scholarly journals Coordinating cell polarization and morphogenesis through mechanical feedback

2021 ◽  
Vol 17 (1) ◽  
pp. e1007971
Author(s):  
Samhita P. Banavar ◽  
Michael Trogdon ◽  
Brian Drawert ◽  
Tau-Mu Yi ◽  
Linda R. Petzold ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Cell Polarization ◽  
Cell Wall Integrity ◽  
Coarse Grained ◽  
Theoretical Approaches ◽  
Cell Wall Integrity Pathway ◽  
Molecular Machinery ◽  
Mating Projection ◽  
Mechanical Feedback

Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.

scholarly journals Coordinating cell polarization and morphogenesis through mechanical feedback

2020 ◽  
Author(s):  
Samhita P. Banavar ◽  
Michael Trogdon ◽  
Brian Drawert ◽  
Tau-Mu Yi ◽  
Linda R. Petzold ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Cell Polarization ◽  
Cell Wall Integrity ◽  
Coarse Grained ◽  
Cellular Processes ◽  
Cell Wall Integrity Pathway ◽  
Molecular Machinery ◽  
Mating Projection ◽  
Mechanical Feedback

AbstractMany cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity Pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.Author summaryCell migration, morphogenesis and secretion are among the vast number of cellular processes that require cells to define a preferred spatial direction to perform essential tasks. This is achieved by setting an intracellular molecular gradient that polarizes the cell. While the molecular players involved in cell polarization and some of the mechanisms that cells use to establish such molecular gradients are known, it remains unclear how cells maintain polarization as they dramatically change shape during morphogenesis, migration, etc. Here we identify a potential feedback control mechanism, encoded genetically in cells, that provides the molecular polarization machinery with the necessary information about cell geometry to maintain cell polarization during cell shape changes.

Pneumocystis carinii BCK1 Complements the Saccharomyces cerevisiae Cell Wall Integrity Pathway

2003 ◽  
Vol 50 (s1) ◽  
pp. 676-677 ◽  
Author(s):  
PAWAN K. VOHRA ◽  
THEODORE J. KOTTOM ◽  
ANDREW H. LIMPER ◽  
CHARLES F. THOMAS
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Wall ◽  
Pneumocystis Carinii ◽  
Cell Wall Integrity ◽  
Cell Wall Integrity Pathway

scholarly journals Aspergillus fumigatus G-Protein Coupled Receptors GprM and GprJ Are Important for the Regulation of the Cell Wall Integrity Pathway, Secondary Metabolite Production, and Virulence

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Aílton Pereira da Costa Filho ◽  
Guilherme Thomaz Pereira Brancini ◽  
Patrícia Alves de Castro ◽  
Clara Valero ◽  
Jaire Alves Ferreira Filho ◽  
...  
Keyword(s):  
Cell Wall ◽  
G Protein ◽  
Galleria Mellonella ◽  
G Protein Coupled Receptors ◽  
Cell Wall Integrity ◽  
Fungal Development ◽  
Content Type ◽  
Cell Wall Integrity Pathway ◽  
Mycotoxin Biosynthesis ◽  
G Protein Coupled

ABSTRACT G-protein coupled receptors (GPCRs) are extracellular signaling receptors that sense environmental cues. Fungi sense their environment primarily through GPCR-mediated signaling pathways, which, in turn, regulate fungal development, metabolism, virulence, and mycotoxin biosynthesis. Aspergillus fumigatus is an important human pathogen that causes aspergillosis, a heterogeneous group of diseases that present a wide range of clinical manifestations. Here, we investigate in detail the role of the GPCRs GprM and GprJ in growth and gene expression. GprM and GprJ are important for melanin production and the regulation of the cell wall integrity (CWI) pathway. Overexpression of gprM and gprJ causes a 20 and 50% reduction in growth rate compared to the wild-type (WT) strain and increases sensitivity to cell wall-damaging agents. Phosphorylation of the CWI protein kinase MpkA is increased in the ΔgprM and ΔgprJ strains and decreased in the overexpression mutants compared to the WT strain. Furthermore, differences in cell wall polysaccharide concentrations and organization were observed in these strains. Transcriptome sequencing suggests that GprM and GprJ negatively regulate genes encoding secondary metabolites (SMs). Mass spectrometry analysis confirmed that the production of fumagillin, pyripyropene, fumigaclavine C, fumiquinazoline, and fumitremorgin is reduced in the ΔgprM and ΔgprJ strains, at least partially through the activation of MpkA. Overexpression of grpM also resulted in the regulation of many transcription factors, with AsgA predicted to function downstream of GprM and MpkA signaling. Finally, we show that the ΔgprM and ΔgprJ mutants are reduced in virulence in the Galleria mellonella insect model of invasive aspergillosis. IMPORTANCE A. fumigatus is the main etiological agent of invasive pulmonary aspergillosis, a life-threatening fungal disease that occurs in severely immunocompromised humans. Withstanding the host environment is essential for A. fumigatus virulence, and sensing of extracellular cues occurs primarily through G-protein coupled receptors (GPCRs) that activate signal transduction pathways, which, in turn, regulate fungal development, metabolism, virulence, and mycotoxin biosynthesis. The A. fumigatus genome encodes 15 putative classical GPCRs, with only three having been functionally characterized to date. In this work, we show that the two GPCRs GprM and GprJ regulate the phosphorylation of the mitogen-activated protein kinase MpkA and thus control the regulation of the cell wall integrity pathway. GprM and GprJ are also involved in the regulation of the production of the secondary metabolites fumagillin, pyripyropene, fumigaclavine C, fumiquinazoline, melanin, and fumitremorgin, and this regulation partially occurs through the activation of MpkA. Furthermore, GprM and GprJ are important for virulence in the insect model Galleria mellonella. This work therefore functionally characterizes two GPCRs and shows how they regulate several intracellular pathways that have been shown to be crucial for A. fumigatus virulence.

scholarly journals Mpt5p, a Stress Tolerance- and Lifespan-Promoting PUF Protein in Saccharomyces cerevisiae, Acts Upstream of the Cell Wall Integrity Pathway

2006 ◽  
Vol 6 (2) ◽  
pp. 262-270 ◽  
Author(s):  
Mark S. Stewart ◽  
Sue Ann Krause ◽  
Josephine McGhie ◽  
Joseph V. Gray
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Wall ◽  
Life Span ◽  
Stress Tolerance ◽  
Synthetic Medium ◽  
Cell Wall Integrity ◽  
Puf Proteins ◽  
Downstream Target ◽  
Cell Wall Integrity Pathway ◽  
Puf Protein

ABSTRACT Pumilio family (PUF) proteins affect specific genes by binding to, and inhibiting the translation or stability of, their transcripts. The PUF domain is required and sufficient for this function. One Saccharomyces cerevisiae PUF protein, Mpt5p (also called Puf5p or Uth4p), promotes stress tolerance and replicative life span (the maximum number of doublings a mother cell can undergo before entering into senescence) by an unknown mechanism thought to partly overlap with, but to be independent of, the cell wall integrity (CWI) pathway. Here, we found that mpt5Δ mutants also display a short chronological life span (the time cells stay alive in saturated cultures in synthetic medium), a defect that is suppressed by activation of CWI signaling. We found that Mpt5p is an upstream activator of the CWI pathway: mpt5Δ mutants display the appropriate phenotypes and genetic interactions, display low basal activity of the pathway, and are defective in activation of the pathway upon thermal stress. A set of mRNAs that specifically bind to Mpt5p was recently reported. One such putative target, LRG1, encodes a GTPase-activating protein for Rho1p that directly links Mpt5p to CWI signaling: Lrg1p inhibits CWI signaling, LRG1 mRNA contains a consensus Mpt5p-binding site in its putative 3′ untranslated region, loss of Lrg1p suppresses the temperature sensitivity and CWI signaling defects of mpt5Δ mutants, and LRG1 mRNA abundance is inhibited by Mpt5p. We conclude that Mpt5p is required for normal replicative and chronological life spans and that the CWI pathway is a key and direct downstream target of this PUF protein.

scholarly journals Cell fusion in yeast is negatively regulated by components of the cell wall integrity pathway

2019 ◽  
Vol 30 (4) ◽  
pp. 441-452 ◽  
Author(s):  
Allison E. Hall ◽  
Mark D. Rose
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Death ◽  
Cell Wall ◽  
Yeast Cell ◽  
Cell Fusion ◽  
Cell Walls ◽  
Cell Wall Integrity ◽  
Fusion Genes ◽  
Cell Wall Degradation ◽  
Cell Wall Integrity Pathway

During mating, Saccharomyces cerevisiae cells must degrade the intervening cell wall to allow fusion of the partners. Because improper timing or location of cell wall degradation would cause lysis, the initiation of cell fusion must be highly regulated. Here, we find that yeast cell fusion is negatively regulated by components of the cell wall integrity (CWI) pathway. Loss of the cell wall sensor, MID2, specifically causes “mating-induced death” after pheromone exposure. Mating-induced death is suppressed by mutations in cell fusion genes ( FUS1, FUS2, RVS161, CDC42), implying that mid2Δ cells die from premature fusion without a partner. Consistent with premature fusion, mid2Δ shmoos had thinner cell walls and lysed at the shmoo tip. Normally, Cdc42p colocalizes with Fus2p to form a focus only when mating cells are in contact (prezygotes) and colocalization is required for cell fusion. However, Cdc42p was aberrantly colocalized with Fus2p to form a focus in mid2Δ shmoos. A hyperactive allele of the CWI kinase Pkc1p ( PKC1*) caused decreased cell fusion and Cdc42p localization in prezygotes. In shmoos, PKC1* increased Cdc42p localization; however, it was not colocalized with Fus2p or associated with cell death. We conclude that Mid2p and Pkc1p negatively regulate cell fusion via Cdc42p and Fus2p.

scholarly journals To preserve or to destroy, that is the question: the role of the cell wall integrity pathway in pollen tube growth

2019 ◽  
Vol 52 ◽  
pp. 131-139 ◽  
Author(s):  
Hannes Vogler ◽  
Gorka Santos-Fernandez ◽  
Martin A Mecchia ◽  
Ueli Grossniklaus
Keyword(s):  
Cell Wall ◽  
Pollen Tube ◽  
Pollen Tube Growth ◽  
Cell Wall Integrity ◽  
Tube Growth ◽  
Cell Wall Integrity Pathway

scholarly journals Quercetin Protects Saccharomyces cerevisiae against Oxidative Stress by Inducing Trehalose Biosynthesis and the Cell Wall Integrity Pathway

PLoS ONE ◽  
2012 ◽  
Vol 7 (9) ◽  
pp. e45494 ◽  
Author(s):  
Rita Vilaça ◽  
Vanda Mendes ◽  
Marta Vaz Mendes ◽  
Laura Carreto ◽  
Maria Amélia Amorim ◽  
...  
Keyword(s):  
Oxidative Stress ◽  
Saccharomyces Cerevisiae ◽  
Cell Wall ◽  
Cell Wall Integrity ◽  
Cell Wall Integrity Pathway ◽  
Trehalose Biosynthesis

scholarly journals Dynamics of cell wall elasticity pattern shapes the cell during yeast mating morphogenesis

Open Biology ◽  
2016 ◽  
Vol 6 (9) ◽  
pp. 160136 ◽  
Author(s):  
Björn Goldenbogen ◽  
Wolfgang Giese ◽  
Marie Hemmen ◽  
Jannis Uhlendorf ◽  
Andreas Herrmann ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Experimental Approach ◽  
Time Resolved ◽  
Force Microscopy ◽  
Cell Wall Elasticity ◽  
Atomic Force ◽  
Stiff Material ◽  
Mating Projection

The cell wall defines cell shape and maintains integrity of fungi and plants. When exposed to mating pheromone, Saccharomyces cerevisiae grows a mating projection and alters in morphology from spherical to shmoo form. Although structural and compositional alterations of the cell wall accompany shape transitions, their impact on cell wall elasticity is unknown. In a combined theoretical and experimental approach using finite-element modelling and atomic force microscopy (AFM), we investigated the influence of spatially and temporally varying material properties on mating morphogenesis. Time-resolved elasticity maps of shmooing yeast acquired with AFM in vivo revealed distinct patterns, with soft material at the emerging mating projection and stiff material at the tip. The observed cell wall softening in the protrusion region is necessary for the formation of the characteristic shmoo shape, and results in wider and longer mating projections. The approach is generally applicable to tip-growing fungi and plants cells.

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