Capu and Spire Assemble a Cytoplasmic Actin Mesh that Maintains Microtubule Organization in the Drosophila Oocyte

Dahlgaard, Katja; Raposo, Alexandre A.S.F.; Niccoli, Teresa; Johnston, Daniel St

doi:10.1016/j.devcel.2007.09.003

Cited by 152 publications

(251 citation statements)

References 47 publications

Supporting

Mentioning

225

Contrasting

Order By: Relevance

“…Actin has been thought to play an inhibitory role in ooplasmic streaming because depolymerization of F-actin by latrunculin A or cytochalasin D (64,65) or mutations of the actin regulators chickadee, cappuccino, and spire (64-69) cause premature streaming. However, both of these drug treatments and actin regulator mutations abolish only the cytoplasmic actin meshwork in stage 9-10A oocytes, whereas the cortical actin filaments remain intact (62). We confirmed these data and found that even very high concentrations of latrunculin B (up to 100 μM) failed to decrease phalloidin staining at the cortex, suggesting that cortical actin filaments, just like immobilized cortical microtubules, are extremely stable during mid-to late oogenesis.…”

Section: Discussionsupporting

confidence: 79%

“…Besides microtubules, actin filaments play an important role in streaming. Two subsets of F-actin have been described in the oocyte cytoplasm during midto late oogenesis (stages 9-11): a transient cytoplasmic meshwork assembled at stage 9 and disassembled at stage 10B and a more stable layer of cortical actin filaments that persisted from stage 9 to stage 11 (62,63). Actin has been thought to play an inhibitory role in ooplasmic streaming because depolymerization of F-actin by latrunculin A or cytochalasin D (64,65) or mutations of the actin regulators chickadee, cappuccino, and spire (64-69) cause premature streaming.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

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

View full text Add to dashboard Cite

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

show abstract

Section: Discussionsupporting

confidence: 79%

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

View full text Add to dashboard Cite

show abstract

“…Recently, Pfender et al (2011) found that Spire 1 and 2, another type of actin nucleators, cooperate with formin-2 to nucleate actin filaments in mouse oocytes. In Drosophila oocytes, Spire and Cappuccino (the fly formin-2) are required for establishing oocyte polarity by organizing an actin network, although the precise function of the actin network differs from that present in mouse oocytes [Dahlgaard et al, 2007;Quinlan et al, 2007]. In vitro biochemical studies have also established the interactions of these two types of actin nucleators [Bosch et al, 2007;Quinlan et al, 2007], but it remains to be determined how formin-2 and Spire synergize in vivo to nucleate actin filaments.…”

Section: Spindle Migration: Where and How The Force Is Generatedmentioning

confidence: 99%

Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation

2012

Cytoskeleton

104

View full text Add to dashboard Cite

Mammalian oocyte maturation involves two successive rounds of extremely asymmetric cell divisions (known as polar body extrusion) to generate a functional haploid egg. Successful polar body extrusion relies on establishment of an asymmetric spindle position and cortical polarity. Decades of studies using mouse oocytes as a model have revealed critical roles for a dynamic actin cytoskeleton in this process. Here, we review the contribution of actin to the critical events during oocyte meiotic cell divisions with an emphasis on recent advances in understanding the underlying molecular and physical mechanisms. V C 2012 Wiley Periodicals, Inc

show abstract

“…both induce premature ooplasmic streaming (5,6). Later it was shown that both proteins cooperate in the generation of a dynamic actin mesh in the oocyte that prevents premature ooplasmic streaming (7). Spire and Cappuccino do not solely have the same mutant phenotype; the proteins also physically interact and cross-regulate each other.…”

mentioning

confidence: 99%

Identification of a Short Spir Interaction Sequence at the C-terminal End of Formin Subgroup Proteins

Pechlivanis

Samol

Kerkhoff

2009

Journal of Biological Chemistry

View full text Add to dashboard Cite

The actin nucleation factors Spire and Cappuccino interact with each other and regulate essential cellular events during Drosophila oogenesis in a cooperative fashion. The interaction blocks formin actin nucleation activity and enhances the Spire activity. Analogous to Spire and Cappuccino, the mammalian homologs Spir-1 and formin-2 show a regulatory interaction. To get an understanding of the nature of the Spir-formin cooperation, we have analyzed the interaction biochemically and biophysically. Our data shows that the association of Spir-1 and formin-2 is not significantly mediated by binding of the Spir-1-KIND domain to the formin FH2 core domain. Instead, a short sequence motif C-terminal adjacent to the formin-2-FH2 domain could be characterized that mediates the interaction and is conserved among the members of the Fmn subgroup of formins. In line with this, we found that both mammalian Spir proteins, Spir-1 and Spir-2, interact with mammalian Fmn subgroup proteins formin-1 and formin-2.Basic cell biological functions such as proliferation, migration, division, and vesicle transport rely on the organization of the actin cytoskeleton. The initiation of actin polymerization from free actin monomers is regulated by actin nucleation factors (NF), 2 which help to overcome the kinetic barrier of spontaneous G-actin nucleation and, thus, catalyze the formation of filamentous actin structures and networks (1). To date, three different classes of NFs are described, the ARP2/3 complex, FH2 domain containing NFs of the formin superfamily, and NFs containing one or multiple WH2 domains (Spire/Cordonbleu/Leiomodin) (2). The formin superfamily is subdivided into seven subfamilies (Dia, FRL, DAAM, Delphilin, INF, FHOD, Fmn) (3). The mechanisms of actin nucleation as well as the regulation of the NFs vary significantly between the three classes (and also show variances in between the distinct superfamilies). Spire and Cappuccino are NFs that belong to the Spire subfamily of WH2 containing nucleators and to the Fmn subfamily of the FH2 domain containing formins, respectively. In contrast to the Arp2/3 complex that nucleates branched filaments, Spire and the formin Cappuccino nucleate unbranched actin filaments (4).Almost two decades ago it was found that mutants of the two Drosophila NFs (Spire/Cappuccino) have an identical phenotype in early Drosophila oogenesis, i.e. both induce premature ooplasmic streaming (5, 6). Later it was shown that both proteins cooperate in the generation of a dynamic actin mesh in the oocyte that prevents premature ooplasmic streaming (7). Spire and Cappuccino do not solely have the same mutant phenotype; the proteins also physically interact and cross-regulate each other. The Cappuccino C-terminal half, encoding the FH2 domain and flanking sequences, enhances the nucleation activity of Spire, whereas the nucleation activity of Cappuccino is decreased in the presence of the Spire-KIND domain (8).Cappuccino belongs to the Fmn subgroup of formins (3, 9). In mammals, two Fmn subgroup members (form...

show abstract

Capu and Spire Assemble a Cytoplasmic Actin Mesh that Maintains Microtubule Organization in the Drosophila Oocyte

Cited by 152 publications

References 47 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

Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation

Identification of a Short Spir Interaction Sequence at the C-terminal End of Formin Subgroup Proteins

Contact Info

Product

Resources

About