Advertisement
JOURNAL ARTICLES
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
H. Nakato, T.A. Futch, S.B. Selleck
Development 1995 121: 3687-3702;

Summary

We have devised a genetic screen to obtain mutants affecting cell division patterning in the developing central nervous system of Drosophila. The division abnormally delayed (dally) locus was identified using a combination of “enhancer trap” and behavioral screening methods. The ordered cell cycle progression of lamina precursor cells, which generate synaptic target neurons for photoreceptors, is disrupted in dally mutants. The first of two lamina precursor cell divisions shows a delayed entry into mitosis. The second division, one that is triggered by an intercellular signal from photoreceptor axons, fails to take place. Similar to lamina precursors, cells that generate the ommatidia of the adult eye show two synchronized divisions found along the morphogenetic furrow in the eye disc and the first division cycle in dally mutants displays a delayed progression into M phase like that found in the first lamina precursor cell division. dally mutations also affect viability and produce morphological defects in several adult tissues, including the eye, antenna, wing and genitalia. Sequencing of a dally cDNA reveals a potential open reading frame of 626 amino acids with homology to a family of Glypican-related integral membrane proteoglycans. These heparan sulfate-containing proteins are attached to the external leaflet of the plasma membrane via a glycosylphosphatidylinositol linkage. Heparan sulfate proteoglycans may serve as co-receptors for a variety of secreted proteins including fibroblast growth factor, vascular endothelial growth factor, hepatocyte growth factor and members of the Wnt, TGF-beta and Hedgehog families. The cell division defects found in dally mutants implicate the Glypican group of integral membrane proteoglycans in the control of cell division during development.

Reference

    1. Baker N. E.
    (1988) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102, 489–497
    OpenUrlAbstract
    1. Benzer S.
    (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natn. Acad. Sci. USA 58, 1112–1119
    OpenUrlFREE Full Text
    1. Boynton S.,
    2. Tully T.
    (1992) latheo, a new gene involved in associative learning and memory in Drosophila melanogaster, identified from P element mutagenesis. Genetics 131, 655–672
    OpenUrlAbstract/FREE Full Text
    1. Bradley R. S.,
    2. Brown A. M. C.
    (1990) The proto-oncogene int-1 encodes a secreted protein associated with the extracellular matrix. EMBO J 9, 1569–1575
    OpenUrlPubMedWeb of Science
    1. Brown N. H.,
    2. Kafatos F. C.
    (1988) Functional cDNA libraries from Drosophila embyros. J. Mol. Biol 203, 425–437
    OpenUrlCrossRefPubMedWeb of Science
    1. Buckles G. R.,
    2. Smith Z. D.,
    3. Katz F. N.
    (1992) mip causes hyperinnervation of a retinotopic map in Drosophila by excessive recruitment of R7 photoreceptor cells. Neuron 8, 1015–1029
    OpenUrlCrossRefPubMed
    1. David G.,
    2. Lories V.,
    3. Decock B.,
    4. Marynen P.,
    5. Cassiman J.-J.,
    6. Van den Berghe H.
    (1990) Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J. Cell Biol 111, 3165–3176
    OpenUrlAbstract/FREE Full Text
    1. David G.
    (1993) Integral membrane heparan sulfate proteoglycans. FASEB J 7, 1023–1030
    OpenUrlAbstract
    1. Daniels S. B.,
    2. McCarron M.,
    3. Love C.,
    4. Chovnick A.
    (1985) Dysgenesis-induced instability of rosy locus transformation in Drosophila melanogaster: analysis of excision events and the selective recovery of control element deletions. Genetics 109, 95–117
    OpenUrlAbstract/FREE Full Text
    1. Ebens A. J.,
    2. Garren H.,
    3. Cheyette B. N. R.,
    4. Zipursky S. L.
    (1993) The Drosophilaanachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74, 15–27
    OpenUrlCrossRefPubMedWeb of Science
    1. Filmus J.,
    2. Church J. G.,
    3. Buick R. N.
    (1988) Isolation of a cDNA corresponding to a developmentally regulated transcript in rat intestine. Mol. Cell. Biol 8, 4243–4249
    OpenUrlAbstract/FREE Full Text
    1. Fujita S. C.,
    2. Zipursky S. L.,
    3. Benzer S.,
    4. Ferrus A.,
    5. Shotwell S. L.
    (1982) Monoclonal antibodies against the Drosophila nervous system. Proc. Natn. Acad. Sci. USA 79, 7929–7933
    OpenUrlAbstract/FREE Full Text
    1. Gaul U.,
    2. Mardon G.,
    3. Rubin G. M.
    (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the sevenless receptor tyrosine kinase. Cell 68, 1007–1019
    OpenUrlCrossRefPubMedWeb of Science
    1. Karpen G. H.,
    2. Spradling A. C.
    (1992) Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P-element insertional mutagenesis. Genetics 132, 737–753
    OpenUrlAbstract/FREE Full Text
    1. Karthikeyan L.,
    2. Maurel P.,
    3. Rauch U.,
    4. Margolis R. K.,
    5. Margolis R. U.
    (1992) Cloning of a major heparan sulfate proteoglycan from brain and identification as a rat form of glypican. Biochem. Biophys. Res. Comm 188, 395–401
    OpenUrlCrossRefPubMed
    1. Lee J. J.,
    2. Ekker S. C.,
    3. von Kessler D. P.,
    4. Porter J. A.,
    5. Sun B. I.,
    6. Beachy P. A.
    (1994) Autoproteolysis in hedgehog protein biogenesis. Science 266, 1528–1537
    OpenUrlAbstract/FREE Full Text
    1. Luo L.,
    2. Tully T.,
    3. White K.
    (1992) Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9, 595–605
    OpenUrlCrossRefPubMedWeb of Science
    1. Macagno E. R.
    (1979) Cellular interactions and pattern formation in the development of the visual system of Daphnia magna (Crustacea, Brachiopoda). I. Interactions between embryonic retinular fibers and lamina neurons. Dev. Biol 73, 206–238
    OpenUrlCrossRefPubMed
    1. Maniatis T.,
    2. Hardison R. C.,
    3. Lacy E.,
    4. Lauer J.,
    5. O'Connell C.,
    6. Quon D.,
    7. Sim G. K.,
    8. Efstratiadis A.
    (1978) The isolation of structural genes from libraries of eukaryotic DNA. Cell 15, 687–701
    OpenUrlCrossRefPubMedWeb of Science
    1. Norbury C.,
    2. Nurse P.
    (1992) Animal cell cycles and their control. Ann. Rev. Biochem 61, 441–470
    OpenUrlCrossRefPubMedWeb of Science
    1. Ornitz D. M.,
    2. Yayon A.,
    3. Flanagan J. G.,
    4. Svahn C. M.,
    5. Levi E.,
    6. Leder P.
    (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol. Cell. Biol 12, 240–247
    OpenUrlAbstract/FREE Full Text
    1. Rapraeger A. C.,
    2. Krufka A.,
    3. Olwin B. B.
    (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast and myoblast differentiation. Science 252, 1705–1708
    OpenUrlAbstract/FREE Full Text
    1. Ready D. F.,
    2. Hanson T. E.,
    3. Benzer S.
    (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol 53, 217–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Restifo L. L.,
    2. Merrill V. K.
    (1993) Two Drosophila regulatory genes, Deformed and the Broad-Complex, share common functions in development of adult CNS, head, and salivary glands. Dev. Biol 162, 465–485
    1. Robinow S.,
    2. White K.
    (1991) Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol 22, 443–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Rogge R.,
    2. Cagan R.,
    3. Majumdar A.,
    4. Dulaney T.,
    5. Banerjee U.
    (1992) Neuronal development in the Drosophila retina: the sextra gene defines an inhibitory component in the developmental pathway of R7 photoreceptor cells. Proc. Nat. Acad. Sci. USA 89, 5271–5275
    OpenUrlAbstract/FREE Full Text
    1. Selleck S. B.,
    2. Steller H.
    (1991) The influence of retinal innervation on neurogenesis in the first optic ganglion of Drosophila. Neuron 6, 83–99
    OpenUrlCrossRefPubMedWeb of Science
    1. Selleck S. B.,
    2. Gonzalez C.,
    3. Glover D. M.,
    4. White K.
    (1992) Regulation of the G1-S transition in post-embryonic neuronal precursors by axon ingrowth. Nature 355, 253–255
    OpenUrlCrossRefPubMed
    1. Spivak-Kroizman T.,
    2. Lemmon M. A.,
    3. Dikic I.,
    4. Ladbury J. E.,
    5. Pinchasi D.,
    6. Huang J.,
    7. Jaye M.,
    8. Crumley G.,
    9. Schlessinger J.,
    10. Lax I.
    (1994) Heparin-Induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79, 1015–1024
    OpenUrlCrossRefPubMedWeb of Science
    1. Stipp C. S.,
    2. Litwack E. D.,
    3. Lander A. D.
    (1994) Cerebroglycan: An integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system and expressed specifically during neuronal differentiation. J. Cell Biol 124, 149–160
    OpenUrlAbstract/FREE Full Text
    1. Tamkun J. W.,
    2. Deuring R.,
    3. Scott M. P.,
    4. Kaufman T. C.,
    5. Kennison J. A.
    (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561–572
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas B. J.,
    2. Gunning D. A.,
    3. Cho J.,
    4. Zipursky S. L.
    (1994) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1. Cell 77, 1003–1014
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas U.,
    2. Speicher S. A.,
    3. Knust E.
    (1991) The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs. Development 111, 749–761
    OpenUrlAbstract
    1. Tomlinson A.
    (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J. Embryol. Exp. Morph 89, 313–331
    OpenUrlPubMedWeb of Science
    1. Tomlinson A.
    (1988) Cellular interactions in the developing Drosophila eye. Development 104, 183–193
    OpenUrlPubMedWeb of Science
    1. Trayhurn P.,
    2. Duncan J. S.,
    3. Thomas M. E. A.,
    4. Nestor A.,
    5. Rayner D. V.
    (1994) Chemiluminescent detection of mRNAs on Northern blots with DIG-labeled oligonucleotides. Biochemica 11, 25–27
    1. Truman J. W.,
    2. Bate M.
    (1988) Spatial and temporal patterns ofneurogenesis in the central nervous system of Drosophilamelanogaster. Dev. Biol 125, 145–157
    OpenUrlCrossRefPubMedWeb of Science
    1. van Leeuwen F.,
    2. Samos C. H.,
    3. Nusse R.
    (1994) Biological activity of soluble wingless protein in cultured Drosophila imaginal disc cells. Nature 368, 342–344
    OpenUrlCrossRefPubMedWeb of Science
    1. White K.,
    2. Kankel D. R.
    (1978) Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster. Dev. Biol 65, 296–321
    OpenUrlCrossRefPubMedWeb of Science
    1. Whitfield W. G. F.,
    2. Gonzalez C.,
    3. Maldonado-Codina G.,
    4. Glover D. M.
    (1990) The A-and B-type cyclins of Drosophila are accumulated and destroyed in temporally distinct events that define separable phases of the G2-M transition. EMBO J 9, 2563–2572
    OpenUrlPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
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
H. Nakato, T.A. Futch, S.B. Selleck
Development 1995 121: 3687-3702;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.