A functional link between localized Oskar, dynamic microtubules, and endocytosis

Sanghavi, Paulomi; Lu, Sumin; Gonsalvez, Graydon B.

doi:10.1016/j.ydbio.2012.04.024

Cited by 12 publications

(18 citation statements)

References 67 publications

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“…Oocytes contain many different populations of microtubules that reorganize and change throughout different developmental stages. The microtubule network is initially polarized during early stages, with the majority of plus-ends at the posterior pole and minus-ends at the anterior pole (55,56), but later becomes less organized, with minus-ends associating with the cortex (31,(57)(58)(59)(60)(61). Microtubules are also concentrated at the posterior pole during early stages, and these microtubules reorganize and relocate to the anterior pole during stages 8-10A, forming a gradient of microtubules from anterior to posterior.…”

Section: Discussionmentioning

confidence: 99%

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Lü

Winding

Lakonishok

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

122

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Cytoplasmic streaming in Drosophila oocytes is a microtubulebased bulk cytoplasmic movement. Streaming efficiently circulates and localizes mRNAs and proteins deposited by the nurse cells across the oocyte. This movement is driven by kinesin-1, a major microtubule motor. Recently, we have shown that kinesin-1 heavy chain (KHC) can transport one microtubule on another microtubule, thus driving microtubule-microtubule sliding in multiple cell types. To study the role of microtubule sliding in oocyte cytoplasmic streaming, we used a Khc mutant that is deficient in microtubule sliding but able to transport a majority of cargoes. We demonstrated that streaming is reduced by genomic replacement of wild-type Khc with this sliding-deficient mutant. Streaming can be fully rescued by wild-type KHC and partially rescued by a chimeric motor that cannot move organelles but is active in microtubule sliding. Consistent with these data, we identified two populations of microtubules in fast-streaming oocytes: a network of stable microtubules anchored to the actin cortex and free cytoplasmic microtubules that moved in the ooplasm. We further demonstrated that the reduced streaming in sliding-deficient oocytes resulted in posterior determination defects. Together, we propose that kinesin-1 slides free cytoplasmic microtubules against cortically immobilized microtubules, generating forces that contribute to cytoplasmic streaming and are essential for the refinement of posterior determinants.kinesin-1 | microtubules | cytoplasmic streaming | Drosophila | axis determination

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Section: Discussionmentioning

confidence: 99%

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Lü

Winding

Lakonishok

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

122

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“…The first marker used was an antibody against End binding protein 1 (Eb1), a highly conserved plus-end binding protein (Schuyler and Pellman 2001). In wild-type egg chambers, Eb1 foci were detected throughout the oocyte, with enrichment at the posterior pole (Sanghavi et al 2012) (Figure 6D). In Egl-depleted egg chambers, Eb1 foci were scattered throughout the oocyte with no obvious enrichment at the posterior pole ( Figure 6E).…”

Section: Microtubule Organization Is Disrupted Upon Depletion Of Eglmentioning

confidence: 98%

“…Prior to this, oocyte microtubules are arranged with minus ends enriched at the posterior pole (Theurkauf et al 1992). However, the redistribution of microtubules that takes place in response to Grk signaling results in minus ends enriched along the anterior and lateral cortex and plus ends that display a slight enrichment at the posterior pole of the oocyte (Theurkauf et al 1992;Clark et al 1994Clark et al , 1997Parton et al 2011;Sanghavi et al 2012). This reorganization is required for migration of the oocyte nucleus from the posterior to the anterior of the oocyte (Gonzalez-Reyes et al 1995;Roth et al 1995) (Figure 1A).…”

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confidence: 99%

Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

et al. 2016

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The Drosophila egg chamber provides a useful model for examining mechanisms by which cell fates are specified and maintained in the context of a complex tissue. The egg chamber is also an excellent model for understanding the mechanism by which cytoskeletal filaments are organized and the critical interplay between cytoskeletal organization, polarity establishment, and cell fate specification. Previous work has shown that Egalitarian (Egl) is required for specification and maintenance of oocyte fate. Mutants in egl either completely fail to specify an oocyte, or if specified, the oocyte eventually reverts back to nurse cell fate. Due to this very early role for Egl in egg chamber maturation, it is unclear whether later stages of egg chamber development also require Egl function. In this report, we have depleted Egl at specific stages of egg chamber development. We demonstrate that in early-stage egg chambers, Egl has an additional role in organization of oocyte microtubules. In the absence of Egl function, oocyte microtubules completely fail to reorganize. As such, the localization of microtubule motors and their cargo is disrupted. In addition, Egl also appears to function in regulating the translation of critical polarity determining messenger RNAs (mRNAs). Finally, we demonstrate that in midstage egg chambers, Egl does not appear to be required for microtubule organization, but rather for the correct spatial localization of oskar, bicoid, and gurken mRNAs.

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“…Imaging was with a Leica TCS-SP2 confocal microscope. Mouse anti-α-tubulin DM1A staining of ovaries is described by Sato et al (Sato et al, 2011) and EB1 staining by Sanghavi et al (Sanghavi et al, 2012).…”

Section: Immunostainingmentioning

confidence: 99%

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

et al. 2014

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Bicaudal-D (Bic-D), Egalitarian (Egl), microtubules and their motors form a transport machinery that localizes a remarkable diversity of mRNAs to specific cellular regions during oogenesis and embryogenesis. Bic-D family proteins also promote dynein-dependent transport of Golgi vesicles, lipid droplets, synaptic vesicles and nuclei. However, the transport of these different cargoes is still poorly understood. We searched for novel proteins that either mediate Bic-Ddependent transport processes or are transported by them. Clathrin heavy chain (Chc) co-immunopurifies with Bic-D in embryos and ovaries, and a fraction of Chc colocalizes with Bic-D. Both proteins control posterior patterning of the Drosophila oocyte and endocytosis. Although the role of Chc in endocytosis is well established, our results show that Bic-D is also needed for the elevated endocytic activity at the posterior of the oocyte. Apart from affecting endocytosis indirectly by its role in osk mRNA localization, Bic-D is also required to transport Chc mRNA into the oocyte and for transport and proper localization of Chc protein to the oocyte cortex, pointing to an additional, more direct role of Bic-D in the endocytic pathway. Furthermore, similar to Bic-D, Chc also contributes to proper localization of osk mRNA and to oocyte growth. However, in contrast to other endocytic components and factors of the endocytic recycling pathway, such as Rabenosyn-5 (Rbsn-5) and Rab11, Chc is needed during early stages of oogenesis (from stage 6 onwards) to localize osk mRNA correctly. Moreover, we also uncovered a novel, presumably endocytosis-independent, role of Chc in the establishment of microtubule polarity in stage 6 oocytes.

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A functional link between localized Oskar, dynamic microtubules, and endocytosis

Cited by 12 publications

References 67 publications

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber

Clathrin heavy chain plays multiple roles in polarizing the Drosophila oocyte downstream of Bic-D

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