Mechanisms of Granule Membrane Recapture following Exocytosis in Intact Mast Cells

Deogracias, José Cabeza San; Acosta, José Ángel; Alés, Eva

doi:10.1074/jbc.m113.459065

Cited by 25 publications

(30 citation statements)

References 53 publications

(71 reference statements)

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“…Our data suggest that approximately 30% of retrieved granules in mast cells use the kiss-and-run mechanism to recycle membrane. This proportion is quite similar to that estimated by using combined cell capacitance and amperometry analyses (Cabeza et al, 2013). During this type of fusion, 5-HT can escape and a slow amperometric signal can be detected (Alvarez de Toledo et al, 1993).…”

Section: Discussionsupporting

confidence: 70%

“…Granule shapes suggest the fusion of two or more mature granules, which has been previously observed in mast cells (Alvarez de Toledo and Fernandez, 1990;Cabeza et al, 2013). This process has been identified by taking membrane capacitance measurements and could be explained as follows: after sequential fusion of several granules with the plasma membrane, a degranulation sac is formed.…”

Section: Discussionmentioning

confidence: 99%

“…Reloading with 5-HT permits the cell to be ready to release large amounts of transmitter in a new single fusion event. Because endocytosis of large granules, detected by making capacitance measurements (Cabeza et al, 2013), are in the same size range (0-15 µm 2 ) as large organelles visualized by FM1-43, we can rule out that these events are due to multigranular fusion of previously internalized regular granules. In contrast, 48 h after degranulation, fluorescence imaging showed reductions in the number of larger endocytic events and the mean spot area (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Because of its smaller size, FM can label recaptured granules created by transient fusion, for instance, that are formed by kiss-and-run. The mean pore diameter, which has been measured during transient fusion events ('capacitance flickers') by analysing fusion-pore conductance in mouse mast cells, is approximately 2 nm (Cabeza et al, 2013). For this reason, the larger pHrodo dye cannot, presumably, enter through a nonexpanded fusion pore (<5 nm); therefore, it could not be used to detect kiss-and-run fusion events (Fig.…”

Section: Transient Fusion Events Account For Most Releasable Granulesmentioning

confidence: 99%

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Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

Balseiro-Gómez

Flores

Acosta

et al. 2016

Journal of Cell Science

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To ensure normal immune function, mast cells employ different pathways to release mediators. Here, we report a thus far unknown capacity of mast cells to recycle and reuse secretory granules after an antigen-evoked degranulation process under physiological conditions; this phenomenon involves the existence of a recycling secretory granule pool that is available for release in a short time scale. Rapid endocytic modes contributed to the recycling of ∼60% of the total secretory granule population, which involved kiss-and-run and cavicapture mechanisms, causing retention of the intragranular matrix. We found the presence of normal-size granules and giant actomyosin-and dynamin-dependent granules, which were characterized by large quantal content. These large structures allowed the recovered mast cells to release a large amount of 5-HT, compensating for the decrease in the number of exocytosed secretory granules. This work uncovers a new physiological role of the exo-endocytosis cycle in the immunological plasticity of mast cells and reveals a new property of their biological secretion.

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Section: Discussionsupporting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Transient Fusion Events Account For Most Releasable Granulesmentioning

confidence: 99%

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Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

Balseiro-Gómez

Flores

Acosta

et al. 2016

Journal of Cell Science

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“…The release of mast cell mediators stored in granules requires the fusion of the opposing bilayers of vesicles and plasma membranes (39). In granu-locytes, including mast cells, ternary SNARE complexes are enriched in lipid rafts (40).…”

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confidence: 99%

SNAP23-Dependent Surface Translocation of Leukotriene B ₄ (LTB ₄ ) Receptor 1 Is Essential for NOX2-Mediated Exocytotic Degranulation in Human Mast Cells Induced by Trichomonas vaginalis-Secreted LTB ₄

et al. 2017

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Trichomonas vaginalis is a sexually transmitted parasite that causes vaginitis in women and itself secretes lipid mediator leukotriene B 4 (LTB 4 ). Mast cells are important effector cells of tissue inflammation during infection with parasites.Membrane-bridging SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) complexes are critical for fusion during exocytosis. Although T. vaginalis-derived secretory products (TvSP) have been shown to induce exocytosis in mast cells, information regarding the signaling mechanisms between mast cell activation and TvSP is limited. In this study, we found that SNAP23-dependent surface trafficking of LTB 4 receptor 1 (BLT1) is required for nicotinamide adenine dinucleotide phosphate oxidase 2 (NOX2)-mediated exocytotic degranulation of mast cells induced by TvSP. First, stimulation with TvSP induced exocytotic degranulation and reactive oxygen species (ROS) generation in HMC-1 cells. Next, TvSP-induced ROS generation and exocytosis were strongly inhibited by transfection of BLT1 small interfering RNA (siRNA). TvSP induced trafficking of BLT1 from the cytosol to the plasma membrane. We also found that knockdown of SNAP23 abrogated TvSPinduced ROS generation, exocytosis, and surface trafficking of BLT1 in HMC-1 cells. By coimmunoprecipitation, there was a physical interaction between BLT1 and SNAP23 in TvSP-stimulated HMC-1 cells. Taken together, our results suggest that SNAP23-dependent surface trafficking of BLT1 is essential for exocytosis in human mast cells induced by T. vaginalis-secreted LTB 4 . Our data collectively demonstrate a novel regulatory mechanism for SNAP23-dependent mast cell activation of T. vaginalis-secreted LTB 4 involving surface trafficking of BLT1. These results can help to explain how the cross talk mechanism between parasite and host can govern deliberately tissue inflammatory responses.KEYWORDS Trichomonas vaginalis, LTB 4 , human mast cells, SNAP23, NOX2, BLT1, surface trafficking, exocytotic degranulation T richomonas vaginalis is a lumen-dwelling protozoan parasite with flagella, which infects the genitourinary tract in humans via sexual intercourse (1, 2). Of note, in women it causes vaginitis or cervicitis leading to inflammatory and allergic symptoms, including vaginal discharge with a foul odor and an increased number of leukocytes, and vulvovaginal pruritus (3-6). During the infection, tight junctional proteins between

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Mast Cell Biology at Molecular Level: a Comprehensive Review

Komi

Wöhrl²,

Bielory

2019

Clinic Rev Allerg Immunol

250

194

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Mechanisms of Granule Membrane Recapture following Exocytosis in Intact Mast Cells

Cited by 25 publications

References 53 publications

Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

SNAP23-Dependent Surface Translocation of Leukotriene B ₄ (LTB ₄ ) Receptor 1 Is Essential for NOX2-Mediated Exocytotic Degranulation in Human Mast Cells Induced by Trichomonas vaginalis-Secreted LTB ₄

Mast Cell Biology at Molecular Level: a Comprehensive Review

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Mechanisms of Granule Membrane Recapture following Exocytosis in Intact Mast Cells

Cited by 25 publications

References 53 publications

Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation

SNAP23-Dependent Surface Translocation of Leukotriene B 4 (LTB 4 ) Receptor 1 Is Essential for NOX2-Mediated Exocytotic Degranulation in Human Mast Cells Induced by Trichomonas vaginalis-Secreted LTB 4

Mast Cell Biology at Molecular Level: a Comprehensive Review

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SNAP23-Dependent Surface Translocation of Leukotriene B ₄ (LTB ₄ ) Receptor 1 Is Essential for NOX2-Mediated Exocytotic Degranulation in Human Mast Cells Induced by Trichomonas vaginalis-Secreted LTB ₄