Novel features on the regulation by mitochondria of calcium and secretion transients in chromaffin cells challenged with acetylcholine at 37°C
Open accessAbstract
From experiments performed at room temperature, we know that the buffering of Ca(2+) by mitochondria contributes to the shaping of the bulk cytosolic calcium transient ([Ca(2+)]c) and secretion transients of chromaffin cells stimulated with depolarizing pulses. We also know that the mitochondrial Ca(2+) transporters and the release of catecholamine are faster at 37°C with respect to room temperature. Therefore, we planned this investigation to gain further insight into the contribution of mitochondrial Ca(2+) buffering to the shaping of [Ca(2+)]c and catecholamine release transients, using some novel experimental conditions that have not been yet explored namely: (1) perifusion of bovine chromaffin cells (BCCs) with saline at 37°C and their repeated challenging with the physiological neurotransmitter acetylcholine (ACh); (2) separate blockade of mitochondrial Ca(2+) uniporter (mCUP) with Ru360 or the mitochondrial Na(+)/Ca(2+) exchanger (mNCX) with CGP37157; (3) full blockade of the mitochondrial Ca(2+) cycling (mCC) by the simultaneous inhibition of the mCUP and the mNCX. Ru360 caused a pronounced delay of [Ca(2+)]c clearance and augmented secretion. In contrast, CGP37157 only caused a tiny delay of [Ca(2+)]c clearance and a mild decrease in secretion. The mCC resulting in continued Ca(2+) uptake and its release back into the cytosol was interrupted by combined Ru360 + CGP37157 (Ru/CGP), the protonophore carbonyl cyanide-p-trifluoromethoxyphenylhydrazone, or combined oligomycin + rotenone (O/R); these three treatments caused a mild but sustained elevation of basal [Ca(2+)]c that, however, was not accompanied by a parallel increase in basal secretion. Nevertheless, all treatments caused a pronounced augmentation of ACh-induced secretion, with minor changes of the ACh-induced [Ca(2+)]c transients. Combined Ru/CGP did not alter the resting membrane potential in current-clamped cells. Additionally, Ru/CGP did not increase basal [Ca(2+)]c near subplasmalemmal sites and caused a mild decrease in the size of the readily releasable vesicle pool. Our results provide new functional features in support of the view that in BCCs there are two subpopulations of mitochondria, M1 underneath the plasmalemma nearby exocytotic sites and M2 at the core cell nearby vesicle transport sites. While M1 serves to shape the ACh-elicited exocytotic response through its efficient Ca(2+) removal by the mCUP, M2 shapes the lower [Ca(2+)]c elevations required for new vesicle supply to the exocytotic machinery, from the large reserve vesicle pool at the cell core. The mCUP of the M1 pool seems to play a more prominent role in controlling the ACh responses, in comparison with the mNCX.
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Use of CCCP or FCCP decreases the Ca2+ buffering capacity of mitochondria and increases global exocytosis in bovine and rat chromaffin cells but not in the same cell type in mice.
“In accordance with this theory, use of CCCP or FCCP decreases the Ca2+ buffering capacity of mitochondria and increases global exocytosis in bovine [164,165] and rat chromaffin cells [166] but not in the same cell type in mice [167], suggesting species differences.”
From Mitochondrial Uncoupling: A Key Controller of Biological Processes in Physiology and Diseases (2019) · cites this paper as [165]
By decreasing the Ca2+ buffering capacity of mitochondria, CCCP or FCCP increases global exocytosis in chromaffin cells.
“By decreasing the Ca2+ buffering capacity of mitochondria, CCCP or FCCP increases global exocytosis in chromaffin cells [164,165,166].”
From Mitochondrial Uncoupling: A Key Controller of Biological Processes in Physiology and Diseases (2019) · cites this paper as [165]
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Mitochondrial Uncoupling: A Key Controller of Biological Processes in Physiology and Diseases
Demine, S., Renard, P., & Arnould, T. (2019) · Cells · doi:10.3390/cells8080795 · Cited by 476 · see citing works
- Authors
- Caricati-Neto, A., Padín, J.-F., Silva-Junior, E.-D., Fernández-Morales, J.-C., de Diego, A.-M. G., Jurkiewicz, A., & García, A. G.
- Affiliations
- Departamento de Farmacología; Escola Paulista de Medicina; Universidade Federal de São Paulo; São Paulo Brazil
- Universidad Autónoma de Madrid (ES)
- Universidade Federal de São Paulo (BR)
- Instituto Teófilo Hernando; Facultad de Medicina; Universidad Autónoma de Madrid; C/Arzobispo Morcillo, 4 28029 Madrid Spain
- ORCID
- Padín, Juan-Fernando
- Venue
- Physiological Reports
- Publisher
- Wiley
- Published
- 2013-12
- Volume
- 1
- Issue
- 7
- Pages
- e00182
- ISSN
- 2051-817X (ISSN-L)
- PMC
- PMC3970745
- OpenAlex
- W2137168605
- Cited by
- 12
- References
- 65
- Citations by year
- 2022: 2 · 2021: 1 · 2020: 3 · 2019: 3 · 2016: 2 · 2015: 1
- FWCI
- 0.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Physiological Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Ministerio de Economía y Competitividad (SAF 2010-21795)
- Brazilian Spanish Program Co-interuniversity (PHB-2011-0029-PC)
- UAM-EPM-Santander
- Fundación Teófilo Hernando
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- chromaffin cells, mitochondrial calcium buffering, calcium transients, catecholamine release, acetylcholine, mitochondrial calcium uniporter, mitochondrial Na+/Ca2+ exchanger, Ru360, FCCP, oligomycin, rotenone, membrane potential, temperature effects
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