Phagocytosis is coupled to the formation of phagosome-associated podosomes and a transient disruption of podosomes in human macrophages

Tertrais, Margot; Bigot, Claire; Martin, Emmanuel; Poincloux, Renaud; Labrousse, Arnaud; Maridonneau‐Parini, Isabelle

doi:10.1016/j.ejcb.2021.151161

Cited by 9 publications

(7 citation statements)

References 66 publications

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“…While actin-based puncta have been previously observed during phagocytosis of stiffer polystyrene beads ( Barger et al, 2019 ; Ostrowski et al, 2019 ), their presence in multiple phagocytic cell types ( Figure 4c ) and during complement-mediated phagocytosis ( Ostrowski et al, 2019 ) suggests a common role in internalization. Structures with podosome-like features, albeit resistant to CK666 treatment, have also been reported on closed phagosomes containing IgG or serum-opsonized polystyrene targets ( Tertrais et al, 2021 ). We find that phagocytic actin teeth are podosome-like in protein composition, consisting of mostly branched F-actin and actin regulatory proteins.…”

Section: Discussionmentioning

confidence: 94%

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

Vorselen

Barger

Wang

et al. 2021

eLife

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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.

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Section: Discussionmentioning

confidence: 94%

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

Vorselen

Barger

Wang

et al. 2021

eLife

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“…Podosomes and podosome-like structures all appear to consist of a tightly packed actin core surrounded by a looser actin meshwork which includes radial actin fibers that extend away from the core 12 . The structures formed during phagocytosis have been called podosome-like structures 13 – 15 , phagocytic teeth 16 and phagosome-associated podosomes 17 . Phagocytic podosomes recruit proteins like those in other podosomes, but they are shorter-lived, with higher turnover at the phagocytic cup 15 .…”

Section: Introductionmentioning

confidence: 99%

“…Phagocytic podosomes recruit proteins like those in other podosomes, but they are shorter-lived, with higher turnover at the phagocytic cup 15 . On closed phagosomes, podosomes were found to be partially resistant to inhibition of the actin nucleator Arp2/3 17 , a key component of conventional podosomes. In contrast, the number of phagocytic teeth at the phagocytic cup were significantly reduced upon the inhibition of Arp2/3 16 .…”

Section: Introductionmentioning

confidence: 99%

Actin nano-architecture of phagocytic podosomes

Herron

Watanabe

et al. 2022

Nat Commun

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Podosomes are actin-enriched adhesion structures important for multiple cellular processes, including migration, bone remodeling, and phagocytosis. Here, we characterize the structure and organization of phagocytic podosomes using interferometric photoactivated localization microscopy, a super-resolution microscopy technique capable of 15–20 nm resolution, together with structured illumination microscopy and localization-based super-resolution microscopy. Phagocytic podosomes are observed during frustrated phagocytosis, a model in which cells attempt to engulf micropatterned IgG antibodies. For circular patterns, this results in regular arrays of podosomes with well-defined geometry. Using persistent homology, we develop a pipeline for semi-automatic identification and measurement of podosome features. These studies reveal an hourglass shape of the podosome actin core, a protruding knob at the bottom of the core, and two actin networks extending from the core. Additionally, the distributions of paxillin, talin, myosin II, α-actinin, cortactin, and microtubules relative to actin are characterized.

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Section: Introductionmentioning

confidence: 99%

“…Podosomes and podosome-like structures all appear to consist of a tightly packed actin core surrounded by a looser actin meshwork which includes radial actin fibers that extend away from the core 12 . The structures formed during phagocytosis have been called "podosome-like structures" [13][14][15] , phagocytic "teeth" 16 and phagosome-associated podosomes 17 . Phagocytic podosomes recruit proteins like those in other podosomes, but they are shorter-lived, with higher turnover at the phagocytic cup 15 .…”

Section: Introductionmentioning

confidence: 99%

Actin nano-architecture of phagocytic podosomes

Herron

Watanabe

et al. 2022

Preprint

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Podosomes are actin-enriched adhesion structures important for multiple cellular processes, including migration, bone remodeling, and phagocytosis. Here, we characterized the structure and organization of phagocytic podosomes using interferometric photoactivated localization microscopy (iPALM), a super-resolution microscopy technique capable of 15-20 nm resolution, together with structured illumination microscopy (SIM) and localization-based superresolution microscopy. Phagocytic podosomes were observed during frustrated phagocytosis, a model in which cells attempt to engulf micro-patterned IgG antibodies. For circular patterns, this resulted in regular arrays of podosomes with well-defined geometry. Using persistent homology, we developed a pipeline for semi-automatic identification and measurement of podosome features. These studies revealed an “hourglass” shape of the podosome actin core, a protruding “knob” at the bottom of the core, and two actin networks extending from the core. Additionally, the distributions of paxillin, talin, myosin II, α-actinin, cortactin, and microtubules relative to actin were characterized.

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Phagocytosis is coupled to the formation of phagosome-associated podosomes and a transient disruption of podosomes in human macrophages

Cited by 9 publications

References 66 publications

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

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

Actin nano-architecture of phagocytic podosomes

Actin nano-architecture of phagocytic podosomes

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