092-8674(00)81819-x. [DOI] [PubMed] [Google Scholar]
  97. zur Lage P., Shrimpton A. D., Flavell A. J., Mackay T. F., Brown A. J. Genetic and molecular analysis of smooth, a quantitative trait locus affecting bristle number in Drosophila melanogaster. Genetics. 1997 Jun;146(2):607–618. doi: 10.1093/genetics/146.2.607. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES