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Differing requirements for Augmin in male meiotic and mitotic spindle formation in Drosophila

Savoian, Matthew S. and Glover, David M. (2014) Differing requirements for Augmin in male meiotic and mitotic spindle formation in Drosophila. Open Biology, 4 (5). Art. No. 140047. ISSN 2046-2441. PMCID PMC4042853. doi:10.1098/rsob.140047. https://resolver.caltech.edu/CaltechAUTHORS:20200807-114541570

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Abstract

Animal cells divide using a microtubule-based, bipolar spindle. Both somatic, mitotic cells and sperm-producing male meiotic spermatocytes use centrosome-dependent and acentrosomal spindle-forming mechanisms. Here, we characterize the largely undefined, centrosome-independent spindle formation pathway used during male meiosis. Our live and fixed cell analyses of Drosophila spermatocytes reveal that acentrosomal microtubules are nucleated at kinetochores and in the vicinity of chromatin and that together these assemble into functional spindles. Mutational studies indicate that γ-tubulin and its extra-centrosomal targeting complex, Augmin, are vital for this process. In addition, Augmin facilitates efficient spindle assembly in the presence of centrosomes. In contrast to the pronounced recruitment of Augmin on spindles in other cell types, the complex is absent from those of spermatocytes but does accumulate on kinetochores. Polo kinase facilitates this kinetochore recruitment while inhibiting Augmin's spindle association, and this in turn dictates γ-tubulin distribution and spindle density. Polo's negative regulation of Augmin in male meiosis contrasts with its requirement in loading Augmin along mitotic spindles in somatic Drosophila cells. Together our data identify a novel mechanism of acentrosomal spindle formation in spermatocytes and reveal its divergence from that used in mitotic cells.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1098/rsob.140047DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4042853/PubMed CentralArticle
ORCID:
AuthorORCID
Savoian, Matthew S.0000-0002-2594-3879
Glover, David M.0000-0003-0956-0103
Additional Information:© 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. Received: 11 March 2014. Accepted: 14 April 2014. We would like to thank the following for their kind gift of reagents: H. Ohkura and J. Wakefield for flies and G. Goshima and P. Somma for providing Dgt5 and Dgt6 antibodies, respectively. We acknowledge the Segal and Glover laboratories for insightful discussions and Zs. Venkei and Y. Ladak for allowing us to use the Aurora B::mCherry flies prior to publication. M.S.S. designed, carried out and analysed the experiments. The authors declare they have no competing financial interests. This work was made possible by a CRUK Programme Grant to D.M.G.
Funders:
Funding AgencyGrant Number
Cancer Research UKUNSPECIFIED
Subject Keywords:division, γ-tubulin, microtubule, spermatocyte, kinetochore, nucleation
Issue or Number:5
PubMed Central ID:PMC4042853
DOI:10.1098/rsob.140047
Record Number:CaltechAUTHORS:20200807-114541570
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200807-114541570
Official Citation:Savoian Matthew S. and Glover David M. 2014Differing requirements for Augmin in male meiotic and mitotic spindle formation in Drosophila Open Biol. 4:140047 http://doi.org/10.1098/rsob.140047
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104832
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:10 Aug 2020 14:57
Last Modified:16 Nov 2021 18:36

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