The F-BAR domain of SRGP-1 facilitates cell–cell adhesion during <i>C. elegans</i> morphogenesis

Zaidel-Bar, Ronen; Joyce, Michael; Lynch, Allison M.; Witte, K. H.; Audhya, Anjon; Hardin, Jeff

doi:10.1083/jcb.201005082

Cited by 57 publications

(89 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Although the most characterized function of F-BAR proteins is their role in endocytosis, many F-BAR proteins including CIP4 have also been shown to play a role in filopodial and lamellipodial protrusion (Carlson et al, 2011;Guerrier et al, 2009;Lee et al, 2010;Saengsawang et al, 2012;Zaidel-Bar et al, 2010). In nonneuronal cells, CIP4 induces polymerization associated with actin comet tails, endocytosis, and tubulation through its interaction with Cdc42, N-WASP and dynamin (Hartig et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils

Saengsawang

Taylor

Lumbard

et al. 2013

Journal of Cell Science

View full text Add to dashboard Cite

SummaryCdc42-interacting protein 4 (CIP4), a member of the F-BAR family of proteins, plays important roles in a variety of cellular events by regulating both membrane and actin dynamics. In many cell types, CIP4 functions in vesicle formation, endocytosis and membrane tubulation. However, recent data indicate that CIP4 is also involved in protrusion in some cell types, including cancer cells (lamellipodia and invadopodia) and neurons (ribbed lamellipodia and veils). In neurons, CIP4 localizes specifically to extending protrusions and functions to limit neurite outgrowth early in development. The mechanism by which CIP4 localizes to the protruding edge membrane and induces lamellipodial/veil protrusion and actin rib formation is not known. Here, we show that CIP4 localization to the protruding edge of neurons is dependent on both the phospholipid content of the plasma membrane and the underlying organization of actin filaments. Inhibiting phosphatidylinositol (3,4,5)-trisphosphate (PIP 3 ) production decreases CIP4 at the membrane. CIP4 localization to the protruding edge is also dependent on Rac1/WAVE1, rather than Cdc42/N-WASP. Capping actin filaments with low concentrations of cytochalasin D or by overexpressing capping protein dramatically decreases CIP4 at the protruding edge, whereas inactivating Arp2/3 drives CIP4 to the protruding edge. We also demonstrate that CIP4 dynamically colocalizes with Ena/VASP and DAAM1, two proteins known to induce unbranched actin filament arrays and play important roles in neuronal development. Together, this is the first study to show that the localization of an F-BAR protein depends on both actin filament architecture and phospholipids at the protruding edge of developing neurons.

show abstract

Section: Introductionmentioning

confidence: 99%

CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils

Saengsawang

Taylor

Lumbard

et al. 2013

Journal of Cell Science

View full text Add to dashboard Cite

show abstract

“…The RhoGAP domain of srGAP1 has been shown to promote GTP hydrolysis of Cdc42 and RhoA, depending on the concentration of Slit1 (Wong et al, 2001), whereas the GAP domains of srGAP2 and srGAP3 are both specific for Rac1 (Guerrier et al, 2009;Soderling et al, 2002), and ArhGAP4 can act on both Cdc42 and Rac1 (Vogt et al, 2007). All four family members display spatially and temporally distinct patterns of expression in the central nervous system (Bacon et al, 2009;Foletta et al, 2002) and have been shown to regulate cell migration and neuronal morphology in mammalian cells (Guerrier et al, 2009;Soderling et al, 2002;Vogt et al, 2007;Wong et al, 2001;Yang et al, 2006), a function that seems evolutionary conserved in invertebrates (Zaidel-Bar et al, 2010). srGAP3 has been implicated in a severe form of mental retardation, the 3p2 syndrome, giving srGAP3 the alternate name of mental-disorder associated GAP protein (MEGAP) (Endris et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

The F-BAR domains from srGAP1, srGAP2, and srGAP3 differentially regulate membrane deformation

Coutinho-Budd

Ghukasyan

Zylka

et al. 2012

Journal of Cell Science

View full text Add to dashboard Cite

Coordination of membrane deformation and cytoskeletal dynamics lies at the heart of many biological processes critical for cell polarity, motility and morphogenesis. We recently showed that slit-robo GTPase-activating protein 2 (srGAP2) regulates neuronal morphogenesis through the ability of its F-BAR domain to regulate membrane deformation and induce filopodia formation. Here we demonstrate that the F-BAR domains of two closely related family members, srGAP1 and srGAP3 (F-BAR(1) and F-BAR(3), respectively) display significantly different membrane deformation properties in non-neuronal COS7 cells and in cortical neurons. F-BAR(3) induces filopodia in both cell types, though less potently than F-BAR(2), whereas F-BAR(1) prevents filopodia formation in cortical neurons and reduces plasma membrane dynamics. These three F-BAR domains can heterodimerize and act synergistically towards filopodia induction in COS7 cells. At the molecular level, F-BAR(2) displays faster molecular dynamics than F-BAR(3) and F-BAR(1) respectively at the plasma membrane which correlates well with its increased potency to induce filopodia. We also show that the molecular dynamic properties of F-BAR(2) at the membrane are partially dependent on F-Actin. Interestingly, acute phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) depletion in cells does not interfere with plasma membrane localization of F-BAR(2), which is compatible with our result showing that F-BAR(2) binds to a broad range of negatively-charged phospholipids present at the plasma membrane, including phosphatidylserine (PS). Overall, our results provide novel insights into the functional diversity of the membrane deformation properties of this subclass of F-BAR-domains required for cell morphogenesis.

show abstract

“…The only worm homolog of mammalian srGAPs, SRGP-1, contributes to membrane dynamics at nascent cell-cell contacts and the formation of new AJs during gastrulation. This localization to, and regulation of, new AJs occurs independently of the cadherin homolog, HMR-1 (Zaidel-Bar et al 2010). This raises the possibility that Slit-Robo signaling through mammalian srGAPs may contribute to AJ formation during embryogenesis in a cadherin-independent manner.…”

Section: Slit-robo Regulation Of Adherens Junctionsmentioning

confidence: 99%

Making Connections: Guidance Cues and Receptors at Nonneural Cell–Cell Junctions

Beamish

Hinck

Kennedy

2017

Cold Spring Harb Perspect Biol

View full text Add to dashboard Cite

The field of axon guidance was revolutionized over the past three decades by the identification of highly conserved families of guidance cues and receptors. These proteins are essential for normal neural development and function, directing cell and axon migration, neuron-glial interactions, and synapse formation and plasticity. Many of these genes are also expressed outside the nervous system in which they influence cell migration, adhesion and proliferation. Because the nervous system develops from neural epithelium, it is perhaps not surprising that these guidance cues have significant nonneural roles in governing the specialized junctional connections between cells in polarized epithelia. The following review addresses roles for ephrins, semaphorins, netrins, slits and their receptors in regulating adherens, tight, and gap junctions in nonneural epithelia and endothelia.

show abstract

The F-BAR domain of SRGP-1 facilitates cell–cell adhesion during C. elegans morphogenesis

Abstract: SRGP-1 activity leads to outward bending and projections of membranes at cell–cell junctions, promoting robust adhesion between cells during embryonic closure events.

Cited by 57 publications

References 45 publications

CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils

CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils

The F-BAR domains from srGAP1, srGAP2, and srGAP3 differentially regulate membrane deformation

Making Connections: Guidance Cues and Receptors at Nonneural Cell–Cell Junctions

Contact Info

Product

Resources

About