RhoA GTPase inhibition organizes contraction during epithelial morphogenesis

Mason, Frank M.; Xie, Shicong; Vasquez, Claudia G.; Tworoger, Michael; Martin, Adam C.

doi:10.1083/jcb.201603077

Cited by 140 publications

(193 citation statements)

References 87 publications

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“…A challenge in addressing the function of pulsing is to find perturbations that disrupt pulsing without obliterating the actomyosin machine. In a system involving a folding epithelium, the Drosophila ventral furrow, numerous perturbations have been found that abrogate actomyosin pulsing, while leaving the actomyosin machinery more-or-less intact (Jodoin et al, 2015; Mason et al, 2016; Vasquez et al, 2014). These perturbations include disrupting either Myo2 or F-actin turnover directly, or disrupting this dynamic turnover by interfering with upstream RhoA signaling dynamics.…”

Section: Biological Functions Of Actomyosin Pulsingmentioning

confidence: 99%

“…For example, during Drosophila ventral furrow formation, early actomyosin pulses initially produce reversible, or “unratcheted”, contractions, where cell area expands after the pulse induces contraction (Xie and Martin, 2015). Relaxation was recently found to depend on the presence of a negative regulator of RhoA activity (see below), suggesting that pulse relaxation, or the unratcheted state, represents transient RhoA inactivation (Mason et al, 2016). This state then evolves to one in which more persistent actomyosin correlates with sustained, or “ratcheted”, cell constriction (Xie and Martin, 2015).…”

Section: Biological Functions Of Actomyosin Pulsingmentioning

confidence: 99%

“…ROCK, “active” RhoA, and even a RhoGEF ( Drosophila RhoGEF2) have all been observed to pulse in Drosophila epithelia (Mason et al, 2016; Munjal et al, 2015; Vasquez et al, 2014). This suggested the possibility that there is dynamic regulation of the RhoA GTPase.…”

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

“…Such dynamics would require a negative regulator of RhoA. In the Drosophila ventral furrow, negative regulation was recently found to be mediated by a RhoGAP, C-GAP (Mason et al, 2016). In this system, the peak in RhoGEF2 signal precedes the peak Myo2 signal by about 10 seconds.…”

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

“…Thus, in the ventral furrow, RhoGEF2 appears to initiate pulses, presumably by increasing the actomyosin assembly rate, and C-GAP terminates the pulse, either through constant disassembly (Figure 3, curve 1) or by increasing the disassembly rate after assembly (Figure 3, curve 2). Interestingly, removal of C-GAP from the ventral furrow disrupts not only pulsing, but also the spatial organization of RhoA pathway components (Mason et al, 2016). Future insight into the timing of C-GAP and its mechanism of recruitment will be important for elucidating the mechanism of pulsing.…”

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

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Actomyosin Pulsing in Tissue Integrity Maintenance during Morphogenesis

Coravos

Mason

Martin

2017

Trends in Cell Biology

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Summary The actomyosin cytoskeleton is responsible for many changes in cell and tissue shape. For a long time, the actomyosin cytoskeleton has been known to exhibit dynamic contractile behavior. Recently, discrete actomyosin assembly/disassembly cycles have also been observed in cells. These so-called actomyosin pulses have been observed in a variety of contexts, including cell polarization and division, and in epithelia, where they occur during tissue contraction, folding, and extension. In epithelia, evidence suggests that actomyosin pulsing, and more generally, actomyosin turnover, is required to maintain tissue integrity during contractile processes. This review explores possible functions for pulsing in the many instances during which pulsing has been observed, and also highlights proposed molecular mechanisms that drive pulsing.

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Section: Biological Functions Of Actomyosin Pulsingmentioning

confidence: 99%

Section: Biological Functions Of Actomyosin Pulsingmentioning

confidence: 99%

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

Section: Mechanisms For Actomyosin Pulsingmentioning

confidence: 99%

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Actomyosin Pulsing in Tissue Integrity Maintenance during Morphogenesis

Coravos

Mason

Martin

2017

Trends in Cell Biology

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Feeling Things Out: Bidirectional Signaling of the Cell–ECM Interface, Implications in the Mechanobiology of Cell Spreading, Migration, Proliferation, and Differentiation

Miller

Barker

2020

Adv Healthcare Materials

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Biophysical cues stemming from the extracellular environment are rapidly transduced into discernible chemical messages (mechanotransduction) that direct cellular activities-placing the extracellular matrix (ECM) as a potent regulator of cell behavior. Dynamic reciprocity between the cell and its associated matrix is essential to the maintenance of tissue homeostasis and dysregulation of both ECM mechanical signaling, via pathological ECM turnover, and internal mechanotransduction pathways contribute to disease progression. This review covers the current understandings of the key modes of signaling used by both the cell and ECM to coregulate one another. By taking an outside-in approach, the inherent complexities and regulatory processes at each level of signaling (ECM, plasma membrane, focal adhesion, and cytoplasm) are captured to give a comprehensive picture of the internal and external mechanoregulatory environment. Specific emphasis is placed on the focal adhesion complex which acts as a central hub of mechanical signaling, regulating cell spreading, migration, proliferation, and differentiation. In addition, a wealth of available knowledge on mechanotransduction is curated to generate an integrated signaling network encompassing the central components of the focal adhesion, cytoplasm and nucleus that act in concert to promote durotaxis, proliferation, and differentiation in a stiffness-dependent manner.

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Anillin: The First Proofreading‐like Scaffold?

et al. 2020

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Scaffolds are fundamental to many cellular signaling pathways. In this essay, a novel class of scaffolds are proposed, whose action bears striking resemblance to kinetic proofreading. Commonly, scaffold proteins are thought to work as tethers, bringing different components of a pathway together to improve the likelihood of their interaction. However, recent studies show that the cytoskeletal scaffold, anillin, supports contractile signaling by a novel, non-tethering mechanism that controls the membrane dissociation kinetics of RhoA. More generally, such proofreading like scaffolds are distinguished from tethers by a rare type of cooperativity, manifest as a super-linear relationship between scaffold concentration and signaling efficiency. The evidence for this hypothesis is reviewed, its conceptual ramifications are considered, and research questions for the future are discussed.

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RhoA GTPase inhibition organizes contraction during epithelial morphogenesis

Abstract: Mason et al. show that RhoA activity is regulated in space and time by a GEF/GAP module that tunes cell behavior and is required for proper tissue folding and shape during Drosophila morphogenesis.

Cited by 140 publications

References 87 publications

Actomyosin Pulsing in Tissue Integrity Maintenance during Morphogenesis

Actomyosin Pulsing in Tissue Integrity Maintenance during Morphogenesis

Feeling Things Out: Bidirectional Signaling of the Cell–ECM Interface, Implications in the Mechanobiology of Cell Spreading, Migration, Proliferation, and Differentiation

Anillin: The First Proofreading‐like Scaffold?

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