An Equatorial Contractile Mechanism Drives Cell Elongation but not Cell Division

Sehring, Ivonne Margarete; Dong, Bo; Denker, Elsa; Bhattachan, Punit; Deng, Wei; Mathiesen, Birthe; Jiang, Di

doi:10.1371/journal.pbio.1001781

Cited by 40 publications

(56 citation statements)

References 114 publications

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“…For instance, there are other more specialized structures, such as the immunological synapse in immune cells (Dustin, 2009;Huppa and Davis, 2003), the function and stability of which depends on the formation of an actin ring-like structure at the contact. Another surprising actin ring system has been recently described in Ciona intestinalis, where the elongation of notochord cells is triggered by an actomyosin ring squeezing these cells around their circumference, similar to the cytokinetic furrow during cell division (Sehring et al, 2014). There have been many more actin ring-like structures described in a variety of other species and organs, including fish retina (Lin-Jones et al, 2009;O'Connor and Burnside, 1981), amphibian nerves (Holtfreter, 1946), plant roots (Volkmann and Baluska, 1999), and fruit-fly ovaries (He et al, 2010), the specific function of which is often not entirely clear.…”

Section: Discussionmentioning

confidence: 99%

Actin Rings of Power

et al. 2016

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Circular or ring-like actin structures play important roles in various developmental and physiological processes. Commonly, these rings are composed of actin filaments and myosin motors (actomyosin) that, upon activation, trigger ring constriction. Actomyosin ring constriction, in turn, has been implicated in key cellular processes ranging from cytokinesis to wound closure. Non-constricting actin ring-like structures also form at cell-cell contacts, where they exert a stabilizing function. Here, we review recent studies on the formation and function of actin ring-like structures in various morphogenetic processes, shedding light on how those different rings have been adapted to fulfill their specific roles.

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Section: Discussionmentioning

confidence: 99%

Actin Rings of Power

et al. 2016

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“…Jiang et al have described that tubulogenesis of notochord cells involved the remodeling of cell shape and tissue configuration in the absence of cell proliferation (Denker and Jiang, 2012;Dong et al, 2009;Sehring et al, 2014). In the zebrafish gut, lumen fusion into a single, continuous lumen occurs through both luminal membrane expansion and the loss of adhesion at the fusion site (Alvers et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

P114RhoGEF governs cell motility and lumen formation during tubulogenesis via ROCK-myosin II pathway

Kim

Shewan

Ewald

et al. 2015

Journal of Cell Science

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Tubulogenesis is fundamental to the development of many epithelial organs. Although lumen formation in cysts has received considerable attention, less is known about lumenogenesis in tubes. Here, we utilized tubulogenesis induced by hepatocyte growth factor (HGF) in MDCK cells, which form tubes enclosing a single lumen. We report the mechanism that controls tubular lumenogenesis and limits each tube to a single lumen. Knockdown of p114RhoGEF (also known as ARHGEF18), a guanine nucleotide exchange factor for RhoA, did not perturb the early stages of tubulogenesis induced by HGF. However, this knockdown impaired later stages of tubulogenesis, resulting in multiple lumens in a tube. Inhibition of Rho kinase (ROCK) or myosin IIA, which are downstream of RhoA, led to formation of multiple lumens. We studied lumen formation by live-cell imaging, which revealed that inhibition of this pathway blocked cell movement, suggesting that cell movement is necessary for consolidating multiple lumens into a single lumen. Lumen formation in tubules is mechanistically quite different from lumenogenesis in cysts. Thus, we demonstrate a new pathway that regulates directed cell migration and formation of a single lumen during epithelial tube morphogenesis.

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“…B enaz eraf and colleagues 20 provided evidence that an anterior-toposterior "hardening" or increase in viscosity of pre-somitic mesoderm directly creates tissue motion fluctuations in the amniote embryo. More recently, Sehring and colleagues 51 observed a correlation between discrete local contractions at the individual cell equator and pushing forces at the cell poles during notochord elongation in the simple chordate Ciona intestinalis. In other words, we propose that regionalized motion patterns, in concert with changes in tissue material properties, lead to the large-scale deformations that shape amniote embryos.…”

Section: Global Versus Local Morphogenetic Movementsmentioning

confidence: 99%

Identification of emergent motion compartments in the amniote embryo

Loganathan¹,

Little²,

Joshi³

et al. 2014

Organogenesis

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The tissue scale deformations (1mm) required to form an amniote embryo are poorly understood. Here, we studied »400 mm-sized explant units from gastrulating quail embryos. The explants deformed in a reproducible manner when grown using a novel vitelline membrane-based culture method. Time-lapse recordings of latent embryonic motion patterns were analyzed after disk-shaped tissue explants were excised from three specific regions near the primitive streak: 1) anterolateral epiblast, 2) posterolateral epiblast, and 3) the avian organizer (Hensen's node). The explants were cultured for 8 hours-an interval equivalent to gastrulation. Both the anterolateral and the posterolateral epiblastic explants engaged in concentric radial/centrifugal tissue expansion. In sharp contrast, Hensen's node explants displayed Cartesian-like, elongated, bipolar deformations-a pattern reminiscent of axis elongation. Time-lapse analysis of explant tissue motion patterns indicated that both cellular motility and extracellular matrix fiber (tissue) remodeling take place during the observed morphogenetic deformations. As expected, treatment of tissue explants with a selective Rho-Kinase (p160ROCK) signaling inhibitor, Y27632, completely arrested all morphogenetic movements. Microsurgical experiments revealed that lateral epiblastic tissue was dispensable for the generation of an elongated midline axisprovided that an intact organizer (node) is present. Our computational analyses suggest the possibility of delineating tissue-scale morphogenetic movements at anatomically discrete locations in the embryo. Further, tissue deformation patterns, as well as the mechanical state of the tissue, require normal actomyosin function. We conclude that amniote embryos contain tissue-scale, regionalized morphogenetic motion generators, which can be assessed using our novel computational time-lapse imaging approach. These data and future studies-using explants excised from overlapping anatomical positions-will contribute to understanding the emergent tissue flow that shapes the amniote embryo.

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An Equatorial Contractile Mechanism Drives Cell Elongation but not Cell Division

Abstract: A cytokinesis-like contractile mechanism is co-opted in a different developmental scenario to achieve cell elongation instead of cell division in Ciona intestinalis.

Cited by 40 publications

References 114 publications

Actin Rings of Power

Actin Rings of Power

P114RhoGEF governs cell motility and lumen formation during tubulogenesis via ROCK-myosin II pathway

Identification of emergent motion compartments in the amniote embryo

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