Radial intercalation is regulated by the Par complex and the microtubule-stabilizing protein CLAMP/Spef1

Werner, Michael; Mitchell, Jennifer W.; Putzbach, William; Bacon, Elizabeth; Kim, Sun K.; Mitchell, Brian J.

doi:10.1083/jcb.201312045

Cited by 47 publications

(70 citation statements)

References 34 publications

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“…Likewise, our data here and in previous work (Sedzinski et al, 2016) demonstrate a similar requirement for formins in the emergence of an individual apical epithelial surface in MCCs. Interestingly, the coordinated assembly of multiple apical surfaces during lumen formation also requires Rab11, the Par complex and Slit-Robo signaling (Bryant et al, 2010;Medioni et al, 2008;Santiago-Martinez et al, 2008), and the same is true of radial intercalation and apical emergence in individual MCCs (Chung et al, 2014;Kim et al, 2012;Werner et al, 2014). Further exploration of these issues will provide new insights into the mechanisms of organogenesis and epithelial homeostasis.…”

Section: Discussionmentioning

confidence: 99%

“…1A) (Stubbs et al, 2006). An outline of the molecular framework for the control of radial intercalation of MCCs is now emerging, revealing key roles for dystroglycan, Rab11, the Par complex, Slit2 and the Rfx2 transcription factor (Chung et al, 2014;Kim et al, 2012;Sirour et al, 2011;Werner et al, 2014). In addition, we have recently explored the mechanical basis specifically of apical surface emergence in nascent MCCs, finding that the forces that drive apical emergence are cellautonomous and dependent on the assembly of an apical actin network generating effective two-dimensional (2D) pushing forces (Sedzinski et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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RhoA regulates actin network dynamics during apical surface emergence in multiciliated epithelial cells

Sedzinski¹,

Hannezo²,

Tu³

et al. 2017

Development

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Homeostatic replacement of epithelial cells from basal precursors is a multistep process involving progenitor cell specification, radial intercalation and, finally, apical surface emergence. Recent data demonstrate that actin-based pushing under the control of the formin protein Fmn1 drives apical emergence in nascent multiciliated epithelial cells (MCCs), but little else is known about this actin network or the control of Fmn1. Here, we explore the role of the small GTPase RhoA in MCC apical emergence. Disruption of RhoA function reduced the rate of apical surface expansion and decreased the final size of the apical domain. Analysis of cell shapes suggests that RhoA alters the balance of forces exerted on the MCC apical surface. Finally, quantitative time-lapse imaging and fluorescence recovery after photobleaching studies argue that RhoA works in concert with Fmn1 to control assembly of the specialized apical actin network in MCCs. These data provide new molecular insights into epithelial apical surface assembly and could also shed light on mechanisms of apical lumen formation.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

RhoA regulates actin network dynamics during apical surface emergence in multiciliated epithelial cells

Sedzinski¹,

Hannezo²,

Tu³

et al. 2017

Development

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“…Similarly, the two-layered embryonic skin develops from multi-layered epidermal ectoderm (Deblandre et al, 1999; Drysdale, 1992; Stubbs et al, 2006). These processes involve diverse molecular events including changes in cell adhesion and microtubule-dependent vesicular trafficking (Itoh et al, 2014; Kim et al, 2012; Lepage et al, 2014; Marsden and DeSimone, 2001; Solnica-Krezel and Sepich, 2012; Song et al, 2013; Werner et al, 2014). …”

Section: Introductionmentioning

confidence: 99%

The involvement of PCP proteins in radial cell intercalations during Xenopus embryonic development

Ossipova

Chu

Fillâtre

et al. 2015

Developmental Biology

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The planar cell polarity (PCP) pathway orients cells in diverse epithelial tissues in Drosophila and vertebrate embryos and has been implicated in many human congenital defects and diseases, such as ciliopathies, polycystic kidney disease and malignant cancers. During vertebrate gastrulation and neurulation, PCP signaling is required for convergent extension movements, which are primarily driven by mediolateral cell intercalations, whereas the role for PCP signaling in radial cell intercalations has been unclear. In this study, we examine the function of the core PCP proteins Vangl2, Prickle3 (Pk3) and Disheveled in the ectodermal cells, which undergo radial intercalations during Xenopus gastrulation and neurulation. In the epidermis, multiciliated cell (MCC) progenitors originate in the inner layer, but subsequently migrate to the embryo surface during neurulation. We find that the Vangl2/Pk protein complexes are enriched at the apical domain of intercalating MCCs and are essential for the MCC intercalatory behavior. Addressing the underlying mechanism, we identified KIF13B, as a motor protein that binds Disheveled. KIF13B is required for MCC intercalation and acts synergistically with Vangl2 and Disheveled, indicating that it may mediate microtubule-dependent trafficking of PCP proteins necessary for cell shape regulation. In the neural plate, the Vangl2/Pk complexes were also concentrated near the outermost surface of deep layer cells, suggesting a general role for PCP in radial intercalation. Consistent with this hypothesis, the ectodermal tissues deficient in Vangl2 or Disheveled functions contained more cell layers than normal tissues. We propose that PCP signaling is essential for both mediolateral and radial cell intercalations during vertebrate morphogenesis. These expanded roles underscore the significance of vertebrate PCP proteins as factors contributing to a number of diseases, including neural tube defects, tumor metastases, and various genetic syndromes characterized by abnormal migratory cell behaviors.

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“…Generally, the earliest expression of MCC-specific genes initiates at stage 11.5, with high levels of expression observed at stage 14. Radial intercalation, the process by which MCCs interdigitate from an inner layer to the superficial layer, starts at stage 14 and can be optimally visualized at stage 17e18 (Stubbs, Davidson, Keller, & Kintner, 2006; Werner et al, 2014). At this stage, the formation and dynamics of centrioles, as well as the acentriolar structure, the deuterosome, can be observed.…”

Section: Visualization Of Centrioles and Related Structures In Xenmentioning

confidence: 99%

“…This event provides a unique opportunity to study radial intercalation and the essential role that centrioles play during this process (Werner et al, 2014). However, performing time-lapse confocal imaging on intercalating cells presents a challenge, since intercalation generally occurs perpendicular to the coverglass surface in mounted embryos, which results in a severe decrease in resolution due to the absorption of both excitation lasers and emission light from the tissue itself.…”

Section: Ciliated Epithelial Spheroid Culturementioning

confidence: 99%

Centriole biogenesis and function in multiciliated cells

Zhang

Mitchell

2015

Centrosome &Amp; Centriole

Self Cite

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The use of Xenopus embryonic skin as a model system for the development of ciliated epithelia is well established. This tissue is comprised of numerous cell types, most notably the multiciliated cells (MCCs) that each contain approximately 150 motile cilia. At the base of each cilium lies the centriole-based structure called the basal body. Centriole biogenesis is typically restricted to two new centrioles per cell cycle, each templating from an existing “mother” centriole. In contrast, MCCs are post-mitotic cells in which the majority of centrioles arise “de novo” without templating from a mother centriole, instead, these centrioles nucleate from an electron-dense structure termed the deuterostome. How centriole number is regulated in these cells and the mechanism by which the deuterosome templates nascent centrioles is still poorly understood. Here, we describe methods for regulating MCC cell fate as well as for visualizing and manipulating centriole biogenesis.

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Radial intercalation is regulated by the Par complex and the microtubule-stabilizing protein CLAMP/Spef1

Abstract: During radial intercalation of epithelial cells, Par3 and aPKC promote the apical positioning of centrioles, whereas CLAMP stabilizes microtubules along the axis of migration.

Cited by 47 publications

References 34 publications

RhoA regulates actin network dynamics during apical surface emergence in multiciliated epithelial cells

RhoA regulates actin network dynamics during apical surface emergence in multiciliated epithelial cells

The involvement of PCP proteins in radial cell intercalations during Xenopus embryonic development

Centriole biogenesis and function in multiciliated cells

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