Talin Influences the Dynamics of the Myosin VII-Membrane Interaction

Galdeen, Shawn A.; Stephens, Stephen; Thomas, David D.; Titus, Margaret A.

doi:10.1091/mbc.e06-07-0586

Cited by 14 publications

(12 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Consistent with this notion, talin A is known to interact with myosin VII, which is a submembranous protein (39,40). In preliminary experiments, we have also identified several proteins that bind to talin A, including submembranous and cytoskeletal proteins.…”

Section: F) Migrating Talin A-null Cell Observed By Interference Reflsupporting

confidence: 73%

Talin couples the actomyosin cortex to the plasma membrane during rear retraction and cytokinesis

Tsujioka

Yumura

Inouye

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Contraction of the cortical actin cytoskeleton underlies both rear retraction in directed cell migration and cytokinesis. Here, we show that talin, a central component of focal adhesions, has a major role in these processes. We found that Dictyostelium talin A colocalized with myosin II in the rear of migrating cells and the cleavage furrow. During directed cell migration, talin A-null cells displayed a long thin tail devoid of actin filaments, whereas additional depletion of SibA, a transmembrane adhesion molecule that binds to talin A, reverted this phenotype, suggesting a requirement of the link between actomyosin and SibA by talin A for rear retraction. Disruptions of talin A also resulted in detachment of the actomyosin contractile ring from the cell membrane and concomitant regression of the cleavage furrow under certain conditions. The C-terminal actin-binding domain (ABD) of talin A exhibited a localization pattern identical to that of full-length talin A. The N-terminal FERM domain was found to bind phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2] and phosphatidylinositol 3,4,5-trisphosphate [PtdIns(3,4,5)P3] in vitro. In vivo, however, PtdIns(4,5)P2, which is known to activate talin, is believed to be enriched in the rear of migrating cells and the cleavage furrow in Dictyostelium . From these results, we propose that talin A activated by PtdIns(4,5)P2 in the cell posterior or cleavage furrow links actomyosin cytoskeleton to adhesion molecules or other membrane proteins, and that the force is transmitted through these links to retract the tail during cell migration or to cause efficient ingression of the equator during cytokinesis.

show abstract

Section: F) Migrating Talin A-null Cell Observed By Interference Reflsupporting

confidence: 73%

Talin couples the actomyosin cortex to the plasma membrane during rear retraction and cytokinesis

Tsujioka

Yumura

Inouye

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Spinning-disk confocal microscopy showed DdMyo7 localized to the actin cortex of an active leading edge (Fig. 2B), in filopodia tips, and in the cytosol, as previously reported (2,32).…”

Section: Myo22supporting

confidence: 86%

MyTH4-FERM myosins have an ancient and conserved role in filopod formation

Petersen

Goodson

Arthur

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

The formation of filopodia in Metazoa and Amoebozoa requires the activity of myosin 10 (Myo10) in mammalian cells and of Dictyostelium unconventional myosin 7 (DdMyo7) in the social amoeba Dictyostelium. However, the exact roles of these MyTH4-FERM myosins (myosin tail homology 4-band 4.1, ezrin, radixin, moesin; MF) in the initiation and elongation of filopodia are not well defined and may reflect conserved functions among phylogenetically diverse MF myosins. Phylogenetic analysis of MF myosin domains suggests that a single ancestral MF myosin existed with a structure similar to DdMyo7, which has two MF domains, and that subsequent duplications in the metazoan lineage produced its functional homolog Myo10. The essential functional features of the DdMyo7 myosin were identified using quantitative live-cell imaging to characterize the ability of various mutants to rescue filopod formation in myo7-null cells. The two MF domains were found to function redundantly in filopod formation with the C-terminal FERM domain regulating both the number of filopodia and their elongation velocity. DdMyo7 mutants consisting solely of the motor plus a single MyTH4 domain were found to be capable of rescuing the formation of filopodia, establishing the minimal elements necessary for the function of this myosin. Interestingly, a chimeric myosin with the Myo10 MF domain fused to the DdMyo7 motor also was capable of rescuing filopod formation in the myo7-null mutant, supporting fundamental functional conservation between these two distant myosins. Together, these findings reveal that MF myosins have an ancient and conserved role in filopod formation.C ells interact with their environment through protrusions such as filopodia that form in response to extracellular cues and mediate initial contact with the substrate. Filopodia are slender, actin-filled membrane projections that are highly dynamic, growing and shrinking from peripheral regions of cells, such as lamellipodia and the dorsal surface (1). A wide variety of cell types including amoebae such as Dictyostelium discoideum (2) and Acanthamoeba (3), as well as mammalian vascular endothelial cells (4) and developing neurons (5), extend filopodia. Filopodia are typically 1-10 μm long and 0.1-0.3 μm in diameter and have a core of 10-30 parallel actin filaments with a protein-rich complex at their tip (1, 6, 7). Modified forms of filopodia such as dendritic spines, cytonemes, and tunneling nanotubes promote intercellular communication during multicellular development (8-10). Defects in filopod formation alter cell spreading and adhesion (2, 11, 12), whereas overproduction of filopodia or filopodia-like protrusions is associated with increased invasiveness of metastatic cancer cells (13)(14)(15).Filopod elongation is triggered by small GTPase activity (1, 16) and is driven by the activity of actin elongation factors including vasodilator-stimulated phosphoprotein (VASP) and formins, and the actin core is stabilized by actin cross-linking proteins (1). A MyTH4-FERM (myosin tail homology ...

show abstract

“…NMHC IIB and N-RAP are partially colocalized in cardiomyocytes (figure 10), and the nonmuscle myosin IIB rod binds recombinant N-RAP fragments in vitro (figure 9), suggesting that direct interaction of these two proteins in the cardiomyocyte may protect N-RAP from degradation. A precedent for stabilization of a cytoskeletal protein by interaction with myosin has been demonstrated in Dictyostelium , where binding to myosin VII stabilizes cytosolic talin (Galdeen et al 2007). …”

Section: Discussionmentioning

confidence: 99%

Role of nonmuscle myosin IIB and N‐RAP in cell spreading and myofibril assembly in primary mouse cardiomyocytes

Horowits

2008

Cell Motil. Cytoskeleton

View full text Add to dashboard Cite

We investigated the role of nonmuscle myosin heavy chain (NMHC) IIB in cultured embryonic mouse cardiomyocytes by specific knockdown using RNA interference. NMHC IIB protein levels decreased 90% compared with mock-transfected cells by 3 days post transfection. NMHC IIB knockdown resulted in a slow decrease in N-RAP protein levels over 6 days with no change in N-RAP transcript levels. N-RAP is a scaffold for α-actinin and actin assembly during myofibrillogenesis, and we quantitated myofibril accumulation by morphometric analysis of α-actinin organization. Between 3 and 6 days, NMHC IIB knockdown was accompanied by the abolishment of cardiomyocyte spreading. During this period the rate of myofibril accumulation steadily decreased, correlating with the slowly decreasing levels of N-RAP. Between 6 and 8 days NMHC IIB and N-RAP protein levels recovered, and cardiomyocyte spreading and myofibril accumulation resumed. Inhibition of proteasome function using MG132 led to accumulation of excess N-RAP, and the secondary decrease in N-RAP that otherwise accompanied NMHC IIB knockdown was abolished. The results show that NMHC IIB knockdown led to decreased N-RAP levels through proteasome-mediated degradation. Furthermore, these proteins have distinct functional roles, with NMHC IIB playing a role in cardiomyocyte spreading and N-RAP functioning in myofibril assembly.

show abstract

Talin Influences the Dynamics of the Myosin VII-Membrane Interaction

Cited by 14 publications

References 32 publications

Talin couples the actomyosin cortex to the plasma membrane during rear retraction and cytokinesis

Talin couples the actomyosin cortex to the plasma membrane during rear retraction and cytokinesis

MyTH4-FERM myosins have an ancient and conserved role in filopod formation

Role of nonmuscle myosin IIB and N‐RAP in cell spreading and myofibril assembly in primary mouse cardiomyocytes

Contact Info

Product

Resources

About