Plasma Membrane Potential Oscillations in Insulin Secreting Ins-1 832/13 Cells Do Not Require Glycolysis and Are Not Initiated by Fluctuations in Mitochondrial Bioenergetics
Open accessAbstract
Oscillations in plasma membrane potential play a central role in glucose-induced insulin secretion from pancreatic β-cells and related insulinoma cell lines. We have employed a novel fluorescent plasma membrane potential (Δψ(p)) indicator in combination with indicators of cytoplasmic free Ca(2+) ([Ca(2+)](c)), mitochondrial membrane potential (Δψ(m)), matrix ATP concentration, and NAD(P)H fluorescence to investigate the role of mitochondria in the generation of plasma membrane potential oscillations in clonal INS-1 832/13 β-cells. Elevated glucose caused oscillations in plasma membrane potential and cytoplasmic free Ca(2+) concentration over the same concentration range required for insulin release, although considerable cell-to-cell heterogeneity was observed. Exogenous pyruvate was as effective as glucose in inducing oscillations, both in the presence and absence of 2.8 mM glucose. Increased glucose and pyruvate each produced a concentration-dependent mitochondrial hyperpolarization. The causal relationships between pairs of parameters (Δψ(p) and [Ca(2+)](c), Δψ(p) and NAD(P)H, matrix ATP and [Ca(2+)](c), and Δψ(m) and [Ca(2+)](c)) were investigated at single cell level. It is concluded that, in these β-cells, depolarizing oscillations in Δψ(p) are not initiated by mitochondrial bioenergetic changes. Instead, regardless of substrate, it appears that the mitochondria may simply be required to exceed a critical bioenergetic threshold to allow release of insulin. Once this threshold is exceeded, an autonomous Δψ(p) oscillatory mechanism is initiated.
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Insulin-secreting pancreatic β-cells and islets from people with type 2 diabetes show mitochondrial physiology alterations, including membrane hyperpolarization and decreased activities of glycerol phosphate dehydrogenase, pyruvate carboxylase, and succinyl-CoA-3-ketoacid-CoA transferase.
“Additionally, analysis of insulin-secreting pancreatic β-cells and islets from patients with T2DM showed alterations in mitochondrial physiology, such as hyperpolarization of the mitochondrial membrane and decreased activities of the enzymes glycerol phosphate dehydrogenase, pyruvate carboxylase and succinyl-CoA–3-ketoacid-CoA transferase147,148.”
From Mitochondrial and metabolic dysfunction in ageing and age-related diseases (2022) · cites this paper as [147]
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- Authors
- Goehring, I., Gerencser, A. A., Schmidt, S., Brand, M. D., Mulder, H., & Nicholls, D. G.
- Affiliations
- Buck Institute for Research on Aging (US)
- Lund University (SE)
- Corresponding author
- Nicholls, David G.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-05
- Volume
- 287
- Issue
- 19
- Pages
- 15706-15717
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3346073
- OpenAlex
- W1987930017
- Cited by
- 42
- References
- 54
- Citations by year
- 2025: 3 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 1 · 2018: 4 · 2017: 2 · 2016: 3 · 2015: 6 · 2014: 6 · 2013: 7 · 2012: 1
- FWCI
- 6.51
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- National Institute on Aging (P01AG025901, P30AG025708)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- insulin secretion, INS-1 832/13 cells, pancreatic beta cells, insulinoma, mitochondrial membrane potential, mitochondrial hyperpolarization, mitochondrial bioenergetics, cytosolic free calcium, pyruvate, glucose, glycolysis, NAD(P)H, single-cell heterogeneity
- MeSH terms
- Insulin Secretion, Adenosine Triphosphate, Animals, Calcium, Dose-Response Relationship, Drug, Energy Metabolism, Glucose, Glycolysis, Insulin, Insulinoma, Membrane Potentials, Microscopy, Fluorescence, Mitochondria, Pyruvic Acid, Cell Line, Tumor, Rats, Membrane Potential, Mitochondrial
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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