Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis

Phagocytosis requires rapid actin reorganization and spatially controlled force generation to ingest targets ranging from pathogens to apoptotic cells. How actomyosin activity directs membrane extensions to engulf such diverse targets remains unclear. Here, we combine lattice light-sheet microscopy...

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Autores principales: Daan Vorselen, Sarah R Barger, Yifan Wang, Wei Cai, Julie A Theriot, Nils C Gauthier, Mira Krendel
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Publicado: eLife Sciences Publications Ltd 2021
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spelling oai:doaj.org-article:aef0f4ad09434fbab2364d8bb7e93e642021-11-24T12:33:37ZPhagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis10.7554/eLife.686272050-084Xe68627https://doaj.org/article/aef0f4ad09434fbab2364d8bb7e93e642021-10-01T00:00:00Zhttps://elifesciences.org/articles/68627https://doaj.org/toc/2050-084XPhagocytosis requires rapid actin reorganization and spatially controlled force generation to ingest targets ranging from pathogens to apoptotic cells. How actomyosin activity directs membrane extensions to engulf such diverse targets remains unclear. Here, we combine lattice light-sheet microscopy (LLSM) with microparticle traction force microscopy (MP-TFM) to quantify actin dynamics and subcellular forces during macrophage phagocytosis. We show that spatially localized forces leading to target constriction are prominent during phagocytosis of antibody-opsonized targets. This constriction is largely driven by Arp2/3-mediated assembly of discrete actin protrusions containing myosin 1e and 1f (‘teeth’) that appear to be interconnected in a ring-like organization. Contractile myosin-II activity contributes to late-stage phagocytic force generation and progression, supporting a specific role in phagocytic cup closure. Observations of partial target eating attempts and sudden target release via a popping mechanism suggest that constriction may be critical for resolving complex in vivo target encounters. Overall, our findings present a phagocytic cup shaping mechanism that is distinct from cytoskeletal remodeling in 2D cell motility and may contribute to mechanosensing and phagocytic plasticity.Daan VorselenSarah R BargerYifan WangWei CaiJulie A TheriotNils C GauthierMira KrendeleLife Sciences Publications LtdarticlephagocytosiscytoskeletonactinmyosinMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic phagocytosis
cytoskeleton
actin
myosin
Medicine
R
Science
Q
Biology (General)
QH301-705.5
spellingShingle phagocytosis
cytoskeleton
actin
myosin
Medicine
R
Science
Q
Biology (General)
QH301-705.5
Daan Vorselen
Sarah R Barger
Yifan Wang
Wei Cai
Julie A Theriot
Nils C Gauthier
Mira Krendel
Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
description Phagocytosis requires rapid actin reorganization and spatially controlled force generation to ingest targets ranging from pathogens to apoptotic cells. How actomyosin activity directs membrane extensions to engulf such diverse targets remains unclear. Here, we combine lattice light-sheet microscopy (LLSM) with microparticle traction force microscopy (MP-TFM) to quantify actin dynamics and subcellular forces during macrophage phagocytosis. We show that spatially localized forces leading to target constriction are prominent during phagocytosis of antibody-opsonized targets. This constriction is largely driven by Arp2/3-mediated assembly of discrete actin protrusions containing myosin 1e and 1f (‘teeth’) that appear to be interconnected in a ring-like organization. Contractile myosin-II activity contributes to late-stage phagocytic force generation and progression, supporting a specific role in phagocytic cup closure. Observations of partial target eating attempts and sudden target release via a popping mechanism suggest that constriction may be critical for resolving complex in vivo target encounters. Overall, our findings present a phagocytic cup shaping mechanism that is distinct from cytoskeletal remodeling in 2D cell motility and may contribute to mechanosensing and phagocytic plasticity.
format article
author Daan Vorselen
Sarah R Barger
Yifan Wang
Wei Cai
Julie A Theriot
Nils C Gauthier
Mira Krendel
author_facet Daan Vorselen
Sarah R Barger
Yifan Wang
Wei Cai
Julie A Theriot
Nils C Gauthier
Mira Krendel
author_sort Daan Vorselen
title Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
title_short Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
title_full Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
title_fullStr Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
title_full_unstemmed Phagocytic ‘teeth’ and myosin-II ‘jaw’ power target constriction during phagocytosis
title_sort phagocytic ‘teeth’ and myosin-ii ‘jaw’ power target constriction during phagocytosis
publisher eLife Sciences Publications Ltd
publishDate 2021
url https://doaj.org/article/aef0f4ad09434fbab2364d8bb7e93e64
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