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A critical role for Cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster

Nature Cell Biology volume 7, pages 56–62 (2005)Cite this article

Abstract

We have examined the process by which cell diversity is generated in neuroblast (NB) lineages in the central nervous system of Drosophila melanogaster. Thoracic NB6-4 (NB6-4t) generates both neurons and glial cells, whereas NB6-4a generates only glial cells in abdominal segments1. This is attributed to an asymmetric first division of NB6-4t, localizing prospero (pros) and glial cell missing (gcm) only to the glial precursor cell, and a symmetric division of NB6-4a, where both daughter cells express pros and gcm2,3,4,5. Here we show that the NB6-4t lineage represents the ground state, which does not require the input of any homeotic gene, whereas the NB6-4a lineage is specified by the homeotic genes abd-A and Abd-B. They specify the NB6-4a lineage by down-regulating levels of the G1 cyclin, DmCycE (CycE). CycE, which is asymmetrically expressed after the first division of NB6-4t, functions upstream of pros and gcm to specify the neuronal sublineage. Loss of CycE function causes homeotic transformation of NB6-4t to NB6-4a, whereas ectopic CycE induces reverse transformations. However, other components of the cell cycle seem to have a minor role in this process, suggesting a critical role for CycE in regulating cell fate in segment-specific neural lineages.

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Figure 1: NB6-4 lineages in thoracic and abdominal segments of wild-type embryos.
Figure 2: Segment-specificity of the NB6-4 lineage is determined by the homeotic genes abdA and AbdB.
Figure 3: NB6-4 lineages show homeotic transformations in the backgrounds of loss- and gain-of-CycE-function.
Figure 4: Loss- and gain-of-function phenotypes of dacapo, E2F, Rbf, cdc2 and CycA in NB6-4 lineages.
Figure 5: CycE is differentially expressed between NB6-4t and NB6-4a lineages.

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Acknowledgements

We thank J. Urban, C. Lehner and A. Rogulja-Ortmann for comments; G. Vogler and O. Vef for advice on methods; and C. Lehner, I. Duncan, M. Freeman, C.Q. Doe, A. Michelson, E. Sanchez-Herrero, the Developmental Studies Hybridoma Bank (DSHB) and the Bloomington stock center for fly strains, antibodies and cDNA clones. We thank members of both of our laboratories for technical help and advice. This work was supported by the Deutsche Forschungs-gemeinschaft (grant to G.M.T.) and the Volkswagen-Stiftung (grant to L.S.S. and G.M.T.)

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Authors and Affiliations

  1. Institute for Genetics, University of Mainz, Mainz, D-55099, Germany

    Christian Berger & Gerhard M. Technau

  2. Center for Cellular and Molecular Biology, Uppal Road, Hyderabad, 500 007, India

    S. K. Pallavi, Mohit Prasad & L. S. Shashidhara

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  1. Christian Berger
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Correspondence to L. S. Shashidhara or Gerhard M. Technau.

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Berger, C., Pallavi, S., Prasad, M. et al. A critical role for Cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat Cell Biol 7, 56–62 (2005). https://doi.org/10.1038/ncb1203

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