Integrin Mechano-chemical Signaling Generates Plasma Membrane Nanodomains that Promote Cell Spreading

Kalappurakkal, Joseph Mathew; Anilkumar, Anupama Ambika; Patra, Chandrima; Zanten, Thomas S. van; Sheetz, Michael P.; Mayor, Satyajit

doi:10.1016/j.cell.2019.04.037

Cited by 115 publications

(123 citation statements)

References 96 publications

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“…To study the detailed physical interactions of FLS2 receptors in the multivalent nanoclusters, we took advantage of a well-established living cell imaging approaches in studying mammalian receptor clustering and activation (38, 39). We quantitatively measured the lateral self-interaction of FLS2 on the plasma membrane directly under ligand activation by performing FRET between identical fluorophores (homo-FRET) coupled with VAEM, which allows sensitive measurement of fast cargo-induced receptor activation (40).…”

Section: Resultsmentioning

confidence: 99%

“…Dynamic behaviors of PM proteins, including the endocytic invagination, lateral diffusion, and inter-molecular interactions, rely on the lipid-compartmentalization and a balanced sterol composition of the plasma membrane (39, 48). We next sought to determine if the lipid profile of Arabidopsis was also altered by DSF, given that this QS signal is a short-chain fatty acid-like molecule that could serve as a building block to create diverse biologically active molecules (2).…”

Section: Resultsmentioning

confidence: 99%

“…Similar to many other immune-receptors (99), unstimulated Arabidopsis FLS2 could be in a dimer form (41). Our living cell homo-FRET approach allowed us to quantitatively measure the dynamic formation of the nanoclusters of plant surface molecules (39). Homo-FRET experiments revealed that flagellin triggered the nano-clustering of FLS2 from a less to more oligomerized, representing a transition from the unstimulated to active state during early immune responses.…”

Section: Discussionmentioning

confidence: 99%

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The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

Tran

Triebl

et al. 2020

Preprint

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36Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-37 related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is 38 largely under-studied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) 39 produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular 40 pattern (PAMP)-triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation 41 of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of 42 oligomerization states and endocytic internalization of plasma membrane FLS2. DSF altered the lipid 43 profile of Arabidopsis, with a particular increase of the phytosterol species, which impairs the general 44 endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF 45 effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. 46Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization 47 and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to 48 manipulate PAMP-triggered host immunity. 49 50 Keywords: quorum sensing, plasma membrane, endocytosis, plant-pathogen interaction 51 52 SIGNIFICANCE STATEMENT 53Bacteria rely on small signalling molecules called quorum sensing (QS) signals to communicate 54 and coordinate their behaviors. QS is known to regulate gene expression, production of virulence factors, 55 and biofilm formation for pathogenic bacteria to effectively colonize their hosts and cause diseases. In this 56 work, we found a class of QS molecule called diffusible-signal factor (DSF), produced by devastating 57 phytopathogenic bacteria such as Xanthomonas spp. and Xylella fastidiosa, could communicate directly 58 with plant host and subvert plant innate immunity by inducing plant sterol production and thereby, 59 attenuating receptor signalling through hindering the receptor clustering and plant endocytosis. The 60 results significantly enrich our understanding of the mechanisms in the tug-of-war between bacterial 61 pathogenesis and host immunity. 62 63 infection (4). The 3OC12-HSL was also shown to be recognized by the bitter taste receptor, T2R family 73 protein, T2R38 in neutrophils, lymphocytes and monocytes to activate innate immune responses (5). 74Similarly, plant pathogenic bacteria also secrete small-molecule virulence factors to cross-talk with host 75 and manipulate host immunity during infection. QS molecules produced by several bacterial 76 phytopathogens showed a wide range of interference in host development and defence mechanisms, 77including the root morphological development in an auxin-dependent manner or callose deposition during 78 immune responses (6-8). However, the detailed mechanisms of how QS molecules directly influence 79 plant host development and pathology, especially the PAMP-mediated host immunity,...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

Tran

Triebl

et al. 2020

Preprint

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“…Our study shows that in the absence of stratification, steric effects would preclude such lateral nanoscale proximity. This has functional implications, since for example, cholesterol-dependent GPIanchored protein nanoclustering is necessary for promoting integrin function [47,48]. We take up some of these issues in a later study.…”

Section: Discussionmentioning

confidence: 99%

Assemblies of F-actin and myosin-II minifilaments: steric hindrance and stratification at the membrane cortex

Das

Bhat

Sknepnek

et al. 2019

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Recent in-vivo studies have revealed that several membrane proteins are driven to form nanoclusters by active contractile flows arising from F-actin and myosin at the cortex. The mechanism of clustering was shown to be arising from the dynamic patterning of transient contractile platforms (asters) generated by actin and myosin. Myosin-II, which assemble as minifilaments consisting of tens of myosin heads, are rather bulky structures and hence a concern could be that steric considerations might obstruct the emergence of nanoclustering. Here, using coarse-grained, agent-based simulations that respect the size of constituents, we find that in the presence of steric hindrance, the patterns exhibited by actomyosin in two dimensions, do not resemble the steady state patterns observed in our in-vitro reconstitution of actomyosin on a supported bilayer. We then perform simulations in a thin rectangular slab, allowing the separation of a layer of actin filaments from those of myosin-II minifilaments. This recapitulates the observed features of in-vitro patterning. Using super resolution microscopy, we find direct evidence for stratification in our in-vitro system. Our study suggests the possibility that molecular stratification may be an important organising feature of the cortical cytoskeleton in-vivo. † Equal contribution

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“…These systems are expected to play crucial roles in many cellular mechanoadaptive processes by shaping PM topology in association with the underlying cell cortex. Such processes have been investigated at nanoscale resolution through electron microscopy or advance light microscopy, and their nanoscale dynamics has just begun to be revealed by a handful of high-end microscopy techniques including fluorescence life-time, Föster resonance energy transfer, or fluorescence correlation spectroscopy (Kalappurakkal et al ., 2019; Saka et al ., 2014; Chugh et al ., 2017). However, the mesoscale architectural organization and dynamics of the PM-cortex association are far less understood.…”

Section: Introductionmentioning

confidence: 99%

Mesoscale Dynamics of Spectrin and Acto-Myosin shape Membrane Territories during Mechanoresponse

Ghisleni

Galli

Monzo

et al. 2019

Preprint

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The spectrin cytoskeleton is a major component of the cell cortex. While ubiquitously expressed, its dynamic interaction with the other cortex components, including the plasma membrane or the acto-myosin cytoskeleton, is poorly understood. Here, we investigated how the spectrin cytoskeleton re-organizes spatially and dynamically under the membrane during changes in cell mechanics. We found spectrin and acto-myosin cytoskeletons to be spatially distinct but cooperating during mechanical challenges, such as cell adhesion and contraction, or compression, stretch and osmolarity fluctuations, creating a cohesive cortex supporting the plasma membrane. Actin territories control protrusions and contractile structures while spectrin territories concentrate in retractile zones and low-actin density/inter-contractile regions, acting as a fence to organize membrane trafficking events. We unveil here the existence of a dynamic interplay between acto-myosin and spectrin cytoskeletons necessary to support a mesoscale organization of the lipid bilayer into spatially-confined cortical territories during cell mechanoresponse.

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Integrin Mechano-chemical Signaling Generates Plasma Membrane Nanodomains that Promote Cell Spreading

Cited by 115 publications

References 96 publications

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

Assemblies of F-actin and myosin-II minifilaments: steric hindrance and stratification at the membrane cortex

Mesoscale Dynamics of Spectrin and Acto-Myosin shape Membrane Territories during Mechanoresponse

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