Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system

Wu, Min; Huang, Bo; Graham, Morven; Raimondi, Andrea; Heuser, John E.; Zhuang, Xiaowei; Camilli, Pietro De

doi:10.1038/ncb2094

Cited by 144 publications

(128 citation statements)

References 41 publications

Supporting

Mentioning

124

Contrasting

Order By: Relevance

“…In this context, it is important to note that calcium oscillations induced by stimulation in mast cells and other secretory cells were shown to correlate with oscillatory bursts of secretion (31)(32)(33). Interestingly, FBP17 is an F-BAR domain-containing protein (34) that can participate in endocytosis (35,36). Though feedback regulatory mechanisms mediated by Cdc42 activation and actin polymerization are involved in the collective events described here, irrespective of their spatial pattern, they can be coupled to, or decoupled from, those underlying calcium oscillations, resulting in either standing oscillations or traveling waves (Fig.…”

Section: Resultsmentioning

confidence: 99%

Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations

Camilli

2013

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

Self Cite

110

View full text Add to dashboard Cite

Dynamic spatial patterns of signaling factors or macromolecular assemblies in the form of oscillations or traveling waves have emerged as important themes in cell physiology. Feedback mechanisms underlying these processes and their modulation by signaling events and reciprocal cross-talks remain poorly understood. Here we show that antigen stimulation of mast cells triggers cyclic changes in the concentration of actin regulatory proteins and actin in the cell cortex that can be manifested in either spatial pattern. Recruitment of FBP17 and active Cdc42 at the plasma membrane, leading to actin polymerization, are involved in both events, whereas calcium oscillations, which correlate with global fluctuations of plasma membrane PI(4,5)P 2 , are tightly linked to standing oscillations and counteract wave propagation. These findings demonstrate the occurrence of a calcium-independent oscillator that controls the collective dynamics of factors linking the actin cytoskeleton to the plasma membrane. Coupling between this oscillator and the one underlying global plasma membrane PI(4,5)P2 and calcium oscillations spatially regulates actin dynamics, revealing an unexpected pattern-rendering mechanism underlying plastic changes occurring in the cortical region of the cell.curvature | pattern formation | plasticity | GTPase | frequency A ctin waves have emerged as important cell oscillators that may impact cell polarity (1, 2), motility (3-6), and division (7). Another prominent example of rhythmic cell activity is the oscillations of cytosolic calcium, a second messenger that has also been implicated in these actin-dependent processes, although its precise involvement remains debated (8-11). Calcium oscillations are most strikingly observed in excitatory or secretory cells, but can occur in all cells in response to hormones or growth factors stimulation (12). Though such oscillations provide an attractive mechanism to encode information with frequency and amplitude (13,14), calcium oscillation-specific functions remain elusive, partially because of the difficulty in dissecting the effects of calcium oscillations from those due to sustained calcium elevations. Considering that rhythmic changes of actin and calcium are likely to have overlapping function in the regulation of fundamental cellular events, here we have investigated their potential coupling in mast cells, a model system where stimulus-evoked changes in cytosolic calcium and actin dynamics have been extensively documented (15). We report the occurrence of both actin waves and actin oscillations in an activity-dependent manner, and the coupling of actin oscillations but not of waves with calcium oscillations. Our results suggest that calcium oscillations, rather than elevation of calcium levels per se, are key factors responsible for the conversion of actin waves into actin oscillations. Thus, calcium oscillations, coupled to PI(4,5)P 2 oscillations, can be used specifically to regulate actin dynamics. Results and DiscussionOscillations and Waves of FBP17, Actin, a...

show abstract

Section: Resultsmentioning

confidence: 99%

Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations

Camilli

2013

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

Self Cite

110

View full text Add to dashboard Cite

show abstract

“…FCHo1/2 and the epsins contain an F-BAR domain and an ENTH domain, respectively, that bind preferentially to curved membranes. At high concentrations in vitro, they can drive tubulation of liposomes (Ford et al 2002;Wu et al 2010;Boucrot et al 2012). The SH3 domain of intersectin may participate in dynamin recruitment.…”

Section: Bar-domain Proteinsmentioning

confidence: 99%

Molecular Structure, Function, and Dynamics of Clathrin-Mediated Membrane Traffic

Kirchhausen

Owen

Harrison

2014

Cold Spring Harbor Perspectives in Biology

431

442

View full text Add to dashboard Cite

Clathrin is a molecular scaffold for vesicular uptake of cargo at the plasma membrane, where its assembly into cage-like lattices underlies the clathrin-coated pits of classical endocytosis. This review describes the structures of clathrin, major cargo adaptors, and other proteins that participate in forming a clathrin-coated pit, loading its contents, pinching off the membrane as a lattice-enclosed vesicle, and recycling the components. It integrates as much of the structural information as possible at the time of writing into a sketch of the principal steps in coated-pit and coated-vesicle formation.

show abstract

“…Among the SH3-domain-mediated interactions of syndapins and of CIP4/Toca subfamily members are for instance those with dynamin, a crucial factor for receptor-mediated endocytosis (Qualmann et al, 1999;Qualmann and Kelly, 2000;Kamioka et al, 2004;Fricke et al, 2009;Bu et al, 2009;Wu et al, 2010) and the neural Wiskott-Aldrich syndrome protein (N-WASP) (Qualmann et al, 1999;Qualmann and Kelly, 2000;Ho et In contrast, proteins of the I-BAR subfamily and iF-BAR proteins (brown) promote negative, concave curvatures, such as those found inside of outward-pointing plasma membrane protrusions (right panel).…”

Section: The Power Of Physical Integrationmentioning

confidence: 99%

Different functional modes of BAR domain proteins in formation and plasticity of mammalian postsynapses

Kessels

Qualmann

2015

Journal of Cell Science

View full text Add to dashboard Cite

A plethora of cell biological processes involve modulations of cellular membranes. By using extended lipid-binding interfaces, some proteins have the power to shape membranes by attaching to them. Among such membrane shapers, the superfamily of Bin–Amphiphysin–Rvs (BAR) domain proteins has recently taken center stage. Extensive structural work on BAR domains has revealed a common curved fold that can serve as an extended membrane-binding interface to modulate membrane topologies and has allowed the grouping of the BAR domain superfamily into subfamilies with structurally slightly distinct BAR domain subtypes (N-BAR, BAR, F-BAR and I-BAR). Most BAR superfamily members are expressed in the mammalian nervous system. Neurons are elaborately shaped and highly compartmentalized cells. Therefore, analyses of synapse formation and of postsynaptic reorganization processes (synaptic plasticity) – a basis for learning and memory formation – has unveiled important physiological functions of BAR domain superfamily members. These recent advances, furthermore, have revealed that the functions of BAR domain proteins include different aspects. These functions are influenced by the often complex domain organization of BAR domain proteins. In this Commentary, we review these recent insights and propose to classify BAR domain protein functions into (1) membrane shaping, (2) physical integration, (3) action through signaling components, and (4) suppression of other BAR domain functions.

show abstract

Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system

Cited by 144 publications

References 41 publications

Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations

Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations

Molecular Structure, Function, and Dynamics of Clathrin-Mediated Membrane Traffic

Different functional modes of BAR domain proteins in formation and plasticity of mammalian postsynapses

Contact Info

Product

Resources

About