Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes

Duan, Xing; Li, Yizeng; Yi, Kexi; Guo, Fei; Wang, Hai Yang; Wu, Pei Hsun; Yang, Jing; Mair, Devin B.; Morales, E. Angelo; Kaláb, Petr; Wirtz, Denis; Sun, Sean X.; Li, Rong

doi:10.1038/s41467-019-14068-3

Cited by 60 publications

(41 citation statements)

References 51 publications

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“…Mechanical roles of mitochondria are not limited to muscle fibers. Pushing forces of polymerising actin filaments against a mitochondria network surrounding the spindle in mouse oocytes demonstrated a mechanical role of mitochondria in spindle positioning 39 . Also in this system, a fine balance between mitochondrial fusion and fission was necessary for normal spindle positioning 39 .…”

Section: Discussionmentioning

confidence: 99%

“…Pushing forces of polymerising actin filaments against a mitochondria network surrounding the spindle in mouse oocytes demonstrated a mechanical role of mitochondria in spindle positioning 39 . Also in this system, a fine balance between mitochondrial fusion and fission was necessary for normal spindle positioning 39 . Similarly, mitochondrial remodelling into long giant mitochondria has been shown to be essential for sperm tail elongation during Drosophila spermatogenesis 40 .…”

Section: Discussionmentioning

confidence: 99%

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Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle

Avellaneda

Rodier

Daian

et al. 2020

Preprint

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Complex animals build specialised muscle to match specific biomechanical and energetic needs. Hence, composition and architecture of sarcomeres as well as mitochondria are muscle type specific. However, mechanisms coordinating mitochondria with sarcomere morphogenesis are elusive. Here we use Drosophila muscles to demonstrate that myofibril and mitochondria morphogenesis are intimately linked. In flight muscles, the muscle selector spalt instructs mitochondria to intercalate between myofibrils, which in turn mechanically constrain mitochondria into elongated shapes. Conversely in cross-striated muscles, mitochondria networks surround myofibril bundles, contacting myofibrils only with thin extensions. To investigate the mechanism causing these differences, we manipulated mitochondrial dynamics and found that increased mitochondrial fusion during myofibril assembly prevents mitochondrial intercalation in flight muscles. Strikingly, this coincides with the expression of cross-striated muscle specific sarcomeric proteins. Consequently, flight muscle myofibrils convert towards a partially cross-striated architecture. Together, these data suggest a biomechanical feedback mechanism downstream of spalt synchronizing mitochondria with myofibril morphogenesis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle

Avellaneda

Rodier

Daian

et al. 2020

Preprint

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“…However, it is important to note that spindle organization and polar body extrusion are not coordinated by a single gene. Many cytokinesis-related proteins, including actin, formin, profilin, cofilin, myosin, and tubulin, are effectors of the ROCK signaling pathway though which spindle positioning is regulated [43,[52][53][54][61][62][63][64]. Moreover, ROCK inhibitor increased cellular microtubule acetylation because ROCK regulates microtubule acetylation via phosphorylation of tubulin polymerization-promoting protein 1 [44,50].…”

Section: Discussionmentioning

confidence: 99%

Effects of Short-Term Inhibition of Rho Kinase on Dromedary Camel Oocyte In Vitro Maturation

Tukur

Aljumaah

Swelum

et al. 2020

Animals

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This is the first report on a biphasic in vitro maturation (IVM) approach with a meiotic inhibitor to improve dromedary camel IVM. Spontaneous meiotic resumption poses a major setback for in vitro matured oocytes. The overall objective of this study was to improve in vitro maturation of dromedary camel oocytes using ROCK inhibitor (Y-27632) in a biphasic IVM to prevent spontaneous meiotic resumption. In the first experiment, we cultured immature cumulus–oocyte complexes (COCs, n = 375) in a prematuration medium supplemented with ROCK inhibitor (RI) for 2 h, 4 h, 6 h, and 24 h before submission to normal in vitro maturation to complete 28 h. The control was cultured for 28 h in the absence of RI. In the first phase of experiment two, we cultured COCs (n = 480) in the presence or absence (control) of RI for 2 h, 4 h, 6 h, and 24 h, and conducted real-time relative quantitative PCR (qPCR) on selected mRNA transcripts. The same was done in the second phase, but qPCR was done after completion of normal IVM. Assessment of nuclear maturation showed that pre-IVM for 4 h yielded an increase in MII oocyte (54.67% vs. 26.6% of control; p < 0.05). As expected, the same group showed the highest degree (2) of cumulus expansion. In experiment 2, qPCR results showed significantly higher expression of ACTB and BCL2 in the RI group treated for 4 h when compared with the other groups. However, their relative quantification after biphasic IVM did not reveal any significant difference, except for the positive response of BCL2 and BAX/BCL2 ratio after 4 and 6 h biphasic IVM. In conclusion, RI prevents premature oocyte maturation and gave a significantly positive outcome during the 4 h treatment. This finding is a paradigm for future investigation on dromedary camel biphasic IVM and for improving the outcome of IVM in this species.

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“…The spindle migration depends on a cytoplasmic network of filaments, assembled by the Formin-2 and Spire1/2 nucleators (10)(11)(12)(13). This network indeed supports both pushing and pulling forces that are necessary to relocate the spindle (14)(15)(16)(17)(18). Once fully migrated, the anaphase I occurs, and half of the homologous chromosomes are discarded into the first polar body.…”

Section: Introductionmentioning

confidence: 90%

RhoA- and Ran-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes

Dehapiot

Clément

Bourdais

et al. 2020

Preprint

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Mammalian oocyte meiotic divisions are highly asymmetric and produce a large haploid gamete and two small polar bodies. This relies on the ability of the cell to break symmetry and position its spindle close to the cortex before the anaphase occurs. In metaphase II arrested mouse oocytes, the spindle is actively maintained close and parallel to the cortex, until the fertilization triggers the sister chromatids segregation and the rotation of the spindle. The latter must indeed reorient perpendicular to the cortex to enable the cytokinesis ring closure at the base of the polar body. However, the mechanisms underlying symmetry breaking and spindle rotation have remained elusive. In this study, we show that the spindle rotation results from two antagonistic forces. First, an inward contraction of the cytokinesis furrow dependent on RhoA signaling and second, an outward attraction exerted on both lots of chromatids by a RanGTP dependent polarization of the actomyosin cortex. By combining live segmentation and tracking with numerical modelling, we demonstrate that this configuration becomes unstable as the ingression progresses. This leads to spontaneous symmetry breaking, which implies that neither the rotation direction nor the lot of chromatids that eventually gets discarded are biologically predetermined.

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Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes

Cited by 60 publications

References 51 publications

Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle

Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle

Effects of Short-Term Inhibition of Rho Kinase on Dromedary Camel Oocyte In Vitro Maturation

RhoA- and Ran-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes

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