Physicochemical Analysis from Real-Time Imaging of Liposome Tubulation Reveals the Characteristics of Individual F-BAR Domain Proteins

Tanaka-Takiguchi, Yohko; Itoh, Toshiki; Tsujita, Kazuya; Yamada, Shunsuke; Yanagisawa, Miho; Fujiwara, Keigi; Yamamoto, Akihisa; Ichikawa, Masatoshi; Takiguchi, K.

doi:10.1021/la303902q

Cited by 45 publications

(63 citation statements)

References 39 publications

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“…PSTPIP1-WT and -R405C localized to the dorsal plasma membrane and could induce membrane tubulation, as previously reported (Figure 4C-D). 46,47 Interestingly, and in contrast to PSTPIP2, PSTPIP1 did not localize to podosomes. 32 As expected, PSTPIP1-deficient cells expressing GFP had approximately double the number of podosomes compared with control cells expressing GFP.…”

Section: Pstpip1-r405c Impairs Podosome Formation and Promotes Filopomentioning

confidence: 90%

The F-BAR protein PSTPIP1 controls extracellular matrix degradation and filopodia formation in macrophages

Starnes

Bennin

Bing

et al. 2014

Blood

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Key Points• PSTPIP1 regulates the transition from podosomes to filopodia in macrophages by modulating WASP activity.• The novel PSTPIP1-R405C mutant induces filopodia formation, increases matrix degradation, and is associated with severe pyoderma gangrenosum.PSTPIP1 is a cytoskeletal adaptor and F-BAR protein that has been implicated in autoinflammatory disease, most notably in the PAPA syndrome: pyogenic sterile arthritis, pyoderma gangrenosum, and acne. However, the mechanism by which PSTPIP1 regulates the actin cytoskeleton and contributes to disease pathogenesis remains elusive. Here, we show that endogenous PSTPIP1 negatively regulates macrophage podosome organization and matrix degradation. We identify a novel PSTPIP1-R405C mutation in a patient presenting with aggressive pyoderma gangrenosum. Identification of this mutation reveals that PSTPIP1 regulates the balance of podosomes and filopodia in macrophages. The PSTPIP1-R405C mutation is in the SRC homology 3 (SH3) domain and impairs Wiskott-Aldrich syndrome protein (WASP) binding, but it does not affect interaction with protein-tyrosine phosphatase (PTP)-PEST. Accordingly, WASP inhibition reverses the elevated F-actin content, filopodia formation, and matrix degradation induced by PSTPIP1-R405C. Our results uncover a novel role for PSTPIP1 and WASP in orchestrating different types of actin-based protrusions. Our findings implicate the cytoskeletal regulatory functions of PSTPIP1 in the pathogenesis of pyoderma gangrenosum and suggest that the cytoskeleton is a rational target for therapeutic intervention in autoinflammatory disease. (Blood. 2014;123(17):2703-2714 Introduction Dynamic regulation of the actin cytoskeleton and cell migration is essential for cellular immunity, because leukocytes travel long distances between tissues to perform their effector functions. Indeed, immunodeficiency syndromes, including Wiskott-Aldrich syndrome, leukocyte adhesion deficiency, and warts-hypogammaglobulinemiainfections-myelokathexis syndrome, are secondary to defects in the cytoskeleton and motility of leukocytes.1 Colchicine, which inhibits microtubule polymerization, is used to treat inflammatory conditions, and several other compounds that target cell motility are in development as immunomodulators, which indicates the importance of regulating the cytoskeleton to control immunity and inflammation.2,3 Conversely, neutrophils from patients with the autoinflammatory disease, neonatal onset multisystem inflammatory disease/ Muckle-Wells syndrome, have impaired chemotaxis, which suggests that altered leukocyte migration may also promote a proinflammatory state. 4 While altered leukocyte motility has been established as a cause of immunodeficiency, the role of cytoskeletal dysregulation and altered motility in inflammation and tissue damage remains poorly characterized.Proline-serine-threonine phosphatase interacting protein 1 (PSTPIP1) is a cytoskeleton-associated adaptor and F-BAR domaincontaining protein that is linked to PAPA syndrome, the human inflammatory disea...

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Section: Pstpip1-r405c Impairs Podosome Formation and Promotes Filopomentioning

confidence: 90%

The F-BAR protein PSTPIP1 controls extracellular matrix degradation and filopodia formation in macrophages

Starnes

Bennin

Bing

et al. 2014

Blood

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“…The most basic method consists of incubating GUVs (doped with fluorescent lipids) with fluorescently tagged proteins. Under appropriate conditionsusually relatively low membrane tension and high enough protein bulk concentration [33]membrane tubulations or invaginations can be observed with confocal microscopy (see [41] for a review and [42][43][44] for examples on BAR proteins). However, no quantitative measurement of protein shaping can be extracted from these observations.…”

Section: (B) Spontaneous Tubulation Of Giant Vesiclesmentioning

confidence: 99%

Physical basis of some membrane shaping mechanisms

Šimunović

Prévost

Callan-Jones

et al. 2016

Phil. Trans. R. Soc. A.

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In vesicular transport pathways, membrane proteins and lipids are internalized, externalized or transported within cells, not by bulk diffusion of single molecules, but embedded in the membrane of small vesicles or thin tubules. The formation of these 'transport carriers' follows sequential events: membrane bending, fission from the donor compartment, transport and eventually fusion with the acceptor membrane. A similar sequence is involved during the internalization of drug or gene carriers inside cells. These membrane-shaping events are generally mediated by proteins binding to membranes. The mechanisms behind these biological processes are actively studied both in the context of cell biology and biophysics. Bin/amphiphysin/Rvs (BAR) domain proteins are ideally suited for illustrating how simple soft matter principles can account for membrane deformation by proteins. We review here some experimental methods and corresponding theoretical models to measure how these proteins affect the mechanics and the shape of membranes. In more detail, we show how an experimental method employing optical tweezers to pull a tube from a giant vesicle may give important quantitative insights into the mechanism by which proteins sense and generate membrane curvature and the mechanism of membrane scission.This article is part of the themed issue 'Soft interfacial materials: from fundamentals to formulation'.

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“…Some of the BAR superfamily proteins, such as N-BAR proteins, also have hydrophobic insertions. Experimentally, the membrane tubulation and curvaturesensing by various types of BAR superfamily proteins have been observed [7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22].…”

Section: Introductionmentioning

confidence: 99%

Membrane structure formation induced by two types of banana-shaped proteins

Noguchi

Fournier

2017

Soft Matter

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The assembly of banana-shaped rodlike proteins on membranes, and the associated membrane shape transformations, are investigated by analytical theory and coarse-grained simulations. The membrane-mediated interactions between two banana-shaped inclusions are derived theoretically using a point-like formalism based on fixed anisotropic curvatures, both for zero surface tension and for finite surface tension. On a larger scale, the interactions between assemblies of such rodlike inclusions are determined analytically. Meshless membrane simulations are performed in the presence of a large number of inclusions of two types, corresponding to curved rods of opposite curvatures, both for flat membranes and vesicles. Rods of the same type aggregate into linear assemblies perpendicular to the rod axis, leading to membrane tubulation. However, rods of the other type, those of opposite curvature, are attracted to the lateral sides of these assemblies, and stabilize a straight bump structure that prevents tubulation. When the two types of rods have almost opposite curvatures, the bumps attract one another, forming a stripe structure. Positive surface tension is found to stabilize the stripe formation. The simulation results agree well with the theoretical predictions provided the point-like curvatures of the model are scaled-down to account for the effective flexibility of the simulated rods.

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Physicochemical Analysis from Real-Time Imaging of Liposome Tubulation Reveals the Characteristics of Individual F-BAR Domain Proteins

Cited by 45 publications

References 39 publications

The F-BAR protein PSTPIP1 controls extracellular matrix degradation and filopodia formation in macrophages

The F-BAR protein PSTPIP1 controls extracellular matrix degradation and filopodia formation in macrophages

Physical basis of some membrane shaping mechanisms

Membrane structure formation induced by two types of banana-shaped proteins

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