Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster
M.L. Winberg, S.E. Perez, H. Steller
Development 1992 115: 903-911;
M.L. Winberg
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
S.E. Perez
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
H. Steller
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

We have examined the generation and development of glial cells in the first optic ganglion, the lamina, of Drosophila melanogaster. Previous work has shown that the growth of retinal axons into the developing optic lobes induces the terminal cell divisions that generate the lamina monopolar neurons. We investigated whether photoreceptor ingrowth also influences the development of lamina glial cells, using P element enhancer trap lines, genetic mosaics and birthdating analysis. Enhancer trap lines that mark the differentiating lamina glial cells were found to require retinal innervation for expression. In mutants with only a few photoreceptors, only the few glial cells near ingrowing axons expressed the marker. Genetic mosaic analysis indicates that the lamina neurons and glial cells are readily separable, suggesting that these are derived from distinct lineages. Additionally, BrdU pulse-chase experiments showed that the cell divisions that produce lamina glia, unlike those producing lamina neurons, are not spatially or temporally correlated with the retinal axon ingrowth. Finally, in mutants lacking photoreceptors, cell divisions in the glial lineage appeared normal. We conclude that the lamina glial cells derive from a lineage that is distinct from that of the L-neurons, that glia are generated independently of photoreceptor input, and that completion of the terminal glial differentiation program depends, directly or indirectly, on an inductive signal from photoreceptor axons.

REFERENCES

    1. Banerjee U.,
    2. Zipursky S. L.
    (1990) The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4, 177–187
    OpenUrlCrossRefPubMedWeb of Science
    1. Campos A. R.,
    2. Fischbach K.-F.,
    3. Steller H.
    (1992) Survival of photoreceptor neurons in the compound eye of Drosophila depends on connections within the optic ganglia. Development 114, 355–366
    OpenUrlAbstract
    1. Carr V. M.,
    2. Simpson S. B., Jr
    (1978) Proliferative and degenerative events in the early development of chick dorsal root ganglion cells. J. Comp. Neurol 182, 727–740
    OpenUrlCrossRefPubMedWeb of Science
    1. Cline T. W.
    (1978) Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90, 683–698
    OpenUrlAbstract/FREE Full Text
    1. Frank E.,
    2. Sanes J. R.
    (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111, 895–908
    OpenUrlAbstract/FREE Full Text
    1. Gratzner H. G.
    (1982) Monoclonal antibody to 5-bromo and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218, 474–475
    OpenUrlAbstract/FREE Full Text
    1. Hafen E.,
    2. Basler K.
    (1991) Specification of cell fate in the developing eye of Drosophila. Development Supp 1, 123–130
    OpenUrlPubMed
    1. Hall A. K.,
    2. Landis S. C.
    (1991) Early commitment of precursor cells from the rat superior cervical ganglion to neuronal or non-neuronal fates. Neuron 6, 741–752
    OpenUrlCrossRefPubMed
    1. Jacobs R. J.,
    2. Hiromi Y.,
    3. Patel N. H.,
    4. Goodman C. S.
    (1989) Lineage, migration, and morphogenesis of longitudinal glia in theM. Winberg, S.E.Perez and H. Steller911Lamina glia in Drosophila Drosophila CNS as revealed by a molecular lineage marker. Neuron 2, 1625–1631
    OpenUrlCrossRefPubMedWeb of Science
    1. Jan L. Y.,
    2. Jan Y. N.
    (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc. Natl. Acad. Sci. USA 79, 2700–2704
    OpenUrlAbstract/FREE Full Text
    1. Laski F. A.,
    2. Rio D. C.,
    3. Rubin G. M.
    (1986) Tissue-specificity of Drosophila P element transposition is regulated at the level of messenger-RNA splicing. Cell 44, 7–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Moses K.,
    2. Rubin G. M.
    (1991) glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5, 583–593
    OpenUrlAbstract/FREE Full Text
    1. Oland L. A.,
    2. Orr G.,
    3. Tolbert L. P.
    (1990) Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain. J. Neurosci 10, 2096–2112
    OpenUrlAbstract
    1. Oland L. A.,
    2. Tolbert L. P.
    (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2, 10–24
    OpenUrlCrossRefPubMedWeb of Science
    1. Power M. E.
    (1943) The effect of reduction in numbers of ommatidia upon the brain of Drosophila melanogaster. J. Exp. Zool 94, 33–71
    OpenUrlCrossRef
    1. Raff M. C.
    (1989) Glial cell diversification in the optic nerve. Science 243, 1450–1455
    OpenUrlAbstract/FREE Full Text
    1. Ready D. F.
    (1989) A multifaceted approach to neural development. Trends Neurosci 12, 102–110
    OpenUrlCrossRefPubMedWeb of Science
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Denz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P-element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    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. Rubin G. M.
    (1989) Development of the Drosophila retina: inductive events studied at single cell resolution. Cell 57, 519–520
    OpenUrlCrossRefPubMed
    1. Saint Marie R. L.,
    2. Carlson S. D.
    (1983) The fine structure of neuroglia in the lamina ganglionaris of the housefly, Musca domestica L. J. Neurocytology 12, 213–241
    OpenUrlCrossRefPubMedWeb of Science
    1. Saint Marie R. L.,
    2. Carlson S. D.
    (1983) Glial membrane specializations and the compartmentalization of the lamina ganglionaris of the housefly compound eye. J. Neurocytology 12, 243–275
    OpenUrlCrossRefPubMedWeb of Science
    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. Shaw S. R.,
    2. Meinertzhagen I. A.
    (1986) Evolutionary progression at synaptic connections made by identified homologous neurones. Proc. Natl. Acad. Sci. USA 83, 7961–7965
    OpenUrlAbstract/FREE Full Text
    1. Simon J. A.,
    2. Sutton C. A.,
    3. Lobell R. B.,
    4. Glaser R. B.,
    5. Lis J. T.
    (1985) Determinants of heat shock-induced chromosome puffing. Cell 40, 805–817
    OpenUrlCrossRefPubMedWeb of Science
    1. Stark W. S.,
    2. Carlson S. D.
    (1986) Ultrastructure of capitate projections in the optic neuropil of Diptera. Cell Tissue Res 246, 481–486
    OpenUrlCrossRefPubMedWeb of Science
    1. Steindler D. A.,
    2. O'Brien T. F.,
    3. Laywell E.,
    4. Harrington K.,
    5. Faissner A.,
    6. Schachner M.
    (1990) Boundaries during normal and abnormal brain development: in vivo and in vitro studies of glia and glycoconjugates. Exp. Neurol 109, 35–56
    OpenUrlCrossRefPubMedWeb of Science
    1. Sved J.
    (1986) eyes absent. Dros. Inf. Serv 63, 169–.
    OpenUrl
    1. Tolbert L. P.,
    2. Oland L. A.
    (1989) A role for glia in the development of organized neuropilar structures. Trends Neurosci 12, 70–75
    OpenUrlCrossRefPubMed
    1. Tolbert L. P.,
    2. Oland L. A.
    (1990) Glial cells form boundaries for developing insect olfactory glomeruli. Exp. Neurol 109, 19–28
    OpenUrlCrossRefPubMedWeb of Science
    1. Tomlinson A.
    (1988) Cellular interactions in the developing Drosophila eye. Development 104, 183–193
    OpenUrlPubMedWeb of Science
    1. Trujillo-Cenoz O.
    (1965) Some aspects of the structural organization of the intermediate retina of Dipterans. J. Ultrastruct. Res 13, 1–33
    OpenUrlPubMedWeb of Science
    1. Trujillo-Cenoz O.,
    2. Melamed J.
    (1973) The development of the retina-lamina complex in Muscoid flies. J. Ultrastruct Res 42, 554–581
    OpenUrlCrossRefPubMed
    1. Turner D. L.,
    2. Snyder E. Y.,
    3. Cepko C. L.
    (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833–845
    OpenUrlCrossRefPubMedWeb of Science
    1. Zipursky S. L.,
    2. Venkatesh T. R.,
    3. Teplow D. B.,
    4. Benzer S.
    (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36, 15–26
    OpenUrlCrossRefPubMedWeb of Science
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster
M.L. Winberg, S.E. Perez, H. Steller
Development 1992 115: 903-911;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster
M.L. Winberg, S.E. Perez, H. Steller
Development 1992 115: 903-911;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome
  • Germline and developmental roles of the nuclear transport factor importin (α)3 in C. elegans
  • Monofocal origin of telencephalic oligodendrocytes in the anterior entopeduncular area of the chick embryo
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.


Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.


Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.


Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

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

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.


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. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992