Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate

Abstract

The generation of cellular diversity is essential in embryogenesis, especially in the central nervous system. During neurogenesis, cell interactions or asymmetric protein localization during mitosis can generate daughter cells with different fates1,2,3,4. Here we describe the asymmetric localization of a messenger RNA and an RNA-binding protein that creates molecular and developmental differences between Drosophila neural precursors (neuroblasts) and their daughter cells, ganglion mother cells (GMCs). The prospero (pros) mRNA and the RNA-binding protein Staufen (Stau) are asymmetrically localized in mitotic neuroblasts and are specifically partitioned into the GMC, as is Pros protein5,6,7. Stau is required for localization of pros RNA but not of Pros protein. Loss of localization of Stau or of pros RNA alters GMC development, but only in embryos with reduced levels of Pros protein, suggesting that pros RNA and Pros protein act redundantly to specify GMC fate. We also find that GMCs do not transcribe the pros gene, showing that inheritance of pros RNA and/or Pros protein from the neuroblast is essential for GMC specification.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Asymmetric localization of pros RNA in neuroblasts requires Stau but not microtubules.
Figure 2: Asymmetric localization of Stau and Pros proteins in neuroblasts.
Figure 3: pros is transcribed in neuroblasts but not GMCs.
Figure 4: Localization and function of Stau and pros RNA in neuroblasts.

Similar content being viewed by others

References

  1. McConnell, S. K. Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15, 761–768 (1995).

    Article  CAS  Google Scholar 

  2. Guenther, C. & Garriga, G. Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates. Development 122, 3509–3518 (1996).

    CAS  PubMed  Google Scholar 

  3. Jan, Y. N. & Jan, L. Y. Maggot's hair and bug's eye: role of cell interactions and intrinsic factors in cell fate specification. Neuron 14, 1–5 (1995).

    Article  CAS  Google Scholar 

  4. Lin, H. & Schagat, T. Neuroblasts: a model for the asymmetric division of stem cells. Trends Genet. 13, 33–39 (1996).

    Article  Google Scholar 

  5. Hirata, J., Nakagoshi, H., Nabeshima, Y. & Matsuzaki, F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377, 627–630 (1995).

    Article  ADS  CAS  Google Scholar 

  6. 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 

  7. Spana, E. & Doe, C. Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121, 3187–3195 (1995).

    CAS  Google Scholar 

  8. Doe, C. Q., Chu-LaGraff, Q., Wright, D. M. & Scott, M. P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65, 451–464 (1991).

    Article  CAS  Google Scholar 

  9. Vaessin, H. et al. prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67, 941–953 (1991).

    Article  CAS  Google Scholar 

  10. Ferrandon, D., Elphick, L., Nüsslein-Volhard, C. & St Johnston, D. Staufen protein associates with the 3′ UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79, 1221–1232 (1994).

    Article  CAS  Google Scholar 

  11. St Johnston, D., Beuchle, D. & Nüsslein-Volhard, C. staufen, a gene required to localize maternal RNA in the Drosophila egg. Cell 66, 51–63 (1991).

    Article  CAS  Google Scholar 

  12. Li, P., Yang, X., Wasser, M., Cai, Y. & Chia, W. Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions. Cell 90, 437–447 (1997).

    Article  CAS  Google Scholar 

  13. Broadus, J. & Doe, C. Q. Extrinsic cues, intrinsic cues, and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr. Biol. 7, 827–835 (1997).

    Article  CAS  Google Scholar 

  14. Matsuzaki, F., Koisumi, K., Hama, C., Yoshioka, T. & Nabeshima, Y. Cloning of the Drosophila prospero gene and its expression in ganglion mother cells. Biochem. Biophys. Res. Commun. 182, 1326–1332 (1992).

    Article  CAS  Google Scholar 

  15. Long, R. M. et al. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277, 383–387 (1997).

    Article  CAS  Google Scholar 

  16. Takizawa, P. A., Sil, A., Swedlow, J. R., Herskowitz, I. & Vale, R. D. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93 (1997).

    Article  ADS  CAS  Google Scholar 

  17. Bobola, N., Jansen, R.-P., Shin, T. & Nasmyth, K. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84, 699–709 (1996).

    Article  CAS  Google Scholar 

  18. Bodmer, R., Carretto, R. & Jan, Y. N. Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3, 21–32 (1989).

    Article  CAS  Google Scholar 

  19. Lundell, M. J. & Hirsch, J. Anew visible light fluorochrome for confocal microscopy. Biotechniques 16, 434–440 (1994).

    CAS  PubMed  Google Scholar 

  20. Broadus, J. B. & Doe, C. Q. Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent cell fates in Drosophila and Schistocerca. Development 121, 3989–3996 (1995).

    CAS  PubMed  Google Scholar 

  21. Patel, N. H., Schafer, B., Goodman, C. S. & Holmgren, R. The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 3, 890–904 (1989).

    Article  CAS  Google Scholar 

  22. Shen, C.-P., Jan, L. Y. & Jan, Y. N. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90, 449–458 (1997).

    Article  CAS  Google Scholar 

  23. Ikeshima-Kataoka, H., Skeath, J. B., Nabeshima, Y., Doe, C. Q. & Matsuzaki, F. Miranda directs Propsero to a daughter cell during Drosophila asymmetric divisions. Nature 390, 625–629 (1997).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank C.-Y. Peng for help with genetics; C.-Y. Peng, F. Matsuzaki and B. Chia for sharing unpublished results; D. St Johnston for Stau antiserum; E. Spana for pros intron DNA; and C.Thummel and F. Gertler for comments. This work was supported by an NIH postdoctoral fellowship to S.F. and by the HHMI, of which C.Q.D. is an associate investigator.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Broadus, J., Fuerstenberg, S. & Doe, C. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391, 792–795 (1998). https://doi.org/10.1038/35861

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35861

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing