APC binds intermediate filaments and is required for their reorganization during cell migration

Sakamoto, Yasuhisa; Boëda, Batiste; Etienne-Manneville, Sandrine

doi:10.1083/jcb.201206010

Cited by 84 publications

(106 citation statements)

References 43 publications

(52 reference statements)

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“…Interestingly, in migrating cells, Rab7a-positive vesicles localize in the perinuclear region facing the wound while vimentin filaments are reorganized and reoriented in the direction of the wound (Fig. 7A-C), in line with what has been previously demonstrated [55].…”

Section: Discussionsupporting

confidence: 74%

“…The creation of a polarized network of intermediate filaments coordinated with microtubules is fundamental for cell migration [55]. Intermediate filament assembly is dependent on their phosphorylation state.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, we have previously shown that Rab7a interacts with vimentin and that depletion of Rab7a determines a lower phosphorylated state of the head domain of vimentin and a higher abundance of vimentin in the insoluble, filamentous fraction [17]. As both Rab7a and Rac1 regulate vimentin assembly and since it has previously been shown that vimentin filaments are oriented towards the leading edge during migration [55], we tested whether vimentin filament orientation was impaired in Rab7a-depleted cells in a wound healing assay. In control migrating cells there was about 50% of cells showing vimentin facing the wound, whereas after 3 hours about 85% of cells had vimentin oriented towards the leading edge.…”

Section: Rab7a Regulates Vimentin Filaments Orientation During Cell Mmentioning

confidence: 99%

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Rab7a regulates cell migration through Rac1 and vimentin

Margiotta

Progida

Bakke

et al. 2017

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

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Rab7a, a small GTPase of the Rab family, is localized to late endosomes and controls late endocytic trafficking. The discovery of several Rab7a interacting proteins revealed that Rab7a function is closely connected to cytoskeletal elements. Indeed, Rab7a recruits on vesicles RILP and FYCO that are responsible for the movement of Rab7a-positive vesicles and/or organelles on microtubule tracks, but also directly interacts with Rac1, a fundamental regulator of actin cytoskeleton, and with peripherin and vimentin, two intermediate filament proteins. Considering all these interactions and, in particular, the fact that Rac1 and vimentin are key factors for cellular motility, we investigated a possible role of Rab7a in cell migration. We show here that Rab7a is needed for cell migration as Rab7a depletion causes slower migration of NCI H1299 cells affecting cell velocity and directness.Rab7a depletion negatively affects adhesion and spreading onto fibronectin substrates, altering β1-integrin activation, localization and intracellular trafficking, and myosin X localization. In fact, Rab7a-depleted cells show 40% less filopodia and active integrin accumulates at the leading edge of migrating cells. Furthermore, Rab7a depletion decreases the amount of active Rac1 but not its abundance and reduces the number of cells with vimentin filaments facing the wound, indicating that Rab7a has a role in the orientation of vimentin filaments during migration. In conclusion, our results demonstrate a key role of Rab7a in the regulation of different aspects of cell migration.

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Section: Discussionsupporting

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Rab7a Regulates Vimentin Filaments Orientation During Cell Mmentioning

confidence: 99%

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Rab7a regulates cell migration through Rac1 and vimentin

Margiotta

Progida

Bakke

et al. 2017

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

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“…Indeed, VIFs are known to interact with microtubules through a multitude of proteins, including microtubule associated motors , the cytoskeletonbinder plectin , and the tumor suppressor adenomatous polyposis coli (Sakamoto et al, 2013). We, therefore, hypothesized that VIF networks could enhance directed cell migration by increasing the persistence of the microtubule network architecture and thus of the whole-cell front-rear polarity.…”

Section: Introductionmentioning

confidence: 99%

Vimentin Intermediate Filaments Template Microtubule Networks to Enhance Persistence in Cell Polarity and Directed Migration

Gan¹,

Ding²,

Burckhardt³

et al. 2016

Cell Systems

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SUMMARYIncreased expression of vimentin intermediate filaments (VIF) enhances directed cell migration, but the mechanism behind VIF's effect on motility is not understood. VIF interact with microtubules, whose organization contributes to polarity maintenance in migrating cells. Here we characterize the dynamic coordination of VIF and microtubule networks in wounded monolayers of Retinal Pigment Epithelial cells. By genome editing we fluorescently labelled endogenous vimentin and α-tubulin and we developed computational image analysis to delineate architecture and interactions of the two networks. Our results show that VIF assemble an ultrastructural copy of the previously polarized microtubule network. Because the VIF network is long-lived compared to the microtubule network, VIF template future microtubule growth along previous microtubule tracks, thus providing a feedback mechanism that maintains cell polarity. VIF knockdown prevents cells from polarizing and migrating properly during wound healing. We suggest that VIF's templating function establishes a memory in microtubule organization that enhances persistence in cell polarization in general and migration in particular.

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“…APC is a multi-domain protein that is known to complex with and modulate the activities of microtubules (MTs), intermediate filaments, actin, β-catenin, Axin, and cytoskeletal regulators, EB1, mDia1, Asef1, and IQGAP1 (Aoki and Taketo, 2007; Sakamoto et al, 2013; Preitner et al, 2014). Mutational analysis of APC indicates that β-catenin and MTs are the two major targets of APC activity (Aoki and Taketo, 2007; McCartney and Nathke, 2008; Wen et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Differential Regulation of Microtubule Severing by APC Underlies Distinct Patterns of Projection Neuron and Interneuron Migration

et al. 2014

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Coordinated migration of distinct classes of neurons to appropriate positions leads to the formation of functional neuronal circuitry in the cerebral cortex. Two major classes of cortical neurons, interneurons and projection neurons, utilize distinctly different modes (radial vs. tangential) and routes of migration to arrive at their final positions in the cerebral cortex. Here, we show that adenomatous polyposis coli (APC) modulates microtubule (MT) severing in interneurons to facilitate tangential mode of interneuron migration, but not the glial-guided, radial migration of projection neurons. APC regulates the stability and activity of the MT severing protein p60-katanin in interneurons to promote the rapid remodeling of neuronal processes necessary for interneuron migration. These findings reveal how severing and restructuring of MTs facilitate distinct modes of neuronal migration necessary for laminar organization of neurons in the developing cerebral cortex.

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APC binds intermediate filaments and is required for their reorganization during cell migration

Abstract: The tumor suppressor APC binds to the intermediate filament vimentin and is required for its microtubule-dependent rearrangements during astrocyte migration.

Cited by 84 publications

References 43 publications

Rab7a regulates cell migration through Rac1 and vimentin

Rab7a regulates cell migration through Rac1 and vimentin

Vimentin Intermediate Filaments Template Microtubule Networks to Enhance Persistence in Cell Polarity and Directed Migration

Differential Regulation of Microtubule Severing by APC Underlies Distinct Patterns of Projection Neuron and Interneuron Migration

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