Advertisement
JOURNAL ARTICLES
The fusome organizes the microtubule network during oocyte differentiation in Drosophila
N.C. Grieder, M. de Cuevas, A.C. Spradling
Development 2000 127: 4253-4264;

Summary

Differentiation of the Drosophila oocyte takes place in a cyst of 16 interconnected germ cells and is dependent on a network of microtubules that becomes polarized as differentiation progresses (polarization). We have investigated how the microtubule network polarizes using a GFP-tubulin construct that allows germ-cell microtubules to be visualized with greater sensitivity than in previous studies. Unexpectedly, microtubules are seen to associate with the fusome, an asymmetric germline-specific organelle, which elaborates as cysts form and undergoes complex changes during cyst polarization. This fusome-microtubule association occurs periodically during late interphases of cyst divisions and then continuously in 16-cell cysts that have entered meiotic prophase. As meiotic cysts move through the germarium, microtubule minus ends progressively focus towards the center of the fusome, as visualized using a NOD-lacZ marker. During this same period, discrete foci rich in gamma tubulin that very probably correspond to migrating cystocyte centrosomes also associate with the fusome, first on the fusome arms and then in its center, subsequently moving into the differentiating oocyte. The fusome is required for this complex process, because microtubule network organization and polarization are disrupted in hts(1) mutant cysts, which lack fusomes. Our results suggest that the fusome, a specialized membrane-skeletal structure, which arises in early germ cells, plays a crucial role in polarizing 16-cell cysts, at least in part by interacting with microtubules and centrosomes.

REFERENCES

    1. Bello B.,
    2. Resendez-Perez D.,
    3. Gehring W. J.
    (1998) Spatial and temporal targeting of gene expression in Drosophila by means of a tetracycline-dependent transactivator system. Development 125, 2193–2202
    OpenUrlAbstract
    1. Bowerman B.,
    2. Shelton C. A.
    (1999) Cell polarity in the early Caenorhabditis elegans embryo. Curr. Opin. Genet. Dev 9, 390–395
    OpenUrlCrossRefPubMedWeb of Science
    1. Carminati J. L.,
    2. Stearns T.
    (1997) Microtubules orient the mitoticspindle in yeast through dynein-dependent interactions with the cell cortex. J. Cell Biol 138, 629–641
    OpenUrlAbstract/FREE Full Text
    1. Carpenter A. T. C.
    (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. Carpenter A. T. C.
    (1979) Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females. Genetics 92, 511–541
    OpenUrlAbstract/FREE Full Text
    1. Clark I. E.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1997) Reciprocal localization of Nod and Kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124, 461–470
    OpenUrlAbstract
    1. Cooley L.,
    2. Theurkauf W. E.
    (1994) Cytoskeletal functions during Drosophila oogenesis. Science 266, 590–596
    OpenUrlAbstract/FREE Full Text
    1. de Cuevas M.,
    2. Lee J. K.,
    3. Spradling A. C.
    (1996) -spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122, 3959–3968
    OpenUrlAbstract
    1. de Cuevas M.,
    2. Lilly M. A.,
    3. Spradling A. C.
    (1997) Germline cyst formation in Drosophila. Annu. Rev. Genet 31, 405–428
    OpenUrlCrossRefPubMedWeb of Science
    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. Deng W.,
    2. Lin H.
    (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of polarized microtubule array for oocyte specification in Drosophila. Dev. Biol 189, 79–94
    OpenUrlCrossRefPubMedWeb of Science
    1. Desai A.,
    2. Mitchison T. J.
    (1997) Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol 13, 83–117
    OpenUrlCrossRefPubMedWeb of Science
    1. Ephrussi A.,
    2. Dickinson L. K.,
    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. Heim R.,
    2. Cubitt A. B.,
    3. Tsien R. Y.
    (1995) Improved green fluorescence. Nature 373, 663–664
    OpenUrlCrossRefPubMed
    1. Kalfayan L.,
    2. Wensink P. C.
    (1981) -tubulin genes of Drosophila. Cell 24, 97–106
    OpenUrlCrossRefPubMed
    1. Kellogg D. R.,
    2. Mitchison T. J.,
    3. Alberts B. M.
    (1988) Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103, 675–686
    OpenUrlAbstract/FREE Full Text
    1. Khodjakov A.,
    2. Rieder C. L.
    (1999) The sudden recruitment of-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J. Cell Biol 146, 585–596
    OpenUrlAbstract/FREE Full Text
    1. Knowles B. A.,
    2. Cooley L.
    (1994) The specialized cytoskeleton of the Drosophila egg chamber. Trends Genet 10, 235–241
    OpenUrlCrossRefPubMedWeb of Science
    1. Koch E. A.,
    2. King R. C.
    (1966) The origin and early differentiation of the egg chamber of Drosophila melanogaster. J. Morphol 119, 283–303
    OpenUrlCrossRefPubMed
    1. Koch E. A.,
    2. Spitzer R. H.
    (1983) 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
    OpenUrlPubMedWeb of Science
    1. Lantz V.,
    2. Chang J. S.,
    3. Horabin J. I.,
    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. Li M.,
    2. McGrail M.,
    3. Serr M.,
    4. Hays T. S.
    (1994) Drosophila cytoplasmic Dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol 126, 1475–1494
    OpenUrlAbstract/FREE Full Text
    1. Lilly M. A.,
    2. de Cuevas M.,
    3. Spradling A. C.
    (2000) Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Dev. Biol 218, 53–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin H.,
    2. Yue L.,
    3. Spradling A. C.
    (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947–956
    OpenUrlAbstract
    1. Lin H.,
    2. Spradling A. C.
    (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet 16, 6–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin H.,
    2. Spradling A. C.
    (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463–2476
    OpenUrlAbstract
    1. Liu Z.,
    2. Xie T.,
    3. Steward R.
    (1999) Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 126, 4477–4488
    OpenUrlAbstract
    1. Lu B.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1998) Asymmetric cell division: lessons from flies and worms. Curr. Opin. Genet. Dev 8, 392–399
    OpenUrlCrossRefPubMedWeb of Science
    1. Mach J. M.,
    2. Lehmann R.
    (1997) An Egalitarian-Bicaudal-D complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev 11, 423–435
    OpenUrlAbstract/FREE Full Text
    1. Mahowald A. P.,
    2. Strassheim J. M.
    (1970) Intercellular migration of centrioles in the germarium of Drosophila melanogaster. J. Cell Biol 45, 306–320
    OpenUrlAbstract/FREE Full Text
    1. McGrail M.,
    2. Hays T. S.
    (1997) The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409–2419
    OpenUrlAbstract
    1. Miller R. K.,
    2. Matheos D.,
    3. Rose M. D.
    (1999) The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J. Cell Biol 144, 963–975
    OpenUrlAbstract/FREE Full Text
    1. Palmer R. E.,
    2. Sullivan D. S.,
    3. Huffaker T.,
    4. Koshland D.
    (1992) Roleof astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol 119, 583–593
    OpenUrlAbstract/FREE Full Text
    1. Piperno G.,
    2. Fuller M. T.
    (1985) Monoclonal antibodies specific for an acetylated form of-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J. Cell Biol 101, 2085–2094
    OpenUrlAbstract/FREE Full Text
    1. Pokrywka N. J.,
    2. Stephenson E. C.
    (1995) Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol 167, 363–370
    OpenUrlCrossRefPubMedWeb of Science
    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. Rørth P.
    (1998) Gal4 in the Drosophila female germline. Mech. Dev 78, 113–118
    OpenUrlCrossRefPubMedWeb of Science
    1. Robinson D. N.,
    2. Cant K.,
    3. Cooley L.
    (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015–2025
    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. Spradling A. C.,
    2. Rubin G. M.
    (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341–347
    OpenUrlAbstract/FREE Full Text
    1. Storto P. D.,
    2. King R. C.
    (1989) The role of polyfusomes in generating branched chains of cystocytes during Drosophila oogenesis. Dev. Genet 10, 70–86
    OpenUrlCrossRefPubMedWeb of Science
    1. Suter B.,
    2. Romberg L. M.,
    3. Steward R.
    (1989) Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript acculmulation 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. Takizawa P. A.,
    2. Sil A.,
    3. Swedlow J. R.,
    4. Herskowitz I.,
    5. Vale R. D.
    (1997) Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93
    OpenUrlCrossRefPubMedWeb of Science
    1. Theesfeld C. L.,
    2. Irazoqui J. E.,
    3. Bloom K.,
    4. Lew D. J.
    (1999) The role of actin in spindle orientation changes during the Saccharomyces cerevisiae cell cycle. J. Cell Biol 146, 1019–1032
    OpenUrlAbstract/FREE Full Text
    1. Theurkauf W. E.,
    2. Baum H.,
    3. Bo J.,
    4. Wensink P. C.
    (1986) Tissue-specific and constitutive-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl. Acad. Sci. U S A 83, 8477–8481
    OpenUrlAbstract/FREE Full Text
    1. Theurkauf W. E.,
    2. Smiley S.,
    3. Wong M. L.,
    4. Alberts B. M.
    (1992) Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923–936
    OpenUrlAbstract
    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. Theurkauf W. E.
    (1994) Microtubules and cytoplasm organization during Drosophila oogenesis. Dev. Biol 165, 352–360
    OpenUrlCrossRefPubMed
    1. Tracey W. D.,
    2. Ning X., Jr.,
    3. Klingler M.,
    4. Kramer S. G.,
    5. Gergen J. P.
    (2000) Quantitative analysis of gene function in the Drosophila embryo. Genetics 154, 273–284
    OpenUrlAbstract/FREE Full Text
    1. Tulin A. V.,
    2. Naumova N. M.,
    3. Aravin A. A.,
    4. Gvozdev V. A.
    (1998) Repeated, protein-encoding heterochromatic genes cause inactivation of a juxtaposed euchromatic gene. FEBS Lett 425, 513–516
    OpenUrlCrossRefPubMed
    1. Van Doren M.,
    2. Williamson A. L.,
    3. Lehmann R.
    (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol 8, 243–246
    OpenUrlCrossRefPubMedWeb of Science
    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. Wiese C.,
    2. Zheng Y.
    (1999) -tubulin complexes and their interaction with microtubule-organizing centers. Curr. Opin. Struct. Biol 9, 250–259
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. G.,
    2. Zheng Y.,
    3. Oakley C. E.,
    4. Oakley B. R.,
    5. Borisy G. G.,
    6. Fuller M. T.
    (1997) Differential expression of two-tubulin isoforms during gametogenesis and development in Drosophila. Dev. Biol 184, 207–221
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. G.
    (1999) BimC motor protein KLP61F cycles between mitotic spindles and fusomes in Drosophila germ cells. Curr. Biol 9, 923–926
    OpenUrlCrossRefPubMed
    1. Yue L.,
    2. Spradling A. C.
    (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolg of adducin. Genes Dev 6, 2443–2454
    OpenUrlAbstract/FREE Full Text
    1. Zaccai M.,
    2. Lipshitz H. D.
    (1996) Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4, 159–166
    OpenUrlCrossRefPubMed
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The fusome organizes the microtubule network during oocyte differentiation in Drosophila
N.C. Grieder, M. de Cuevas, A.C. Spradling
Development 2000 127: 4253-4264;
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

The Node is looking for a new Community Manager!

If you're interested in science communication, publishing and the developmental biology community, we're hiring for a new Community Manager for our community site, the Node.

The position is an exciting opportunity to develop an already successful and well-known site, engaging with the academic, publishing and online communities. Find out more and how to apply.

Upcoming special issue: call for papers

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

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

The people behind the papers - Clément Dubois, Shivam Gupta, Andrew Mugler and Marie-Anne Félix

A new paper investigates the robustness of neuroblast migration in the C. elegans larva in the face of both genetic and environmental variation. In an interview, the paper's four authors tell us more about the story.

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. Every talk is recorded and since launching in August last year, the series has clocked up almost 10k views on YouTube.

Here, Swann Floc'hlay discusses her work modelling dorsal-ventral axis specification in the sea urchin embryo.

Save your spot at our next session:

14 April
Time: 17:00 BST
Chaired by: François Guillemot

12 May
Time: TBC
Chaired by: Paola Arlotta

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