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An unconventional myosin in Drosophila reverses the default handedness in visceral organs

Nature volume 440, pages 798–802 (2006)Cite this article

Abstract

The internal organs of animals often have left–right asymmetry1,2. Although the formation of the anterior–posterior and dorsal–ventral axes in Drosophila is well understood, left–right asymmetry has not been extensively studied. Here we find that the handedness of the embryonic gut and the adult gut and testes is reversed (not randomized) in viable and fertile homozygous Myo31DF mutants. Myo31DF encodes an unconventional myosin, Drosophila MyoIA (also referred to as MyoID in mammals; refs 3, 4), and is the first actin-based motor protein to be implicated in left–right patterning. We find that Myo31DF is required in the hindgut epithelium for normal embryonic handedness. Disruption of actin filaments in the hindgut epithelium randomizes the handedness of the embryonic gut, suggesting that Myo31DF function requires the actin cytoskeleton. Consistent with this, we find that Myo31DF colocalizes with the cytoskeleton. Overexpression of Myo61F, another myosin I (ref. 4), reverses the handedness of the embryonic gut, and its knockdown also causes a left–right patterning defect. These two unconventional myosin I proteins may have antagonistic functions in left–right patterning. We suggest that the actin cytoskeleton and myosin I proteins may be crucial for generating left–right asymmetry in invertebrates.

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Figure 1: Myo31DF mutation inverses the handedness of embryonic and adult visceral organs.
Figure 2: Embryonic expression of Myo31DF and the subcellular localization of Myo31DF.
Figure 3: Myo31DF is dependent on the actin cytoskeleton to develop left–right asymmetry.

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Acknowledgements

We thank the Developmental Studies Hybridoma Bank at the University of Iowa, the Bloomington Stock Center, and the Drosophila Genetic Resource Center at the Kyoto Institute of Technology. We thank J. Lengyel for byn–Gal4 and S. Hayashi for UAS-gfp–moesin transgenic strains. This work was supported by grants-in-aid from the Japanese Ministry of Education, Culture, Sports and Science. Author Contributions Experimental work was performed by S.H., R.M., K.T., M.K., S.S., T.S., P.S. and T.A. Data analysis was by S.H., R.M., K.T. and K.M., and project planning was coordinated by S.N., R.M. and K.M.

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Authors and Affiliations

  1. Department of Biological Science and Technology,

    Shunya Hozumi, Reo Maeda, Kiichiro Taniguchi, Maiko Kanai, Syuichi Shirakabe, Takeshi Sasamura & Kenji Matsuno

  2. Genome and Drug Research Center, Tokyo University of Science, 2641 Yamazaki, 278-8510, Chiba, Noda, Japan

    Kenji Matsuno

  3. Institute of Signalling, Developmental Biology & Cancer, UMR6543-CNRS, University of Nice Sophia-Antipolis, Parc Valrose, 06108, Nice, France, Cedex 2

    Pauline Spéder & Stéphane Noselli

  4. Cancer, UMR6543-CNRS, University of Nice Sophia-Antipolis, Parc Valrose, 06108

    Pauline Spéder & Stéphane Noselli

  5. Department of Biological Science, Tokyo Metropolitan University, 1-1 Minami-osawa, Hachioji, 192-0397, Tokyo, Japan

    Toshiro Aigaki

  6. Department of Physics, Biology, and Informatics, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8512, Yamaguchi, Japan

    Ryutaro Murakami

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Correspondence to Kenji Matsuno.

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Supplementary information

Supplementary Tables

This file contains Supplementary Tables 1 and 2. Supplementary Table 1 summarizes the results of this paper as the percentage of individual animals with handedness defects in each mutant or expression line. Supplementary Table 2 shows the phenocritical periods for inducing the LR defect by Myo31DF knockdown and by GFP–Moe misexpression. (PDF 136 kb)

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Hozumi, S., Maeda, R., Taniguchi, K. et al. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 440, 798–802 (2006). https://doi.org/10.1038/nature04625

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