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Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage

Nature Cell Biology volume 3, pages 58–67 (2001)Cite this article

Abstract

Asymmetric partitioning of cell-fate determinants during development requires coordinating the positioning of these determinants with orientation of the mitotic spindle. In the Drosophila peripheral nervous system, sensory organ progenitor cells (SOPs) undergo several rounds of division to produce five cells that give rise to a complete sensory organ. Here we have observed the asymmetric divisions that give rise to these cells in the developing pupae using green fluorescent protein fusion proteins. We find that spindle orientation and determinant localization are tightly coordinated at each division. Furthermore, we find that two types of asymmetric divisions exist within the sensory organ precursor cell lineage: the anterior–posterior pI cell-type division, where the spindle remains symmetric throughout mitosis, and the strikingly neuroblast-like apical–basal division of the pIIb cell, where the spindle exhibits a strong asymmetry at anaphase. In both these divisions, the spindle reorientates to position itself perpendicular to the region of the cortex containing the determinant. On the basis of these observations, we propose that two distinct mechanisms for controlling asymmetric cell divisions occur within the same lineage in the developing peripheral nervous system in Drosophila.

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Figure 1: The sensory organ precursor lineage and the external sensory organ.
Figure 2: Numb–GFP is asymmetrically localized in the pI and pIIb cell divisions in the SOP lineage.
Figure 3: Spindles reorientate during mitosis in the SOP lineage.
Figure 4: Initiation of the Pon–GFP crescent localization precedes spindle positioning in the pI SOP division.
Figure 5: frizzled mutants show randomization of positioning of the Pon–GFP crescent.
Figure 6: Both Miranda and Inscuteable are expressed in the pIIb cell, and Inscuteable is required for the proper apical–basal positioning of the mitotic spindle.
Figure 7: The divisions of the sensory organ precursor cell lineage.

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Acknowledgements

We thank Y. M. Chan for critical reading of the manuscript, B. Lu for Sca–Gal4 UAS–Pon–GFP/Cyo and UAS–Numb–GFP flies. We thank F. Schweisguth, D. Kiehart, W. Chia and the Bloomington Stock Center for flies and reagents. We also thank members of the Jan lab for helpful discussions. F.R. is supported by the NIH Neuroscience Training Grant and the Human Frontiers Science Program (HFSP) postdoctoral fellowship. L.Y.J. and Y.N.J. are investigators at the Howard Hughes Medical Institute.

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  1. Departments of Physiology and Biochemistry, Howard Hughes Medical Institute, University of California, San Francisco, 94143-0725, California, USA

    Fabrice Roegiers, Susan Younger-Shepherd, Lily Yeh Jan & Yuh Nung Jan

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Correspondence to Yuh Nung Jan.

Supplementary information

Movie 1a

(See Fig. 4a) Dorsal view of pupa 16^h after formation. The spindle seesaws while the Pon crescent accumulates at the anterior cortex during SOP cell mitosis. When the Pon crescent completes its accumulation the spindle stops moving and undergoes anaphase. Microtubules were labelled with tau-GFP, Pon with Pon-GFP. Frames were recorded every 40^s. Anterior is to the bottom right. (AVI 1504 kb)

Movie 2b (See Fig. 5d)

Dorsal view of pupa ~16^h after formation. The spindle seesaws while the Pon crescent accumulates at the anterior cortex during SOP cell mitosis in an fz mutant. When the Pon crescent completes its accumulation the spindle stops moving and undergoes anaphase. Microtubules were labelled with tau-GFP, Pon with Pon-GFP. Frames were recorded every 15^s. Anterior is to the bottom right. (AVI 823 kb)

Movie 2b (See Fig. 5d)

As Movie 2a. (AVI 823 kb)

Movie 3a

(See Fig. 5e) Dorsal view of pupa ~16^h after formation. In 10% of fz-mutant SOPs the mitotic spindle remains parallel to the Pon-GFP crescent (SOP lower right). In 90% of cases the spindle is orientated perpendicular to the Pon crescent (SOP upper left). At anaphase, in both cases, the Pon-GFP crescent segregates to one of the two daughter cells. Microtubules were labeled with tau-GFP, Pon with Pon-GFP. Frames were recorded every 15^s. Anterior is to the upper right. (AVI 3269 kb)

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Roegiers, F., Younger-Shepherd, S., Jan, L. et al. Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat Cell Biol 3, 58–67 (2001). https://doi.org/10.1038/35050568

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