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.

  • Article
  • Published:

Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning

Nature Cell Biology volume 1, pages 444–449 (1999)Cite this article

Abstract

Here we show that the Drosophila homologue of Lissencephaly-1 , DLis-1, acts together with Bicaudal-D (Bic-D), Egalitarian (Egl), dynein and microtubules to determine oocyte identity. DLis-1 is further required for nurse-cell-to-oocyte transport during oocyte growth, and for the positioning of the nucleus in the oocyte. Immunostaining of DLis-1 protein reveals a cortical localization that is independent of microtubules. DLis-1 may function in this position as a cortical anchor for the other nuclear-localization factors. DLis-1 and Bic-D are further required for nuclear localization in the developing nervous system, indicating that homologues of Bic-D, dynein and Egl-like proteins may also be involved in vertebrate neural migration and that their absence may cause a Miller–Dieker-like lissencephaly.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: E415 is necessary for oocyte determination and nurse-cell-to-oocyte transport.
Figure 2: E415 functions in mid-oogenesis to localize factors within the oocyte.
Figure 3: Structure of DLis-1.
Figure 4: Cortical DLis-1 and its requirement for dynein localization.
Figure 5: DLis-1 and Bic-D are required for nuclear positioning in photoreceptor cells.
Figure 6: Model for DLis-1 function in nuclear positioning and nurse-cell-to-oocyte transport in the Drosophila ovary.

Similar content being viewed by others

References

  1. Mach, J. M. & Lehmann, R. An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila . Genes Dev. 11, 423– 435 (1997).

    Article  CAS  Google Scholar 

  2. Swan, A. & Suter, B. Role of Bicaudal-D in patterning the Drosophila egg chamber in mid-oogenesis. Development 122, 3577–3586 ( 1996).

    CAS  PubMed  Google Scholar 

  3. Cooley, L. & Theurkauf, W. E. Cytoskeletal functions during Drosophila oogenesis. Science 266, 590– 596 (1994).

  4. Ran, B., Bopp, R. & Suter, B. Null alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development. Development 120, 1233–1242 (1994).

    CAS  PubMed  Google Scholar 

  5. Schupbach, T. & Wieschaus, E. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119–1136 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Lin, H., Yue, L. & Spradling, A. C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation . Development 120, 947– 956 (1994).

    CAS  PubMed  Google Scholar 

  7. de Cuevas, M., Lee, J. K. & Spradling, A. C. Alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122, 3959–3968 ( 1996).

    CAS  PubMed  Google Scholar 

  8. McGrail, M. & Hays, T. S. The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409–2419 (1997).

    CAS  PubMed  Google Scholar 

  9. Koch, E. A. & Spitzer, R. H. Multiple effects of colchicine on oogenesis in Drosophila: induced sterility and switch of potential oocyte to nurse-cell developmental pathway. Cell Tissue Res. 228, 21–32 (1983).

    Article  CAS  Google Scholar 

  10. Theurkauf, W. E., Smiley, S., Wong, M. L. & Alberts, B. M. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923–936 (1992).

    CAS  PubMed  Google Scholar 

  11. Pokrywka, N. J. & Stephenson, E. C. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis . Development 113, 55–66 (1991).

    CAS  PubMed  Google Scholar 

  12. Clark, I., Giniger, E., Ruohola-Baker, H., Jan, L. Y. & Jan, Y. N. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4, 289– 300 (1994).

    Article  CAS  Google Scholar 

  13. Pokrywka, N. J. & Stephenson, E. C. Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167, 363– 370 (1995).

    Article  CAS  Google Scholar 

  14. Reiner, O. et al. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364, 717–721 (1993).

    Article  CAS  Google Scholar 

  15. Xiang, X., Osmani, A. H., Osmani, S. A., Xin, M. & Morris, N. R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6, 297–310 (1995).

    Article  CAS  Google Scholar 

  16. Geiser, J. R. et al. Saccharomyces cerevisiae genes required in the absence of the CIN8-encoded spindle motor act in functionally diverse mitotic pathways. Mol. Biol. Cell 8, 1035– 1050 (1997).

    Article  CAS  Google Scholar 

  17. Neer, E. J. & Smith, T. F. G protein heterodimers: new structures propel new questions. Cell 84, 175– 178 (1996).

    Article  CAS  Google Scholar 

  18. McGrail, M. et al. Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J. Cell Biol. 131, 411–425 (1995).

    Article  CAS  Google Scholar 

  19. Li, M., McGrail, M., Serr, M. & Hays, T. S. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol. 126, 1475– 1494 (1994).

    Article  CAS  Google Scholar 

  20. Rasmusson, K., Serr, M., Gepner, J., Gibbons, I. & Hays, T. S. A family of dynein genes in Drosophila melanogaster . Mol. Biol. Cell 5, 45– 55 (1994).

    Article  CAS  Google Scholar 

  21. Rakic, P. Principles of neural cell migration. Experientia 46 , 882–891 (1990).

    Article  CAS  Google Scholar 

  22. Tomlinson, A. The cellular dynamics of pattern formation in the eye of Drosophila. J. Embryol. Exp. Morphol. 89, 313– 331 (1985).

    CAS  PubMed  Google Scholar 

  23. Fan, S. S. & Ready, D. F. Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 124, 1497–1507 (1997).

    CAS  PubMed  Google Scholar 

  24. Reinsch, S. & Gonczy, P. Mechanisms of nuclear positioning . J. Cell Sci. 111, 2283– 2295 (1998).

    CAS  PubMed  Google Scholar 

  25. Wang, D. S. et al. Binding of pleckstrin homology domains to WD40/beta-transducin repeat containing segments of the protein product of the Lis-1 gene. Biochem. Biophys. Res. Commun. 209, 622– 629 (1995).

    Article  CAS  Google Scholar 

  26. Holleran, E. A., Tokito, M. K., Karki, S. & Holzbaur, E. L. Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135, 1815–1829 (1996).

    Article  CAS  Google Scholar 

  27. Karki, S. & Holzbaur, E. L. Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 11, 45–53 ( 1999).

    Article  CAS  Google Scholar 

  28. Suter, B. & Steward, R. Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation . Cell 67, 917–926 (1991).

    Article  CAS  Google Scholar 

  29. Sapir, T., Elbaum, M. & Reiner, O. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J. 16, 6977–6984 (1997).

    Article  CAS  Google Scholar 

  30. Micklem, D. R. et al. The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr. Biol. 7, 468–478 ( 1997).

    Article  CAS  Google Scholar 

  31. Liu, Z., Xie, T. & Steward, R. Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 126, 4477– 4488 (1999).

Download references

Acknowledgements

We thank E. Patrick and J. Pandur for technical assistance and Y. Rao for reagents and advice on work on eye imaginal discs. This work is supported by the National Cancer Institute of Canada with funds from the Canadian Cancer Society, and by the Québec ‘Fonds pour la Formation de Chercheurs et l’Aide à la Recherche’ (FCAR). B.S. is a Research Scientist of the National Cancer Institute of Canada supported by funds from the Canadian Cancer Society. A.S. was supported in part by a Québec FCAR postgraduate scholarship.

Correspondence and requests for materials should be addressed to B.S. The DLis-1 cDNA sequence has been deposited at GenBank under accession number AF117606.

Supplementary information is available on Nature Cell Biology’s World-Wide Web site (http://cellbio.nature.com ) or as paper copy from the London editorial office of Nature Cell Biology.

Author information

Authors and Affiliations

  1. Department of Biology, McGill University, 1205 Dr Penfield, Montreal, H3A 1B1, Quebec, Canada

    Andrew Swan, Thuy Nguyen & Beat Suter

Authors
  1. Andrew Swan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thuy Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beat Suter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Beat Suter.

Supplementary information

Figure 1 DLis-1 is required for cyst encapsulation.

Figure 2 Confocal optical sections from wild-type. (PDF 351 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Swan, A., Nguyen, T. & Suter, B. Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat Cell Biol 1, 444–449 (1999). https://doi.org/10.1038/15680

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/15680

Search

Advanced 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