Advertisement
JOURNAL ARTICLES
The role of BicD, egl, orb and the microtubules in the restriction of meiosis to the Drosophila oocyte
J. Huynh, D. St Johnston
Development 2000 127: 2785-2794;

Summary

The oocyte is the only cell in Drosophila that goes through meiosis with meiotic recombination, but several germ cells in a 16-cell cyst enter meiosis and form synaptonemal complexes (SC) before one cell is selected to become the oocyte. Using an antibody that recognises a component of the SC or the synapsed chromosomes, we have analysed how meiosis becomes restricted to one cell, in relation to the other events in oocyte determination. Although BicD and egl mutants both cause the development of cysts with no oocyte, they have opposite effects on the behaviour of the SC: none of the cells in the cyst form SC in BicD null mutants, whereas all of the cells do in egl and orb mutants. Furthermore, unlike all cytoplasmic markers for the oocyte, the SC still becomes restricted to one cell when the microtubules are depolymerised, even though the BicD/Egl complex is not localised. These results lead us to propose a model in which BicD, Egl and Orb control entry into meiosis by regulating translation.

REFERENCES

    1. Burchard S.,
    2. Paululat A.,
    3. Hinz U.,
    4. Renkawitz-Pohl R.
    (1995) The mutant not enough muscles (nem) reveals reduction of the Drosophila embryonic muscle pattern. J. Cell Sci 108, 1443–1454
    OpenUrlAbstract/FREE Full Text
    1. Carpenter A.
    (1994) Egalitarian and the choice of cell fates in Drosophila melanogaster oogenesis. Ciba Found. Symp 182, 223–246
    OpenUrlPubMed
    1. Carpenter A. T.
    (1975) Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51, 157–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Chang J.,
    2. Tan L.,
    3. Schedl P.
    (1999) The Drosophila CPEB homolog, Orb is required for Oskar protein expression in oocytes. Dev. Biol 215, 91–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Chou T.,
    2. Perrimon N.
    (1996) The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673–1679
    OpenUrlAbstract/FREE Full Text
    1. Christerson L.,
    2. McKearin D.
    (1994) orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev 8, 614–628
    OpenUrlAbstract/FREE Full Text
    1. de Cuevas M.,
    2. Spradling A. C.
    (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781–2789
    OpenUrlAbstract
    1. Ephrussi A.,
    2. Dickinson L.,
    3. Lehmann R.
    (1991) Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghabrial A.,
    2. Ray R. P.,
    3. Schupbach T.
    (1998) okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev 12, 2711–2723
    OpenUrlAbstract/FREE Full Text
    1. Godt D.,
    2. Tepass U.
    (1998) Drosophila oocyte localisation is mediated by differential cadherin-based adhesion. Nature 395, 387–391
    OpenUrlCrossRefPubMed
    1. González-Reyes A.,
    2. Elliott H.,
    3. St Johnston D.
    (1997) Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. Development 124, 4927–4937
    OpenUrlAbstract
    1. González-Reyes A.,
    2. St Johnston D.
    (1994) Role of oocyte position in establishment of anterior-posterior polarity in Drosophila. Science 266, 639–642
    OpenUrlAbstract/FREE Full Text
    1. González-Reyes A.,
    2. St Johnston D.
    (1998) The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125, 3635–3644
    OpenUrlAbstract
    1. Grzeschik N.,
    2. Breuer S.,
    3. Renkawitz-Pohl R.,
    4. Paululat A.
    (1999) Molecular characterization of a point mutation in the Drosophila inscuteable gene. Drosophila Information Service 82, 27–29
    OpenUrl
    1. Hake L. E.,
    2. Richter J. D.
    (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617–627
    OpenUrlCrossRefPubMedWeb of Science
    1. Keyes L.,
    2. Spradling A.
    (1997) The Drosophila gene fs (2)cup interacts with otu to define a cytoplasmic pathway required for the structure and function of germ-line chromosomes. Development 124, 1419–1431
    OpenUrlAbstract
    1. Kim-Ha J.,
    2. Smith J. L.,
    3. Macdonald P. M.
    (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Knirr S.,
    2. Breuer S.,
    3. Paululat A.,
    4. Renkawitz-Pohl R.
    (1997) Somatic mesoderm differentiation and the development of a subset of pericardial cells depend on the not enough muscles (nem) locus, which contains the inscuteable gene and the intron located gene, skittles. Mech. Dev 67, 69–81
    OpenUrlCrossRefPubMed
    1. Kooistra R.,
    2. Vreeken K.,
    3. Zonneveld J. B.,
    4. de Jong A.,
    5. Eeken J. C.,
    6. Osgood C. J.,
    7. Buerstedde J. M.,
    8. Lohman P. H.,
    9. Pastink A.
    (1997) The Drosophila melanogaster RAD54 homolog, DmRAD54, is involved in the repair of radiation damage and recombination. Mol. Cell. Biol 17, 6097–6104
    OpenUrlAbstract/FREE Full Text
    1. Lantz V.,
    2. Ambrosio L.,
    3. Schedl P.
    (1992) The Drosophila orb gene ispredicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. Development 115, 75–88
    OpenUrlAbstract
    1. Lantz V.,
    2. Chang J.,
    3. Horabin J.,
    4. Bopp D.,
    5. Schedl P.
    (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8, 598–613
    OpenUrlAbstract/FREE Full Text
    1. Lin H.,
    2. Spradling A.
    (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet 16, 6–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin H.,
    2. Yue L.,
    3. Spradling A.
    (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947–956
    OpenUrlAbstract
    1. Mahowald A.,
    2. Strassheim J. M.
    (1970) Intercellular migration of the centrioles in the germarium of Drosophila melanogaster. J. Cell Biol 45, 306–320
    OpenUrlAbstract/FREE Full Text
    1. McKearin D.,
    2. Ohlstein B.
    (1995) A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121, 2937–2947
    OpenUrlAbstract
    1. McKim K. S.,
    2. Green-Marroquin B. L.,
    3. Sekelsky J. J.,
    4. Chin G.,
    5. Steinberg C.,
    6. Khodosh R.,
    7. Hawley R. S.
    (1998) Meiotic synapsis in the absence of recombination. Science 279, 876–878
    OpenUrlAbstract/FREE Full Text
    1. Minshall N.,
    2. Walker J.,
    3. Dale M.,
    4. Standart N.
    (1999) Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RNA 5, 27–38
    OpenUrlAbstract
    1. Mohler J.,
    2. Wieschaus E.
    (1986) Dominant maternal-effect mutations of Drosophila melanogaster causing the production of double-abdomen embryos. Genetics 112, 803–822
    OpenUrlAbstract/FREE Full Text
    1. Ran B.,
    2. Bopp R.,
    3. Suter B.
    (1994) Null alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development. Development 120, 1233–1242
    OpenUrlAbstract
    1. Schupbach T.,
    2. Wieschaus E.
    (1991) Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119–1136
    OpenUrlAbstract/FREE Full Text
    1. St Johnston D.,
    2. Beuchle D.,
    3. Nusslein-Volhard C.
    (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Story R. M.,
    2. Bishop D. K.,
    3. Kleckner N.,
    4. Steitz T. A.
    (1993) Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast. Science 259, 1892–1896
    OpenUrlAbstract/FREE Full Text
    1. Styhler S.,
    2. Nakamura A.,
    3. Swan A.,
    4. Suter B.,
    5. Lasko P.
    (1998) vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125, 1569–1578
    OpenUrlAbstract
    1. Suter B.,
    2. Romberg L.,
    3. Steward R.
    (1989) Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains. Genes Dev 3, 1957–1968
    OpenUrlAbstract/FREE Full Text
    1. Suter B.,
    2. Steward R.
    (1991) Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation. Cell 67, 917–926
    OpenUrlCrossRefPubMedWeb of Science
    1. Tearle R.,
    2. Nusslein-Volhard C.
    (1987) Tubingen mutants stocklist. Drosophila Information Service 66, 209–226
    OpenUrl
    1. Theurkauf W.
    (1994) Microtubules and cytoplasm organization during Drosophila oogenesis. Dev. Biol 165, 352–360
    OpenUrlCrossRefPubMed
    1. Theurkauf W. E.,
    2. Alberts B. M.,
    3. Jan Y. N.,
    4. Jongens T. A.
    (1993) A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169–1180
    OpenUrlAbstract/FREE Full Text
    1. Tinker R.,
    2. Silver D.,
    3. Montell D. J.
    (1998) Requirement for the vasa RNA helicase in gurken mRNA localization. Dev. Biol 199, 1–10
    OpenUrlCrossRefPubMed
    1. Tomancak P.,
    2. Guichet A.,
    3. Zavorszky P.,
    4. Ephrussi A.
    (1998) Oocyte polarity depends on regulation of gurken by Vasa. Development 125, 1723–1732
    OpenUrlAbstract
    1. van Eeden F.,
    2. St Johnston D.
    (1999) The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev 9, 396–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Walker J.,
    2. Minshall N.,
    3. Hake L.,
    4. Richter J.,
    5. Standart N.
    (1999) The clam 3UTR masking element-binding protein p82 is a member of the CPEB family. RNA 5, 14–26
    OpenUrlAbstract
    1. Wharton R. P.,
    2. Struhl G.
    (1989) Structure of the Drosophila BicaudalD protein and its role in localizing the the posterior determinant nanos. Cell 59, 881–892
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The role of BicD, egl, orb and the microtubules in the restriction of meiosis to the Drosophila oocyte
J. Huynh, D. St Johnston
Development 2000 127: 2785-2794;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.