<i>Drosophila</i>Mon2 couples Oskar-induced endocytosis with actin remodeling for cortical anchorage of the germ plasm

Tanaka, Tsubasa; Kato, Yasuko; Matsuda, Kazuki; Hanyu-Nakamura, Kazuko; Nakamura, Akira

doi:10.1242/dev.062208

Cited by 43 publications

(54 citation statements)

References 48 publications

(82 reference statements)

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“…Given that Capu and Spir are actin nucleators that can directly regulate actin remodeling, they are likely to act downstream of Mon2 in the genetic hierarchy for pole plasm anchoring to the oocyte cortex. 16 We also found that the small GTPase Rho1, which forms a complex with Capu and Spir to regulate their actin nucleation activity, is highly concentrated at the oocyte posterior. 16 Furthermore, this posterior concentration of Rho1 requires Mon2, indicating that Mon2 might regulate the Capu/Spir activity to remodel cortical F-actin.…”

mentioning

confidence: 64%

“…13 This defect was also observed in rab5 mutant oocytes. 16 These data clearly demonstrated that the endocytic pathway is required for the anchorage of pole plasm components to the oocyte cortex ( fig. 2).…”

Section: Osk-induced Rearrangement Of F-actinmentioning

confidence: 76%

“…We found that, in rbsn-5 or rab5 oocytes, ectopic anteriorly localized Osk did not induce the long F-actin projections, and instead caused aberrant F-actin aggregates, which diffused into the cytoplasm, often engulfing pole plasm components. 13,16 These results revealed a novel role of the endocytic F-actin structures nor F-actin projections. Instead, the ectopic Osk induced faint F-actin granules, as observed in the mon2 single mutant.…”

mentioning

confidence: 80%

“…From the same genetic screen, however, we identified the Golgi/endosomal protein Mon2 as a factor involved in this process. 16 In oocytes lacking Mon2, the initial accumulation of GFP-Vas and other pole plasm components at the posterior pole was intact, but their localization was not maintained, resulting in their complete loss from the posterior pole in late-stage oocytes. Yeast Mon2p (Ysl2p) forms a plasm assembly.…”

Section: Osk-induced Rearrangement Of F-actinmentioning

confidence: 99%

“…13,16,20 Furthermore, when only long or short Osk is misexpressed at the anterior pole of the oocyte, only long Osk induces the ectopic F-actin projections, indicating that it is long Osk but not short Osk that remodels the actin cytoskeleton. 20 Since long Osk resides on the endosomal membrane, 11 we next examined whether the Osk-induced rearrangement of F-actin is dependent on the activity of endocytic components.…”

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confidence: 98%

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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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mentioning

confidence: 64%

Section: Osk-induced Rearrangement Of F-actinmentioning

confidence: 76%

mentioning

confidence: 80%

Section: Osk-induced Rearrangement Of F-actinmentioning

confidence: 99%

mentioning

confidence: 98%

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

Tanaka¹,

Nakamura²

2011

BioArchitecture

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Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis

Kugler¹,

Lasko²

2020

Encyclopedia of Life Sciences

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Studies of the maternal processes that specify the Drosophila anteroposterior embryonic axis have yielded rich insight into various biological processes required for animal development. As the oocyte is a single cell with a single, largely quiescent nucleus, polarising and symmetry‐breaking events must be executed through molecular mechanisms other than transcriptional control. These include intercellular interactions such as signal transduction and differential cell adhesion. mRNA‐based mechanisms are also prominent in establishing the anteroposterior embryonic axis. Specific mRNAs become enriched at the anterior or posterior poles through motor‐protein driven microtubule‐dependent transport, or through bulk cytoplasmic movement followed by anchoring. Proteins encoded by these mRNAs establish gradients through spatiotemporal control of translation and by diffusion coupled with degradation. Ovary structure determines the activities of polarising pathways that establish the anteroposterior embryonic axis. Initial asymmetries correlate with unequal cell divisions, a polarised cytoskeleton and differential cell adhesion. Germ cell – follicle cell interactions establish and maintain polarity in developing follicles. Microtubule‐dependent mRNA localisation is critical to axis establishment. Localised determinants initiate regulatory cascades that establish the anteroposterior body axis of the embryo and specify primordial germ cells. Various ribonucleoprotein complexes (RNPs) are essential for germ line development and for axis formation. Phase transition of proteins with intrinsically disordered domains are involved in the formation of several classes of these RNPs.

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Regulation of the formin cappuccino is critical for polarity of Drosophila oocytes

2015

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The Drosophila formin Cappuccino (Capu) creates an actin mesh-like structure that traverses the oocyte during mid-oogenesis. This mesh is thought to prevent premature onset of fast cytoplasmic streaming which normally happens during late-oogenesis. Proper cytoskeletal organization and cytoplasmic streaming are crucial for localization of polarity determinants such as osk, grk, bcd and nanos mRNAs. Capu mutants disrupt these events, leading to female sterility. Capu is regulated by another nucleator, Spire, as well as by autoinhibition in vitro. Studies in vivo confirm that Spire modulates Capu’s function in oocytes; however, how autoinhibition contributes is still unclear. To study the role of autoinhibition in flies, we expressed a Capu construct that is missing the Capu Inhibitory Domain, CapuΔN. Consistent with a gain of activity due to loss of autoinhibition, the actin mesh was denser in CapuΔN oocytes. Further, cytoplasmic streaming was delayed and fertility levels decreased. Localization of osk mRNA in early stages, and bcd and nanos in late stages, were disrupted in CapuΔN-expressing oocytes. Finally, evidence that these phenotypes were due to a loss of autoinhibition comes from co-expression of the N-terminal half of Capu with CapuΔN, which suppressed the defects in actin, cytoplasmic streaming and fertility. From these results, we conclude that Capu can be autoinhibited during Drosophila oocyte development.

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DrosophilaMon2 couples Oskar-induced endocytosis with actin remodeling for cortical anchorage of the germ plasm

Cited by 43 publications

References 48 publications

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

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

Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis

Regulation of the formin cappuccino is critical for polarity of Drosophila oocytes

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