SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS
Under basal conditions the action potential firing rate of adrenal chromaffin cells is lower than 0.5 Hz. The maintenance of the secretory response at such frequencies requires a continuous replenishment of releasable vesicles. However, the mechanism that allows such vesicle replenishment remains un...
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Frontiers Media S.A.
2016-07-01
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Series: | Frontiers in Cellular Neuroscience |
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Online Access: | http://journal.frontiersin.org/Journal/10.3389/fncel.2016.00184/full |
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author | José Moya-Díaz Yanina Daniela Álvarez Mauricio Norman Montenegro Lucas Bayonés Ana Verónica Belingheri ARLEK MARION GONZALEZ-JAMETT Ana María Cárdenas Fernando Diego Marengo |
author_facet | José Moya-Díaz Yanina Daniela Álvarez Mauricio Norman Montenegro Lucas Bayonés Ana Verónica Belingheri ARLEK MARION GONZALEZ-JAMETT Ana María Cárdenas Fernando Diego Marengo |
author_sort | José Moya-Díaz |
collection | DOAJ |
description | Under basal conditions the action potential firing rate of adrenal chromaffin cells is lower than 0.5 Hz. The maintenance of the secretory response at such frequencies requires a continuous replenishment of releasable vesicles. However, the mechanism that allows such vesicle replenishment remains unclear. Here, using membrane capacitance measurements on mouse chromaffin cells, we studied the mechanism of replenishment of a group of vesicles released by a single action potential-like stimulus (APls). The exocytosis triggered by APls (ETAP) represents a fraction (40%) of the immediately releasable pool, a group of vesicles highly coupled to voltage dependent calcium channels. ETAP was replenished with a time constant of 0.73 +/- 0.11 s, fast enough to maintain synchronous exocytosis at 0.2-0.5 Hz stimulation. Regarding the mechanism involved in rapid ETAP replenishment, we found that it depends on the ready releasable pool; indeed depletion of this vesicle pool significantly delays ETAP replenishment. On the other hand, ETAP replenishment also correlates with a dynamin-dependent fast endocytosis process (τ=0.53±0.01 s). In this regard, disruption of dynamin function markedly inhibits the fast endocytosis and delays ETAP replenishment, but also significantly decreases the synchronous exocytosis during repetitive APls stimulation at low frequencies (0.2 and 0.5 Hz). Considering these findings, we propose a model in where both the transfer of vesicles from ready releasable pool and fast endocytosis allow rapid ETAP replenishment during low stimulation frequencies. |
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spelling | doaj.art-2fe040af0889429d819b3c5a97f06ba72022-12-22T03:37:04ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022016-07-011010.3389/fncel.2016.00184196852SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESSJosé Moya-Díaz0Yanina Daniela Álvarez1Mauricio Norman Montenegro2Lucas Bayonés3Ana Verónica Belingheri4ARLEK MARION GONZALEZ-JAMETT5Ana María Cárdenas6Fernando Diego Marengo7IFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.IFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.IFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.IFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.IFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.Universidad de ValparaísoUniversidad de ValparaísoIFIByNE - CONICET. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires.Under basal conditions the action potential firing rate of adrenal chromaffin cells is lower than 0.5 Hz. The maintenance of the secretory response at such frequencies requires a continuous replenishment of releasable vesicles. However, the mechanism that allows such vesicle replenishment remains unclear. Here, using membrane capacitance measurements on mouse chromaffin cells, we studied the mechanism of replenishment of a group of vesicles released by a single action potential-like stimulus (APls). The exocytosis triggered by APls (ETAP) represents a fraction (40%) of the immediately releasable pool, a group of vesicles highly coupled to voltage dependent calcium channels. ETAP was replenished with a time constant of 0.73 +/- 0.11 s, fast enough to maintain synchronous exocytosis at 0.2-0.5 Hz stimulation. Regarding the mechanism involved in rapid ETAP replenishment, we found that it depends on the ready releasable pool; indeed depletion of this vesicle pool significantly delays ETAP replenishment. On the other hand, ETAP replenishment also correlates with a dynamin-dependent fast endocytosis process (τ=0.53±0.01 s). In this regard, disruption of dynamin function markedly inhibits the fast endocytosis and delays ETAP replenishment, but also significantly decreases the synchronous exocytosis during repetitive APls stimulation at low frequencies (0.2 and 0.5 Hz). Considering these findings, we propose a model in where both the transfer of vesicles from ready releasable pool and fast endocytosis allow rapid ETAP replenishment during low stimulation frequencies.http://journal.frontiersin.org/Journal/10.3389/fncel.2016.00184/fullEndocytosissecretioncalcium currentdynaminmembrane capacitanceimmediately releasable pool |
spellingShingle | José Moya-Díaz Yanina Daniela Álvarez Mauricio Norman Montenegro Lucas Bayonés Ana Verónica Belingheri ARLEK MARION GONZALEZ-JAMETT Ana María Cárdenas Fernando Diego Marengo SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS Frontiers in Cellular Neuroscience Endocytosis secretion calcium current dynamin membrane capacitance immediately releasable pool |
title | SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS |
title_full | SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS |
title_fullStr | SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS |
title_full_unstemmed | SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS |
title_short | SUSTAINED EXOCYTOSIS AFTER ACTION POTENTIAL-LIKE STIMULATION AT LOW FREQUENCIES IN MOUSE CHROMAFFIN CELLS DEPENDS ON A DYNAMIN-DEPENDENT FAST ENDOCYTOTIC PROCESS |
title_sort | sustained exocytosis after action potential like stimulation at low frequencies in mouse chromaffin cells depends on a dynamin dependent fast endocytotic process |
topic | Endocytosis secretion calcium current dynamin membrane capacitance immediately releasable pool |
url | http://journal.frontiersin.org/Journal/10.3389/fncel.2016.00184/full |
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