Microtubule-binding myosin required for nuclear anchoring and spindle assembly

Department of Zoology, University of Wisconsin, Madison, Madison, Wisconsin 53706, USA.
Nature (Impact Factor: 41.46). 10/2004; 431(7006):325-9. DOI: 10.1038/nature02834
Source: PubMed


Proper spindle positioning and orientation are essential for asymmetric cell division and require microtubule-actin filament (F-actin) interactions in many systems. Such interactions are particularly important in meiosis, where they mediate nuclear anchoring, as well as meiotic spindle assembly and rotation, two processes required for asymmetric cell division. Myosin-10 proteins are phosphoinositide-binding, actin-based motors that contain carboxy-terminal MyTH4 and FERM domains of unknown function. Here we show that Xenopus laevis myosin-10 (Myo10) associates with microtubules in vitro and in vivo, and is concentrated at the point where the meiotic spindle contacts the F-actin-rich cortex. Microtubule association is mediated by the MyTH4-FERM domains, which bind directly to purified microtubules. Disruption of Myo10 function disrupts nuclear anchoring, spindle assembly and spindle-F-actin association. Thus, this myosin has a novel and critically important role during meiosis in integrating the F-actin and microtubule cytoskeletons.

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    • "Actin filaments were well known for their significant roles in spindle migration and anchorage to the cortex in oocyte maturation processes in mouse oocytes (Field and Lénárt, 2011; Yi and Li, 2012; Li and Albertini, 2013; Almonacid et al., 2014). In addition, actin and myosin also play major roles in spindle assembly during meiosis and mitosis (Weber et al., 2004; Sandquist et al., 2011). The actin filaments in Xenopus oocytes, which grow to a tremendous size (~1.2 mm in diameter) and possess a giant nucleus (the GV; 400-500 μm in diameter), localize in three cellular domains: the cortex, the nucleus, and a network of cytoplasmic cables surrounding the GV (Loeder and Gard, 1994). "
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    ABSTRACT: We have examined reorganization of actin filaments and microtubules during Xenopus oocyte maturation. Surrounding the germinal vesicle (GV) in immature oocytes, the cytoplasmic actin filaments reorganized to accumulate beneath the vegetal side of GV, where MTOC-TMA assembled, just before GV breakdown (GVBD). Immediately after GVBD, both Xenopus ADF/cofilin (XAC) and its phosphatase Slingshot (XSSH) accumulated into the nuclei and intranuclear actin filaments disassembled from the vegetal side with the shrinkage of GV. As the MTOC-TMA developed well, cytoplasmic actin filaments were retained at the MTOC-TMA base region. Suppression of XAC dephosphorylation by anti-XSSH antibody injection inhibited both the actin filament reorganization and the proper formation and localization of both the MTOC-TMA and meiotic spindles. Stabilization of actin filaments by phalloidin also inhibited the formation of the MTOC-TMA and the disassembly of intranuclear actin filaments without affecting the nuclear shrinkage. Nocodazole also caused the MTOC-TMA and the cytoplasmic actin filaments at its base region to disappear which further impeded disassembly of intranuclear actin filaments from the vegetal side. Taken together, XAC appears to reorganize cytoplasmic actin filaments required for precise assembly of the MTOC and, together with the MTOC-TMA, to regulate the intranuclear actin filament disassembly essential for meiotic spindle formation.
    Preview · Article · Sep 2015 · Molecular Biology of the Cell
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    • "Myo VII contains a pair of MyTH4-FERM tandem domains, the second FERM domain of the Drosophila Myo VIIa binds to actin at high density (Yang et al., 2009). Unlike Myo VII, the MyTH-FERM tandem of Myo X, but not either of the isolated domains, was shown to bind to MTs (Weber et al., 2004; Kerber and Cheney, 2011) and also binds its cargo proteins, including β-integrins and the axonal guidance receptor DCC (Zhang et al., 2004; Zhu et al., 2007; Wei et al., 2011). Interestingly, in Drosophila myosin XV Sisyphus, the MyTH4 domain binds to MTs, whereas the FERM domain binds to various cargos including the MT-severing protein, Katanin p60 subunit (Liu et al., 2008). "
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    ABSTRACT: Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction of the MyTH4-FERM tandem into KCBP (kinesin-like calmodulin-binding protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further, livecell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination.
    Full-text · Article · Aug 2015 · eLife Sciences
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    • "in cytoskeleton , MTs and their regulated interplay are required for successful chromosome segregation ( Rodriguez et al . , 2003 ; Woolner et al . , 2008 ) . Recent studies demonstrated that myosin - 10 is an essential integrator of spindle MTs with cortical F - actin required for nuclear anchoring and spindle assembly in Xenopus laevis oocytes ( Weber et al . , 2004 ) . Other examples include the association of nonmuscle myosin - 2 ( MHC - A ) with MTs of the spindle apparatus ( Kelley et al . , 1996 ) and the localization of myosin - 5 at the MT organizing center during melanocyte cell division ( Wu et al . , 1998 ) . Diffusive interactions of myosin - 5 with MTs are assumed to be required for eff"

    Full-text · Dataset · Jan 2015
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