Advertisement
JOURNAL ARTICLES
The Drosophila kinesin-like protein KLP3A is required for proper behavior of male and female pronuclei at fertilization
B.C. Williams, A.F. Dernburg, J. Puro, S. Nokkala, M.L. Goldberg
Development 1997 124: 2365-2376;

Summary

Drosophila melanogaster females homozygous for mutations in the gene encoding the kinesin-like protein KLP3A are sterile (Williams et al., 1995). We have investigated the basis of this sterility. The eggs produced by KLP3A mutant mothers are fertilized by sperm, and female meiosis appears to occur normally. However, the large majority of these embryos arrest their development soon thereafter with a characteristic phenotype. The four nuclei produced by female meiosis associate together in a polar body-like structure, while a bipolar spindle is established around the metaphase-arrested male pronucleus. Thus, the major defect caused by depletion of the KLP3A protein is either in specification of the female pronucleus, or in migration of the male and female pronuclei toward each other. We have also found that the KLP3A protein is located throughout the metaphase spindle during meiosis and the early embryonic mitotic divisions, but later accumulates specifically at the midzone of these same spindles during telophase. The protein is also present on two other microtubule structures: the sperm aster; and the radial, monastral array of microtubules established between the two meiosis II spindles. We discuss these results in light of possible functions of the KLP3A protein in pronuclear specification and migration.

REFERENCES

    1. Baker B. S.,
    2. Carpenter A. T. C.
    (1972) Genetic analysis of sex chromosomal meiotic mutants in Drosophila melanogaster. Genetics 71, 255–286
    OpenUrlAbstract/FREE Full Text
    1. Callaini G.,
    2. Riparbelli M. G.
    (1996) Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev. Biol 176, 199–208
    OpenUrlCrossRefPubMedWeb of Science
    1. Das C. C.,
    2. Kaufman B. P.,
    3. Gay H.
    (1964). Histone protein transition in Drosophila melanogaster. II. Changes during early embryonic development. J. Cell Biol 23, 423–430
    OpenUrlAbstract/FREE Full Text
    1. Dernburg A. F.,
    2. Daily D. R.,
    3. Yook K. J.,
    4. Corbin J. A.,
    5. Sedat J. W.,
    6. Sullivan W.
    (1996) Selective loss of sperm bearing a compound chromosome in the Drosophila female. Genetics 143, 1629–1642
    OpenUrlAbstract/FREE Full Text
    1. Endow S. A.,
    2. Kang S. J.,
    3. Satterwhite L. L.,
    4. Rose M. D.,
    5. Skeen V. P.,
    6. Salmon E. D.
    (1994) Yeast Kar3 is a minus-end microtuble motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J 13, 2708–2713
    OpenUrlPubMedWeb of Science
    1. Freeman M.,
    2. Nusslein-Vollhard 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. Girdham C. H.,
    2. Glover D. M.
    (1991) Chromosome tangling and breakage at anaphase result from mutations in lodestar, a Drosophila gene encoding a putative nucleoside triphosphate binding protein. Genes Dev 5, 1786–1789
    OpenUrlAbstract/FREE Full Text
    1. Goldberg M. L.,
    2. Colvin R. A.,
    3. Mellin A. F.
    (1989) The Drosophila zeste locus is nonessential. Genetics 123, 145–155
    OpenUrlAbstract/FREE Full Text
    1. Goldstein L. S. B.
    (1993) With apologies to Scheherazade: tails of 1001 kinesin motors. Annu. Rev. Genet 27, 319–51
    OpenUrlCrossRefPubMedWeb of Science
    1. Gomes R.,
    2. Karess R.,
    3. Ohkura H.,
    4. Glover D. M.,
    5. Sunkel C. E.
    (1993) Abnormal anaphase resolution (aar): a locus required for progression through mitosis in Drosophila. J. Cell Sci 104, 583–593
    OpenUrlAbstract/FREE Full Text
    1. González C.,
    2. Saunders R. D. C.,
    3. Casal J.,
    4. Molina I.,
    5. Carmena M.,
    6. Ripoll P.,
    7. Glover D. M.
    (1990) Mutations in the asp locus of Drosophila lead to multiple free centrosomes in syncytial embryos, but restrict centrosome duplication in larval neuroblasts. J. Cell Sci 96, 605–616
    OpenUrlAbstract/FREE Full Text
    1. Goodson H. V.,
    2. Kang S. J.,
    3. Endow S. A.
    (1994) Molecular phylogeny of the kinesin family of microtubule motor proteins. J. Cell Sci 107, 1875–1884
    OpenUrlAbstract/FREE Full Text
    1. Hatsumi M.,
    2. Endow S. A.
    (1992) Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis. J. Cell Sci 101, 547–559
    OpenUrlAbstract/FREE Full Text
    1. Hsieh T.,
    2. Brutlag D.
    (1979). Sequence and sequence variation within the 1.688 g/cm3 satellite of Drosophila melanogaster. J. Mol. Biol 135, 465–481
    OpenUrlCrossRefPubMedWeb of Science
    1. Karr T. L.,
    2. Alberts B. M.
    (1986) Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol 102, 1494–1509
    OpenUrlAbstract/FREE Full Text
    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. McDonald H. B.,
    2. Stewart R. J.,
    3. Goldstein L. S. B.
    (1990) The kinesin-like ncd protein of Drosophila is a minus-end directed microtubule motor. Cell 63, 1159–1165
    OpenUrlCrossRefPubMedWeb of Science
    1. McKim K. S.,
    2. Jang J. K.,
    3. Theurkauf W. E.,
    4. Hawley R. S.
    (1993) Mechanical basis of meiotic metaphase arrest. Nature 362, 364–366
    OpenUrlCrossRefPubMed
    1. Mohler D.,
    2. Carroll A.
    (1984) Female sterile mutations in the Iowa collection. Dros. Info. Serv 60, 236–241
    OpenUrl
    1. Moore J. D.,
    2. Endow S. A.
    (1996) Kinesin proteins: a phylum of motors for microtubule-based motility. BioEssays 18, 207–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Perrimon N.,
    2. Engstrom. L.,
    3. Mahowald A. P.
    (1989) Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121, 333–352
    OpenUrlAbstract/FREE Full Text
    1. Puro J.,
    2. Nokkala S.
    (1977) Meiotic segregation of chromosomes in Drosophila melanogaster oocytes: a cytological approach. Chromosoma 63, 273–286
    OpenUrlCrossRefWeb of Science
    1. Riparbelli M. G.,
    2. Callaini G.
    (1996) Meiotic spindle organization in fertilized Drosophila oocyte: presence of centrosomal components in the meiotic apparatus. J. Cell Sci 109, 911–918
    OpenUrlAbstract/FREE Full Text
    1. Sekine Y.,
    2. Yasushi O.,
    3. Noda Y.,
    4. Kondo S.,
    5. Aizawa H.,
    6. Takemura R.,
    7. Hirokawa N.
    (1994) A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol 127, 187–201
    OpenUrlAbstract/FREE Full Text
    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. Thrower D. A.,
    2. Jordan M. A.,
    3. Schaar B. T.,
    4. Yen T. J.,
    5. Wilson L.
    (1995) Mitotic HeLa cells contain a CENP-E associated minus end-directed microtubule motor. EMBO J 14, 918–926
    OpenUrlPubMedWeb of Science
    1. Walker R. A.,
    2. Salmon E. D.,
    3. Endow S. A.
    (1990) The Drosophila claret segregation protein is a minus-end directed motor molecule. Nature 347, 780–782
    OpenUrlCrossRefPubMedWeb of Science
    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. Williams B. C.,
    2. Goldberg M. L.
    (1994) Determinants of Drosophila zw10 protein localization and function. J. Cell Sci 107, 785–798
    OpenUrlAbstract/FREE Full Text
    1. Williams B. C.,
    2. Riedy M. F.,
    3. Williams E. V.,
    4. Gatti M.,
    5. Goldberg M. L.
    (1995) The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis. J. Cell Biol 129, 709–723
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The Drosophila kinesin-like protein KLP3A is required for proper behavior of male and female pronuclei at fertilization
B.C. Williams, A.F. Dernburg, J. Puro, S. Nokkala, M.L. Goldberg
Development 1997 124: 2365-2376;
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

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

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.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

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.