Adhesion to nanofibers drives cell membrane remodeling through one-dimensional wetting

Charles-Orszag, Arthur; Tsai, Feng-Ching; Bonazzi, Daria; Manrı́quez, V.; Sachse, Martin; Mallet, Adeline; Salles, Audrey; Melican, Keira; Staneva, Ralitza; Bertin, Aurélie; Millien, Corinne; Goussard, Sylvie; Lafaye, Pierre; Shorte, Spencer; Piel, Matthieu; Krijnse‐Locker, Jacomine; Brochard‐Wyart, Françoise; Bassereau, Patricia; Duménil, Gérard

doi:10.1038/s41467-018-06948-x

Cited by 26 publications

(17 citation statements)

References 78 publications

(79 reference statements)

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“…Furthermore, the membrane-MT interface, with the membrane partly wrapping around the MT cylinder, might lead to a higher number of contacts that together can sustain higher forces compared to a MT interface with a spherical bead. The forces generated by the combination of membrane-MT shaft interactions and the TAC complex are of the same order of magnitude as the forces generating membrane tubes by one-dimensional wetting 39 . Interestingly, the forces generated when the same MT-membrane connecting molecules are attached to shrinking MTs are an order of magnitude higher than those mediated by TACs, possibly because the attachment geometry is significantly different at depolymerizing ends.…”

Section: Discussionmentioning

confidence: 91%

Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules

Rodríguez-García

Chen

Katrukha

et al. 2019

Preprint

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Microtubule-dependent organization of membrane organelles, such as the endoplasmic reticulum, occurs through motor-based pulling and by coupling polymer dynamics to membrane remodeling. Membrane binding to dynamic microtubule ends involves transient interactions, but how such interactions can lead to membrane deformation is unclear.Here, we reconstitute membrane tubulation in a minimal system with giant unilamellar vesicles, dynamic microtubules, End-Binding (EB) proteins and a membrane-targeted polypeptide that interacts with EBs and microtubules. We demonstrate that these components are sufficient to induce not only membrane tubulation by growing microtubule ends, but also motor-independent membrane sliding along microtubule shafts and tube pulling by shrinking microtubules. Experiments and modeling reveal that the first two mechanisms can be explained by adhesion-driven biased membrane spreading on microtubules. Attachments to growing and shrinking microtubule ends can sustain forces of ~0.5 and ~5 pN, respectively. Rapidly exchanging molecules that connect membranes to dynamic microtubules can thus induce membrane tubulation and processive tube motility. 7 linked to membranes can promote some membrane tubulation, but the generation of long membrane tubes occurs much more efficiently when an EB3 protein is combined with a MT-binding membrane-attached peptide. MT-dependent membrane tubulation is limited by tensionPrevious studies have shown that ligand-dependent adhesion of GUVs to the surface of a solid substrate or to a nanofiber triggered the formation of membrane tubules 37-39 . When a GUV faces an adhesive substrate in the presence of mobile ligands, the ligands that bind to the substrate move to the contact region and increase the adhesion strength 40, 41 . We investigated whether His-GFP-SxIP was enriched in the regions where GUVs interacted with MTs and found that the average fluorescence intensity of the His-GFP-SxIP on MTs bound to the membrane was indeed higher than on free MTs or membranes that were not in contact with MTs (Fig. 3a,b). His-GFP-SxIP proteins thus converged towards the sites of MT-membrane contact, suggesting an increase in the number of bonds between the two structures.Next, we investigated the dynamics of formation of tubular membrane networks by measuring GUV sphericity 36 over time. At the beginning of the assay, sphericity quickly decreased, indicating that the network of membrane tubes rapidly expanded (Fig. 3c,d). At later time points, the sphericity value became almost constant as tube extension slowed down ( Fig. 3c,d, and Supplementary Video 1). We hypothesized that this was caused by the increase in lateral tension after the excess of membrane area was used up due to membrane redistribution into tubes [42][43][44][45] . To test this possibility, we characterized thermal membrane fluctuations, which are controlled by the balance between thermal energy, lateral tension and membrane stiffness 4, 5 . Flickering spectroscopy 46, 47 was used to analyze membrane undulations in fre...

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Section: Discussionmentioning

confidence: 91%

Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules

Rodríguez-García

Chen

Katrukha

et al. 2019

Preprint

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“…First described as epithelial microvilli‐like structures due to their shape and ezrin content (Eugene et al, ), these protrusions are reminiscent of the leukocytes docking structures that form at sites of inflammation upon binding to endothelial cells and allow leukocyte endothelial transmigration (Doulet et al, ). As for leukocytes, these protrusions, formed alongside Tfp fibres (Charles‐Orszag et al, ), strengthen bacterial‐endothelial interactions for resisting shear‐force exerted by the blood flow (Mikaty et al, ). In addition, these protrusions promote bacterial invagination within intracellular vacuoles.…”

Section: Bacterial Stabilisation At the Endothelial Cell Surface And mentioning

confidence: 99%

Meningococcal disease: A paradigm of type‐IV pilus dependent pathogenesis

Souza

Maïssa

Ziveri

et al. 2020

Cellular Microbiology

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Neisseria meningitidis (meningococcus) is a Gram‐negative bacterium responsible for two devastating forms of invasive diseases: purpura fulminans and meningitis. Interaction with both peripheral and cerebral microvascular endothelial cells is at the heart of meningococcal pathogenesis. During the last two decades, an essential role for meningococcal type IV pili in vascular colonisation and disease progression has been unravelled. This review summarises 20 years of research on meningococcal type IV pilus‐dependent virulence mechanisms, up to the identification of promising anti‐virulence compounds that target type IV pili.

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“…This cell signalling is responsible for the elongation of host‐cell membrane protrusions that stabilise bacterial colonies at the surface of blood vessels (Coureuil et al, ; Lambotin et al, ; Mikaty et al, ). Besides, it has been recently proposed that the interaction of Tfp with host‐cell plasma membrane triggers its remodelling as discrete and dynamic protrusions in a process reminiscent of membrane wetting (referred to as 1D‐wetting; Charles‐Orszag et al, ). The authors suggest that membrane 1D‐wetting drives subsequent actin polymerisation and recruitment of cortical plaque associated proteins.…”

Section: Blood‐borne Colonisation Of the Vascular Compartmentmentioning

confidence: 99%

Molecular interactions betweenNeisseria meningitidisand its human host

Coureuil

Jamet

Bille

et al. 2019

Cellular Microbiology

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Neisseria meningitidis is a Gram‐negative bacterium that asymptomatically colonises the nasopharynx of humans. For an unknown reason, N. meningitidis can cross the nasopharyngeal barrier and invade the bloodstream where it becomes one of the most harmful extracellular bacterial pathogen. This infectious cycle involves the colonisation of two different environments. (a) In the nasopharynx, N. meningitidis grow on the top of mucus‐producing epithelial cells surrounded by a complex microbiota. To survive and grow in this challenging environment, the meningococcus expresses specific virulence factors such as polymorphic toxins and MDAΦ. (b) Meningococci have the ability to survive in the extra cellular fluids including blood and cerebrospinal fluid. The interaction of N. meningitidis with human endothelial cells leads to the formation of typical microcolonies that extend overtime and promote vascular injury, disseminated intravascular coagulation, and acute inflammation. In this review, we will focus on the interplay between N. meningitidis and these two different niches at the cellular and molecular level and discuss the use of inhibitors of piliation as a potent therapeutic approach.

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Adhesion to nanofibers drives cell membrane remodeling through one-dimensional wetting

Cited by 26 publications

References 78 publications

Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules

Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules

Meningococcal disease: A paradigm of type‐IV pilus dependent pathogenesis

Molecular interactions betweenNeisseria meningitidisand its human host

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