Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Dec;156(4):1691–1715. doi: 10.1093/genetics/156.4.1691

Mutations affecting the development of the peripheral nervous system in Drosophila: a molecular screen for novel proteins.

S N Prokopenko 1, Y He 1, Y Lu 1, H J Bellen 1
PMCID: PMC1461357  PMID: 11102367

Abstract

In our quest for novel genes required for the development of the embryonic peripheral nervous system (PNS), we have performed three genetic screens using MAb 22C10 as a marker of terminally differentiated neurons. A total of 66 essential genes required for normal PNS development were identified, including 49 novel genes. To obtain information about the molecular nature of these genes, we decided to complement our genetic screens with a molecular screen. From transposon-tagged mutations identified on the basis of their phenotype in the PNS we selected 31 P-element strains representing 26 complementation groups on the second and third chromosomes to clone and sequence the corresponding genes. We used plasmid rescue to isolate and sequence 51 genomic fragments flanking the sites of these P-element insertions. Database searches using sequences derived from the ends of plasmid rescues allowed us to assign genes to one of four classes: (1) previously characterized genes (11), (2) first mutations in cloned genes (1), (3) P-element insertions in genes that were identified, but not characterized molecularly (1), and (4) novel genes (13). Here, we report the cloning, sequence, Northern analysis, and the embryonic expression pattern of candidate cDNAs for 10 genes: astray, chrowded, dalmatian, gluon, hoi-polloi, melted, pebble, skittles, sticky ch1, and vegetable. This study allows us to draw conclusions about the identity of proteins required for the development of the nervous system in Drosophila and provides an example of a molecular approach to characterize en masse transposon-tagged mutations identified in genetic screens.

Full Text

The Full Text of this article is available as a PDF (522.6 KB).

Selected References

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

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Adams R. R., Tavares A. A., Salzberg A., Bellen H. J., Glover D. M. pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 1998 May 15;12(10):1483–1494. doi: 10.1101/gad.12.10.1483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Artero R., Prokop A., Paricio N., Begemann G., Pueyo I., Mlodzik M., Perez-Alonso M., Baylies M. K. The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2. Dev Biol. 1998 Mar 15;195(2):131–143. doi: 10.1006/dbio.1997.8833. [DOI] [PubMed] [Google Scholar]
  4. Ayer D. E., Lawrence Q. A., Eisenman R. N. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell. 1995 Mar 10;80(5):767–776. doi: 10.1016/0092-8674(95)90355-0. [DOI] [PubMed] [Google Scholar]
  5. Baker B. S., Hoff G., Kaufman T. C., Wolfner M. F., Hazelrigg T. The doublesex locus of Drosophila melanogaster and its flanking regions: a cytogenetic analysis. Genetics. 1991 Jan;127(1):125–138. doi: 10.1093/genetics/127.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beall E. L., Rio D. C. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev. 1997 Aug 15;11(16):2137–2151. doi: 10.1101/gad.11.16.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Begemann G., Paricio N., Artero R., Kiss I., Pérez-Alonso M., Mlodzik M. muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development. 1997 Nov;124(21):4321–4331. doi: 10.1242/dev.124.21.4321. [DOI] [PubMed] [Google Scholar]
  8. Bellen H. J. Ten years of enhancer detection: lessons from the fly. Plant Cell. 1999 Dec;11(12):2271–2281. doi: 10.1105/tpc.11.12.2271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Berg C. A., Spradling A. C. Studies on the rate and site-specificity of P element transposition. Genetics. 1991 Mar;127(3):515–524. doi: 10.1093/genetics/127.3.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bhat M. A., Izaddoost S., Lu Y., Cho K. O., Choi K. W., Bellen H. J. Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell. 1999 Mar 19;96(6):833–845. doi: 10.1016/s0092-8674(00)80593-0. [DOI] [PubMed] [Google Scholar]
  11. Bhat M. A., Philp A. V., Glover D. M., Bellen H. J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell. 1996 Dec 13;87(6):1103–1114. doi: 10.1016/s0092-8674(00)81804-8. [DOI] [PubMed] [Google Scholar]
  12. Boudjelal M., Taneja R., Matsubara S., Bouillet P., Dolle P., Chambon P. Overexpression of Stra13, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells. Genes Dev. 1997 Aug 15;11(16):2052–2065. doi: 10.1101/gad.11.16.2052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Breen T. R., Duncan I. M. Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster. Dev Biol. 1986 Dec;118(2):442–456. doi: 10.1016/0012-1606(86)90015-1. [DOI] [PubMed] [Google Scholar]
  14. Buff E., Carmena A., Gisselbrecht S., Jiménez F., Michelson A. M. Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development. 1998 Jun;125(11):2075–2086. doi: 10.1242/dev.125.11.2075. [DOI] [PubMed] [Google Scholar]
  15. Burchard S., Paululat A., Hinz U., Renkawitz-Pohl R. The mutant not enough muscles (nem) reveals reduction of the Drosophila embryonic muscle pattern. J Cell Sci. 1995 Apr;108(Pt 4):1443–1454. doi: 10.1242/jcs.108.4.1443. [DOI] [PubMed] [Google Scholar]
  16. Byars C. L., Bates K. L., Letsou A. The dorsal-open group gene raw is required for restricted DJNK signaling during closure. Development. 1999 Nov;126(21):4913–4923. doi: 10.1242/dev.126.21.4913. [DOI] [PubMed] [Google Scholar]
  17. Caudy M., Vässin H., Brand M., Tuma R., Jan L. Y., Jan Y. N. daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex. Cell. 1988 Dec 23;55(6):1061–1067. doi: 10.1016/0092-8674(88)90250-4. [DOI] [PubMed] [Google Scholar]
  18. Chen Y., Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 1996 Nov 1;87(3):553–563. doi: 10.1016/s0092-8674(00)81374-4. [DOI] [PubMed] [Google Scholar]
  19. Chen Y., Struhl G. In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex. Development. 1998 Dec;125(24):4943–4948. doi: 10.1242/dev.125.24.4943. [DOI] [PubMed] [Google Scholar]
  20. Christodoulou S., Lockyer A. E., Foster J. M., Hoheisel J. D., Roberts D. B. Nucleotide sequence of a Drosophila melanogaster cDNA encoding a calnexin homologue. Gene. 1997 Jun 3;191(2):143–148. doi: 10.1016/s0378-1119(97)00025-5. [DOI] [PubMed] [Google Scholar]
  21. Collet J. F., Gerin I., Rider M. H., Veiga-da-Cunha M., Van Schaftingen E. Human L-3-phosphoserine phosphatase: sequence, expression and evidence for a phosphoenzyme intermediate. FEBS Lett. 1997 May 26;408(3):281–284. doi: 10.1016/s0014-5793(97)00438-9. [DOI] [PubMed] [Google Scholar]
  22. Collet J. F., Stroobant V., Pirard M., Delpierre G., Van Schaftingen E. A new class of phosphotransferases phosphorylated on an aspartate residue in an amino-terminal DXDX(T/V) motif. J Biol Chem. 1998 Jun 5;273(23):14107–14112. doi: 10.1074/jbc.273.23.14107. [DOI] [PubMed] [Google Scholar]
  23. Collet J. F., Stroobant V., Van Schaftingen E. Mechanistic studies of phosphoserine phosphatase, an enzyme related to P-type ATPases. J Biol Chem. 1999 Nov 26;274(48):33985–33990. doi: 10.1074/jbc.274.48.33985. [DOI] [PubMed] [Google Scholar]
  24. Coppolino M. G., Woodside M. J., Demaurex N., Grinstein S., St-Arnaud R., Dedhar S. Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature. 1997 Apr 24;386(6627):843–847. doi: 10.1038/386843a0. [DOI] [PubMed] [Google Scholar]
  25. D'Andrea R. J., Stratmann R., Lehner C. F., John U. P., Saint R. The three rows gene of Drosophila melanogaster encodes a novel protein that is required for chromosome disjunction during mitosis. Mol Biol Cell. 1993 Nov;4(11):1161–1174. doi: 10.1091/mbc.4.11.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Dambly-Chaudière C., Vervoort M. The bHLH genes in neural development. Int J Dev Biol. 1998;42(3):269–273. [PubMed] [Google Scholar]
  27. Dawson S. R., Turner D. L., Weintraub H., Parkhurst S. M. Specificity for the hairy/enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Mol Cell Biol. 1995 Dec;15(12):6923–6931. doi: 10.1128/mcb.15.12.6923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Dobens L. L., Hsu T., Twombly V., Gelbart W. M., Raftery L. A., Kafatos F. C. The Drosophila bunched gene is a homologue of the growth factor stimulated mammalian TSC-22 sequence and is required during oogenesis. Mech Dev. 1997 Jul;65(1-2):197–208. doi: 10.1016/s0925-4773(97)00080-4. [DOI] [PubMed] [Google Scholar]
  29. Dobens L. L., Peterson J. S., Treisman J., Raftery L. A. Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary. Development. 2000 Feb;127(4):745–754. doi: 10.1242/dev.127.4.745. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Fisher A., Caudy M. The function of hairy-related bHLH repressor proteins in cell fate decisions. Bioessays. 1998 Apr;20(4):298–306. doi: 10.1002/(SICI)1521-1878(199804)20:4<298::AID-BIES6>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]
  32. Gamo S., Dodo K., Matakatsu H., Tanaka Y. Molecular genetical analysis of Drosophila ether sensitive mutants. Toxicol Lett. 1998 Nov 23;100-101:329–337. doi: 10.1016/s0378-4274(98)00203-3. [DOI] [PubMed] [Google Scholar]
  33. Gao F. B., Brenman J. E., Jan L. Y., Jan Y. N. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 1999 Oct 1;13(19):2549–2561. doi: 10.1101/gad.13.19.2549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. Gottschalk A., Neubauer G., Banroques J., Mann M., Lührmann R., Fabrizio P. Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6.U5] tri-snRNP. EMBO J. 1999 Aug 16;18(16):4535–4548. doi: 10.1093/emboj/18.16.4535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Grieder N. C., Nellen D., Burke R., Basler K., Affolter M. Schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell. 1995 Jun 2;81(5):791–800. doi: 10.1016/0092-8674(95)90540-5. [DOI] [PubMed] [Google Scholar]
  38. Hartmann E., Rapoport T. A., Lodish H. F. Predicting the orientation of eukaryotic membrane-spanning proteins. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5786–5790. doi: 10.1073/pnas.86.15.5786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Higson T. S., Tessiatore J. E., Bennett S. A., Derk R. C., Kotarski M. A. The molecular organization of the Star/asteroid region, a region necessary for proper eye development in Drosophila melanogaster. Genome. 1993 Apr;36(2):356–366. doi: 10.1139/g93-049. [DOI] [PubMed] [Google Scholar]
  41. Hime G., Saint R. Zygotic expression of the pebble locus is required for cytokinesis during the postblastoderm mitoses of Drosophila. Development. 1992 Jan;114(1):165–171. doi: 10.1242/dev.114.1.165. [DOI] [PubMed] [Google Scholar]
  42. Hirano T., Kobayashi R., Hirano M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell. 1997 May 16;89(4):511–521. doi: 10.1016/s0092-8674(00)80233-0. [DOI] [PubMed] [Google Scholar]
  43. Hirano T. SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates? Genes Dev. 1999 Jan 1;13(1):11–19. doi: 10.1101/gad.13.1.11. [DOI] [PubMed] [Google Scholar]
  44. Hooper J. E., Scott M. P. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell. 1989 Nov 17;59(4):751–765. doi: 10.1016/0092-8674(89)90021-4. [DOI] [PubMed] [Google Scholar]
  45. Ivanov I. P., Simin K., Letsou A., Atkins J. F., Gesteland R. F. The Drosophila gene for antizyme requires ribosomal frameshifting for expression and contains an intronic gene for snRNP Sm D3 on the opposite strand. Mol Cell Biol. 1998 Mar;18(3):1553–1561. doi: 10.1128/mcb.18.3.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Jaeken J., Detheux M., Fryns J. P., Collet J. F., Alliet P., Van Schaftingen E. Phosphoserine phosphatase deficiency in a patient with Williams syndrome. J Med Genet. 1997 Jul;34(7):594–596. doi: 10.1136/jmg.34.7.594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Jaeken J., Detheux M., Van Maldergem L., Foulon M., Carchon H., Van Schaftingen E. 3-Phosphoglycerate dehydrogenase deficiency: an inborn error of serine biosynthesis. Arch Dis Child. 1996 Jun;74(6):542–545. doi: 10.1136/adc.74.6.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Jan Y. N., Jan L. Y. Asymmetric cell division. Nature. 1998 Apr 23;392(6678):775–778. doi: 10.1038/33854. [DOI] [PubMed] [Google Scholar]
  49. Jimenez J., Alphey L., Nurse P., Glover D. M. Complementation of fission yeast cdc2ts and cdc25ts mutants identifies two cell cycle genes from Drosophila: a cdc2 homologue and string. EMBO J. 1990 Nov;9(11):3565–3571. doi: 10.1002/j.1460-2075.1990.tb07567.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. 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]
  51. Klämbt C., Jacobs J. R., Goodman C. S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 1991 Feb 22;64(4):801–815. doi: 10.1016/0092-8674(91)90509-w. [DOI] [PubMed] [Google Scholar]
  52. Knirr S., Breuer S., Paululat A., Renkawitz-Pohl R. Somatic mesoderm differentiation and the development of a subset of pericardial cells depend on the not enough muscles (nem) locus, which contains the inscuteable gene and the intron located gene, skittles. Mech Dev. 1997 Sep;67(1):69–81. doi: 10.1016/s0925-4773(97)00109-3. [DOI] [PubMed] [Google Scholar]
  53. Knoblich J. A., Sauer K., Jones L., Richardson H., Saint R., Lehner C. F. Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell. 1994 Apr 8;77(1):107–120. doi: 10.1016/0092-8674(94)90239-9. [DOI] [PubMed] [Google Scholar]
  54. Kolodkin A. L., Matthes D. J., Goodman C. S. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell. 1993 Dec 31;75(7):1389–1399. doi: 10.1016/0092-8674(93)90625-z. [DOI] [PubMed] [Google Scholar]
  55. Kolodkin A. L., Pickup A. T., Lin D. M., Goodman C. S., Banerjee U. Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila. Development. 1994 Jul;120(7):1731–1745. doi: 10.1242/dev.120.7.1731. [DOI] [PubMed] [Google Scholar]
  56. Kolodziej P. A., Jan L. Y., Jan Y. N. Mutations that affect the length, fasciculation, or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron. 1995 Aug;15(2):273–286. doi: 10.1016/0896-6273(95)90033-0. [DOI] [PubMed] [Google Scholar]
  57. Kolodziej P. A., Timpe L. C., Mitchell K. J., Fried S. R., Goodman C. S., Jan L. Y., Jan Y. N. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell. 1996 Oct 18;87(2):197–204. doi: 10.1016/s0092-8674(00)81338-0. [DOI] [PubMed] [Google Scholar]
  58. Koshland D., Strunnikov A. Mitotic chromosome condensation. Annu Rev Cell Dev Biol. 1996;12:305–333. doi: 10.1146/annurev.cellbio.12.1.305. [DOI] [PubMed] [Google Scholar]
  59. Kotarski M. A., Leonard D. A., Bennett S. A., Bishop C. P., Wahn S. D., Sedore S. A., Shrader M. The Drosophila gene asteroid encodes a novel protein and displays dosage-sensitive interactions with Star and Egfr. Genome. 1998 Apr;41(2):295–302. doi: 10.1139/g98-021. [DOI] [PubMed] [Google Scholar]
  60. Krause K. H., Michalak M. Calreticulin. Cell. 1997 Feb 21;88(4):439–443. doi: 10.1016/s0092-8674(00)81884-x. [DOI] [PubMed] [Google Scholar]
  61. Kraut R., Campos-Ortega J. A. inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev Biol. 1996 Feb 25;174(1):65–81. doi: 10.1006/dbio.1996.0052. [DOI] [PubMed] [Google Scholar]
  62. Langer-Safer P. R., Levine M., Ward D. C. Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4381–4385. doi: 10.1073/pnas.79.14.4381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Lehner C. F., O'Farrell P. H. Expression and function of Drosophila cyclin A during embryonic cell cycle progression. Cell. 1989 Mar 24;56(6):957–968. doi: 10.1016/0092-8674(89)90629-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Lehner C. F., O'Farrell P. H. The roles of Drosophila cyclins A and B in mitotic control. Cell. 1990 May 4;61(3):535–547. doi: 10.1016/0092-8674(90)90535-m. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Lehner C. F. The pebble gene is required for cytokinesis in Drosophila. J Cell Sci. 1992 Dec;103(Pt 4):1021–1030. doi: 10.1242/jcs.103.4.1021. [DOI] [PubMed] [Google Scholar]
  66. Leimeister C., Externbrink A., Klamt B., Gessler M. Hey genes: a novel subfamily of hairy- and Enhancer of split related genes specifically expressed during mouse embryogenesis. Mech Dev. 1999 Jul;85(1-2):173–177. doi: 10.1016/s0925-4773(99)00080-5. [DOI] [PubMed] [Google Scholar]
  67. Li Y. F., Hata Y., Fujii T., Hisano T., Nishihara M., Kurihara T., Esaki N. Crystal structures of reaction intermediates of L-2-haloacid dehalogenase and implications for the reaction mechanism. J Biol Chem. 1998 Jun 12;273(24):15035–15044. doi: 10.1074/jbc.273.24.15035. [DOI] [PubMed] [Google Scholar]
  68. Maiorano D., Brimage L. J., Leroy D., Kearsey S. E. Functional conservation and cell cycle localization of the Nhp2 core component of H + ACA snoRNPs in fission and budding yeasts. Exp Cell Res. 1999 Oct 10;252(1):165–174. doi: 10.1006/excr.1999.4607. [DOI] [PubMed] [Google Scholar]
  69. Marigo V., Davey R. A., Zuo Y., Cunningham J. M., Tabin C. J. Biochemical evidence that patched is the Hedgehog receptor. Nature. 1996 Nov 14;384(6605):176–179. doi: 10.1038/384176a0. [DOI] [PubMed] [Google Scholar]
  70. Martín-Blanco E., Gampel A., Ring J., Virdee K., Kirov N., Tolkovsky A. M., Martinez-Arias A. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 1998 Feb 15;12(4):557–570. doi: 10.1101/gad.12.4.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Modolell J. Patterning of the adult peripheral nervous system of Drosophila. Perspect Dev Neurobiol. 1997;4(4):285–296. [PubMed] [Google Scholar]
  72. Nakagawa O., Nakagawa M., Richardson J. A., Olson E. N., Srivastava D. HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol. 1999 Dec 1;216(1):72–84. doi: 10.1006/dbio.1999.9454. [DOI] [PubMed] [Google Scholar]
  73. Neufeld T. P., Tang A. H., Rubin G. M. A genetic screen to identify components of the sina signaling pathway in Drosophila eye development. Genetics. 1998 Jan;148(1):277–286. doi: 10.1093/genetics/148.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Nolo R., Abbott L. A., Bellen H. J. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell. 2000 Aug 4;102(3):349–362. doi: 10.1016/s0092-8674(00)00040-4. [DOI] [PubMed] [Google Scholar]
  75. Palazzolo M. J., Hamilton B. A., Ding D. L., Martin C. H., Mead D. A., Mierendorf R. C., Raghavan K. V., Meyerowitz E. M., Lipshitz H. D. Phage lambda cDNA cloning vectors for subtractive hybridization, fusion-protein synthesis and Cre-loxP automatic plasmid subcloning. Gene. 1990 Mar 30;88(1):25–36. doi: 10.1016/0378-1119(90)90056-w. [DOI] [PubMed] [Google Scholar]
  76. Pennetta G., Pauli D. The Drosophila Sin3 gene encodes a widely distributed transcription factor essential for embryonic viability. Dev Genes Evol. 1998 Nov;208(9):531–536. doi: 10.1007/s004270050212. [DOI] [PubMed] [Google Scholar]
  77. Pennetta G., Pauli D. stand still, a Drosophila gene involved in the female germline for proper survival, sex determination and differentiation. Genetics. 1997 Apr;145(4):975–987. doi: 10.1093/genetics/145.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Philp A. V., Axton J. M., Saunders R. D., Glover D. M. Mutations in the Drosophila melanogaster gene three rows permit aspects of mitosis to continue in the absence of chromatid segregation. J Cell Sci. 1993 Sep;106(Pt 1):87–98. doi: 10.1242/jcs.106.1.87. [DOI] [PubMed] [Google Scholar]
  79. Prober D. A., Edgar B. A. Ras1 promotes cellular growth in the Drosophila wing. Cell. 2000 Feb 18;100(4):435–446. doi: 10.1016/s0092-8674(00)80679-0. [DOI] [PubMed] [Google Scholar]
  80. Prokopenko S. N., Brumby A., O'Keefe L., Prior L., He Y., Saint R., Bellen H. J. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev. 1999 Sep 1;13(17):2301–2314. doi: 10.1101/gad.13.17.2301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Razzaq A., Su Y., Mehren J. E., Mizuguchi K., Jackson A. P., Gay N. J., O'Kane C. J. Characterisation of the gene for Drosophila amphiphysin. Gene. 2000 Jan 4;241(1):167–174. doi: 10.1016/s0378-1119(99)00451-5. [DOI] [PubMed] [Google Scholar]
  82. Rechsteiner M., Rogers S. W. PEST sequences and regulation by proteolysis. Trends Biochem Sci. 1996 Jul;21(7):267–271. [PubMed] [Google Scholar]
  83. Richardson H. E., O'Keefe L. V., Reed S. I., Saint R. A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis. Development. 1993 Nov;119(3):673–690. doi: 10.1242/dev.119.3.673. [DOI] [PubMed] [Google Scholar]
  84. Rieckhof G. E., Casares F., Ryoo H. D., Abu-Shaar M., Mann R. S. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell. 1997 Oct 17;91(2):171–183. doi: 10.1016/s0092-8674(00)80400-6. [DOI] [PubMed] [Google Scholar]
  85. Ring J. M., Martinez Arias A. puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Dev Suppl. 1993:251–259. [PubMed] [Google Scholar]
  86. Roch F., Serras F., Cifuentes F. J., Corominas M., Alsina B., Amorós M., López-Varea A., Hernández R., Guerra D., Cavicchi S. Screening of larval/pupal P-element induced lethals on the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs. Mol Gen Genet. 1998 Jan;257(2):103–112. doi: 10.1007/pl00008620. [DOI] [PubMed] [Google Scholar]
  87. Rossner M. J., Dörr J., Gass P., Schwab M. H., Nave K. A. SHARPs: mammalian enhancer-of-split- and hairy-related proteins coupled to neuronal stimulation. Mol Cell Neurosci. 1997;9(5-6):460–475. doi: 10.1006/mcne.1997.0640. [DOI] [PubMed] [Google Scholar]
  88. Rubin G. M., Hong L., Brokstein P., Evans-Holm M., Frise E., Stapleton M., Harvey D. A. A Drosophila complementary DNA resource. Science. 2000 Mar 24;287(5461):2222–2224. doi: 10.1126/science.287.5461.2222. [DOI] [PubMed] [Google Scholar]
  89. Rubin G. M., Yandell M. D., Wortman J. R., Gabor Miklos G. L., Nelson C. R., Hariharan I. K., Fortini M. E., Li P. W., Apweiler R., Fleischmann W. Comparative genomics of the eukaryotes. Science. 2000 Mar 24;287(5461):2204–2215. doi: 10.1126/science.287.5461.2204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. 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]
  91. Saito H., Fujiwara T., Shin S., Okui K., Nakamura Y. Cloning and mapping of a human novel cDNA (NHP2L1) that encodes a protein highly homologous to yeast nuclear protein NHP2. Cytogenet Cell Genet. 1996;72(2-3):191–193. doi: 10.1159/000134186. [DOI] [PubMed] [Google Scholar]
  92. Saka Y., Sutani T., Yamashita Y., Saitoh S., Takeuchi M., Nakaseko Y., Yanagida M. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J. 1994 Oct 17;13(20):4938–4952. doi: 10.1002/j.1460-2075.1994.tb06821.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. 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]
  94. Salzberg A., Golden K., Bodmer R., Bellen H. J. gutfeeling, a Drosophila gene encoding an antizyme-like protein, is required for late differentiation of neurons and muscles. Genetics. 1996 Sep;144(1):183–196. doi: 10.1093/genetics/144.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Sasamura T., Kobayashi T., Kojima S., Qadota H., Ohya Y., Masai I., Hotta Y. Molecular cloning and characterization of Drosophila genes encoding small GTPases of the rab and rho families. Mol Gen Genet. 1997 May 20;254(5):486–494. doi: 10.1007/s004380050443. [DOI] [PubMed] [Google Scholar]
  96. Satoh A. K., Tokunaga F., Ozaki K. Rab proteins of Drosophila melanogaster: novel members of the Rab-protein family. FEBS Lett. 1997 Mar 3;404(1):65–69. doi: 10.1016/s0014-5793(97)00094-x. [DOI] [PubMed] [Google Scholar]
  97. Schreiber-Agus N., DePinho R. A. Repression by the Mad(Mxi1)-Sin3 complex. Bioessays. 1998 Oct;20(10):808–818. doi: 10.1002/(SICI)1521-1878(199810)20:10<808::AID-BIES6>3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  98. Schultz J., Copley R. R., Doerks T., Ponting C. P., Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 2000 Jan 1;28(1):231–234. doi: 10.1093/nar/28.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Schultz J., Milpetz F., Bork P., Ponting C. P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857–5864. doi: 10.1073/pnas.95.11.5857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Shen M., Kawamoto T., Yan W., Nakamasu K., Tamagami M., Koyano Y., Noshiro M., Kato Y. Molecular characterization of the novel basic helix-loop-helix protein DEC1 expressed in differentiated human embryo chondrocytes. Biochem Biophys Res Commun. 1997 Jul 18;236(2):294–298. doi: 10.1006/bbrc.1997.6960. [DOI] [PubMed] [Google Scholar]
  101. 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]
  102. Smith M. J. Nucleotide sequence of a Drosophila melanogaster gene encoding a calreticulin homologue. DNA Seq. 1992;3(4):247–250. doi: 10.3109/10425179209034025. [DOI] [PubMed] [Google Scholar]
  103. Spradling A. C., Stern D. M., Kiss I., Roote J., Laverty T., Rubin G. M. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824–10830. doi: 10.1073/pnas.92.24.10824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Spradling A. C., Stern D., Beaton A., Rhem E. J., Laverty T., Mozden N., Misra S., Rubin G. M. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 1999 Sep;153(1):135–177. doi: 10.1093/genetics/153.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Staehling-Hampton K., Laughon A. S., Hoffmann F. M. A Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development. 1995 Oct;121(10):3393–3403. doi: 10.1242/dev.121.10.3393. [DOI] [PubMed] [Google Scholar]
  106. Strunnikov A. V. SMC proteins and chromosome structure. Trends Cell Biol. 1998 Nov;8(11):454–459. doi: 10.1016/s0962-8924(98)01370-1. [DOI] [PubMed] [Google Scholar]
  107. Sutani T., Yuasa T., Tomonaga T., Dohmae N., Takio K., Yanagida M. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev. 1999 Sep 1;13(17):2271–2283. doi: 10.1101/gad.13.17.2271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  109. Treisman J. E., Lai Z. C., Rubin G. M. Shortsighted acts in the decapentaplegic pathway in Drosophila eye development and has homology to a mouse TGF-beta-responsive gene. Development. 1995 Sep;121(9):2835–2845. doi: 10.1242/dev.121.9.2835. [DOI] [PubMed] [Google Scholar]
  110. Török T., Tick G., Alvarado M., Kiss I. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics. 1993 Sep;135(1):71–80. doi: 10.1093/genetics/135.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. 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]
  112. Wheeler D. L., Chappey C., Lash A. E., Leipe D. D., Madden T. L., Schuler G. D., Tatusova T. A., Rapp B. A. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2000 Jan 1;28(1):10–14. doi: 10.1093/nar/28.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. 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]
  114. Zaffran S. Molecular cloning and embryonic expression of dFKBP59, a novel Drosophila FK506-binding protein. Gene. 2000 Apr 4;246(1-2):103–109. doi: 10.1016/s0378-1119(00)00058-5. [DOI] [PubMed] [Google Scholar]
  115. Zinn K., McAllister L., Goodman C. S. Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell. 1988 May 20;53(4):577–587. doi: 10.1016/0092-8674(88)90574-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES