Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes

In many animal species the meiosis I spindle in oocytes is anastral and lacks centrosomes. Previous studies of Drosophila oocytes failed to detect the native form of the germline-specific γ-tubulin (γTub37C) in meiosis I spindles, and genetic studies have yielded conflicting data regarding the role...

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Published in:PLoS genetics Vol. 7; no. 8; p. e1002209
Main Authors: Hughes, Stacie E, Beeler, J Scott, Seat, Angela, Slaughter, Brian D, Unruh, Jay R, Bauerly, Elisabeth, Matthies, Heinrich J G, Hawley, R Scott
Format: Journal Article
Language:English
Published: United States Public Library of Science 01-08-2011
Public Library of Science (PLoS)
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Summary:In many animal species the meiosis I spindle in oocytes is anastral and lacks centrosomes. Previous studies of Drosophila oocytes failed to detect the native form of the germline-specific γ-tubulin (γTub37C) in meiosis I spindles, and genetic studies have yielded conflicting data regarding the role of γTub37C in the formation of bipolar spindles at meiosis I. Our examination of living and fixed oocytes carrying either a null allele or strong missense mutation in the γtub37C gene demonstrates a role for γTub37C in the positioning of the oocyte nucleus during late prophase, as well as in the formation and maintenance of bipolar spindles in Drosophila oocytes. Prometaphase I spindles in γtub37C mutant oocytes showed wide, non-tapered spindle poles and disrupted positioning. Additionally, chromosomes failed to align properly on the spindle and showed morphological defects. The kinetochores failed to properly co-orient and often lacked proper attachments to the microtubule bundles, suggesting that γTub37C is required to stabilize kinetochore microtubule attachments in anastral spindles. Although spindle bipolarity was sometimes achieved by metaphase I in both γtub37C mutants, the resulting chromosome masses displayed highly disrupted chromosome alignment. Therefore, our data conclusively demonstrate a role for γTub37C in both the formation of the anastral meiosis I spindle and in the proper attachment of kinetochore microtubules. Finally, multispectral imaging demonstrates the presences of native γTub37C along the length of wild-type meiosis I spindles.
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Conceived and designed the experiments: SEH RSH HJGM BDS JRU. Performed the experiments: SEH JSB AS EB BDS JRU. Analyzed the data: SEH BDS JRU. Wrote the paper: SEH RSH BDS JRU. Designed figures and tables: AS.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1002209