Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila (original) (raw)
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- Published: 14 May 1998
Nature volume 393, pages 178–181 (1998)Cite this article
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Abstract
During metazoan development, cell-fate diversity is brought about, in part, by asymmetric cell divisions1. In Drosophila, bristle mechanosensory organs are composed of four different cells that originate from a single precursor cell, pI, after two rounds of asymmetric division2. At each division, distinct fates are conferred on sister cells by the asymmetric segregation of Numb, a negative regulator of Notch signalling3,4,5,6. Here we show that the orientation of the mitotic spindles and the localization of the Numb crescent follow a stereotyped pattern. Mitosis of pI is orientated parallel to the anteroposterior axis of the fly. We show that signalling mediated by the Frizzled receptor polarizes pI along this axis, thereby specifying the orientation of the mitotic spindle and positioning the Numb crescent. The mitoses of the two cells produced by mitosis of pI are orientated parallel and orthogonal, respectively, to the division axis of pI. This difference in cell-division orientation is largely independent of the identity of the secondary precursor cells, and is regulated by Frizzled-independent mechanisms.
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References
- Horvitz, H. & Herskowitz, I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68, 237–255 (1992).
Article CAS Google Scholar - Hartenstein, V. & Posakony, J. W. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 398–405 (1989).
Google Scholar - Rhyu, M. S., Jan, L. Y. & Jan, Y. N. Asymmetric distribution of Numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477–491 (1994).
Article CAS Google Scholar - Knoblich, J. A., Jan, L. Y. & Jan, Y. N. Asymmetric segregation of Numb and Prospero during cell division. Nature 377, 624–627 (1995).
Article ADS CAS Google Scholar - Frise, E., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y. & Jan, Y. N. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl Acad. Sci. USA 93, 11925–11932 (1996).
Article ADS CAS Google Scholar - Guo, M., Jan, L. Y. & Jan, Y. N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17, 27–41 (1996).
Article Google Scholar - Gho, M., Lecourtois, M., Géraud, G., Posakony, J. W. & Schweisguth, F. Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signalling. Development 122, 1673–1682 (1996).
CAS PubMed Google Scholar - Wang, S., Younger-Shepherd, S., Jan, L. Y. & Jan, Y. N. Only a subset of binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless. Development 124, 4435–4446 (1997).
CAS PubMed Google Scholar - Lawrence, P. A. Gradients in the insect segment: the orientation of hairs in the milkweed bug Oncopeltus fasciatus. J. Exp. Biol. 44, 607–620 (1996).
Google Scholar - Bate, C. M. in Handbook of Sensory Physiology (ed. Jakobson, M.) 1–52 (Springer, Berlin, 1978).
Google Scholar - Lieber, T., Kidd, S., Alcano, E., Corbin, V. & Young, M. W. Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev. 7, 1949–1965 (1993).
Article CAS Google Scholar - Adler, P. N. The genetic control of tissue polarity in Drosophila. Bioessays 14, 735–741 (1992).
Article CAS Google Scholar - Park, W.-J., Lin, J. & Adler, P. N. The frizzled gene of Drosophila encodes a membrane protein with an odd number of transmembrane domains. Mech. Dev. 45, 127–137 (1994).
Article CAS Google Scholar - Krasnow, R. E., Wong, L. L. & Adler, P. N. dishevelled is a component of the frizzled signaling pathway in Drosophila. Development 121, 4095–4102 (1996).
Google Scholar - Jones, K. H., Lin, J. & Adler, P. N. Molecular analysis of EMS-induced frizzled mutations in Drosophila melanogaster. Genetics 142, 205–215 (1996).
CAS PubMed PubMed Central Google Scholar - Gonczy, P. & Hyman, A. Cortical domains and the mechanisms of asymmetric cell division. Trends Cell Biol. 6, 382–387 (1996).
Article CAS Google Scholar - Kraut, R., Chia, W., Jan, L. Y., Jan, Y. N. & Knoblich, J. A. Role of inscuteable in orientating asymmetric cell divisions in Drosophila. Nature 383, 50–55 (1996).
Article ADS CAS Google Scholar - Thorpe, C. J., Schlesinger, A., Clayton Carter, J. & Bowerman, B. Wnt signaling polarizes an early C.elegans blastomere to distinguish endoderm from mesoderm. Cell 90, 695–705 (1997).
Article CAS Google Scholar - Rocheleau, C.et al. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90, 707–716 (1997).
Article CAS Google Scholar - Sawa, H., Lobel, L. & Horvitz, H. R. The Caenorhabditis elegans lin-17, which is required for certain asymmetric cell division, encodes a putative seven-transmembrane protein similar to the Drosophila Frizzled protein. Genes Dev. 10, 2189–2197 (1996).
Article CAS Google Scholar - Usui, K. & Kimura, K. Sequential emergence of the evenly spaced microchaetes on the notum of Drosophila. Arch. Dev. Biol. 203, 151–158 (1993).
Article Google Scholar - Emery, J. F. & Bier, E. Specificity of CNS and PNS regulatory subelements comprising pan-neural enhancers of the deadpan and scratch genes is achieved by repression. Development 121, 3549–3560 (1995).
CAS PubMed Google Scholar
Acknowledgements
We thank P. Adler, E. Bier, D.Coen, F. Chanut, C. Doe, Y.-N. Jan, T. Lieber and the Developmental Studies Hybridoma Bank for flies and antibodies; F. Rosa and M. Wassef for critical reading of the manuscript; and the Imaging facility of the Institut Jacques Monod for use of confocal microscopes. This work was supported by grants from the CNRS, the MENESR, the Fondation pour la Recherche Medicale, the Association pour la Recherche contre le Cancer and the Ligue Nationale contre le Cancer — Comité de Paris.
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- Laboratoire de G´nétique du Développement de la Drosophile, URA 1857, Ecole Normale Supérieure, 46 rue d'Ulm, Paris, 75005, France
Michel Gho & François Schweisguth
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- Michel Gho
- François Schweisguth
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Correspondence toMichel Gho.
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Gho, M., Schweisguth, F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila.Nature 393, 178–181 (1998). https://doi.org/10.1038/30265
- Received: 19 November 1997
- Accepted: 10 March 1998
- Issue Date: 14 May 1998
- DOI: https://doi.org/10.1038/30265