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Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino

Nature Cell Biology volume 8, pages 367–376 (2006)Cite this article

Abstract

The actin-nucleation factors Spire and Cappuccino (Capu) regulate the onset of ooplasmic streaming in Drosophila melanogaster1,2,3,4,5. Although this streaming event is microtubule-based, actin assembly is required for its timing. It is not understood how the interaction of microtubules and microfilaments is mediated in this context. Here, we demonstrate that Capu and Spire have microtubule and microfilament crosslinking activity. The spire locus encodes several distinct protein isoforms (SpireA, SpireC and SpireD). SpireD was recently shown to nucleate actin, but the activity of the other isoforms has not been addressed. We find that SpireD does not have crosslinking activity, whereas SpireC is a potent crosslinker. We show that SpireD binds to Capu and inhibits F-actin/microtubule crosslinking, and activated Rho1 abolishes this inhibition, establishing a mechanistic basis for the regulation of Capu and Spire activity. We propose that Rho1, cappuccino and spire are elements of a conserved developmental cassette that is capable of directly mediating crosstalk between microtubules and microfilaments.

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Figure 1: Rho1-capu, reduced Rho1, and capu-spire oocytes undergo premature ooplasmic streaming.
Figure 2: Rho1, Capu and Spire expression is enriched at the oocyte cortex, where stable microtubules are also localized.
Figure 3: Protein–protein interactions between Rho1, Capu and Spire indicate a complex regulatory network.
Figure 4: Capu and Spire affect actin dynamics.
Figure 5: Rho1 regulates crosslinking of F-actin and microtubules by Capu and Spire.

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Acknowledgements

We thank J. Infante, J. Nance, S. Parks, T. Phippen, J. Priess, P. Soriano and V. Vasioukhin for their advice and interest during the course of this work and for comments on the manuscript. We also thank C. Berg, L. Cooley, A. Ephrussi, B. Kaiser, A. Koleske, P. Lasko, M. Maurer, L. Manseau, H. Oda, J. Roe, S. Roth, T. Schüpbach, L. Serbus, D. St. Johnston, R. Strong, W. Theurkauf, T. Tsukiyama, J. Vazquez, V. Vigdorovich, A. Wittinghofer and the Bloomington Stock Center for advice, equipment, protocols, antibodies, DNAs, flies and other reagents used in this study. This work was supported by a National Institutes of Health grant (GM066847, to S.M.P.).

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  1. Alicia E. Rosales-Nieves, James E. Johndrow and Lani C. Keller: These authors contributed equally to this work.

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  1. Division of Basic Sciences, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, 98109-1024, WA, USA

    Alicia E. Rosales-Nieves, James E. Johndrow, Lani C. Keller, Craig R. Magie, Delia M. Pinto-Santini & Susan M. Parkhurst

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  1. Alicia E. Rosales-Nieves
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Correspondence to Susan M. Parkhurst.

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Rosales-Nieves, A., Johndrow, J., Keller, L. et al. Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat Cell Biol 8, 367–376 (2006). https://doi.org/10.1038/ncb1385

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