Correction: Dynamic Endothelial Cell Rearrangements Drive Developmental Vessel Regression

Franco, Cláudio A.; Jones, Martin L.; Bernabéu, Miguel O.; Geudens, Ilse; Mathivet, Thomas; Rosa, André; Lopes, Felicia M.; Lima, Aida P.; Ragab, Anan; Collins, Russell T.; Phng, Li-Kun; Coveney, Peter V.; Gerhardt, Holger

doi:10.1371/journal.pbio.1002163

Cited by 28 publications

(23 citation statements)

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“…Axial polarity correlates with the direction of migration in endothelial cells in vivo and in vitro (Franco et al, 2015; Kwon et al, 2016). Taking advantage of this feature, we generated a simplified method, compared to PIV analysis, to quantify the degree of coordination between cells by measuring the front-rear cell polarity (nucleus-to-Golgi apparatus axis) at the population level.…”

Section: Resultsmentioning

confidence: 99%

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Carvalho

Fortunato

Fonseca

et al. 2019

eLife

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Morphogenesis of hierarchical vascular networks depends on the integration of multiple biomechanical signals by endothelial cells, the cells lining the interior of blood vessels. Expansion of vascular networks arises through sprouting angiogenesis, a process involving extensive cell rearrangements and collective cell migration. Yet, the mechanisms controlling angiogenic collective behavior remain poorly understood. Here, we show this collective cell behavior is regulated by non-canonical Wnt signaling. We identify that Wnt5a specifically activates Cdc42 at cell junctions downstream of ROR2 to reinforce coupling between adherens junctions and the actin cytoskeleton. We show that Wnt5a signaling stabilizes vinculin binding to alpha-catenin, and abrogation of vinculin in vivo and in vitro leads to uncoordinated polarity and deficient sprouting angiogenesis in Mus musculus. Our findings highlight how non-canonical Wnt signaling coordinates collective cell behavior during vascular morphogenesis by fine-tuning junctional mechanocoupling between endothelial cells.

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Section: Resultsmentioning

confidence: 99%

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Carvalho

Fortunato

Fonseca

et al. 2019

eLife

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“…EC migration is an integral part of sprouting angiogenesis and vessel remodelling 13 . These events are not only controlled by tissue and serum-derived growth factors, but are also strongly influenced by flow mediated shear forces 6 , 10 , 11 , 35 , 36 . To fully understand the impact of flow on these properties requires in vivo live imaging approaches, pioneering work has been made in zebrafish 9 , 10 , 37 , 38 and chicken embryos 39 – 41 but mammalians are far less explored 6 .…”

Section: Discussionmentioning

confidence: 99%

“…In vascular development flow-mediated shear forces induce EC shape changes, polarization and directional migration 35 , 42 , 43 . Although the precise importance of such EC flow sensing in vascular patterning is not fully clarified it is affected in diseases such as atherosclerosis and Hereditary Haemorrhagic Telangiectasia (HHT), a vascular anomaly with arterio-venous malformations 6 , 44 – 46 .…”

Section: Discussionmentioning

confidence: 99%

“…Vascular morphogenesis requires pruning of superfluous connections, a process promoted by low shear, suggested to involve flow-instructed EC migration 15 , 16 , 35 , 47 . Through high resolution live imaging of the zebra fish vasculature, Affolter and colleagues presented two conceptually different ways of pruning 34 , one characterised by early stage condensation of multicellular lumens followed by bidirectional cellular retraction, and the other by separation into unicellular vessel segments (one cell per circumference), self-cell fusion and thereby lumen collapse 34 .…”

Section: Discussionmentioning

confidence: 99%

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Characterization of multi-cellular dynamics of angiogenesis and vascular remodelling by intravital imaging of the wounded mouse cornea

Wang

Jin

Laviña

et al. 2018

Sci Rep

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Establishment of the functional blood vasculature involves extensive cellular rearrangement controlled by growth factors, chemokines and flow-mediated shear forces. To record these highly dynamic processes in mammalians has been technically demanding. Here we apply confocal and wide field time-lapse in vivo microscopy to characterize the remodelling vasculature of the wounded mouse cornea. Using mouse lines with constitutive or inducible endogenous fluorescent reporters, in combination with tracer injections and mosaic genetic recombination, we follow processes of sprouting angiogenesis, sprout fusion, vessel expansion and pruning in vivo, at subcellular resolution. We describe the migratory behaviour of endothelial cells of perfused vessels, in relation to blood flow directionality and vessel identity. Live-imaging following intravascular injection of fluorescent tracers, allowed for recording of VEGFA-induced permeability. Altogether, live-imaging of the remodelling vasculature of inflamed corneas of mice carrying endogenous fluorescent reporters and conditional alleles, constitutes a powerful platform for investigation of cellular behaviour and vessel function.

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“…Two sprouts eventually fuse to form vessel loops that can then support blood flow (figure 1a). This process repeats iteratively, building up a dense looped network (the 'primary plexus') that is later remodelled and pruned through cell rearrangement and blood flow to a more familiar hierarchical tree-like structure [18,19].…”

Section: Introductionmentioning

confidence: 99%

Active perception during angiogenesis: filopodia speed up Notch selection of tip cells in silico and* in vivo*

Zakirov

Charalambous

Thuret

et al. 2021

Phil. Trans. R. Soc. B

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How do cells make efficient collective decisions during tissue morphogenesis? Humans and other organisms use feedback between movement and sensing known as ‘sensorimotor coordination’ or ‘active perception’ to inform behaviour, but active perception has not before been investigated at a cellular level within organs. Here we provide the first proof of concept in silico / in vivo study demonstrating that filopodia (actin-rich, dynamic, finger-like cell membrane protrusions) play an unexpected role in speeding up collective endothelial decisions during the time-constrained process of ‘tip cell’ selection during blood vessel formation (angiogenesis). We first validate simulation predictions in vivo with live imaging of zebrafish intersegmental vessel growth. Further simulation studies then indicate the effect is due to the coupled positive feedback between movement and sensing on filopodia conferring a bistable switch-like property to Notch lateral inhibition, ensuring tip selection is a rapid and robust process. We then employ measures from computational neuroscience to assess whether filopodia function as a primitive (basal) form of active perception and find evidence in support. By viewing cell behaviour through the ‘basal cognitive lens' we acquire a fresh perspective on the tip cell selection process, revealing a hidden, yet vital time-keeping role for filopodia. Finally, we discuss a myriad of new and exciting research directions stemming from our conceptual approach to interpreting cell behaviour. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.

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Correction: Dynamic Endothelial Cell Rearrangements Drive Developmental Vessel Regression

Cited by 28 publications

References 1 publication

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Characterization of multi-cellular dynamics of angiogenesis and vascular remodelling by intravital imaging of the wounded mouse cornea

Active perception during angiogenesis: filopodia speed up Notch selection of tip cells in silico and* in vivo*

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Correction: Dynamic Endothelial Cell Rearrangements Drive Developmental Vessel Regression

Cited by 28 publications

References 1 publication

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Non-canonical Wnt signaling regulates junctional mechanocoupling during angiogenic collective cell migration

Characterization of multi-cellular dynamics of angiogenesis and vascular remodelling by intravital imaging of the wounded mouse cornea

Active perception during angiogenesis: filopodia speed up Notch selection of tip cells in silico and in vivo

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Product

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Active perception during angiogenesis: filopodia speed up Notch selection of tip cells in silico and* in vivo*