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The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors

Nature Cell Biology volume 11, pages 815–824 (2009)Cite this article

Abstract

Cell fate decisions mediated by the Notch signalling pathway require direct cell–cell contact between adjacent cells. In Drosophila melanogaster, an external sensory organ (ESO) develops from a single sensory organ precursor (SOP) and its fate specification is governed by differential Notch activation. Here we show that mutations in actin-related protein-3 (Arp3) compromise Notch signalling, leading to a fate transformation of the ESO. Our data reveal that during ESO fate specification, most endocytosed vesicles containing the ligand Delta traffic to a prominent apical actin-rich structure (ARS) formed in the SOP daughter cells. Using immunohistochemistry and transmission electron microscopy (TEM) analyses, we show that the ARS contains numerous microvilli on the apical surface of SOP progeny. In Arp2/3 and WASp mutants, the surface area of the ARS is substantially reduced and there are significantly fewer microvilli. More importantly, trafficking of Delta-positive vesicles from the basal area to the apical portion of the ARS is severely compromised. Our data indicate that WASp-dependent Arp2/3 actin polymerization is crucial for apical presentation of Delta, providing a mechanistic link between actin polymerization and Notch signalling.

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Figure 1: Arp3 mutations cause a pIIa-to-pIIb transformation in the ESO lineage
Figure 2: Arp3 is required in the signal sending cells during Notch signalling
Figure 3: Delta is normally endocytosed in Arp3 and Arpc1 mutant pIIa-pIIb.
Figure 4: The ARS forms specifically in the pIIa-pIIb progeny and is reduced in Arp3, Arpc1 and WASp mutant SOP progeny.
Figure 5: TEM analysis reveals enrichment of actin-filled finger-like projections in pIIa-pIIb cells at 18 h APF.
Figure 6: Finger-like projections in pIIa-pIIb cells are enriched with F-actin bundles and are marked by a microvillar marker Myo1B.
Figure 7: Delta localization to the ARS is reduced in Arpc1 mutants.
Figure 8: Arp2/3 and WASp are required for trafficking of endocytosed Delta to the apical ARS 1 h post-endocytosis.

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Acknowledgements

We are grateful to W. Theurkauf, L. Cooley, E. Schejter, J. Skeath, D. F. Ready, P. Badenhorst, Y. N. Jan, P. Bryant, M. González Gaitán, G. Struhl, E. C. Lai, M. Muskavitch, A. L. Parks, F. B. Gertler, L. M. Lanier, J. Knoblich, F. Schweisguth, R. Dubreuil, W. Sullivan, M. S. Mooseker, G.M. Guild, the Bloomington Stock Center and the Developmental Studies Hybridoma Bank for reagents. We thank G. Emery for advice regarding the Delta endocytosis assay. We would like to thank H. Jafar-Nejad for suggestions and advice during the screen and comments on the manuscript. We thank P. Verstreken and C. V. Ly for their help with the screen, and R. Atkinson for advice on imaging. Confocal microscopy was supported by the BCM Mental Retardation and Developmental Disabilities Research Center. H.J.B. is an investigator of the Howard Hughes Medical Institute.

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  1. Akhila Rajan

    Present address: Current address: Department of Genetics, Harvard Medical School, Boston, MA 021155, USA.,

  2. An-Chi Tien

    Present address: Current address: University of California, San Francisco, CA 94143, USA.,

  3. Akhila Rajan and An-Chi Tien: These authors contributed equally to the work.

Authors and Affiliations

  1. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, 77030, TX, USA

    Akhila Rajan & Hugo J. Bellen

  2. Program in Developmental Biology, Baylor College of Medicine, Houston, 77030, TX, USA

    An-Chi Tien & Hugo J. Bellen

  3. Howard Hughes Medical Institute, Baylor College of Medicine, Houston, 77030, TX, USA

    Claire M. Haueter, Karen L. Schulze & Hugo J. Bellen

  4. Department of Neuroscience, Baylor College of Medicine, Houston, 77030, TX, USA

    Hugo J. Bellen

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Contributions

A.R., A.T. and H.B. conceived the project. A.R. and A.T. carried out the screen, mapped the genes and executed the project. K.S. was involved in the screen and mapping of the genes. C.M.H. in collaboration with A.R. and A.T. designed the TEM experiments and C.M.H. carried out the TEM experiments.

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Correspondence to Hugo J. Bellen.

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Rajan, A., Tien, AC., Haueter, C. et al. The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors. Nat Cell Biol 11, 815–824 (2009). https://doi.org/10.1038/ncb1888

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