F-Actin and Myosin II Accelerate Catecholamine Release from Chromaffin Granules

Berberian, Khajak; Torres, Alexis J.; Fang, Qinghua; Kisler, Kassandra; Lindau, Manfred

doi:10.1523/jneurosci.2818-08.2009

Cited by 98 publications

(111 citation statements)

References 44 publications

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“…The longer t foot in presence of the fully active dynamin might indicate that the foot feature corresponds to the formation of the dynamin assembly and the initiation of GTPase activity, followed by the pore expansion. This concept, supported by several studies (Berberian et al 2009;Burgoyne et al 2001;Fulop et al 2008;Guzman et al 2007;Wang & Richards, 2011) suggests that the mechanochemical activity of dynamin is involved in exocytosis, and that this activity relies on its GTPase properties.…”

Section: Regulation Of Open and Closed Exocytosismentioning

confidence: 72%

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: Regulation Of Open and Closed Exocytosismentioning

confidence: 72%

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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“…Both partial actin depolymerization immediately after stimulation 37 as well as N-WASP-and Cdc42-dependent actin polymerization 7,38 have been shown to contribute to neuroexocytosis, demonstrating the pleiotropic role of the cortical actin network as both a retaining barrier and a means of SV transport. Myosin II has previously been implicated in a number of steps leading to SV fusion, with most studies showing that it is directly involved in controlling fusion pore dynamics 12,14,17,39 . Our data add another layer to our understanding of the function of myosin II in exocytosis.…”

Section: Discussionmentioning

confidence: 99%

“…This is probably due to other cytoskeletal effects, as described previously 9 . It is also important to note that myosin II is involved in regulating fusion pore dynamics, which also affects the release process 12,17,47 .…”

Section: Discussionmentioning

confidence: 99%

“…SVs can be tethered to the cortical actin network by myosin VI in an activity-dependent manner 10 , and can also be transported along actin fibres by myosin Va 11 . Recent work has also highlighted a role for myosin II in exocytosis [12][13][14][15][16][17] , as well as demonstrating its ability to maintain the cortical actin network under tension [18][19][20] . How these molecular motors act to direct SVs towards their docking sites remains unclear.…”

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confidence: 99%

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Activity-driven relaxation of the cortical actomyosin II network synchronizes Munc18-1-dependent neurosecretory vesicle docking

et al. 2015

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In neurosecretory cells, secretory vesicles (SVs) undergo Ca 2 þ -dependent fusion with the plasma membrane to release neurotransmitters. How SVs cross the dense mesh of the cortical actin network to reach the plasma membrane remains unclear. Here we reveal that, in bovine chromaffin cells, SVs embedded in the cortical actin network undergo a highly synchronized transition towards the plasma membrane and Munc18-1-dependent docking in response to secretagogues. This movement coincides with a translocation of the cortical actin network in the same direction. Both effects are abolished by the knockdown or the pharmacological inhibition of myosin II, suggesting changes in actomyosin-generated forces across the cell cortex. Indeed, we report a reduction in cortical actin network tension elicited on secretagogue stimulation that is sensitive to myosin II inhibition. We reveal that the cortical actin network acts as a 'casting net' that undergoes activity-dependent relaxation, thereby driving tethered SVs towards the plasma membrane where they undergo Munc18-1-dependent docking.

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“…In chromaffin cells, the initial fusion pore between secretory granules and plasma membranes has been proposed to be essentially of a lipid nature and controlled by physicochemical laws (Oleinick et al, 2013). However, it is clear that the formation of this initial fusion pore formation requires SNARE proteins (Kesavan et al, 2007;Bretou et al, 2008) and can be influenced by local substructures like the acto-myosin system (Doreian et al, 2008;Neco et al, 2008;Berberian et al, 2009). RhoA might interfere with SNARE functions through the RhoA/ROCK (Rho-kinase) pathway, which has been described to phosphorylate syntaxin1A and/or promote its associa- ϩ/y and Ophn1 Ϫ /y mice subjected to an anti-DBH antibody internalization assay.…”

Section: Discussionmentioning

confidence: 99%

Oligophrenin-1 Connects Exocytotic Fusion to Compensatory Endocytosis in Neuroendocrine Cells

Houy

Estay-Ahumada

Croisé

et al. 2015

Journal of Neuroscience

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Oligophrenin-1 (OPHN1) is a protein with multiple domains including a Rho family GTPase-activating (Rho-GAP) domain, and aBin-Amphiphysin-Rvs (BAR) domain. Involved in X-linked intellectual disability, OPHN1 has been reported to control several synaptic functions, including synaptic plasticity, synaptic vesicle trafficking, and endocytosis. In neuroendocrine cells, hormones and neuropeptides stored in large dense core vesicles (secretory granules) are released through calcium-regulated exocytosis, a process that is tightly coupled to compensatory endocytosis, allowing secretory granule recycling. We show here that OPHN1 is expressed and mainly localized at the plasma membrane and in the cytosol in chromaffin cells from adrenal medulla. Using carbon fiber amperometry, we found that exocytosis is impaired at the late stage of membrane fusion in Ophn1 knock-out mice and OPHN1-silenced bovine chromaffin cells. Experiments performed with ectopically expressed OPHN1 mutants indicate that OPHN1 requires its Rho-GAP domain to control fusion pore dynamics. On the other hand, compensatory endocytosis assessed by measuring dopamine-␤-hydroxylase (secretory granule membrane) internalization is severely inhibited in Ophn1 knock-out chromaffin cells. This inhibitory effect is mimicked by the expression of a truncated OPHN1 mutant lacking the BAR domain, demonstrating that the BAR domain implicates OPHN1 in granule membrane recapture after exocytosis. These findings reveal for the first time that OPHN1 is a bifunctional protein that is able, through distinct mechanisms, to regulate and most likely link exocytosis to compensatory endocytosis in chromaffin cells.

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F-Actin and Myosin II Accelerate Catecholamine Release from Chromaffin Granules

Cited by 98 publications

References 44 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

Activity-driven relaxation of the cortical actomyosin II network synchronizes Munc18-1-dependent neurosecretory vesicle docking

Oligophrenin-1 Connects Exocytotic Fusion to Compensatory Endocytosis in Neuroendocrine Cells

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