Wnt/Frizzled Signaling Controls C. elegans Gastrulation by Activating Actomyosin Contractility

Lee, Jen Yi; Marston, Daniel J.; Walston, Timothy; Hardin, Jeff; Halberstadt, Ari I.; Goldstein, Bob

doi:10.1016/j.cub.2006.08.090

Cited by 130 publications

(171 citation statements)

References 56 publications

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“…4B, left and Table S2). Previous work has demonstrated the importance of Wnt signaling in regulating actomyosin contractility (37). Furthermore, high levels of the noncanonical Wnt downstream effector ROCK has been shown to trigger osteogenesis through a myosin-generated tension feedback loop (23,38).…”

Section: Resultsmentioning

confidence: 99%

“…Recent studies have also shown how Wnts are activated by mechanical stimuli during bone development (43,44) with additional functions in regulating cell contractility during tissue morphogenesis (37,45). p38, ERK, and JNK cascades are known to be activated by mechanical stimuli but have also been implicated as targets of Wnt signaling through canonical (40) and noncanonical pathways (41,46,47) for regulation of osteogenesis.…”

Section: Discussionmentioning

confidence: 99%

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Geometric cues for directing the differentiation of mesenchymal stem cells

Kilian

Bugarija

Lahn

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

1,650

1,559

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Significant efforts have been directed to understanding the factors that influence the lineage commitment of stem cells. This paper demonstrates that cell shape, independent of soluble factors, has a strong influence on the differentiation of human mesenchymal stem cells (MSCs) from bone marrow. When exposed to competing soluble differentiation signals, cells cultured in rectangles with increasing aspect ratio and in shapes with pentagonal symmetry but with different subcellular curvature-and with each occupying the same area-display different adipogenesis and osteogenesis profiles. The results reveal that geometric features that increase actomyosin contractility promote osteogenesis and are consistent with in vivo characteristics of the microenvironment of the differentiated cells. Cytoskeletal-disrupting pharmacological agents modulate shape-based trends in lineage commitment verifying the critical role of focal adhesion and myosin-generated contractility during differentiation. Microarray analysis and pathway inhibition studies suggest that contractile cells promote osteogenesis by enhancing c-Jun N-terminal kinase (JNK) and extracellular related kinase (ERK1/2) activation in conjunction with elevated winglesstype (Wnt) signaling. Taken together, this work points to the role that geometric shape cues can play in orchestrating the mechanochemical signals and paracrine/autocrine factors that can direct MSCs to appropriate fates. were initially isolated from bone marrow and noted for their ability to differentiate into bone cells (osteoblasts), cartilage cells (chondrocytes), and fat cells (adipocytes) (1, 2). As an autologous source of stem cells, MSCs are under considerable scrutiny for regenerative therapies (3). A combination of physical, chemical, and biological cues present in the stem cell microenvironment have been implicated as directors of stem cell fate in vivo (4). This concept of a stem cell "niche" has motivated empirical studies to identify optimal combinations of extracellular matrix, culture conditions, and temporally administered growth factors to direct stem cell fate in the laboratory (5-7). However, the physical forces and geometry of the MSC microenvironment remain poorly defined and have begun to emerge as critical parameters for regulating cell fate (8, 9).Physical cues, which were postulated as important factors in tissue development over a century ago (10), have also been recognized as important factors in controlling cell function. Research along these lines has been driven in the past decades with the maturation of microengineering techniques (11-13). Ingber, Whitesides, and colleagues demonstrated the use of substrates that were geometrically patterned to control the microenvironment of individual cells and in turn the decision of cells to initiate apoptosis (14). Patterned substrates have also been used to study cytoskeletal dynamics (15-18) and motility (19-22) with singlecell resolution. Chen and coworkers recently demonstrated the important role that cell shape and size can play ...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Geometric cues for directing the differentiation of mesenchymal stem cells

Kilian

Bugarija

Lahn

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

1,650

1,559

View full text Add to dashboard Cite

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“…NM IIB is the subtype most frequently reported to mediate directional cell migration in vertebrates (17,39). In several cases canonical Wnt signaling lies upstream of NM II (40)(41)(42). In feather buds, anterior dermal cells (NM IIB-) remain relatively stationary whereas the posterior dermal cells (NM IIB+) exhibit polarized movements.…”

Section: Discussionmentioning

confidence: 99%

Shaping organs by a wingless-int/Notch/nonmuscle myosin module which orients feather bud elongation

Chen

Jiang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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How organs are shaped to specific forms is a fundamental issue in developmental biology. To address this question, we used the repetitive, periodic pattern of feather morphogenesis on chicken skin as a model. Avian feathers within a single tract extend from dome-shaped primordia to thin conical structures with a common axis of orientation. From a systems biology perspective, the process is precise and robust. Using tissue transplantation assays, we demonstrate that a "zone of polarizing activity," localized in the posterior feather bud, is necessary and sufficient to mediate the directional elongation. This region contains a spatially well-defined nuclear β-catenin zone, which is induced by wingless-int (Wnt)7a protein diffusing in from posterior bud epithelium. Misexpressing nuclear β-catenin randomizes feather polarity. This dermal nuclear β-catenin zone, surrounded by Notch1 positive dermal cells, induces Jagged1. Inhibition of Notch signaling disrupts the spatial configuration of the nuclear β-catenin zone and leads to randomized feather polarity. Mathematical modeling predicts that lateral inhibition, mediated by Notch signaling, functions to reduce Wnt7a gradient variations and fluctuations to form the sharp boundary observed for the dermal β-catenin zone. This zone is also enriched for nonmuscle myosin IIB. Suppressing nonmuscle myosin IIB disrupts directional cell rearrangements and abolishes feather bud elongation. These data suggest that a unique molecular module involving chemical-mechanical coupling converts a pliable chemical gradient to a precise domain, ready for subsequent mechanical action, thus defining the position, boundary, and duration of localized morphogenetic activity that molds the shape of growing organs.anterior-posterior axial orientation | boundary formation | denoising | morphogen gradient

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“…Following A/P polarization, chiral cortical actomyosin activity patterns the D/V and L/R axes [187,188,191,192,197] (see above), and cortical contractility drives cell internalization and most likely also cell sorting during gastrulation [197,[262][263][264][265][266][267]. The central inductive cue(s) that drives non-muscle myosin II activation during gastrulation is constituted by Wnt signaling [200,265].…”

Section: Actomyosinmentioning

confidence: 99%

“…The central inductive cue(s) that drives non-muscle myosin II activation during gastrulation is constituted by Wnt signaling [200,265]. This function of Wnt seems to be conserved during later development [268] and among animals: Wnt signaling can cell-autonomously modulate actomyosin distribution, activity, and apical-basal polarization [269,270], and Wnt/planar cell polarity pathway components also seem to directly modulate actin dynamics [271].…”

Section: Actomyosinmentioning

confidence: 99%

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

Pohl

2015

Symmetry

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Animal development relies on repeated symmetry breaking, e.g., during axial specification, gastrulation, nervous system lateralization, lumen formation, or organ coiling. It is crucial that asymmetry increases during these processes, since this will generate higher morphological and functional specialization. On one hand, cue-dependent symmetry breaking is used during these processes which is the consequence of developmental signaling. On the other hand, cells isolated from developing animals also undergo symmetry breaking in the absence of signaling cues. These spontaneously arising asymmetries are not well understood. However, an ever growing body of evidence suggests that these asymmetries can originate from spontaneous symmetry breaking and self-organization of molecular assemblies into polarized entities on mesoscopic scales. Recent discoveries will be highlighted and it will be discussed how actomyosin and microtubule networks serve as common biomechanical systems with inherent abilities to drive spontaneous symmetry breaking.

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Wnt/Frizzled Signaling Controls C. elegans Gastrulation by Activating Actomyosin Contractility

Cited by 130 publications

References 56 publications

Geometric cues for directing the differentiation of mesenchymal stem cells

Geometric cues for directing the differentiation of mesenchymal stem cells

Shaping organs by a wingless-int/Notch/nonmuscle myosin module which orients feather bud elongation

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

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