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Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis

Minestrini, Gianluca and Máthé, Endre and Glover, David M. (2002) Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis. Journal of Cell Science, 115 (4). pp. 725-736. ISSN 0021-9533. https://resolver.caltech.edu/CaltechAUTHORS:20200930-144136349

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Abstract

The kinesin-like protein encoded by pavarotti (Pav-KLP) is essential for cytokinesis and associates with the central part of the late mitotic spindle and interphase nuclei in somatic cells (Adams et al., 1988). Here we define regions of the molecule that regulate its subcellular localisation and study the consequences of overexpressing mutant forms of the protein during oogenesis in Drosophila. Pav-KLP normally associates with the oocyte nucleus, but when over-expressed at moderate levels, its GFP tagged form also accumulates in nurse cell nuclei. At high expression levels this leads to loss of the microfilaments that tether these nuclei, so that they block the ring canals and prevent the 'dumping' of nurse cell cytoplasm into the oocyte, which results in sterility. Localisation to these nuclei is prevented by mutations in either the conserved ATP-binding site of the motor domain or the nuclear localisation sequences in the C-terminal domain. Both such mutations lead to the formation of stable arrays of cytoplasmic microtubules and the progressive disruption of the actin cytoskeleton. The latter is evident by a breakdown of the cortical actin causing disruption of cell membranes; this breakdown ultimately results in the accumulation of cytoplasmic aggregates containing tubulin, actin and at least some of their binding proteins. Pav-KLP is also found associated with the ring canals, actin-rich structures built from remnants of the cytokinesis ring. The stalk domain alone is sufficient for the exclusive association of Pav-KLP to these structures, and this has no consequences for fertility. We discuss whether disruption of actin structures by full-length cytoplasmic forms of Pav-KLP is a consequence of the resulting stabilised cytoplasmic microtubules per se or accumulation of the motor protein at ectopic cortical sites to sequester molecules that regulate actin behaviour.


Item Type:Article
Related URLs:
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https://jcs.biologists.org/content/115/4/725.longPublisherArticle
ORCID:
AuthorORCID
Glover, David M.0000-0003-0956-0103
Additional Information:© The Company of Biologists Limited 2002. Accepted November 12, 2001. Published online February 15, 2002. We would like to thank Pernille Rorth for providing the pUASp vector, Daniel Kiehart for providing the anti-Myosin antibody and Daniel St Johnston for the anti-Staufen antibody and the α4 tubulin-driven GAL4-VP16 line. We are grateful for a Programme Grant from the Cancer Research Campaign, and to the European Union, which supported Gianluca Minestrini through a Training Network.
Funders:
Funding AgencyGrant Number
Cancer Research CampaignUNSPECIFIED
Marie Curie FellowshipUNSPECIFIED
Subject Keywords:Pavarotti, MKLP-1, Actinomyosin, Drosophila oogenesis, Contractile rings
Issue or Number:4
Record Number:CaltechAUTHORS:20200930-144136349
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200930-144136349
Official Citation:Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis Gianluca Minestrini, Endre Máthé, David M. Glover Journal of Cell Science 2002 115: 725-736
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105695
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Oct 2020 13:43
Last Modified:01 Oct 2020 13:43

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