S100A4 regulates macrophage invasion by distinct myosin-dependent and myosin-independent mechanisms

Dulyaninova, Natalya G.; Ruiz, Penelope D.; Gamble, Matthew J.; Backer, Jonathan M.; Bresnick, Anne R.

doi:10.1091/mbc.e17-07-0460

Cited by 22 publications

(24 citation statements)

References 70 publications

(93 reference statements)

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“…The antagonism between myosin-II filaments overproduction and podosome formation was documented in previous studies [46][47][48][49][50], but the mechanism underlying this antagonism is insufficiently understood. Here we studied the time course of podosome disruption upon activation of myosin-II filament assembly under condition when localization of podosomes is defined by a micropatterned substrate ( Figure 1A-D, Supplementary movie 1).…”

Section: Disruptive Effect Of Myosin-ii Filament Assembly On Podosomementioning

confidence: 92%

“…In agreement with this premise, recent experimental evidence shows that myosin-II filaments play an inhibitory rather than stimulatory role in podosome formation. Activation of myosin-IIA filament formation by a number of pathways converging to Rho/ROCK signaling axis [46][47][48][49] as well as depletion of the regulatory protein S100A4 [50] promote podosome disassembly. Proteins known as supervillin and LSP-1 (lymphocyte-specific protein-1) appear to control the disruptive effect of myosin-IIA on podosomes by regulating the recruitment of myosin-IIA to the podosome environs [46,47].…”

Section: Introductionmentioning

confidence: 99%

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Forces and constraints controlling podosome assembly and disassembly

Rafiq

Grenci

Lim

et al. 2019

Phil. Trans. R. Soc. B

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Podosomes are a singular category of integrin-mediated adhesions important in the processes of cell migration, matrix degradation and cancer cell invasion. Despite a wealth of biochemical studies, the effects of mechanical forces on podosome integrity and dynamics are poorly understood. Here, we show that podosomes are highly sensitive to two groups of physical factors. First, we describe the process of podosome disassembly induced by activation of myosin-IIA filament assembly. Next, we find that podosome integrity and dynamics depends upon membrane tension and can be experimentally perturbed by osmotic swelling and deoxycholate treatment. We have also found that podosomes can be disrupted in a reversible manner by single or cyclic radial stretching of the substratum. We show that disruption of podosomes induced by osmotic swelling is independent of myosin-II filaments. The inhibition of the membrane sculpting protein, dynamin-II, but not clathrin, resulted in activation of myosin-IIA filament formation and disruption of podosomes. The effect of dynamin-II inhibition on podosomes was, however, independent of myosin-II filaments. Moreover, formation of organized arrays of podosomes in response to microtopographic cues (the ridges with triangular profile) was not accompanied by reorganization of myosin-II filaments. Thus, mechanical elements such as myosin-II filaments and factors affecting membrane tension/sculpting independently modulate podosome formation and dynamics, underlying a versatile response of these adhesion structures to intracellular and extracellular cues. This article is part of a discussion meeting issue ‘Forces in cancer: interdisciplinary approaches in tumour mechanobiology’.

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Section: Disruptive Effect Of Myosin-ii Filament Assembly On Podosomementioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Forces and constraints controlling podosome assembly and disassembly

Rafiq

Grenci

Lim

et al. 2019

Phil. Trans. R. Soc. B

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show abstract

Section: Disruptive Effect Of Myosin-ii Filament Assembly On Podosomementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Forces and constraints controlling podosome assembly and disassembly

Rafiq

Grenci

Kozlov

et al. 2018

Preprint

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Podosomes are a singular category of integrin-mediated adhesions important in the processes of cell migration, matrix degradation, and cancer cell invasion.Despite a wealth of biochemical studies, the effects of mechanical forces on podosome integrity and dynamics are poorly understood. Here, we show that podosomes are highly sensitive to two groups of physical factors. First, we describe the process of podosome disassembly induced by activation of myosin-IIA filament assembly. Next, we find that podosome integrity and dynamics depends upon membrane tension and can be experimentally perturbed by osmotic swelling and deoxycholate treatment. We have also found that podosomes can be disrupted in a reversible manner by single or cyclic radial stretching of the substratum. We show that disruption of podosomes induced by osmotic swelling is independent of myosin-II filaments. Inhibition of the membrane sculpting protein, dynamin-II, but not clathrin, resulted in activation of myosin-IIA filament formation and disruption of podosomes. The effect of dynamin-II inhibition on podosomes was however independent of myosin-II filaments. Moreover, formation of organized arrays of podosomes in response to microtopographic cues (the ridges with triangular profile) was not accompanied by reorganization of myosin-II filaments. Thus, mechanical elements such as myosin-II filaments and factors affecting membrane tension/sculpting independently modulate podosome formation and dynamics, underlying a versatile response of these adhesion structures to intracellular and extracellular cues.

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“…The calcium binding family member SA10004A for instance, is overexpressed in a number of human cancers where it promotes cancer metastasis [58]. This effect seems due to both, the fact that S1004A binds to NMIIA and promotes its depolymerization, and its myosin II-independent effect consistent with MT depolymerization [59]. Furthermore, one of the most well-known cell cycle regulators, the cyclin-dependent kinase inhibitor 1B (p27), is both a MT-and a NMII-associated and colocalizing protein and has been show to regulate independently regulate both NMII activity and MTs stability in normal and cancer cells [60][61][62][63][64][65][66].…”

mentioning

confidence: 99%

UNC-45A Weakens and Breaks MT Lattice Independent of its Effect on Non-Muscle Myosin II

Habicht

Mooneyham

Shetty

et al. 2020

Preprint

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In invertebrates, the member of UCS domain family UNC-45 regulates myosin stability and functions. Vertebrates have two distinct isoforms of the protein: UNC-45B, expressed in muscle cells only and responsible for muscle myosin folding and assembly, and UNC-45A, expressed in all cells and implicated in regulating both Non-Muscle Myosin II (NMII)-and microtubule (MT)-associated functions. Here we show for the first time that in vitro UNC-45A binds to the lattice of paclitaxel-stabilized MTs, and destabilizes the lattice integrity, leading to MT depolymerization in a dose-dependent manner. We also show that UNC-45A overexpression causes a dramatic loss of MT mass and increase in MT breakages in cells lacking the MT stabilizing protein tau. We also show for the first time that, both in vitro and in cells, that UNC-45A destabilizes MTs independent of its NMII C-terminal binding domain and destabilization occurs even in presence of the NMII inhibitor blebbistatin. These findings are consistent with a not mutually exclusive but rather dual role of UNC-45A in regulating NMII activity and MT stability. As many human diseases, from cancer to neurodegenerative diseases are caused by or associated with deregulation of MT stability, our findings are important as to ongoing and future studies aimed to understand the mechanisms through which UNC-45A regulates MT stability in the context of health and disease. This includes providing a novel platform for therapeutic intervention of cancer and neurodegenerative diseases.

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S100A4 regulates macrophage invasion by distinct myosin-dependent and myosin-independent mechanisms

Cited by 22 publications

References 70 publications

Forces and constraints controlling podosome assembly and disassembly

Forces and constraints controlling podosome assembly and disassembly

Forces and constraints controlling podosome assembly and disassembly

UNC-45A Weakens and Breaks MT Lattice Independent of its Effect on Non-Muscle Myosin II

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