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Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt

Nature Cell Biology volume 11, pages 569579 (2009) | Download Citation

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Abstract

During development, elaborate patterns of cell differentiation and movement must occur in the correct locations and at the proper times. Developmental timing has been studied less than spatial pattern formation, and the mechanisms integrating the two are poorly understood. Border-cell migration in the Drosophila ovary occurs specifically at stage 9. Timing of the migration is regulated by the steroid hormone ecdysone, whereas spatial patterning of the migratory population requires localized activity of the JAK–STAT pathway. Ecdysone signalling is patterned spatially as well as temporally, although the mechanisms are not well understood. In stage 9 egg chambers, ecdysone signalling is highest in anterior follicle cells including the border cells. We identify the gene abrupt as a repressor of ecdysone signalling and border-cell migration. Abrupt protein is normally lost from border-cell nuclei during stage 9, in response to JAK–STAT activity. This contributes to the spatial pattern of the ecdysone response. Abrupt attenuates ecdysone signalling by means of a direct interaction with the basic helix–loop–helix (bHLH) domain of the P160 ecdysone receptor coactivator Taiman (Tai). Taken together, these findings provide a molecular mechanism by which spatial and temporal cues are integrated.

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Acknowledgements

This work was supported by NIH grants R01 GM46425 and R01 GM73164 to D.J.M.

Author information

Author notes

    • Anna C.-C. Jang
    •  & Yu-Chiuan Chang

    These authors contributed equally to this work.

Affiliations

  1. Department of Biological Chemistry, Johns Hopkins School of Medicine, 725 North Wolfe Street, Baltimore, Maryland 21205-2185, USA.

    • Anna C.-C. Jang
    • , Yu-Chiuan Chang
    •  & Denise Montell
  2. Department of Genetics, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, Massachusetts 02175, USA.

    • Jianwu Bai

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Contributions

In Figs 3 and 8, A.J. and Y.C. contributed equally. A.J. also contributed Figs 1, 2, 4, 5, 6, 7 and Supplementary Information, Figs S1, S3, S4, S5 and S6. The EP screen was performed by Y.C., who also conducted the mutant analysis of Abrupt for Supplementary Information, Fig. S2. The nls-Tai(LXXLL–GFP) transgenic flies were constructed by J.B.. D.M. conceived of the project, participated in experimental design, discussions of results and interpretations, and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Denise Montell.

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DOI

https://doi.org/10.1038/ncb1863

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