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Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans
G. Callaini, R. Dallai, M.G. Riparbelli
Journal of Cell Science 1997 110: 271-280;

Summary

The behavior of parental chromosomes during the first mitosis of Drosophila simulans zygotes obtained from unidirectional incompatible crosses is described and it is demonstrated that the condensation of parental chromatin complements was asynchronous. The timing of paternal chromatin condensation appeared to be delayed in these embryos, so that condensed maternal chromosomes and entangled prophase-like paternal fibers congressed in the equatorial plane of the first metaphase spindle. At anaphase the maternal chromosomes migrated to opposite poles of the spindle, whereas the paternal chromatin lagged in the midzone of the spindle. This resulted in dramatic errors in paternal chromatin inheritance leading to the formation of embryos with aneuploid or haploid nuclei. These observations suggest that the anaphase onset of maternal chromosomes is unaffected by the improper alignment of the paternal complement. Since the first metaphase spindle of the Drosophila zygote consists of twin bundles of microtubules each holding one parental complement, we suspect that each half spindle regulates the timing of anaphase onset of its own chromosome set. In normal developing embryos, the fidelity of chromosome transmission is presumably ensured by the relative timing required to prepare parental complements for the orderly segregation that occurs during the metaphase-anaphase transition.

REFERENCES

    1. Andreassen P. R. and
    2. Margolis R. L.
    (1991). Chromosome motion during attachment to the vertebrate spindle: initial saltatory-like behavior of chromosomes and quantitative analysis of force production by nascent kinetochore fibers. J. Cell Sci 100, 299–310
    OpenUrlAbstract/FREE Full Text
    1. Boyle L.,
    2. O'Neill S. L.,
    3. Robertson H. M. and
    4. Karr T. L.
    (1993). Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260, 1796–1799
    OpenUrlAbstract/FREE Full Text
    1. Breeuwer J. A. J. and
    2. Werren J. H.
    (1990). Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346, 558–560
    OpenUrlCrossRefPubMedWeb of Science
    1. Bressac C. and
    2. Rousset F.
    (1993). The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbiont in sperm cysts. J. Invertebr. Pathol 61, 226–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Buchenau P.,
    2. Saumweber H. and
    3. Arndt-Jovin D. J.
    (1993). Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning confocal microscopy. J. Cell Sci 104, 1175–1185
    OpenUrlAbstract/FREE Full Text
    1. Callaini G. and
    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. Callaini G.,
    2. Riparbelli M. G.,
    3. Giordano R. and
    4. Dallai R.
    (1996). Mitotic defects associated with cytoplasmic incompatibility in Drosophila simulans. J. Invertebr. Pathol 67, 55–64
    OpenUrlCrossRefWeb of Science
    1. Clarke D. J.,
    2. Johnson R. T. and
    3. Downes C. S.
    (1993). Topoisomerase II inhibition prevents anaphase chromatid segregation in mammalian cells independently of the generation of DNA strand breaks. J. Cell Sci 105, 563–569
    OpenUrlAbstract/FREE Full Text
    1. Earnshaw W. C. and
    2. MacKay A. M.
    (1994). Role of nonhistone proteins in the chromosomal events of mitosis. FASEB J 8, 947–956
    OpenUrlAbstract
    1. Freeman M.,
    2. Nusslein-Volhard C. and
    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. Gard D. L.,
    2. Hafezi S.,
    3. Zhang T. and
    4. Doxsey S. J.
    (1990). Centrosome duplication continues in cycloheximide-treated Xenopus blastulae in the absence of a detectable cell cycle. J. Cell Biol 110, 2033–2042
    OpenUrlAbstract/FREE Full Text
    1. Gatti M.,
    2. Pimpinelli S. and
    3. Santini G.
    (1976). Characterization of Drosophila heterochromatin. I. Staining and decondensation with Hoechst 33258 and quinacrine. Chromosoma 57, 351–375
    OpenUrlCrossRefPubMedWeb of Science
    1. Giloh H. and
    2. Sedat J. W.
    (1982). Fluorescence microscopy: Reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science 217, 1252–1255
    OpenUrlAbstract/FREE Full Text
    1. Giordano R.,
    2. O'Neill S. and
    3. Robertson H. M.
    (1995). Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophilasechellia and D. mauritiana. Genetics 140, 1307–1317
    OpenUrlAbstract/FREE Full Text
    1. Gomes R.,
    2. Karess R. E.,
    3. Ohkura H.,
    4. Glover D. M. and
    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. Gorbsky G. J. and
    2. Ricketts W. A.
    (1993). Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J. Cell Biol 122, 1311–1321
    OpenUrlAbstract/FREE Full Text
    1. Gorbsky G. J.
    (1994). Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of the topoisomerase II inhibitors ICRF-187 ((+)-1, 2-bis-(3, 5-dioxopiperazinyl-1-yl) propane; ADR-529) and ICRF-159 (Razoxane). Cancer Res 54, 1042–1048
    OpenUrlAbstract/FREE Full Text
    1. Hartwell L. H. and
    2. Weinert T. A.
    (1989). Checkpoints: controls that ensure the order of the cell cycle events. Science 246, 629–634
    OpenUrlAbstract/FREE Full Text
    1. Hoffmann A. A.,
    2. Turelli M. and
    3. Simmons G. M.
    (1986). Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40, 692–701
    OpenUrlCrossRefWeb of Science
    1. Hoffmann A. A.,
    2. Turelli M. and
    3. Harshman L. G.
    (1990). Factors affecting the distribution of cytoplasmic incompatibility in Drosophilasimulans. Genetics 126, 933–948
    OpenUrlAbstract/FREE Full Text
    1. Hoyt M. A.,
    2. Trotis L. and
    3. Roberts B. T.
    (1991). S. cerevisiae genes requiredfor cell cycle arrest in response to loss of microtubule function. Cell 66, 507–517
    OpenUrlCrossRefPubMedWeb of Science
    1. Humphrey T. and
    2. Enoch T.
    (1995). Keeping mitosis in check. Curr. Biol 5, 376–379
    OpenUrlCrossRefPubMed
    1. Jost E.
    (1970). Genetische Untersuchungen zur Inkompatibilität im Culex pipiens -complex. Theor. Appl. Genet 40, 251–256
    OpenUrl
    1. Kaufmann W. K. and
    2. Paules R. S.
    (1996). DNA damage and cell cycle checkpoints. FASEB J 10, 238–247
    OpenUrlAbstract
    1. Kimelman D.,
    2. Kirschner M. and
    3. Scherson T.
    (1987). The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48, 399–407
    OpenUrlCrossRefPubMedWeb of Science
    1. Larsen P. M. and
    2. Wolniak S. M.
    (1993). Asynchronous entry into anaphase induced by okadaic acid: spindle organization and microtubule/kinetochore attachments. Protoplasma 177, 53–65
    OpenUrlCrossRef
    1. Lassy C. W. and
    2. Karr T. L.
    (1996). Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech. Dev 57, 47–58
    OpenUrlCrossRefPubMedWeb of Science
    1. Li R. and
    2. Murray A. W.
    (1991). Feedback control of mitosis in budding yeast. Cell 66, 519–531
    OpenUrlCrossRefPubMedWeb of Science
    1. McIntosh J. R.
    (1991). Structural and mechanical control of mitotic progression. Cold Spring Harbor Symp. Quant. Biol 55, 613–619
    OpenUrl
    1. Minden J. S.,
    2. Agard D. A.,
    3. Sedat J. W. and
    4. Alberts B. M.
    (1989). Direct cell lineage analysis in Drosophilamelanogaster by time-lapse three-dimensional optical microscopy of living embryos. J. Cell Biol 109, 505–516
    OpenUrlAbstract/FREE Full Text
    1. Murray A. W.
    (1992). Creative blocks: cell-cycle checkpoints and feedback controls. Nature 359, 599–604
    OpenUrlCrossRefPubMedWeb of Science
    1. Murray A. W.
    (1994). Cell cycle checkpoints. Curr. Opin. Cell Biol 6, 872–876
    OpenUrlCrossRefPubMedWeb of Science
    1. Nagano H.,
    2. Hirai S.,
    3. Okano K. and
    4. Ikegami S.
    (1981). Achromosomal cleavage of fertilized starfish embryos in the presence of aphidicolin. Dev. Biol 85, 409–415
    OpenUrlCrossRefPubMed
    1. Ner S. S. and
    2. Travers A. A.
    (1994). HMG-D, the Drosophilamelanogaster homologue of HMG 1 protein, is associated with early embryonic chromatin in the absence of histone H1. EMBOJ 13, 1817–1822
    OpenUrlPubMedWeb of Science
    1. Nicklas R. B.,
    2. Krawitz L. E. and
    3. Ward S. C.
    (1993). Odd chromosome movement and inaccurate chromosome distribution in mitosis and meiosis after treatment with protein kinase inhibitors. J. Cell Sci 104, 961–973
    OpenUrlAbstract/FREE Full Text
    1. O'Neill S. L. and
    2. Karr T. L.
    (1990). Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348, 178–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Raff J. W. and
    2. Glover D. M.
    (1988). Nuclear and cytoplasmic mitotic cyclescontinue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J. Cell Biol 107, 2009–2019
    OpenUrlAbstract/FREE Full Text
    1. Reed K. M. and
    2. Werren J. H.
    (1995). Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Rep. Dev 40, 408–418
    OpenUrlCrossRefPubMedWeb of Science
    1. Reeves R.
    (1992). Chromatin changes during the cell cycle. Curr. Opin. Cell Biol 4, 413–423
    OpenUrlCrossRefPubMed
    1. Rieder C. L.,
    2. Schultz A.,
    3. Cole R. and
    4. Sluder G.
    (1994). Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol 127, 1301–1310
    OpenUrlAbstract/FREE Full Text
    1. Ryan S. and
    2. Saul G.
    (1968). Post-fertilization effect of incompatibility factors in Mormoniella. Mol. Gen. Genet 103, 29–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Shamansky F. L. and
    2. Orr-Weaver T. L.
    (1991). The Drosophilaplutonium and pan gu genes regulate entry into S phase at fertilization. Cell 66, 1289–1300
    OpenUrlCrossRefPubMedWeb of Science
    1. Sluder G. and
    2. Levis K.
    (1987). Relationship between nuclear DNA synthesis and centrosome reproduction in sea urchin eggs. J. Exp. Zool 244, 89–100
    OpenUrlCrossRefPubMedWeb of Science
    1. Sluder G.,
    2. Miller F. J.,
    3. Thompson E. A. and
    4. Wolf D. E.
    (1994). Feedback control of the metaphase-anaphase transition in sea urchin zygotes: role of maloriented chromosomes. J. Cell Biol 126, 189–198
    OpenUrlAbstract/FREE Full Text
    1. Sullivan W.,
    2. Minden J. S. and
    3. Alberts B. M.
    (1990). daughterless-abo-like, a Drosophila maternal-effect mutation that exhibits abnormal centrosome separation during late blastoderm divisions. Development 110, 311–323
    OpenUrlAbstract/FREE Full Text
    1. Sullivan W.,
    2. Daily D. R.,
    3. Fogarty P.,
    4. Yook K. J. and
    5. Pimpinelli S.
    (1993). Delays in anaphase initiation occur in individual nuclei of the syncytial Drosophila embryo. Mol. Biol. Cell 4, 885–896
    OpenUrlAbstract/FREE Full Text
    1. Swedlow J. R.,
    2. Sedat J. W. and
    3. Agard D. A.
    (1993). Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three-dimensional wide-field microscopy. Cell 73, 97–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Weinert T. A. and
    2. Hartwell L. H.
    (1988). The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241, 317–322
    OpenUrlAbstract/FREE Full Text
    1. Zalokar M. and
    2. Erk I.
    (1977). Phase-partition fixation and staining of Drosophila eggs. Stain Technol 52, 89–95
    OpenUrlPubMed
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Journal Articles
Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans
G. Callaini, R. Dallai, M.G. Riparbelli
Journal of Cell Science 1997 110: 271-280;
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