Roles of Bifocal, Homer, and F-actin in anchoring Oskar to the posterior cortex of <i>Drosophila</i> oocytes

Babu, Kavita; Cai, Yu; Bahri, Sami M.; Yang, Xiaohang; Chia, William

doi:10.1101/gad.282604

Cited by 54 publications

(57 citation statements)

References 36 publications

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“…How are the stable microtubules anchored to the cortex? The oocyte cortex has a dense layer of F-actin that has been proposed to anchor mRNA and proteins (37). Therefore, we decided to examine the distribution of F-actin and microtubules in stage 10B oocytes.…”

Section: Sliding Between Cortically Anchored Microtubules and Free Cymentioning

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: Sliding Between Cortically Anchored Microtubules and Free Cymentioning

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 anchoring of Short Oskar and associated pole plasm depends on F-actin and Long Oskar (Jankovics et al 2002;Polesello et al 2002;Vanzo and Ephrussi 2002;Babu et al 2004). In addition, the localization of Oskar to either the anterior or posterior of the oocyte induces the formation of actin filaments from the adjacent cortex (Vanzo et al 2007;Tanaka and Nakamura 2008).…”

Section: Discussionmentioning

confidence: 99%

Anterior–Posterior Axis Specification in Drosophila Oocytes: Identification of Novel bicoid and oskar mRNA Localization Factors

Chang¹,

Nashchekin²,

Wheatley

et al. 2011

Genetics

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The Drosophila melanogaster anterior-posterior axis is established during oogenesis by the localization of bicoid and oskar mRNAs to the anterior and posterior poles of the oocyte. Although genetic screens have identified some trans-acting factors required for the localization of these transcripts, other factors may have been missed because they also function at other stages of oogenesis. To circumvent this problem, we performed a screen for revertants and dominant suppressors of the bicaudal phenotype caused by expressing Miranda-GFP in the female germline. Miranda mislocalizes oskar mRNA/Staufen complexes to the oocyte anterior by coupling them to the bicoid localization pathway, resulting in the formation of an anterior abdomen in place of the head. In one class of revertants, Miranda still binds Staufen/oskar mRNA complexes, but does not localize to the anterior, identifying an anterior targeting domain at the N terminus of Miranda. This has an almost identical sequence to the N terminus of vertebrate RHAMM, which is also a large coiled-coil protein, suggesting that it may be a divergent Miranda ortholog. In addition, we recovered 30 dominant suppressors, including multiple alleles of the spectroplakin, short stop, a lethal complementation group that prevents oskar mRNA anchoring, and a female sterile complementation group that disrupts the anterior localization of bicoid mRNA in late oogenesis. One of the single allele suppressors proved to be a mutation in the actin nucleator, Cappuccino, revealing a previously unrecognized function of Cappuccino in pole plasm anchoring and the induction of actin filaments by Long Oskar protein.

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“…When oocytes are treated with an actin polymerization inhibitor, cytochalasin D, or are deficient in any of several actin-binding proteins, such as Moesin, Bifocal and Homer, pole plasm components are not properly anchored to the posterior cortex. 6,[17][18][19] Interestingly, Osk is reported to remodel cortical F-actin as long F-actin projections from the posterior cortex of the oocyte.…”

Section: Osk-induced Rearrangement Of F-actinmentioning

confidence: 99%

“…In contrast, mon2-deficient oocytes show milder defects in pole plasm anchoring compared to rbsn-5 or rab5-deficient oocytes, and treatment with actin inhibitors such as cytochalasin D or latrunculin A causes similar mild defects in pole plasm anchoring. 6,19 Mon2 is therefore required only for F-actin rearrangement during pole plasm assembly. In other words, Mon2 is specifically involved in the third feedback loop.…”

Section: Actin Remodelers That Act Downstream Of Oskmentioning

confidence: 99%

Oskar-induced endocytic activation and actin remodeling for anchorage of the Drosophila germ plasm

Tanaka¹,

Nakamura²

2011

BioArchitecture

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and akiran@cdb.riken.jp i n many animals, germ-cell fate is specified by inheritance of the germ plasm, which is enriched in maternal rnas and proteins. assembly of the drosophila germ (pole) plasm begins with the localization and translation of oskar (osk) rna at the oocyte posterior pole. osk rna produces two isoforms, long and short osk. short osk recruits other pole plasm components, and long osk restricts them to the oocyte cortex. although molecular functions of long osk remain mysterious, it is known to be involved in endocytic activation and actin cytoskeletal remodeling. We identified several vesicular trafficking machinery components that act downstream of long osk in pole plasm assembly. these included the rab5 effector protein rabenosyn-5 (rbsn-5) and the Golgi/endosomal protein mon2, both of which were crucial for osk-induced actin remodeling and the anchoring of pole plasm components. We propose that, in response to long osk, the rab5/rbsn-5-dependent endocytic pathway promotes the formation of specialized vesicles, and mon2 acts on these vesicles as a scaffold to instruct actin nucleators like cappuccino and spire to remodel the actin cytoskeleton, which anchors pole plasm components to the cortex. this mechanism may be applicable to the asymmetric localization of macromolecular structures such as protein-rna complexes in other systems. Drosophila Germ Plasm AssemblyThe assembly of the germ (pole) plasm in Drosophila oogenesis is a useful model

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Roles of Bifocal, Homer, and F-actin in anchoring Oskar to the posterior cortex of Drosophila oocytes

Cited by 54 publications

References 36 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

Anterior–Posterior Axis Specification in Drosophila Oocytes: Identification of Novel bicoid and oskar mRNA Localization Factors

Oskar-induced endocytic activation and actin remodeling for anchorage of the Drosophila germ plasm

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