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JOURNAL ARTICLES
alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary
M. de Cuevas, J.K. Lee, A.C. Spradling
Development 1996 122: 3959-3968;

Summary

During Drosophila oogenesis, developing germline cysts are spanned by a large cytoplasmic structure called a fusome, containing alpha-spectrin and the adducin-like product of the hu-li tai shao (hts) gene. We found that fusomes contain two additional membrane skeletal proteins: beta-spectrin and ankyrin. hts was shown previously to be required for cyst formation and oocyte differentiation; the role of the fusome itself, however, and the organization and function of its other components, remains unclear. Using the FRT/FLP recombinase system to generate clones of alpha-spectrin-deficient cells in the ovary, we have shown that alpha-spectrin is also required for cyst formation and oocyte differentiation, but that its role in each process is distinct from that of Hts protein. Furthermore, alpha-spectrin is required for these processes in germline cells, but not in the follicle cells that surround each cyst. We have also found that the organization of membrane skeletal proteins is more dependent on alpha-spectrin in the fusome than at the plasma membrane in other cells. Our results suggest that the fusome and its associated membrane skeleton play a central role in regulating the divisions and differentiation of cyst cells.

Reference

    1. Beck K. A.,
    2. Buchanan J. A.,
    3. Malhotra V.,
    4. Nelson J. N.
    (1994) Golgi spectrin: identification of an erythroid-spectrin homolog associated with the Golgi complex. J. Cell Biol 127, 707–723
    OpenUrlAbstract/FREE Full Text
    1. Bennett V.
    (1990) Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Phys. Rev 70, 1029–1065
    OpenUrlFREE Full Text
    1. Bennett V.,
    2. Gilligan D. M.
    (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Ann. Rev. Cell Biol 9, 27–66
    OpenUrlCrossRefWeb of Science
    1. Byers T. J.,
    2. Dubreuil R.,
    3. Branton D.,
    4. Kiehart D. P.,
    5. Goldstein L. S. B.
    (1987) Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J. Cell Biol 105, 2103–2110
    OpenUrlAbstract/FREE Full Text
    1. Byers T. J.,
    2. Husain-Chishti A.,
    3. Dubreuil R.,
    4. Branton D.,
    5. Goldstein L. S. B.
    (1989) Sequence similarity of the amino-terminal domain of Drosophila beta spectrin to alpha actinin and dystrophin. J. Cell Biol 109, 1633–1641
    OpenUrlAbstract/FREE Full Text
    1. Devarajan P.,
    2. Stabach P. R.,
    3. Mann A. S.,
    4. Ardito T.,
    5. Kashgarian M.,
    6. Morrow J. S.
    (1996) Identification of a small cytoplasmic ankyrin (ankG119) in the kidney and muscle that bindsI * spectrin and associates with the Golgi apparatus. J. Cell Biol 133, 819–830
    OpenUrlAbstract/FREE Full Text
    1. Dubreuil R. R.,
    2. MacVicar G.,
    3. Dissanayake S.,
    4. Liu C.,
    5. Homer D.,
    6. Hortsch M.
    (1996) Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell Biol 133, 647–655
    OpenUrlAbstract/FREE Full Text
    1. Fehon R. G.,
    2. Dawson I. A.,
    3. Artavanis-Tsakonas S.
    (1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545–557
    OpenUrlAbstract
    1. Fishkind D. J.,
    2. Bonder E. M.,
    3. Begg D. A.
    (1990) Subcellular localization of sea urchin egg spectrin: evidence for assembly of the membrane-skeleton on unique classes of vesicles in eggs and embryos. Dev. Biol 142, 439–452
    OpenUrlCrossRefPubMed
    1. Forbes A. J.,
    2. Lin H.,
    3. Ingham P. W.,
    4. Spradling A. C.
    (1996) hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122, 1125–1135
    OpenUrlAbstract
    1. Golic K. G.,
    2. Lindquist S.
    (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509
    OpenUrlCrossRefPubMedWeb of Science
    1. Gregorio C. C.,
    2. Repasky E. A.,
    3. Fowler V. M.,
    4. Black J. D.
    (1994) Dynamic properties of ankyrin in T lymphocytes: colocalization with spectrin and protein kinase C. J. Cell Biol 125, 345–358
    OpenUrlAbstract/FREE Full Text
    1. Hawkins N. C.,
    2. Thorpe J.,
    3. Schupbach T.
    (1996) encore, a gene required for the regulation of germ line mitosis and oocyte differentiation during Drosophila oogenesis. Development 122, 281–290
    OpenUrlAbstract
    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. Lee J. K.,
    2. Black J. D.,
    3. Repasky E. A.,
    4. Kubo R. T.,
    5. Bankert R. B.
    (1988) Activation induces a rapid reorganization of spectrin in lymphocytes. Cell 55, 807–816
    OpenUrlCrossRefPubMed
    1. Lee J. K.,
    2. Coyne R. S.,
    3. Dubreuil R. R.,
    4. Goldstein L. S. B.,
    5. Branton D.
    (1993) Cell shape and interaction defects in-spectrin mutants of Drosophilamelanogaster. J. Cell Biol 123, 1797–1809
    OpenUrlAbstract/FREE Full Text
    1. Lin H.,
    2. Spradling A. C.
    (1993) Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol 159, 140–152
    OpenUrlCrossRefPubMedWeb of Science
    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. 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. Mahowald A. P.
    (1971) The formation of ring canals by cell furrows in Drosophila. Z. Zellforsch 118, 162–167
    OpenUrlCrossRefPubMed
    1. Mahowald A. P.,
    2. Strassheim J. M.
    (1970) Intercellular migration of centrioles in the germarium of Drosophila melanogaster: an electron microscopic study. J. Cell Biol 45, 306–320
    OpenUrlAbstract/FREE Full Text
    1. Margolis J.,
    2. Spradling A. C.
    (1995) Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807
    OpenUrlAbstract
    1. McCartney B. M.,
    2. Fehon R. G.
    (1996) Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol 133, 843–852
    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. Nelson W. J.
    (1992) Regulation of cell surface polarity from bacteria to mammals. Science 258, 948–955
    OpenUrlAbstract/FREE Full Text
    1. Perrin D.,
    2. Aunis D.
    (1985) Reorganization of-fodrin induced by stimulation in secretory cells. Nature 315, 589–592
    OpenUrlCrossRefPubMed
    1. Perrin D.,
    2. Langley O. K.,
    3. Aunis D.
    (1987) Anti--fodrin inhibits secretion from permeabilized chromaffin cells. Nature 326, 498–501
    OpenUrlCrossRefPubMed
    1. Pesacreta T. C.,
    2. Byers T. J.,
    3. Dubreuil R.,
    4. Kiehart D. P.,
    5. Branton D.
    (1989) Drosophila spectrin: the membrane skeleton during embryogenesis. J. Cell Biol 108, 1697–1709
    OpenUrlAbstract/FREE Full Text
    1. Robinson D. N.,
    2. Cant K.,
    3. Cooley L.
    (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015–2025
    OpenUrlAbstract
    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. 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. 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.,
    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. Thomas G. H.,
    2. Kiehart D. P.
    (1994) heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis. Development 120, 2039–2050
    OpenUrlAbstract
    1. Yue L.,
    2. Spradling A. C.
    (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. GenesDev 6, 2443–2454
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary
M. de Cuevas, J.K. Lee, A.C. Spradling
Development 1996 122: 3959-3968;
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