Microtubule Dynamic Instability Controls Podosome Patterning in Osteoclasts through EB1, Cortactin, and Src

Duplan, Martin Biosse; Zalli, Detina; Stephens, Sebastien Robert; Zenger, Serhan; Neff, Lynn; Oelkers, J. Margit; Lai, Frank P. L.; Horne, William C.; Rottner, Klemens; Baron, Roland

doi:10.1128/mcb.00578-13

Cited by 50 publications

(86 citation statements)

References 94 publications

(149 reference statements)

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“…Finally, we did not find any effect of tensin 3 silencing on the acetylation of microtubules (Fig. 8C), a marker of microtubule stability, which is also important for the regulation of the podosome belt (Biosse Duplan et al, 2014). These results show that the depletion of tensin 3 disrupts podosome patterning associated with reduced osteoclast activity and increased global levels of RhoA activity.…”

Section: Tensin 3 Stimulates Dock5 Exchange Activity Towards Racmentioning

confidence: 49%

Tensin 3 is a new partner of Dock5 that controls osteoclast podosome organization and activity

Touaitahuata

Morel

Urbach

et al. 2016

Journal of Cell Science

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Bone resorption by osteoclasts is mediated by a typical adhesion structure called the sealing zone or actin ring, whose architecture is based on a belt of podosomes. The molecular mechanisms driving podosome organization into superstructures remain poorly understood to date, in particular at the osteoclast podosome belt. We performed proteomic analyses in osteoclasts and found that the adaptor protein tensin 3 is a partner of Dock5, a Rac exchange factor necessary for podosome belt formation and bone resorption. Expression of tensin 3 and Dock5 concomitantly increase during osteoclast differentiation. These proteins associate with the osteoclast podosome belt but not with individual podosomes, in contrast to vinculin. Super-resolution microscopy revealed that, even if they colocalize in the x-y plane of the podosome belt, Dock5 and tensin 3 differentially localize relative to vinculin in the z-axis. Tensin 3 increases Dock5 exchange activity towards Rac, and suppression of tensin 3 in osteoclasts destabilizes podosome organization, leading to delocalization of Dock5 and a severe reduction in osteoclast activity. Our results suggest that Dock5 and tensin 3 cooperate for osteoclast activity, to ensure the correct organization of podosomes.

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Section: Tensin 3 Stimulates Dock5 Exchange Activity Towards Racmentioning

confidence: 49%

Tensin 3 is a new partner of Dock5 that controls osteoclast podosome organization and activity

Touaitahuata

Morel

Urbach

et al. 2016

Journal of Cell Science

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“…In addition, phosphorylation of CTN may enhance its ability to act as an adaptor or negatively regulate its function. Moreover, phosphorylation of CTN tyrosine is regulated by growing microtubules (28,30,34). This study suggests that EGF-elicited dissociation of the TIP150-CTN complex is needed to accelerate the recycling of TIP150 and CTN to promote leading edge membrane expansion and persistent microtubule growth, respectively.…”

Section: Discussionmentioning

confidence: 92%

The Microtubule Plus End Tracking Protein TIP150 Interacts with Cortactin to Steer Directional Cell Migration

Adams

Zhang

Wang

et al. 2016

Journal of Biological Chemistry

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Cell migration is orchestrated by dynamic interactions of microtubules with the plasma membrane cortex. How these interactions facilitate these dynamic processes is still being actively investigated. TIP150 is a newly characterized microtubule plus end tracking protein essential for mitosis and entosis (Ward, T., Wang, M., Liu, X., Wang, Z., Xia, P., Chu, Y., Wang, X., Liu, L., Jiang, K., Yu, H., Yan, M., Wang, J., Hill, D. L., Huang, Y., Zhu, T., and Yao, X. (2013) Regulation of a dynamic interaction between two microtubule-binding proteins, EB1 and TIP150, by the mitotic p300/CBP-associated factor (PCAF) orchestrates kinetochore microtubule plasticity and chromosome stability during mitosis. J. Biol. Chem. 288, 15771-15785; Xia, P., Zhou, J., Song, X., Wu, B., Liu, X., Li, D., Zhang, S., Wang, Z., Yu, H., Ward, T., Zhang, J., Li, Y., Wang, X., Chen, Y., Guo, Z., and Yao, X. (2014) Aurora A orchestrates entosis by regulating a dynamic MCAK-TIP150 interaction. J. Mol. Cell Biol. 6, 240 -254). Here we show that TIP150 links dynamic microtubules to steer cell migration by interacting with cortactin. Mechanistically, TIP150 binds to cortactin via its C-terminal tail. Interestingly, the C-terminal TIP150 proline-rich region (CT150) binds to the Src homology 3 domain of cortactin specifically, and such an interaction is negatively regulated by EGF-elicited tyrosine phosphorylation of cortactin. Importantly, suppression of TIP150 or overexpression of phospho-mimicking cortactin inhibits polarized cell migration. In addition, CT150 disrupts the biochemical interaction between TIP150 and cortactin in vitro, and perturbation of the TIP150-cortactin interaction in vivo using a membrane-permeable TAT-CT150 peptide results in an inhibition of directional cell migration. We reason that a dynamic TIP150-cortactin interaction orchestrates directional cell migration via coupling dynamic microtubule plus ends to the cortical cytoskeleton.Cell migration is an essential physiological function that is tightly regulated in numerous biological processes, including development, tissue remodeling, wound healing, and tumor metastasis (1, 2). These processes require coordination of dynamic reorganization between the actin filaments and microtubules.Cortactin (CTN) 6 is a multidomain-containing scaffold protein that consists of an N-terminal acidic domain, six and a half tandem repeats, an ␣ helix, a proline-rich region, and an Src Homology (SH3) domain at its C terminus (3). CTN is an important scaffold for promoting the polymerization and rearrangement of the actin cytoskeleton (4). Functionally, CTN, distributed at protrusions and the leading edges, is necessary for cell migration by regulating intercellular adhesion and cell spreading (5). Importantly, CTN is phosphorylated at tyrosine residues in response to growth factor receptors, which regulates cell migration (6).Microtubules, one of the three major components of the cytoskeleton, are required for maintaining the physical and plastic properties of migrating cells (7). The plus en...

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Section: Introductionmentioning

confidence: 99%

“…Podosome dynamics are strongly regulated by MTs (Babb et al, 1997;Linder et al, 2000;Destaing et al, 2003;Evans et al, 2003;Destaing et al, 2005;Jurdic et al, 2006;Kopp et al, 2006;Gil-Henn et al, 2007;Purev et al, 2009;McMichael et al, 2010;Biosse Duplan et al, 2014). It has become clear from a number of recent studies that MT-podosome relationships are multifaceted -both stable (acetylated; Destaing et al, 2005;Purev et al, 2009;Biosse Duplan et al, 2014) and dynamic (Kopp et al, 2006;Biosse Duplan et al, 2014) MT subpopulations are essential for podosome regulation. Moreover, several independent molecular machineries structurally and/ or functionally link MTs to podosomes, including tubulin acetylation enzymes (Destaing et al, 2005;Purev et al, 2009;Biosse Duplan et al, 2014), MT plus-end-associated protein complexes (EB1; Biosse Duplan et al, 2014), actin-dependent molecular motors (myosin-X; McMichael et al, 2010) and several MT-dependent molecular motors (Kopp et al, 2006;Wiesner et al, 2010;Cornfine et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…An important part of this function is locating the sites of actin cytoskeleton assembly and remodeling (Hoogenraad and Akhmanova, 2010;Kaverina and Straube, 2011;EtienneManneville, 2013). Amongst other actin-based structures, MTs regulate invasive protrusions, termed podosomes (Babb et al, 1997;Linder et al, 2000;Destaing et al, 2003;Evans et al, 2003;Destaing et al, 2005;Jurdic et al, 2006;Kopp et al, 2006;Gil-Henn et al, 2007;Purev et al, 2009;McMichael et al, 2010;Biosse Duplan et al, 2014), and their cancer counterparts, invadopodia (Schoumacher et al, 2010;Quintavalle et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Podosome-regulating kinesin KIF1C translocates to the cell periphery in a CLASP-dependent manner

Efimova

Grimaldi

Bachmann

et al. 2014

Journal of Cell Science

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The kinesin KIF1C is known to regulate podosomes, actin-rich adhesion structures, which remodel the extracellular matrix during physiological processes. Here we show that KIF1C is a player in the podosome-inducing signaling cascade. Upon induction of podosome formation by protein kinase C, KIF1C translocation to the cell periphery intensifies and KIF1C accumulates in the proximity of peripheral microtubules enriched with plus tip-associated proteins CLASPs and around podosomes. Importantly, without CLASPs, both KIF1C trafficking and podosome formation are suppressed. Moreover, chimeric mitochondria-targeted CLASP2 recruits KIF1C, suggesting a transient CLASP-KIF1C association. We propose that CLASP creates preferred microtubule tracks for KIF1C to promote podosome induction downstream of PKC.

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Microtubule Dynamic Instability Controls Podosome Patterning in Osteoclasts through EB1, Cortactin, and Src

Cited by 50 publications

References 94 publications

Tensin 3 is a new partner of Dock5 that controls osteoclast podosome organization and activity

Tensin 3 is a new partner of Dock5 that controls osteoclast podosome organization and activity

The Microtubule Plus End Tracking Protein TIP150 Interacts with Cortactin to Steer Directional Cell Migration

Podosome-regulating kinesin KIF1C translocates to the cell periphery in a CLASP-dependent manner

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