Advertisement
JOURNAL ARTICLES
A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila
K.A. Matthews, D. Rees, T.C. Kaufman
Development 1993 117: 977-991;

Summary

Three alpha-tubulin proteins contribute to microtubules during oogenesis and early embryogenesis in Drosophila melanogaster: alpha TUB84B, alpha TUB84D, and alpha TUB67C. alpha TUB67C is unique in two respects. It is a structurally divergent alpha-tubulin, sharing only 67% amino acid identity with the generic isotypes alpha TUB84B and alpha TUB84D, and its expression is exclusively maternal. The genetic analysis of the alpha Tub67C gene described here demonstrates that alpha TUB67C is required for nuclear division in the oocyte and early embryo. Both meiosis and cleavage-stage mitoses are severely affected by mutations that result in a substantial decrease in the ratio of alpha TUB67C/alpha TUB84B+alpha TUB84D. A large increase in this ratio, achieved by increasing the gene dosage of alpha Tub67C, has little or no effect on meiosis, but severely disrupts mitotic spindle function. Thus, both classes of alpha-tubulin isotype present in the mature oocyte, alpha TUB67C and alpha TUB84B/84D, are essential for normal spindle function in early Drosophila development. These alpha-tubulins provide the first example of tubulin isotypes known to be coexpressed in wild-type animals whose encoded variation is required for the normal function of a microtubule array.

REFERENCES

    1. Baker H. N.,
    2. Rothwell S. W.,
    3. Grasser W. A.,
    4. Wallis K. T.,
    5. Murphy D. B.
    (1990) Copolymerization of two distinct tubulin isotypes during microtubule assembly in vitro. J. Cell Biol 110, 97–104
    OpenUrlAbstract/FREE Full Text
    1. Ben-Ze'ev A.,
    2. Farmer S. R.,
    3. Penman S.
    (1979) Mechanisms of regulating tubulin synthesis in cultured mammalian cells. Cell 17, 319–325
    OpenUrlCrossRefPubMedWeb of Science
    1. Bo J.,
    2. Wensink P. C.
    (1989) The promoter region of the Drosophila a2-tubulin gene directs testicular and neural specific expression. Development 106, 581–587
    OpenUrlAbstract
    1. Bond J. F.,
    2. Fridovich-Keil J. L.,
    3. Pillus L.,
    4. Mulligan C. R.,
    5. Solomon F.
    (1986) A chicken-yeast chimeric beta tubulin protein is incorporated into mouse microtubules in vivo. Cell 44, 461–468
    OpenUrlCrossRefPubMedWeb of Science
    1. Caron J. M.,
    2. Jones A. L.,
    3. Rall L. B.,
    4. Kirschner M. W.
    (1985) Autoregulation of tubulin synthesis in enucleated cells. Nature 317, 648–651
    OpenUrlCrossRefPubMed
    1. Cassimeris L.,
    2. Pryor N. K.,
    3. Salmon E. D.
    (1988) Real time observations of microtubule dynamic instability in living cells. J. Cell Biol 107, 2223–2231
    OpenUrlAbstract/FREE Full Text
    1. Church K.,
    2. Nicklas R. B.,
    3. Lin H.-P. P.
    (1986) Micromanipulated bivalents can trigger mini-spindle formation in Drosophila melanogaster spermatocyte cytoplasm. J. Cell Biol 103, 2765–2773
    OpenUrlAbstract/FREE Full Text
    1. Cleveland D. W.
    (1989) Autoregulated control of tubulin synthesis in animal cells. Curr. Opin. Cell Biol 1, 10–14
    OpenUrlCrossRefPubMed
    1. Cleveland D. W.,
    2. Hwo S.,
    3. Kirschner M. W.
    (1977) Purification of tau, a microtubule-associated protein that induces assembly from purified tubulin. J. Mol. Biol 116, 207–225
    OpenUrlCrossRefPubMedWeb of Science
    1. Cleveland D. W.,
    2. Lopata M. A.,
    3. Sherline P.,
    4. Kirschner M. W.
    (1981) Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25, 537–546
    OpenUrlCrossRefPubMedWeb of Science
    1. Diederich R. J.,
    2. Merrill V. K. L.,
    3. Pultz M. A.,
    4. Kaufman T. C.
    (1989) Isolation, structure and expression of labial, a homeotic gene of the Antennapedia Complex involved in Drosophila head development. Genes Dev 3, 399–414
    OpenUrlAbstract/FREE Full Text
    1. Drubin D. G.,
    2. Kirschner M. W.
    (1986) Tau protein function in living cells. J. Cell Biol 103, 2739–2746
    OpenUrlAbstract/FREE Full Text
    1. Foe V. E.,
    2. Alberts B. M.
    (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell. Sci 61, 1–70
    OpenUrlAbstract/FREE Full Text
    1. Freeman M.,
    2. Nusslein-Volhard C.,
    3. Glover D. M.
    (1986) The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell 46, 457–468
    OpenUrlCrossRefPubMedWeb of Science
    1. Glover D. M.
    (1989) Mitosis in Drosophila. J. Cell Sci 92, 137–146
    OpenUrlAbstract/FREE Full Text
    1. Guo L.-H.,
    2. Stepien P.,
    3. Tso J. Y.,
    4. Drousseau R.,
    5. Narang S.,
    6. Thomas D. Y.,
    7. Wu R.
    (1984) Synthesis of human insulin gene. VIII. Construction of expression vectors for fused proinsulin production in Escherichia coli. Gene 29, 251–254
    OpenUrlCrossRefPubMed
    1. Hays T. S.,
    2. Seuring R.,
    3. Robertson B.,
    4. Prout M.,
    5. Fuller M. T.
    (1989) Interacting proteins identified by genetic interactions: a missense mutation in-tubulin fails to complement alleles of the testis-specific -tubulin gene of Drosophila melanogaster. Mol. Cell. Biol 9, 875–884
    OpenUrlAbstract/FREE Full Text
    1. Horio T.,
    2. Hotani H.
    (1986) Visualization of the dynamic instability of individual microtubules by dark field microscopy. Nature 321, 605–607
    OpenUrlCrossRefPubMed
    1. Hoyle H. D.,
    2. Raff E. C.
    (1990) Two Drosophila beta tubulin isoforms are not functionally equivalent. J. Cell Biol 111, 1009–1026
    OpenUrlAbstract/FREE Full Text
    1. Joshi H. C.,
    2. Yen T. J.,
    3. Cleveland D. W.
    (1987) In vivo coassembly of a divergent beta-tubulin subunit (C6) into microtubules of different function. J. Cell Biol 105, 2179–2190
    OpenUrlAbstract/FREE Full Text
    1. Kalfayan L.,
    2. Wensink P. C.
    (1981) -Tubulin genes of Drosophila. Cell 24, 97–106
    OpenUrlCrossRefPubMed
    1. Kalfayan L.,
    2. Wensink P. C.
    (1982) Developmental regulation of Drosophila -tubulin genes. Cell 29, 91–98
    OpenUrlCrossRefPubMedWeb of Science
    1. Karr T. L.
    (1991) Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev 34, 101–112
    OpenUrlCrossRefPubMedWeb of Science
    1. Katz W.,
    2. Weinstein B.,
    3. Solomon F.
    (1990) Regulation of tubulin levels and microtubule assembly in Saccharomyces cerevisiae: Consequences of altered tubulin gene copy number. Mol. Cell. Biol 10, 5286–5294
    OpenUrlAbstract/FREE Full Text
    1. Leicht B. G.,
    2. Bonner J. J.
    (1988) Genetic analysis of the chromosomal region 67A-D of Drosophila melanogaster. Genetics 119, 579–593
    OpenUrlAbstract/FREE Full Text
    1. Lewis E. B.,
    2. Bacher F.
    (1968) Method of feeding ethyl methane sulfonate (EMS) to Drosophila males. Dros. Inform. Serv 43, 193–.
    OpenUrl
    1. Lewis S. A.,
    2. Wei G.,
    3. Cowan N. J.
    (1987) Free intermingling of mammalian-tubulin isotypes among functionally distinct microtubules. Cell 49, 539–548
    OpenUrlCrossRefPubMedWeb of Science
    1. Lewis S. A.,
    2. Ivanov I. E.,
    3. Lee G.-H.,
    4. Cowan N.
    (1989) Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342, 498–505
    OpenUrlCrossRefPubMed
    1. Lopata M. A.,
    2. Cleveland D. W.
    (1987) In vivo microtubules are copolymers of available isotypes: localization of each of six vertebrate-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J. Cell Biol 105, 1707–1720
    OpenUrlAbstract/FREE Full Text
    1. Mahaffey J. W.,
    2. Kaufman T. C.
    (1987) Distribution of the Sex combs reduced gene products in Drosophila melanogaster. Genetics 117, 51–60
    OpenUrlAbstract/FREE Full Text
    1. Mahowald A. P.,
    2. Goralski T. J.,
    3. Caulton J. H.
    (1983) In vitro activation of Drosophila eggs. Dev. Biol 98, 437–445
    OpenUrlCrossRefPubMedWeb of Science
    1. Matthews K. A.,
    2. Kaufman T. C.
    (1987) Developmental consequences of mutations in the 84B-tubulin gene of Drosophila melanogaster. Dev. Biol 119, 100–114
    OpenUrlCrossRefPubMed
    1. Matthews K. A.,
    2. Miller D. F. B.,
    3. Kaufman T. C.
    (1989) Developmental distribution of RNA and protein products of the Drosophila -tubulin gene family. Dev. Biol 132, 45–61
    OpenUrlCrossRefPubMedWeb of Science
    1. Matthews K. A.,
    2. Miller D. F. B.,
    3. Kaufman T. C.
    (1990) Functional implications of the unusual spatial distribution of a minor-tubulin isotype in Drosophila: a common thread among chordotonal ligaments, developing muscle and testis cyst cells. Dev. Biol 137, 171–183
    OpenUrlCrossRefPubMed
    1. Mischke D.,
    2. Pardue M. L.
    (1982) Organization and expression of-tubulin genes in Drosophila melanogaster. J. Mol. Biol 156, 449–466
    OpenUrlCrossRefPubMed
    1. Okabe S.,
    2. Hirokawa N.
    (1990) Turnover of fluorescently labelled tubulin and actin in the axon. Nature 343, 479–482
    OpenUrlCrossRefPubMed
    1. Pachter J. S.,
    2. Yen T. J.,
    3. Cleveland D. W.
    (1987) Autoregulation oftubulin expression is achieved through specific degradation of polysomal tubulin mRNAs. Cell 51, 283–292
    OpenUrlCrossRefPubMedWeb of Science
    1. Raff E. C.
    (1984) Genetics of microtubule systems. J. Cell Biol 99, 1–10
    OpenUrlAbstract/FREE Full Text
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Savage C.,
    2. Hamelin M.,
    3. Culotti J. G.,
    4. Coulson A.,
    5. Albertson D. G.,
    6. Chalfie M.
    (1989) mec-7 is a-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3, 870–881
    OpenUrlAbstract/FREE Full Text
    1. Serrano L.,
    2. Wandosell F.,
    3. Avila J.
    (1986) Location of the regions recognized by five commercial antibodies on the tubulin molecule. Analyt. Biochem 159, 253–259
    OpenUrlCrossRefPubMed
    1. Schatz P. J.,
    2. Solomon F.,
    3. Botstein D.
    (1986) Genetically essential and nonessential-tubulin genes specify functionally interchangable proteins. Mol. Cell. Biol 6, 3722–3733
    OpenUrlAbstract/FREE Full Text
    1. Theurkauf W. E.
    (1992) Behavior of a structurally divergent-tubulin isotype during Drosophila embryogenesis: Evidence for post-translational regulation of isotype abundance. Dev. Biol 154, 205–217
    OpenUrlCrossRefPubMed
    1. Theurkauf W. E.,
    2. Hawley R. S.
    (1992) Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J. Cell Biol 116, 1167–1180
    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. USA 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. Walker R. A.,
    2. O'Brien E. T.,
    3. Pryer N. K.,
    4. Soboeiro M. F.,
    5. Voter W. A.,
    6. Erickson H. P.,
    7. Salmon E. D.
    (1990) Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol 107, 1437–1448
    OpenUrlAbstract/FREE Full Text
    1. Warn R. M.,
    2. Warn A.
    (1986) Microtubule arrays present during the syncytial and cellular blastoderm stages of the early Drosophila embryo. Exp. Cell Res 163, 201–210
    OpenUrlCrossRefPubMed
    1. Yen T. J.,
    2. Gay D. A.,
    3. Pachter J. S.,
    4. Cleveland D. W.
    (1988) Autoregulated changes in stability of polyribosome-bound-tubulin mRNAs are specified by the first 13 translated nucleotides. Mol. Cell. Biol 8, 1224–1235
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
JOURNAL ARTICLES
A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila
K.A. Matthews, D. Rees, T.C. Kaufman
Development 1993 117: 977-991;
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

Interviews — Bénédicte Sanson and Kate Storey

Bénédicte Sanson and Kate Storey

Hear from Bénédicte Sanson, winner of the BSDB’s Cheryll Tickle medal, and Kate Storey, winner of the BSDB’s Waddington Medal, as they discuss their research, the future of the field and the importance of collaboration.

Review Commons launches

We're excited to be an affiliate journal for Review Commons, the ASAPbio/EMBO platform for high-quality journal-independent peer-review in the life sciences, which went live on 09 December.

Early-career researchers can apply for up to £2,500 to offset the cost of travel and expenses to make collaborative visits to other labs around the world. Read about Peter’s experience in Switzerland, where he joined forces with the Lutolf lab to refine a protocol for producing gastruloids.

Publishing peer review reports

To continue working towards transparency around the editorial process, Development now publishes a ‘Peer review history file’ alongside published papers. Read more about the policy and see the reports for yourself in one the first papers to publish the reports (under the ‘Info & metrics’ tab).

Development at a glance — Cell interactions in collective cell migration

Extract from the poster showing specific cell-cell interactions in metastasis.

Take a look at the latest poster and accompanying article by Denise Montell and her colleagues from the University of California, where they describe a sampling of both known and new cells that migrate collectively in vivo.