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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 569–579 (2009)Cite this article

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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Figure 1: Spatial patterns of ecdysone signalling in stage 8–9 egg chambers.
Figure 2: Normal and ectopic expression of ecdysone receptor isoforms.
Figure 3: Abrupt represses ecdysone signalling in Drosophila egg chambers.
Figure 4: Tai and Abrupt proteins interact.
Figure 5: Effects of Tai constructs on ecdysone-dependent transcription in vivo.
Figure 6: Rescue of tai mutant border cells by full length and truncated Tai proteins.
Figure 7: Precocious border-cell migration induced by co-expression of Tai(ΔB) and activated JAK.
Figure 8: Relationship between JAK–STAT, EcR and Abrupt.

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Acknowledgements

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

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  1. Anna C.-C. Jang and Yu-Chiuan Chang: These authors contributed equally to this work.

Authors and Affiliations

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

    Anna C.-C. Jang, Yu-Chiuan Chang & Denise Montell

  2. Department of Genetics, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, 02175, Massachusetts, 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.

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Correspondence to Denise Montell.

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Jang, AC., Chang, YC., Bai, J. et al. Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt. Nat Cell Biol 11, 569–579 (2009). https://doi.org/10.1038/ncb1863

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