Mitochondria Regulate the Ca2+–Exocytosis Relationship of Bovine Adrenal Chromaffin Cells
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The present study expands the contemporary view of mitochondria as important participants in cellular Ca(2+) dynamics and provides evidence that mitochondria regulate the supply of release-competent secretory granules. Using pharmacological probes to inhibit mitochondrial Ca(2+) import, the ability of mitochondria to modulate secretory activity in single, patch-clamped bovine chromaffin cells was examined by simultaneously monitoring rapid changes in membrane surface area (DeltaC(m)) and cytosolic Ca(2+) levels ([Ca(2+)](c)). Repetitive step depolarizations or action potential waveforms were found to raise the [Ca(2+)](c) of chromaffin cells into the 1 microM to tens of micromolar range. Inhibiting mitochondria by treatment with carbonyl cyanide p-(trifuoro-methoxy)phenylhydrazone, antimycin-oligomycin, or ruthenium red revealed that mitochondria are a prominent component for the clearance of Ca(2+) that entered via voltage-activated Ca(2+) channels. Disruption of cellular Ca(2+) homeostasis by poisoning mitochondria enhanced the secretory responsiveness of chromaffin cells by increasing the amplitude of the transient rise and the time course of recovery to baseline of the evoked Delta[Ca(2+)](c). The enhancement of the secretory response was represented by significant deviation of the Ca(2+)-exocytosis relationship from a standard relationship that equates Ca(2+) influx and DeltaC(m). Thus, mitochondria would play a critical role in the control of secretory activity in chromaffin cells that undergo tonic or repetitive depolarizing activity, likely by limiting the Ca(2+)-dependent activation of specific proteins that recruit or prime secretory granules for exocytosis.
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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 [164]
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 [164]
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- Authors
- Giovannucci, D. R., Hlubek, M. D., & Stuenkel, E. L.
- Affiliations
- University of Michigan (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-11-01
- Volume
- 19
- Issue
- 21
- Pages
- 9261-9270
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782892
- OpenAlex
- W1675974676
- Cited by
- 59
- References
- 84
- Citations by year
- 2024: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2019: 1 · 2018: 1 · 2015: 1 · 2014: 2 · 2013: 2 · 2012: 3
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns036227-05)
- National Institute of Neurological Disorders and Stroke (NS36227)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- mitochondria, calcium homeostasis, exocytosis, chromaffin cells, adrenal medulla, secretory granules, mitochondrial calcium uptake, voltage-gated calcium channels, intracellular calcium, membrane surface area, ruthenium red
- MeSH terms
- Action Potentials, Adrenal Cortex, Animals, Cadmium, Calcium, Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone, Cattle, Cells, Cultured, Dimethylphenylpiperazinium Iodide, Egtazic Acid, Exocytosis, Kinetics, Membrane Potentials, Mitochondria, Patch-Clamp Techniques, Chromaffin Cells
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