Regulation of Exocytosis in Chromaffin Cells by <i>Trans</i>‐Insertion of Lysophosphatidylcholine and Arachidonic Acid into the Outer Leaflet of the Cell Membrane

Amatore, Christian; Arbault, Stéphane; Bouret, Yann; Guille, Manon; Lemaître, Frédéric; Verchier, Yann

doi:10.1002/cbic.200600194

Cited by 81 publications

(98 citation statements)

References 40 publications

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“…They found that LPC facilitates catecholamine release (rate, event frequency, charge released) while AA inhibits the exocytotic processes. They also observed that the detected amount of neurotransmitters in the presence of LPC was larger than under control conditions, while the opposite trend is observed with AA (Amatore et al 2006). …”

Section: Lipid Composition Of the Plasma Membranementioning

confidence: 93%

“…The most direct evidence that the fraction released can be altered was presented by both the Amatore and Ewing groups who showed that the amount of neurotransmitter released per event can be quickly altered by influencing the lipid composition of the plasma membrane (Amatore et al 2006;Mellander et al 2012;Uchiyama et al 2007). In one case, they found that a shortterm incubation of PC12 cells with the inverted cone shaped lipid lysophosphatidylcholine (LPC) increased the average amount of dopamine released per exocytosis event while incubation with the cone shaped phosphatidylethanolamine (PE) decreased it.…”

Section: Lipid Composition Of the Plasma Membranementioning

confidence: 99%

“…This was explained by the added positive curvature by addition of LPC to the outer leaflet of the cell, forming the inner leaflet of the fusion pore, which was hypothesized to result in a pore of a larger diameter. Likewise, addition of the negative curvature lipid, AA, resulted in a decrease in foot current, indicating a smaller fusion pore diameter (Amatore et al 2006). Further supporting the hypothesis of membrane regulation of exocytosis, studies have shown that lipid incubation can manipulate the rate of decay of amperometric peaks, indicating that the vesicle is in fact closing again following partial release of its contents since the membrane composition should not influence a decay based on diffusion and consumption of the electroactive neurotransmitter at the electrode alone (Uchiyama et al 2007).…”

Section: Lipid Composition Of the Plasma Membranementioning

confidence: 99%

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The evidence for open and closed exocytosis as the primary release mechanism

Ren

Mellander

Keighron

et al. 2016

Quart. Rev. Biophys.

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Abstract. Exocytosis is the fundamental process by which cells communicate with each other. The events that lead up to the fusion of a vesicle loaded with chemical messenger with the cell membrane were the subject of a Nobel Prize in 2013. However, the processes occurring after the initial formation of a fusion pore are very much still in debate. The release of chemical messenger has traditionally been thought to occur through full distention of the vesicle membrane, hence assuming exocytosis to be all or none. In contrast to the all or none hypothesis, here we discuss the evidence that during exocytosis the vesicle-membrane pore opens to release only a portion of the transmitter content during exocytosis and then close again. This open and closed exocytosis is distinct from kiss-and-run exocytosis, in that it appears to be the main content released during regular exocytosis. The evidence for this partial release via open and closed exocytosis is presented considering primarily the quantitative evidence obtained with amperometry.1. An overview of exocytosis and endocytosis 2 2. Techniques to monitor exocytosis 5 2.1. Patch clamp 6 2.2. Amperometry 6 2.3. Patch amperometry 7 2.4. Cyclic voltammetry 7 2.5. Fluorescence microscopy imaging 83. Traditional models of exocytosis 94. Evidence where partial release during exocytosis appears to be dominant 11 4.1. The total content of a secretory vesicle is greater than the amount released 11 4.2. The majority of exocytotic events are followed by immediate endocytosis 12 4.3. Full distention of the vesicle may not be necessary for quantal release 13 4.4. A flickering fusion pore might regulate quantal release and vesicle recycling 15 4.5. Nanometer-sized pores can be seen as 'feet' associated with amperometric spikes 17 3. Release appears to be only a fraction of vesicle content in mammalian brains 23 7.4. Impact cytometry of adrenal cell vesicles shows a significantly larger catecholamine content then that released 23 7.5. Impact cytometry has been used to measure vesicle content in live cells and this quantity is greater than the amount released 23 7.6. Full distention of the vesicle is not necessary for the measured amperometric current during exocytotic release 23 7.7. Fast changes in cell environment alter the amount of messenger released 23 7.8. Patch amperometry measurements reveal a greater amount of release 23 7.9. Postspike 'feet' are observed with an amperometric spike 23Acknowledgements 24

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Section: Lipid Composition Of the Plasma Membranementioning

confidence: 93%

Section: Lipid Composition Of the Plasma Membranementioning

confidence: 99%

Section: Lipid Composition Of the Plasma Membranementioning

confidence: 99%

See 1 more Smart Citation

The evidence for open and closed exocytosis as the primary release mechanism

Ren

Mellander

Keighron

et al. 2016

Quart. Rev. Biophys.

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“…These brief incubations were performed immediately before stimulating release [71], with the intention of altering the fusogenic and dissipative properties of the membrane assembly [78][79][80][81][82][83]. The brief incubations ensured that exogenous lipids exclusively trans-inserted in the outer leaflet of the cell membrane [82], with opposite consequences for the large positive curvatures at the fusion pore edges [36,[53][54][55][75][76][77]84,85] due to their shapes.…”

Section: Resultsmentioning

confidence: 99%

‘Full fusion’ is not ineluctable during vesicular exocytosis of neurotransmitters by endocrine cells

Oleinick¹,

Svir²,

Amatore³

2017

Proc. R. Soc. A.

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Vesicular exocytosis is an essential and ubiquitous process in neurons and endocrine cells by which neurotransmitters are released in synaptic clefts or extracellular fluids. It involves the fusion of a vesicle loaded with chemical messengers with the cell membrane through a nanometric fusion pore. In endocrine cells, unless it closes after some flickering (‘Kiss-and-Run’ events), this initial pore is supposed to expand exponentially, leading to a full integration of the vesicle membrane into the cell membrane—a stage called ‘full fusion’. We report here a compact analytical formulation that allows precise measurements of the fusion pore expansion extent and rate to be extracted from individual amperometric spike time courses. These data definitively establish that, during release of catecholamines, fusion pores enlarge at most to approximately one-fifth of the radius of their parent vesicle, hence ruling out the ineluctability of ‘full fusion’.

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“…In contrast, incubation of isolated chromaffin granules with arachidonic acid (negative intrinsic curvature) promotes fusion (32). Amatore et al recently showed that these lipids could each produce the opposite effect when added to the extracellular media (the noncontact side of the fusing membranes) of chromaffin cells undergoing exocytosis (33). In a similar experiment PC12 cells were incubated with dipalmitoylphosphatidylcholine, a lamellar lipid (close to no intrinsic curvature), resulting in a decrease in the rate of exocytosis (34).…”

Section: Discussionmentioning

confidence: 99%

Mass spectrometry imaging of mating Tetrahymena show that changes in cell morphology regulate lipid domain formation

Kurczy

Piehowski

Bell

et al. 2010

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

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Mass spectrometry imaging has been used here to suggest that changes in membrane structure drive lipid domain formation in mating single-cell organisms. Chemical studies of lipid bilayers in both living and model systems have revealed that chemical composition is coupled to localized membrane structure. However, it is not clear if the lipids that compose the membrane actively modify membrane structure or if structural changes cause heterogeneity in the surface chemistry of the lipid bilayer. We report that timeof-flight secondary ion mass spectrometry images of mating Tetrahymena thermophila acquired at various stages during mating demonstrate that lipid domain formation, identified as a decrease in the lamellar lipid phosphatidylcholine, follows rather than precedes structural changes in the membrane. Domains are formed in response to structural changes that occur during cellto-cell conjugation. This observation has wide implications in all membrane processes.lipid domains | membranes | phosphatidylcholine

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Regulation of Exocytosis in Chromaffin Cells by Trans‐Insertion of Lysophosphatidylcholine and Arachidonic Acid into the Outer Leaflet of the Cell Membrane

Cited by 81 publications

References 40 publications

The evidence for open and closed exocytosis as the primary release mechanism

The evidence for open and closed exocytosis as the primary release mechanism

‘Full fusion’ is not ineluctable during vesicular exocytosis of neurotransmitters by endocrine cells

Mass spectrometry imaging of mating Tetrahymena show that changes in cell morphology regulate lipid domain formation

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