Adaptive F-Actin Polymerization and Localized ATP Production Drive Basement Membrane Invasion in the Absence of MMPs

Kelley, Laura C.; Chi, Qiuyi; Cáceres, Rodrigo; Hastie, Eric; Schindler, Adam J.; Jiang, Yue; Matus, David Q.; Plastino, Julie; Sherwood, David R.

doi:10.1016/j.devcel.2018.12.018

Cited by 124 publications

(145 citation statements)

References 87 publications

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“…The basement membrane provides a well‐known barrier to epithelial (carcinoma) cell invasion, and a classical feature of malignancy is tumour cell invasion across the basement membrane. Although this process is thought to involve proteases, physical force by a cellular process against the basement membrane can also contribute to cellular invasion across the basement membrane …”

Section: Basement Membrane Dynamicsmentioning

confidence: 99%

Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis

Yamada

Collins

Walma

et al. 2019

Int J Experimental Path

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This review describes how direct visualization of the dynamic interactions of cells with different extracellular matrix microenvironments can provide novel insights into complex biological processes. Recent studies have moved characterization of cell migration and invasion from classical 2D culture systems into 1D and 3D model systems, revealing multiple differences in mechanisms of cell adhesion, migration and signalling-even though cells in 3D can still display prominent focal adhesions.Myosin II restrains cell migration speed in 2D culture but is often essential for effective 3D migration. 3D cell migration modes can switch between lamellipodial, lobopodial and/or amoeboid depending on the local matrix environment. For example, "nuclear piston" migration can be switched off by local proteolysis, and proteolytic invadopodia can be induced by a high density of fibrillar matrix. Particularly, complex remodelling of both extracellular matrix and tissues occurs during morphogenesis. Extracellular matrix supports self-assembly of embryonic tissues, but it must also be locally actively remodelled. For example, surprisingly focal remodelling of the basement membrane occurs during branching morphogenesis-numerous tiny perforations generated by proteolysis and actomyosin contractility produce a microscopically porous, flexible basement membrane meshwork for tissue expansion. Cells extend highly active blebs or protrusions towards the surrounding mesenchyme through these perforations. Concurrently, the entire basement membrane undergoes translocation in a direction opposite to bud expansion. Underlying this slowly moving 2D basement membrane translocation are highly dynamic individual cell movements. We conclude this review by describing a variety of exciting research opportunities for discovering novel insights into cell-matrix interactions. K E Y W O R D S3D culture, basement membrane remodelling, branching morphogenesis, cell migration, extracellular matrix, invasion

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Section: Basement Membrane Dynamicsmentioning

confidence: 99%

Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis

Yamada

Collins

Walma

et al. 2019

Int J Experimental Path

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“…There are recent reports of subcellular enrichment of mitochondria in regions where there is high demand for ATP that, in one case, supports local protein synthesis during dendritic synaptic plasticity (8) or actin network growth in another case (9). It appeared possible that the mitochondria enriched in the vegetal hemisphere might be capable of generating locally elevated amounts of ATP.…”

mentioning

confidence: 96%

“…This is accomplished by the mitochondria-rich remnants of the Bb that generate elevated levels of ATP, likely acting as a hydrotrope, that promote the phase transition needed for formation of the RNA transport granule. This is possibly the first example where a region of clustered mitochondria is used not to meet extraordinary energy demands (8,9), but rather to initiate cellular compartmentalization.…”

mentioning

confidence: 99%

Remnants of the Balbiani body are required for formation of RNA transport granules inXenopusoocytes

Yang

2020

Preprint

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Mitochondria in the remnants of the Balbiani body produce elevated levels of ATP required for the formation of liquid phase condensates containing RNA transport granules. Abstract:Fragmentation of the Balbiani body in Xenopus oocytes engenders a region extending from the germinal vesicle (GV) towards the vegetal pole that is enriched in mitochondria. This area is later transversed by RNA that is being localized to the vegetal cortex. Inhibition of mitochondrial ATP synthesis prevents the perinuclear formation of these RNA transport granules that can be reversed by the nonhydrolyzable ATP analog, adenosine 5'-(b,g-imido) triphosphate. The protein composition and sensitivity of the transport granules to hexanediol indicate that they are liquid phase condensates. Mitochondria in the remnants of the Balbiani body produce a region of elevated ATP that appears to act as a hydrotrope to support the perinuclear phase transition leading to granule formation.

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“…How cells breach basement membrane barriers remains an area of active research. In this issue of Developmental Cell, Kelley et al (2019) reveal that the C. elegans anchor cell uses physical force to breach basement membrane in the absence of matrix metalloproteases during its developmental invasion.…”

mentioning

confidence: 99%

“…The C. elegans anchor cell (AC) expresses only 6 MMP genes (zmp-1-6) from which zmp-1, 2, 3, 4, and 6 are important during AC invasion, and they are located either at the invadopodia (ZMP-1) or near the invading AC. In this issue of Developmental Cell, Kelley et al (2019) deleted the five key MMPs and found to their surprise that even a quintuple knockout did not completely prevent crossing of the BM. The anchor cell instead formed an invasive protrusion that appears to breach BM through physical forces, shown to require branched actin networks produced by Arp2/3 in an accompanying study (Cá ceres et al, 2018).…”

mentioning

confidence: 99%

Invasion by Force: The C. elegans Anchor Cell Leads the Way

Nikolaou

Machesky

2019

Developmental Cell

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Adaptive F-Actin Polymerization and Localized ATP Production Drive Basement Membrane Invasion in the Absence of MMPs

Cited by 124 publications

References 87 publications

Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis

Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis

Remnants of the Balbiani body are required for formation of RNA transport granules inXenopusoocytes

Invasion by Force: The C. elegans Anchor Cell Leads the Way

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