Detection of surface forces by the cell-wall mechanosensor Wsc1 in yeast

Neeli-Venkata, Ramakanth; Diaz, Celia Municio; Celador, Rubén; Sánchez, Yolanda; Minc, Nicolas

doi:10.1016/j.devcel.2021.09.024

Cited by 19 publications

(9 citation statements)

References 63 publications

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“…4B). In S. pombe, cross-talk with the CWI pathway has not been studied, but the accumulation of the mechano-sensor Wsc1 at the site of cell-cell contact [156] suggests an important contribution.…”

Section: Cross Regulation With Cell Wall Integrity and Osmolarity Pat...mentioning

confidence: 99%

A focus on yeast mating: From pheromone signaling to cell-cell fusion

Sieber

Coronas-Serna

Martin

2023

Seminars in Cell & Developmental Biology

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Section: Cross Regulation With Cell Wall Integrity and Osmolarity Pat...mentioning

confidence: 99%

A focus on yeast mating: From pheromone signaling to cell-cell fusion

Sieber

Coronas-Serna

Martin

2023

Seminars in Cell & Developmental Biology

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“…Using single-molecule AFM, Dupres et al demonstrated that Wsc1 behaves like a linear nanospring that is capable of resisting high mechanical forces and responding to cell surface stress (Dupres et al, 2009). Recently, Neeli-Venkata et al reported the formation of large clusters of the surface protein Wsc1 at sites where forces were applied to yeast cell walls (Neeli-Venkata et al, 2021). Wsc1 acts as a bona fide mechanosensor and activates pathways that reinforce the cell wall (Neeli-Venkata et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Recently, Neeli-Venkata et al reported the formation of large clusters of the surface protein Wsc1 at sites where forces were applied to yeast cell walls (Neeli-Venkata et al, 2021). Wsc1 acts as a bona fide mechanosensor and activates pathways that reinforce the cell wall (Neeli-Venkata et al, 2021). Owing to technical difficulties in AFM of observing in a closed vessel under high pressure, it is currently not possible to analyze pressure-induced structural changes in Wsc1 by AFM.…”

Section: Discussionmentioning

confidence: 99%

“…Their architecture is analogous to that of the mammalian transmembrane integrins (Elhasi & Blomberg, 2019). Among the five sensor proteins in S. cerevisiae , Wsc1 has been extensively studied both genetically and biophysically (Banavar et al, 2018, Dupres et al, 2009, Heinisch et al, 2010, Merchan et al, 2004, Neeli-Venkata et al, 2021, Philip & Levin, 2001, Schoppner et al, 2022). It is unevenly distributed at the cell surface and accumulates at sites of polarized growth, in patches with an approximate diameter of 200 nm (Heinisch et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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The CWI pathway is activated through high hydrostatic pressure, enhancing glycerol efflux via the aquaglyceroporin Fps1 inSaccharomyces cerevisiae

Mochizuki

Tanigawa

Shindo

et al. 2022

Preprint

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The fungal cell wall is the first barrier against diverse external stresses, such as high hydrostatic pressure. This study explores the roles of osmoregulation and the cell wall integrity (CWI) pathway in response to the high pressure in the yeast Saccharomyces cerevisiae. We demonstrate the roles of the transmembrane mechanosensor Wsc1 and aquaglyceroporin Fps1 in an underlying protective mechanism to avoid cellular rupture under high pressure. The promotion of water influx into cells at 25 MPa, as evident by an increase in cell volume and a loss of the plasma membrane eisosome structure, promotes the activation of Wsc1, an activator of the CWI pathway. The downstream mitogen-activated protein kinase Slt2 was hyperphosphorylated at 25 MPa. Glycerol efflux increases via Fps1 phosphorylation, which is initiated by downstream components of the CWI pathway, and contributes to the reduction in intracellular osmolarity under high pressure. Herein, the elucidation of a cellular pathway that is used as a protective mechanism against high pressure could potentially be translated to mammalian cells and could help to understand cellular mechanosensation and adaptation.

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“…One class of plausible mechanisms may implicate conserved fungal CW mechanosensors of the WSC and MID families [67]. These act as bona fide CW mechanosensors to activate the CW integrity pathway and reinforce the CW by promoting synthesis [68]. Accordingly, previous work has shown that the Aspergillus WscA sensor may function to support colony growth and CW shapes, with null mutants exhibiting frequent tip bulging and lysis phenotypes in hypo-osmotic conditions [69].…”

Section: A Model For Tip Growth Based On Mechanical Feedbackmentioning

confidence: 99%

Cell wall dynamics stabilize tip growth in a filamentous fungus

et al. 2023

Self Cite

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Hyphal tip growth allows filamentous fungi to colonize space, reproduce, or infect. It features remarkable morphogenetic plasticity including unusually fast elongation rates, tip turning, branching, or bulging. These shape changes are all driven from the expansion of a protective cell wall (CW) secreted from apical pools of exocytic vesicles. How CW secretion, remodeling, and deformation are modulated in concert to support rapid tip growth and morphogenesis while ensuring surface integrity remains poorly understood. We implemented subresolution imaging to map the dynamics of CW thickness and secretory vesicles in Aspergillus nidulans. We found that tip growth is associated with balanced rates of CW secretion and expansion, which limit temporal fluctuations in CW thickness, elongation speed, and vesicle amount, to less than 10% to 20%. Affecting this balance through modulations of growth or trafficking yield to near-immediate changes in CW thickness, mechanics, and shape. We developed a model with mechanical feedback that accounts for steady states of hyphal growth as well as rapid adaptation of CW mechanics and vesicle recruitment to different perturbations. These data provide unprecedented details on how CW dynamics emerges from material secretion and expansion, to stabilize fungal tip growth as well as promote its morphogenetic plasticity.

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Detection of surface forces by the cell-wall mechanosensor Wsc1 in yeast

Cited by 19 publications

References 63 publications

A focus on yeast mating: From pheromone signaling to cell-cell fusion

A focus on yeast mating: From pheromone signaling to cell-cell fusion

The CWI pathway is activated through high hydrostatic pressure, enhancing glycerol efflux via the aquaglyceroporin Fps1 inSaccharomyces cerevisiae

Cell wall dynamics stabilize tip growth in a filamentous fungus

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