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

Mapping Intimacies ◽

10.1101/734665 ◽

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

Download Full-text

Rho-GTPase-regulated vesicle trafficking in plant cell polarity

Biochemical Society Transactions ◽

10.1042/bst20130269 ◽

2014 ◽

Vol 42 (1) ◽

pp. 212-218 ◽

Cited By ~ 14

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.

Download Full-text

Ligation of the cell surface receptor, CD46, alters T cell polarity and response to antigen presentation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0602458103 ◽

2006 ◽

Vol 103 (49) ◽

pp. 18685-18690 ◽

Cited By ~ 38

Author(s):

J. Oliaro ◽

A. Pasam ◽

N. J. Waterhouse ◽

K. A. Browne ◽

M. J. Ludford-Menting ◽

...

Keyword(s):

T Cell ◽

Cell Surface ◽

Antigen Presentation ◽

Cell Polarity ◽

Cell Surface Receptor ◽

Surface Receptor

Download Full-text

The microstructure of laminin-111 compensates for dystroglycan loss in functional differentiation of mammary epithelial cells

10.1101/531053 ◽

2019 ◽

Author(s):

A Kent ◽

N Mayer ◽

JL Inman ◽

C Hochman-Mendez ◽

MJ Bissell ◽

...

Keyword(s):

Epithelial Cells ◽

Cell Surface ◽

Mammary Epithelial Cells ◽

Milk Proteins ◽

Fractal Dimensions ◽

Functional Differentiation ◽

Mammary Epithelial ◽

Cell Surface Receptor ◽

List Type ◽

Surface Receptor

Abstract:Laminin-111, an extracellular matrix (ECM) glycoprotein found in the basement membrane of mammary gland epithelia, is essential for lactation. In mammary epithelial cells, dystroglycan (Dg) is believed to be necessary for polymerization of laminin-111 into networks, thus we asked whether correct polymerization could compensate for Dg loss. Artificially polymerized laminin-111 and the laminin-glycoprotein mix Matrigel, both formed branching, spread networks with fractal dimensions from 1.7-1.8, whereas laminin-111 in media formed small aggregates without fractal properties (a fractal dimension of 2). In Dg knockout cells, either polymerized laminin-111 or Matrigel readily attached to the cell surface, whereas aggregated laminin-111 did not. In contrast, polymerized and aggregated laminin-111 bound similarly to Dg knock-ins. Both polymerized laminin-111 and Matrigel promoted cell rounding, clustering, formation of tight junctions, and expression of milk proteins, whereas aggregated Ln-1 did not attach to cells or promote functional differentiation.HighlightsLaminin assembles into a fractal network when in presence of either the cell surface receptor dystroglycan or acidic glycoproteins or an acidic buffer.When this microstructure is recreated with an acidic treatment, laminin binds readily to dystroglycan null cells and induces functional differentiation of mammary epithelial cells.

Download Full-text

Identification of genes required for normal pheromone-induced cell polarization in Saccharomyces cerevisiae.

Genetics ◽

10.1093/genetics/136.4.1287 ◽

1994 ◽

Vol 136 (4) ◽

pp. 1287-1296 ◽

Cited By ~ 6

Author(s):

J Chenevert ◽

N Valtz ◽

I Herskowitz

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Surface ◽

Cell Polarity ◽

Vegetative Growth ◽

Cell Polarization ◽

Yeast Saccharomyces Cerevisiae ◽

A Cell ◽

Uniform Manner ◽

Mating Factor ◽

Type Strains

Abstract In response to mating pheromones, cells of the yeast Saccharomyces cerevisiae adopt a polarized "shmoo" morphology, in which the cytoskeleton and proteins involved in mating are localized to a cell-surface projection. This polarization is presumed to reflect the oriented morphogenesis that occurs between mating partners to facilitate cell and nuclear fusion. To identify genes involved in pheromone-induced cell polarization, we have isolated mutants defective in mating to an enfeebled partner and studied a subset of these mutants. The 34 mutants of interest are proficient for pheromone production, arrest in response to pheromone, mate to wild-type strains, and exhibit normal cell polarity during vegetative growth. The mutants were divided into classes based on their morphological responses to mating pheromone. One class is unable to localize cell-surface growth in response to mating factor and instead enlarges in a uniform manner. These mutants harbor special alleles of genes required for cell polarization during vegetative growth, BEM1 and CDC24. Another class of mutants forms bilobed, peanut-like shapes when treated with pheromone and defines two genes, PEA1 and PEA2. PEA1 is identical to SPA2. A third class forms normally shaped but tiny shmoos and defines the gene TNY1. A final group of mutants exhibits apparently normal shmoo morphology. The nature of their mating defect is yet to be determined. We discuss the possible roles of these gene products in establishing cell polarity during mating.

Download Full-text

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

10.1101/2020.02.10.942201 ◽

2020 ◽

Cited By ~ 1

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.

Download Full-text

Role of TGF-β receptor III localization in polarity and breast cancer progression

Molecular Biology of the Cell ◽

10.1091/mbc.e14-03-0825 ◽

2014 ◽

Vol 25 (15) ◽

pp. 2291-2304 ◽

Cited By ~ 10

Author(s):

Alison E. Meyer ◽

Catherine E. Gatza ◽

Tam How ◽

Mark Starr ◽

Andrew B. Nixon ◽

...

Keyword(s):

Breast Cancer ◽

Epithelial Cells ◽

Cell Surface ◽

Cell Polarity ◽

Cancer Progression ◽

Breast Cancer Progression ◽

Cell Surface Receptor ◽

Single Amino Acid ◽

Migration And Invasion ◽

Mesenchymal Transition

The majority of breast cancers originate from the highly polarized luminal epithelial cells lining the breast ducts. However, cell polarity is often lost during breast cancer progression. The type III transforming growth factor-β cell surface receptor (TβRIII) functions as a suppressor of breast cancer progression and also regulates the process of epithelial-to-mesenchymal transition (EMT), a consequence of which is the loss of cell polarity. Many cell surface proteins exhibit polarized expression, being targeted specifically to the apical or basolateral domains. Here we demonstrate that TβRIII is basolaterally localized in polarized breast epithelial cells and that disruption of the basolateral targeting of TβRIII through a single amino acid mutation of proline 826 in the cytosolic domain results in global loss of cell polarity through enhanced EMT. In addition, the mistargeting of TβRIII results in enhanced proliferation, migration, and invasion in vitro and enhanced tumor formation and invasion in an in vivo mouse model of breast carcinoma. These results suggest that proper localization of TβRIII is critical for maintenance of epithelial cell polarity and phenotype and expand the mechanisms by which TβRIII prevents breast cancer initiation and progression.

Download Full-text