The interphase microtubule aster is a determinant of asymmetric division orientation in <i>Drosophila</i> neuroblasts

Januschke, Jens; González, Cayetano

doi:10.1083/jcb.200905024

Cited by 89 publications

(114 citation statements)

References 73 publications

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“…In larval neuroblasts, the polarity proteins, including PAR-3, fail to relocalize on the apical side but localize at the cortex adjacent to the centrosome after the centrosome is dislocated, by treatment with a drug that transiently depolymerizes microtubules and in centrosome mutant conditions (Januschke and Gonzalez, 2010). These results indicate that the orientation of the PAR protein localization in Drosophila larval neuroblasts is determined by an intrinsic cue.…”

Section: Introductionmentioning

confidence: 60%

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Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo

Arata¹,

Lee

Goldstein

et al. 2010

Development

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SUMMARYThe axis of asymmetric cell division is controlled to determine the future position of differentiated cells during animal development. The asymmetric localization of PAR proteins in the Drosophila neuroblast and C. elegans embryo are aligned with the axes of the embryo. However, whether extracellular or intracellular signals determine the orientation of the localization of PAR proteins remains controversial. In C. elegans, the P0 zygote and germline cells (P1, P2, and P3) undergo a series of asymmetric cell divisions. Interestingly, the axis of the P0 and P1 divisions is opposite to that of the P2 and P3 divisions. PAR-2, a ring-finger protein, and PAR-1, a kinase, relocalize to the anterior side of the P2 and P3 germline precursors at the site of contact with endodermal precursors. Using an in vitro method, we have found that the PAR-2 protein is distributed asymmetrically in the absence of extracellular signals, but the orientation of the protein localization in the P2 and P3 cells is determined by contact with endodermal precursor cells. Our mutant analyses suggest that mes-1 and src-1, which respectively encode a transmembrane protein and a tyrosine kinase, were not required to establish the asymmetric distribution of PAR-2, but were required to determine its orientation at the site of contact with the endodermal precursors. The PAR-2 localization during the asymmetric P2 and P3 divisions is controlled by extracellular signals via MES-1/SRC-1 signaling. Our findings suggest that Src functions as an evolutionarily conserved molecular link that coordinates extrinsic cues with PAR protein localization.

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Section: Introductionmentioning

confidence: 60%

“…The axis of the division remains roughly unchanged through successive rounds of cell division, and the side of GMC delivery is fixed. During the division, the polarity regulator PAR-3 and aPKC are distributed asymmetrically with respect to the apical-basal axis (Januschke and Gonzalez, 2010;Siegrist and Doe, 2006;Zhong and Chia, 2008).…”

Section: Introductionmentioning

confidence: 99%

Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo

Arata¹,

Lee

Goldstein

et al. 2010

Development

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“…After sample collection, colcemid (Calbiochem) was added to the medium at a final concentration of 100 µM as described previously (Januschke and Gonzalez, 2010). Testes were incubated at 25°C for up to 6 h.…”

Section: Colcemid Treatment Of Testismentioning

confidence: 99%

The centrosome orientation checkpoint is germline stem cell specific and operates prior to the spindle assembly checkpoint in Drosophila testis

Venkei

Yamashita

2015

Development

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Asymmetric cell division is utilized by a broad range of cell types to generate two daughter cells with distinct cell fates. In stem cell populations asymmetric cell division is believed to be crucial for maintaining tissue homeostasis, failure of which can lead to tissue degeneration or hyperplasia/tumorigenesis. Asymmetric cell divisions also underlie cell fate diversification during development. Accordingly, the mechanisms by which asymmetric cell division is achieved have been extensively studied, although the check points that are in place to protect against potential perturbation of the process are poorly understood. Drosophila melanogaster male germline stem cells (GSCs) possess a checkpoint, termed the centrosome orientation checkpoint (COC), that monitors correct centrosome orientation with respect to the component cells of the niche to ensure asymmetric stem cell division. To our knowledge, the COC is the only checkpoint mechanism identified to date that specializes in monitoring the orientation of cell division in multicellular organisms. Here, by establishing colcemid-induced microtubule depolymerization as a sensitive assay, we examined the characteristics of COC activity and find that it functions uniquely in GSCs but not in their differentiating progeny. We show that the COC operates in the G2 phase of the cell cycle, independently of the spindle assembly checkpoint. This study may provide a framework for identifying and understanding similar mechanisms that might be in place in other asymmetrically dividing cell types.

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“…Labelling of the mother and daughter centrosomes has elegantly demonstrated that asymmetric centrosome dynamics correlate with an intrinsic difference in centrosome age (Conduit and Raff, 2010;Januschke et al, 2011;Yamashita et al, 2007). Importantly, the distinct centrosome dynamics in prophase are proposed to participate in the mitotic spindle orientation and to ensure the propagation of cell polarization from one division to the next (Januschke and Gonzalez, 2010;Rebollo et al, 2009;Rebollo et al, 2007;Rusan and Peifer, 2007). Accordingly, the disruption of centrosome structure or the loss of centrosomes have profound consequences on mitotic spindle orientation, stem cell fitness and cell polarization (Basto et al, 2006;Giansanti et al, 2001;Lucas and Raff, 2007;Megraw et al, 2001;Rebollo et al, 2007;Rusan and Peifer, 2007;Yamashita et al, 2003;Yamashita et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Regulation of centrosome movements by Numb and the Collapsin Response Mediator Protein during Drosophila sensory progenitor asymmetric division

et al. 2013

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SUMMARYAsymmetric cell division generates cell fate diversity during development and adult life. Recent findings have demonstrated that during stem cell divisions, the movement of centrosomes is asymmetric in prophase and that such asymmetry participates in mitotic spindle orientation and cell polarization. Here, we have investigated the dynamics of centrosomes during Drosophila sensory organ precursor asymmetric divisions and find that centrosome movements are asymmetric during cytokinesis. We demonstrate that centrosome movements are controlled by the cell fate determinant Numb, which does not act via its classical effectors, Sanpodo and α-Adaptin, but via the Collapsin Response Mediator Protein (CRMP). Furthermore, we find that CRMP is necessary for efficient Notch signalling and that it regulates the duration of the pericentriolar accumulation of Rab11-positive endosomes, through which the Notch ligand, Delta is recycled. Our work characterizes an additional mode of asymmetric centrosome movement during asymmetric divisions and suggests a model whereby the asymmetry in centrosome movements participates in differential Notch activation to regulate cell fate specification.

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The interphase microtubule aster is a determinant of asymmetric division orientation in Drosophila neuroblasts

Abstract: The orientation of stem cell divisions is maintained beyond one cell cycle thanks to microtubule polymerization and apical centrosome positioning.

Cited by 89 publications

References 73 publications

Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo

Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo

The centrosome orientation checkpoint is germline stem cell specific and operates prior to the spindle assembly checkpoint in Drosophila testis

Regulation of centrosome movements by Numb and the Collapsin Response Mediator Protein during Drosophila sensory progenitor asymmetric division

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