Rho-GTPase-regulated vesicle trafficking in plant cell polarity

2014 ◽  
Vol 42 (1) ◽  
pp. 212-218 ◽  
Author(s):  
Xu Chen ◽  
Jiří Friml
Keyword(s):  
Cell Polarity ◽  
Plant Cell ◽  
Rho Gtpase ◽  
Vesicle Trafficking ◽  
Large Family ◽  
Small Gtpases ◽  
Cell Polarization ◽  
Cellular Mechanisms ◽  
Pavement Cells ◽  
Cytoskeleton Organization

ROPs (Rho of plants) belong to a large family of plant-specific Rho-like small GTPases that function as essential molecular switches to control diverse cellular processes including cytoskeleton organization, cell polarization, cytokinesis, cell differentiation and vesicle trafficking. Although the machineries of vesicle trafficking and cell polarity in plants have been individually well addressed, how ROPs co-ordinate those processes is still largely unclear. Recent progress has been made towards an understanding of the co-ordination of ROP signalling and trafficking of PIN (PINFORMED) transporters for the plant hormone auxin in both root and leaf pavement cells. PIN transporters constantly shuttle between the endosomal compartments and the polar plasma membrane domains, therefore the modulation of PIN-dependent auxin transport between cells is a main developmental output of ROP-regulated vesicle trafficking. The present review focuses on these cellular mechanisms, especially the integration of ROP-based vesicle trafficking and plant cell polarity.

Cell motility: can Rho GTPases and microtubules point the way?

2001 ◽  
Vol 114 (21) ◽  
pp. 3795-3803 ◽  
Author(s):  
Torsten Wittmann ◽  
Clare M. Waterman-Storer
Keyword(s):  
Actin Cytoskeleton ◽  
Cell Motility ◽  
Rho Gtpases ◽  
Molecular Mechanisms ◽  
Rho Gtpase ◽  
Cell Types ◽  
Small Gtpases ◽  
Cell Polarization ◽  
Microtubule Cytoskeleton ◽  
Filament Bundles

Migrating cells display a characteristic polarization of the actin cytoskeleton. Actin filaments polymerise in the protruding front of the cell whereas actin filament bundles contract in the cell body, which results in retraction of the cell’s rear. The dynamic organization of the actin cytoskeleton provides the force for cell motility and is regulated by small GTPases of the Rho family, in particular Rac1, RhoA and Cdc42. Although the microtubule cytoskeleton is also polarized in a migrating cell, and microtubules are essential for the directed migration of many cell types, their role in cell motility is not well understood at a molecular level. Here, we discuss the potential molecular mechanisms for interplay of microtubules, actin and Rho GTPase signalling in cell polarization and motility. Recent evidence suggests that microtubules locally modulate the activity of Rho GTPases and, conversely, Rho GTPases might be responsible for the initial polarization of the microtubule cytoskeleton. Thus, microtubules might be part of a positive feedback mechanism that maintains the stable polarization of a directionally migrating cell.

Auxin-induced nanoclustering of membrane signaling complexes underlies cell polarity establishment in Arabidopsis

2019 ◽  
Author(s):  
Xue Pan ◽  
Linjing Fang ◽  
Jianfeng Liu ◽  
Betul Senay-Aras ◽  
Wenwei Lin ◽  
...  
Keyword(s):  
Cell Surface ◽  
Cell Polarity ◽  
Feedback Loop ◽  
Cortical Microtubule ◽  
Cell Polarization ◽  
Feedback Stabilization ◽  
Cell Surface Receptor ◽  
List Type ◽  
Pavement Cells ◽  
Polarity Establishment

AbstractCell polarity is fundamental to the development of both eukaryotic and prokaryotic organisms, yet the mechanism of its establishment remains poorly understood. Here we show that signal-activated nanoclustering of membrane proteins and a cytoskeleton-based feedback loop provide an important mechanism for the establishment of cell polarity. The phytohormone auxin promoted sterol-dependent nanoclustering of cell surface transmembrane receptor-like kinase 1 (TMK1) to initiate cell polarity during the morphogenesis of Arabidopsis puzzle piece-shaped leaf pavement cells (PC). Auxin-triggered nanoclustering of TMK1 stabilized flotillin-associated ordered nanodomains, which were essential for auxin-mediated formation of ROP6 GTPase nanoclusters that act downstream TMK1 to promote cortical microtubule ordering. Mathematical modeling further demonstrated the essential role of this auxin-mediated stabilization of TMK1 and ROP6 nanoclusters, and predicted the additional requirement of ROP6-dependent cortical microtubules for further stabilization of TMK1-sterol nanodomains and the polarization of PC. This prediction was experimentally validated by genetic and biochemical data. Our studies reveal a new paradigm for polarity establishment: A diffusive signal triggers cell polarization by activating cell surface receptor-mediated lateral segregation of signaling components and a cytoskeleton-mediated positive feedback loop of nanodomain stabilization.HighlightsSterols are required for cell polarity in Arabidopsis leaf epidermal cellsAuxin promotes lipid ordering and polar distribution of ordered lipid nanodomains at the plasma membrane (PM)Auxin stabilizes sterol-dependent nanoclustering of transmembrane kinase (TMK1), a PM auxin signal transducerAuxin-induced TMK1 nanoclustering is required but insufficient for cell polarizationMicrotubule-based feedback stabilization of the auxin-induced TMK1 nanodomains can generate cell polarity

scholarly journals Mechanochemical feedback underlies coexistence of qualitatively distinct cell polarity patterns within diverse cell populations

2017 ◽  
Vol 114 (28) ◽  
pp. E5750-E5759 ◽  
Author(s):  
JinSeok Park ◽  
William R. Holmes ◽  
Sung Hoon Lee ◽  
Hong-Nam Kim ◽  
Deok-Ho Kim ◽  
...  
Keyword(s):  
Cell Migration ◽  
Cell Polarity ◽  
Cell Types ◽  
Small Gtpases ◽  
Cell Polarization ◽  
Environmental Perturbations ◽  
Oscillatory Dynamic ◽  
Distinct Cell ◽  
Spatially Distributed ◽  
Directional Cell Migration

Cell polarization and directional cell migration can display random, persistent, and oscillatory dynamic patterns. However, it is not clear whether these polarity patterns can be explained by the same underlying regulatory mechanism. Here, we show that random, persistent, and oscillatory migration accompanied by polarization can simultaneously occur in populations of melanoma cells derived from tumors with different degrees of aggressiveness. We demonstrate that all of these patterns and the probabilities of their occurrence are quantitatively accounted for by a simple mechanism involving a spatially distributed, mechanochemical feedback coupling the dynamically changing extracellular matrix (ECM)–cell contacts to the activation of signaling downstream of the Rho-family small GTPases. This mechanism is supported by a predictive mathematical model and extensive experimental validation, and can explain previously reported results for diverse cell types. In melanoma, this mechanism also accounts for the effects of genetic and environmental perturbations, including mutations linked to invasive cell spread. The resulting mechanistic understanding of cell polarity quantitatively captures the relationship between population variability and phenotypic plasticity, with the potential to account for a wide variety of cell migration states in diverse pathological and physiological conditions.

scholarly journals Turnover Regulation of the Rho GTPase Cdc42 by Heat Shock Protein Chaperones and the MAPK Pathway Scaffold Bem4

2021 ◽  
Author(s):  
Paul J Cullen ◽  
Beatriz Gonzalez
Keyword(s):  
Heat Shock ◽  
Cell Polarity ◽  
Rho Gtpases ◽  
Rho Gtpase ◽  
Mapk Pathway ◽  
Cell Types ◽  
Cell Polarization ◽  
Extrinsic Cues ◽  
Dependent Cell ◽  
Map Kinase Pathway

All cells maintain an axis of polarity that directs the orientation of growth. Cell polarity can be reorganized during development and in response to extrinsic cues to produce new cell types. Rho GTPases are central regulators of cell polarity and signal-dependent cell differentiation. We show here that one of the best understood Rho GTPases, the highly conserved yeast Cdc42p, is turned over by members of the Heat Shock family of Proteins (HSPs). The Hsp40p chaperone, Ydj1p, was required for turnover of Cdc42p by the NEDD4 E3 ubiquitin ligase, Rsp5p, in the proteosome. Cdc42p turnover was regulated by HSPs at high temperatures, and in aging cells where the protein formed aggregates, implicating HSPs in Rho GTPase quality control. We also show that Cdc42pQ61L, which mimics the active (GTP-bound) conformation of the protein, was turned over at elevated levels by Ydj1p and Rsp5p. A turnover-defective version of Cdc42pQ61L led to multibudding phenotypes, implicating Cdc42 turnover in singularity in cell polarization. Cdc42p turnover also impacted MAP kinase pathway specificity. A pathway-specific scaffold, Bem4p, stabilized Cdc42p levels, which biased Cdc42p function in one MAPK pathway over another. Turnover regulation of Rho GTPases by HSPs and scaffolds provides new dimensions to the regulation of cell polarity and signal-dependent morphogenesis.

Rho GTPase–phosphatidylinositol phosphate interplay in fungal cell polarity

2014 ◽  
Vol 42 (1) ◽  
pp. 206-211 ◽  
Author(s):  
Robert A. Arkowitz ◽  
Martine Bassilana
Keyword(s):  
G Proteins ◽  
Cell Polarity ◽  
Rho Gtpase ◽  
Filamentous Growth ◽  
Polarized Growth ◽  
Fungal Cell ◽  
Cytoskeleton Organization ◽  
Phosphatidylinositol Phosphate ◽  
Phosphatidylinositol Phosphates

Rho G-proteins and phosphatidylinositol phosphates, which are important for exocytosis, endocytosis and cytoskeleton organization, are key regulators of polarized growth in a range of organisms. The aim of the present brief review is to highlight recent findings and their implications with respect to the functions and interplay between Rho G-proteins and phosphatidylinositol phosphates in highly polarized fungal filamentous growth.

scholarly journals Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond

2007 ◽  
Vol 71 (1) ◽  
pp. 48-96 ◽  
Author(s):  
Hay-Oak Park ◽  
Erfei Bi
Keyword(s):  
Cell Polarity ◽  
Budding Yeast ◽  
Cell Types ◽  
Mitotic Cell ◽  
Small Gtpases ◽  
Cell Polarization ◽  
Small Molecular Weight ◽  
Cell Wall Assembly ◽  
Substantial Progress ◽  
Wall Assembly

SUMMARY The establishment of cell polarity is critical for the development of many organisms and for the function of many cell types. A large number of studies of diverse organisms from yeast to humans indicate that the conserved, small-molecular-weight GTPases function as key signaling proteins involved in cell polarization. The budding yeast Saccharomyces cerevisiae is a particularly attractive model because it displays pronounced cell polarity in response to intracellular and extracellular cues. Cells of S. cerevisiae undergo polarized growth during various phases of their life cycle, such as during vegetative growth, mating between haploid cells of opposite mating types, and filamentous growth upon deprivation of nutrition such as nitrogen. Substantial progress has been made in deciphering the molecular basis of cell polarity in budding yeast. In particular, it becomes increasingly clear how small GTPases regulate polarized cytoskeletal organization, cell wall assembly, and exocytosis at the molecular level and how these GTPases are regulated. In this review, we discuss the key signaling pathways that regulate cell polarization during the mitotic cell cycle and during mating.

scholarly journals Transcriptional control of apical protein clustering drives de novo cell polarity establishment in the early mouse embryo

2020 ◽  
Author(s):  
Meng Zhu ◽  
Peizhe Wang ◽  
Charlotte E. Handford ◽  
Jie Na ◽  
Magdalena Zernicka-Goetz
Keyword(s):  
Cell Polarity ◽  
Mouse Embryo ◽  
Transcriptional Control ◽  
Molecular Mechanisms ◽  
Rho Gtpase ◽  
De Novo ◽  
Cell Polarization ◽  
Mammalian Embryo ◽  
Lineage Differentiation ◽  
Polarity Establishment

SummaryThe establishment of cell polarity de novo in the early mammalian embryo triggers the transition from totipotency to differentiation to generate embryonic and extra-embryonic lineages. However, the molecular mechanisms governing the timing of cell polarity establishment remain unknown. Here, we identify stage-dependent transcription of Tfap2c and Tead4 as well as Rho GTPase signaling as key for the onset of cell polarization. Importantly, advancing their activity can induce precocious cell polarization and ectopic lineage differentiation in a cell-autonomous manner. Moreover, we show that the asymmetric clustering of apical proteins, regulated by Tfap2c-Tead4, and not actomyosin flow, mediates apical protein polarization. These findings identify the long-sought mechanism for the onset of polarization and the first lineage segregation in the mouse embryo.

scholarly journals The Transforming Rho Family GTPase Wrch-1 Disrupts Epithelial Cell Tight Junctions and Epithelial Morphogenesis

2008 ◽  
Vol 29 (4) ◽  
pp. 1035-1049 ◽  
Author(s):  
Donita C. Brady ◽  
Jamie K. Alan ◽  
James P. Madigan ◽  
Alan S. Fanning ◽  
Adrienne D. Cox
Keyword(s):  
Epithelial Cell ◽  
Cell Polarity ◽  
Rho Gtpase ◽  
Mdck Cells ◽  
3D Culture ◽  
Cell Polarization ◽  
Epithelial Morphogenesis ◽  
Detectable Effect ◽  
Dependent Manner ◽  
Actin Organization

ABSTRACT Wrch-1, an atypical and transforming Rho GTPase, regulates cellular activities including proliferation and actin organization, but its functions and effectors remain poorly characterized. We show here that Wrch-1 distributes along the apical and basolateral membranes in MDCK cells and binds the cell polarity protein Par6 in a GTP-dependent manner. Activated Wrch-1 negatively regulates the kinetics of tight junction (TJ) assembly during epithelial cell polarization but has no detectable effect on overall cell polarity in confluent monolayers. It also causes a dramatic cytoskeletal reorganization and multilayering in cells grown in two-dimensional culture and disrupts cystogenesis of cells grown in three-dimensional (3D) culture. Similarly, short hairpin RNA-mediated knockdown of Wrch-1 perturbs cystogenesis in 3D culture, suggesting that tight regulation of Wrch-1 activity is necessary for normal epithelial morphogenesis. A weakly transforming effector domain mutant of activated Wrch-1 that inhibits Par6 binding abrogates the ability of Wrch-1 to disrupt TJ formation, actin organization, and epithelial morphogenesis. We hypothesize that Wrch-1-induced morphological and growth transformation may occur in part through Par6-mediated disruption of TJs and actin organization.

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