GM130, a cis-Golgi protein, regulates meiotic spindle assembly and asymmetric division in mouse oocyte

Zhang, Chunhui; Wang, Zhenbo; Song, Qisheng; Huang, Xin; Tong, Jingshan; Ma, Jun‐Yu; Guo, Lei; Wei, Yanchang; Ouyang, Ying‐Chun; Hou, Yi; Xing, Fu-qi; Sun, Qing‐Yuan

doi:10.4161/cc.10.11.15797

Cited by 43 publications

(30 citation statements)

References 42 publications

(66 reference statements)

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“…Other molecules that are localized to spindle poles, such as g-tubulin, MAPK, and GM130, have been shown to regulate meiotic spindle assembly and asymmetric division in mouse oocytes. 33,34 This FMNL1 localization pattern prompted us to speculate that FMNL1 might be involved in oocyte meiosis.…”

Section: Discussionmentioning

confidence: 98%

RhoA-mediated FMNL1 regulates GM130 for actin assembly and phosphorylates MAPK for spindle formation in mouse oocyte meiosis

et al. 2015

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Formin-like 1 (FMNL1) is a member of Formin family proteins which are the actin nucleators. Although FMNL1 activities have been shown to be essential for cell adhesion, cytokinesis, cell polarization and migration in mitosis, the functional roles of mammalian FMNL1 during oocyte meiosis remain uncertain. In this study, we investigated the functions of FMNL1 in mouse oocytes using specific morpholino (MO) microinjection and live cell imaging. Immunofluorescent staining showed that in addition to its cytoplasmic distribution, FMNL1 was primarily localized at the spindle poles after germinal vesicle breakdown (GVBD). FMNL1 knockdown caused the low rate of polar body extrusion and resulted in large polar bodies. Time-lapse microscopic and immunofluorescence intensity analysis indicated that this might be due to the aberrant actin expression levels. Cortical polarity was disrupted as shown by a loss of actin cap and cortical granule free domain (CGFD) formation, which was confirmed by a failure of meiotic spindle positioning. And this might be the reason for the large polar body formation. Spindle formation was also disrupted, which might be due to the abnormal localization of p-MAPK. These results indicated that FMNL1 affected both actin dynamics and spindle formation for the oocyte polar body extrusion. Moreover, FMNL1 depletion resulted in aberrant localization and expression patterns of a cis-Golgi marker protein, GM130. Finally, we found that the small GTPase RhoA might be the upstream regulator of FMNL1. Taken together, our data indicate that FMNL1 is required for spindle organization and actin assembly through a RhoA-FMNL1-GM130 pathway during mouse oocyte meiosis.

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Section: Discussionmentioning

confidence: 98%

RhoA-mediated FMNL1 regulates GM130 for actin assembly and phosphorylates MAPK for spindle formation in mouse oocyte meiosis

et al. 2015

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“…Given the lack of functionality of Golgi during meiotic maturation, it could be that the Golgi follows the changes of endoplasmic reticulum export sites (Payne & Schatten 2003). Additionally, matured bovine oocytes are acentrosomal which could explain the contrasting findings in bovine and mouse oocytes regarding Golgi distribution (Schatten 1994, Zhang et al 2011. Presumably, during early embryonic development Golgi fragmentation ensures equal distribution of the organelle between daughter cells since the division during meiosis is unequal.…”

Section: Discussionmentioning

confidence: 89%

Dynamic changes of the Golgi apparatus during bovine in vitro oocyte maturation

Racedo¹,

Rawe

Niemann³

2012

Reproduction

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For successful fertilization by the male gamete, oocyte cytoplasmic organelles such as the Golgi apparatus have to undergo specific changes: the entire process is known as cytoplasmic maturation. The goal of this study was to unravel the dynamics of the Golgi apparatus in bovine oocytes at critical stages ofin vitromaturation, i.e. germinal vesicle (GV), GV breakdown (GVBD), metaphase I (MI) and metaphase II, and to investigate the role of various molecules critically involved therein. The cytoplasmic distribution of proteins was assessed by immunocytochemistry and laser confocal microscopy. We applied specific inhibitors, including nocodazole to unravel the functional role of the microtubular elements; sodium orthovanadate, which primarily inhibits cytoplasmic dynein ATPase activity; monastrol which inhibits the kinesin EG5; and roscovitine to inhibit the kinase cyclin-dependent kinase 2A (CDC2A). Prior to GVBD, the Golgi apparatus was translocated from the centre of the cytoplasm to the cortical area in the periphery, where it underwent fragmentation. A second translocation was observed between GVBD and MI stages, when the Golgi apparatus was moved from the cortex to the centre of the cytoplasm. Incubation with the specific inhibitors revealed that microtubules played an active role in the final localization at GVBD, while CDC2A was essential for Golgi fragmentation at GVBD stage. This partitioning was a precondition for the second movement. In conclusion, for the first time we show basic mechanisms critically involved in the regulation of the dynamic changes of Golgi apparatus during meiosis of the bovine oocyte.

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“…The expression and localization pattern of TGN38 in mouse oocyte maturation was similar with that of GM130. 17 In NRK cells, centrosomes associated with the Golgi resident proteins TGN38 and Golgin-97 throughout the cell cycle. 23 Moreover, this association was stable after the cells were treated with brefeldin A or nocodazole, while GM130 was not associated with centrosomes in mitosis and its localization was disrupted with the drugs.…”

Section: Discussionmentioning

confidence: 99%

“…However, nocodazole treatment of oocytes lead to dispersal of the cis-Golgi protein GM130. 17 Thus, tans-Golgi protein TGN38 may be more involved in the functions of MTOCs than cis-Golgi protein GM130 during oocyte meiotic maturation. In mouse oocytes, spindle assembly originates from MTOCs which contain proteins normally present in centrosomes.…”

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confidence: 99%

TGN38 is required for the metaphase I/anaphase I transition and asymmetric cell division during mouse oocyte meiotic maturation

Chen

Wang

et al. 2014

Cell Cycle

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Sun (2014) TGN38 is required for the metaphase I/anaphase I transition and asymmetric cell division during mouse oocyte meiotic maturation, Cell Cycle, 13:17, 2723-2732, DOI: 10.4161/15384101.2015 Keywords: asymmetric cell division, Golgi apparatus, metaphase I/anaphase I transition, TGN38Abbreviations: GV, germinal vesicle; GVBD, germinal vesicle breakdown; MI, metaphase of the first meiosis; MII, metaphase of the second meiosis; TGN, trans-Golgi network; PB1, first polar body extrusion; MTOCs, microtubule organizing centers.The cellular functions of the trans-Golgi network protein TGN38 remain unknown. In this research, we studied the expression, localization and functions of TGN38 in the meiotic maturation of mouse oocytes. TGN38 was expressed at every stage of oocyte meiotic maturation and colocalized with g-tubulin at metaphase I and metaphase II. The spindle microtubule disturbing agents nocodazole and taxol did not affect the colocalization of TGN38 and g-tubulin. Depletion of TGN38 with specific siRNAs resulted in increased metaphase I arrest, accompanied with spindle assembly checkpoint activation and decreased first polar extrusion (PB1). In the oocytes that had extruded the PB1 after the depletion of TGN38, symmetric division occurred, leading to the production of 2 similarly sized cells. Moreover, the peripheral migration of metaphase I spindle and actin cap formation were impaired in TGN38-depleted oocytes. Our data suggest that TGN38 may regulate the metaphase I/anaphase I transition and asymmetric cell division in mouse oocytes.

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GM130, a cis-Golgi protein, regulates meiotic spindle assembly and asymmetric division in mouse oocyte

Cited by 43 publications

References 42 publications

RhoA-mediated FMNL1 regulates GM130 for actin assembly and phosphorylates MAPK for spindle formation in mouse oocyte meiosis

RhoA-mediated FMNL1 regulates GM130 for actin assembly and phosphorylates MAPK for spindle formation in mouse oocyte meiosis

Dynamic changes of the Golgi apparatus during bovine in vitro oocyte maturation

TGN38 is required for the metaphase I/anaphase I transition and asymmetric cell division during mouse oocyte meiotic maturation

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