Skip to main content
SpringerLink
Log in

Early Neurogenesis in Drosophila

  • Chapter
Development

  • 666 Accesses

Abstract

One of the main questions in developmental biology concerns the origin of cell diversity: how do developing cells differentiate the many types that make up any multicellular organism? This is a difficult problem which has been approached with more or less success in a variety of developmental processes and organisms. A case in point is the development of the neural progenitor cells in the fruitfly Drosophila melanogaster. In insects, the cells of the central nervous system (CNS) and of the sensory organs are generated by the proliferation of special progenitors, the neuroblasts and the sensory organ progenitor cells (SOPs). Whereas the former develop from the neuroectoderm of the embryo, the latter originate within the epidermis during later stages of development. However, both cell types have in common that they arise within groups of equivalent cells called proneural clusters. The cells of these clusters have to decide between taking on a neural fate developing as neuroblasts or as SOPs or taking on an epidermal fate and developing as progenitor cells of the epidermis. Commitment and specification of central and peripheral neural progenitors follow similar principles and obey similar rules. Thanks to the combination of embryological, classical genetic, and molecular approaches, our understanding of how the neural progenitors of Drosophila develop has progressed considerably during the past 20 years.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. 2nd edn. Springer, Berlin Heidelberg New York

    Google Scholar 

  2. Broadus J, Skeath JB, Spana EP, Bossing T, Technau GM, Doe CQ (1993) New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech Dev 53:393–402

    Article  Google Scholar 

  3. Hartenstein V, Rudloff E, Campos-Ortega JA (1987) The pattern of proliferation of the neuroblasts in the wildtype embryo of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 196:473–485

    Article  Google Scholar 

  4. Prokop A, Technau GM (1991) The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111:79–88

    PubMed  CAS  Google Scholar 

  5. Truman JW, Bate CM (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125:145–157

    Article  PubMed  CAS  Google Scholar 

  6. Bossing T, Technau GM (1994) The fate of the CNS midline progenitors of Drosophila as revealed by a new method for single cell labelling. Development 120: 1895–1906

    PubMed  CAS  Google Scholar 

  7. Bossing T, Technau GM, Doe CQ (1996) huckebein is required for glial development and axon finding in the NB1-1 and NB2-2 lineages in the Drosophila CNS. Mech Dev 55:53–64

    Article  PubMed  CAS  Google Scholar 

  8. Bossing T, Udolph G, Doe CQ, Technau GM (1996) The embryonic CNS lineages of Drosophila melanogaster. I The lineages derived from the ventral half of the truncal neuroectoderm. Dev Biol 179:41–64

    Article  PubMed  CAS  Google Scholar 

  9. Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila nervous system. Development 116:855–863

    PubMed  CAS  Google Scholar 

  10. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM (1997) The embryonic CNS lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol 189:186–204

    Article  PubMed  CAS  Google Scholar 

  11. Brand M, Campos-Ortega JA (1988) Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 197:457–470

    Article  Google Scholar 

  12. Brand M, Campos-Ortega JA (1990) Second site modifiers of the split mutation of Notch define genes involved in neurogenesis in Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 198:275–285

    Article  Google Scholar 

  13. Brand M, Jarman AP, Jan LY, Jan YN (1993) asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119:1–17

    PubMed  CAS  Google Scholar 

  14. Caudy M, Grell EH, Dambly-Chaudiere C, Ghysen A, Jan LY, Jan YN (1988) The maternal sex determination gene daughterless has zygotic activity necessary for the formation of peripheral neurons in Drosophila. Genes Dev 2:843–852

    Article  PubMed  CAS  Google Scholar 

  15. Dambly-Chaudière C, Ghysen A (1987) Independent subpatterns of sense organs require independent genes of the achaete-scute complex in Drosophila larvae. Genes Dev 1:297–306

    Article  Google Scholar 

  16. de la Concha A, Dietrich U, Weigel D, Campos-Ortega JA (1988) Functional interactions of neurogenic genes of Drosophila melanogaster. Genetics 118:499–508

    Google Scholar 

  17. Dommguez M, Campuzano S (1993) asense, a member of the Drosophila achaete-scute complex, is a proneural and a neural differentiation gene. EMBOJ 12:2049–2060

    Google Scholar 

  18. Hartenstein V, Campos-Ortega JA (1986) The peripheral nervous system of mutants of early neurogenesis in Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 195:210–221

    Article  Google Scholar 

  19. Jimènez F, Campos-Ortega JA (1979) A region of the Drosophila genome necessary for CNS development. Nature 282:310–312

    Article  PubMed  Google Scholar 

  20. Jimènez F, Campos-Ortega JA (1987) Genes in subdivision IB of the Drosophila melanogaster X-chromosome and their influence on neural development. J Neurogenet 4:179–200

    PubMed  Google Scholar 

  21. Lehmann R, Dietrich U, Jimenez F, Campos-Ortega JA (1981) Mutations of early neurogenesis in Drosophila. Wilhelm. Roux Arch Dev Biol 190:226–229

    Article  Google Scholar 

  22. Lehmann R, Jimenez F, Dietrich U, Campos-Ortega JA (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 192:62–74

    Article  Google Scholar 

  23. Poulson DF (1937) Chromosomal deficiencies and embryonic development of Drosophila melanogaster. Proc Natl Acad Sci USA 23:133–137

    Article  PubMed  CAS  Google Scholar 

  24. White K (1980) Defective neural development in Drosophila melanogaster embryos deficient for the tip of the X-chromosome. Dev Biol 80:322–344

    Article  Google Scholar 

  25. Cabrera CV, Martinez-Arias A, Bate M (1987) The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50:425–433

    Article  PubMed  CAS  Google Scholar 

  26. Campuzano S, Modolell J (1992) Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet 8:202–207

    PubMed  CAS  Google Scholar 

  27. Cubas P, de Celis J-F, Campuzano S, Modolell J (1991) Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5:996–1008

    Article  PubMed  CAS  Google Scholar 

  28. Garcfa-Bellido A (1979) Genetic analysis of the achaetescute system of Drosophila melanogaster. Genetics 91: 491–520

    Google Scholar 

  29. Garcia-Bellido A, Santamaria P (1978) Developmental analysis of the achaete-scute system of Drosophila melanogaster. Genetics 88:469–486

    PubMed  CAS  Google Scholar 

  30. Ghysen A, Dambly-Chaudière C (1988) From DNA to form: the achaete-scute complex. Genes Dev 2:495–501

    Article  PubMed  CAS  Google Scholar 

  31. Giebel B, Stüttem I, Hinz U, Campos-Ortega JA (1997) Ectopic lethal of scute requires overexpression of daughterless to elicit neuronal development during embryogenesis in Drosophila. Mech Dev 63:75–87

    Article  PubMed  CAS  Google Scholar 

  32. Hinz U, Giebel B, Campos-Ortega JA (1994) The basichelix-loop-helix domain of the Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76:77–87

    Article  PubMed  CAS  Google Scholar 

  33. Jarman AP, Grau Y, Jan LY, Jan YN (1993) atonal is a proneural gene that directs chrodotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321

    Article  PubMed  CAS  Google Scholar 

  34. Jimènez F, Campos-Ortega JA (1990) Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of Drosophila melanogaster. Neuron 5:81–89

    Article  PubMed  Google Scholar 

  35. Martin-Bermudo MD, Martinez C, Jimènez F (1991) Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development 113:445–454

    PubMed  CAS  Google Scholar 

  36. Rodriguez I, Hernández R, Modolell J, Ruiz-Gómez M (1990) Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. EMBOJ 9:3583–3592

    CAS  Google Scholar 

  37. Skeath JB, Carroll SB (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114: 939–946

    PubMed  CAS  Google Scholar 

  38. Fehon RG, Kooh PJ, Rebay I, Regan CL, Xu T, Muskavitch MAT, Artavanis-Tsakonas S (1990). Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 62:523–533

    Article  Google Scholar 

  39. Haenlin M, Kramatschek B, Campos-Ortega JA (1990) The pattern of transcription of the neurogenic gene Delta of Drosophila melanogaster. Development 110:905–914

    PubMed  CAS  Google Scholar 

  40. Hartley DA, Xu T, Artavanis-Tsakonas S (1987) The embryonic expression of the Notch locus of Drosophila melanogaster and the implications of point mutations in the extracellular EGF-like domain of the predicted protein. EMBOJ 6:3407–3417

    CAS  Google Scholar 

  41. Heitzler P, Simpson P (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64:1083–1092

    Article  PubMed  CAS  Google Scholar 

  42. Johansen KM, Fehon RG, Artavanis-Tsakonas S (1989) The Notch gene product is a glycoprotein expressed on the cell surface of both epidermal and neuronal precursor cells during Drosophila development. J Cell Biol 109:2427–2440

    Article  PubMed  CAS  Google Scholar 

  43. Kelley MR, Kidd S, Deutsch WA, Young MW (1987) Mutations altering the structure of epidermal growth factor-like coding sequences at the Drosophila Notch locus. Cell 51:539–548

    Article  PubMed  CAS  Google Scholar 

  44. Kidd S, Baylies MK, Gasic GP, Young MW (1989) Structure and distribution of the Notch protein in developing Drosophila. Genes Dev 3:1113–1129

    Article  PubMed  CAS  Google Scholar 

  45. Kidd S, Kelley MR, Young MW (1986) Sequence of the Notch locus of Drosophila melanogaster: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol 6:3094–3108

    PubMed  CAS  Google Scholar 

  46. Kooh PJ, Fehon R Muskavitch MAT (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during a Drosophila development. Development 117:493–507

    PubMed  CAS  Google Scholar 

  47. Kopczynski CC, Alton AK, Fechtel K, Kooh PJ, Muskavitch MAT (1988) Deltay a Drosophila neurogenic gene, is transcriptionally complex and encodes a protein related to blood coagulation factors and epidermal growth factor of vertebrates. Genes Dev 2:1723–1735

    Article  PubMed  CAS  Google Scholar 

  48. Lieber T, Alcamo E, Hassel B, Krane JF, Campos-Ortega JA and Young MW (1992) Single amino acid substitutions in EGF-like elements of the Notch and Delta proteins modify Drosophila development and depress cell adhesion in vitro. Neuron 9:847–859

    Article  PubMed  CAS  Google Scholar 

  49. Lieber T, Kidd S, Alcamo E, Corbin V, Young MW (1993) 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 7:1949–1965

    Article  PubMed  CAS  Google Scholar 

  50. Rebay I, Fleming RJ, Fehon RG, Cherbas L, Cherbas P, Artavanis-Tsakonas S (1991) Specific repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 67:687–699

    Article  PubMed  CAS  Google Scholar 

  51. Struhl G, Fitzgerald K, Greenwald I (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74:331–345

    Article  PubMed  CAS  Google Scholar 

  52. Vassin H, Bremer KA, Knust E, Campos-Ortega JA (1987) The neurogenic locus Delta of Drosophila melanogaster is expressed in neurogenic territories and encodes a putative transmembrane protein with EGF-like repeats. EMBOJ 6:3431–3440

    Google Scholar 

  53. Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S (1985) Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43:567–581

    Article  PubMed  CAS  Google Scholar 

  54. Bailey AM, Posakony J (1995) Supressor of Hairless directly activates transcription of Enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9:2609–2622

    Article  PubMed  CAS  Google Scholar 

  55. Fortini M, Artavanis-Tsakonas S (1994) The Suppressor of Hairless protein participates in Notch receptor signaling. Cell 79:273–282

    Article  PubMed  CAS  Google Scholar 

  56. Gho M, Lecourtois M, Geraud G, Posakony JW, Schweissguth F (1996) Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signaling. Development 122:1673–1682

    PubMed  CAS  Google Scholar 

  57. Jarriault S, Brou C, Logeat F, Schroeter EH, Kopan R, Isräel A (1995) Signalling downstream of activated mammalian Notch. Nature 377:355–358

    Article  PubMed  CAS  Google Scholar 

  58. Lecourtois M, Schweissguth F (1995) The neurogenic Suppressor of Hairless DNA-binding protein mediates the transcriptional activation of the Enhancer of split Complex genes triggered by Notch signalling. Genes Dev 9:2598–2608

    Article  PubMed  CAS  Google Scholar 

  59. Lecourtois M, Schweissguth F (1998) Indirect evidence for De/ta-dependent intracellular processing of Notch in Drosophila embryos. Cur Biol 8:771–774

    Article  CAS  Google Scholar 

  60. Schweissguth F, Posakony J (1992) Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein, sontrols sensory organ cell fates. Cell 69:1199–1212

    Article  Google Scholar 

  61. Struhl G, Adachi A (1998) Muclear access and action of Notch in vivo. Cell 93:649–660

    Article  PubMed  CAS  Google Scholar 

  62. Delidakis C, Artavanis-Tsakonas S (1992) The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc Natl Acad Sci USA 89:8731–8735

    Article  PubMed  CAS  Google Scholar 

  63. Klambt C, Knust E, Tietze K, Campos-Ortega JA (1989) Closely related transcripts encoded by the neurogenic gene complex Enhancer of split of Drosophila melanogaster. EMBOJ 8:203–210

    CAS  Google Scholar 

  64. Knust E, Schrons H, Grawe F, Campos-Ortega JA (1992) Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132:505–518

    PubMed  CAS  Google Scholar 

  65. Nakao K, Campos-Ortega JA (1996) Persistent expression of genes of the Enhancer of split-complex suppresses neural development in Drosophila. Neuron 16:275–286

    Article  PubMed  CAS  Google Scholar 

  66. Oellers N, Dehio M, Knust E (1994) Basic-helix-loop-helix proteins of the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation by proneural proteins. Mol Gen Genet 244:465–473

    Article  PubMed  CAS  Google Scholar 

  67. Paroush Z, Finley RL, Kidd T, Wainwright SM, Ingham PW, Brent R, Ish-Horowicz D (1994) Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell 79:805–815

    Article  PubMed  CAS  Google Scholar 

  68. Schrons H, Knust E, Campos-Ortega JA (1992) The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics 132:481–503

    PubMed  CAS  Google Scholar 

  69. Tata F, Hartley DA (1995) Inhibition of cell fate in Drosophila by Enhancer of split genes. Mech Dev 51:305–315

    Article  PubMed  CAS  Google Scholar 

  70. Tietze K, Oellers N, Knust E (1992) Enhancer of split D, a dominant mutation of Drosophila and its use in the study of functional domains of a helix-loop-helix protein. Proc Natl Acad Sci USA 89:6152–6156

    Article  PubMed  CAS  Google Scholar 

  71. Haenlin M, Kunisch M, Kramatschek B, Campos-Ortega JA (1994) Genomic regions regulating transcription of the neurogenic gene Delta during embryogenesis of Drosophila melanogaster. Mech Dev 47:99–110

    Article  PubMed  CAS  Google Scholar 

  72. Heitzler P, Bourouis M, Ruel L, Carteret C, Simpson P (1996) Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development 122:161–171

    PubMed  CAS  Google Scholar 

  73. Kramatschek B, Campos-Ortega JA (1994) Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes. Development 120:815–826

    PubMed  CAS  Google Scholar 

  74. Kunisch M, Haenlin M, Campos-Ortega JA (1994) Lateral inhibition mediated by the Drosophila neurogenic gene Delta is enhanced by proneural genes. Proc Natl Acad Sci USA 91:10139–10143

    Article  PubMed  CAS  Google Scholar 

  75. Seugnet L, Simpson P, Haenlin M (1997) Transcriptional regulation of Notch and Delta: requirement for neuroblast segregation in Drosophila. Development 124: 2015–2025

    PubMed  CAS  Google Scholar 

  76. Singson A, Leviten MW, Bang AG, Hua XH, Posakony JW (1994) Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signalling. Genes Dev 8: 2058–2071

    Article  PubMed  CAS  Google Scholar 

  77. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C (1995) Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375:761–766

    Article  PubMed  CAS  Google Scholar 

  78. Chitnis A, Kintner C (1996) Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus. Development 122:2295–2301

    PubMed  CAS  Google Scholar 

  79. Dornseifer P, Takke C, Campos-Ortega JA (1997) Overexpression of a zebrafish homologue of the Drosophila neurogenic gene Delta perturbs differentiation of primary neurons and somite development. Mech Dev 63:159–171

    Article  PubMed  CAS  Google Scholar 

  80. Cubas P, Modolell J (1992) The extramacrochaetae gene provides information for sensory organ patterning. EMBOJ 11:3385–3393

    CAS  Google Scholar 

  81. van Doren M, Powell PA, Pasternak D, Singson A, Posakony JW (1992) Spatial regulation of proneural gene activity: auto- and cross-activation of achaete is antagonized by extramacrochaetae. Genes Dev 6:2592–2605.

    Article  PubMed  Google Scholar 

Download references

Authors
  1. Jose A. Campos-Ortega
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. MPI für Molekulare Genetik, Ihnestraße 73, D-14195, Berlin, Germany

    Vincenzo E. A. Russo

  2. Leeds Institute of Plant Biochemistry and Agriculture, University of Leeds, Leeds, LS29JT, Great Britain

    David J. Cove

  3. Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, 80302, CO, USA

    Lois G. Edgar

  4. Whitehead Institute, Nine Cambridge Center, Cambridge, 02141, MA, USA

    Rudolf Jaenisch

  5. MPI für Züchtungsforschung, Carl-von-Linné-Weg 10, Köln, D-50829, Germany

    Francesco Salamini

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag Berlin · Heidelberg New York

About this chapter

Cite this chapter

Campos-Ortega, J.A. (1999). Early Neurogenesis in Drosophila . In: Russo, V.E.A., Cove, D.J., Edgar, L.G., Jaenisch, R., Salamini, F. (eds) Development. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59828-9_20

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-59828-9_20

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64141-1

  • Online ISBN: 978-3-642-59828-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation