TASK-1 Potassium Channels Limit Pancreatic α-Cell Calcium Influx and Glucagon Secretion
Open accessAbstract
Glucose regulation of pancreatic α-cell Ca(2+) entry through voltage-dependent Ca(2+) channels is essential for normal glucagon secretion and becomes defective during the pathogenesis of diabetes mellitus. The 2-pore domain K(+) channel, TWIK-related acid-sensitive K(+) channel 1 (TASK-1), is an important modulator of membrane voltage and Ca(2+) entry. However, its role in α-cells has not been determined. Therefore, we addressed how TASK-1 channels regulate α-cell electrical activity, Ca(2+) entry, and glucagon secretion. We find that TASK-1 channels expressed in human and rodent α-cells are blocked by the TASK-1 channel inhibitor A1899. Alpha-cell 2-pore domain K(+) currents were also significantly reduced after ablation of mouse α-cell TASK-1 channels. Inhibition of TASK-1 channels with A1899 caused plasma membrane potential depolarization in both human and mouse α-cells, which resulted in increased electrical excitability. Moreover, ablation of α-cell TASK-1 channels increased α-cell electrical excitability under elevated glucose (11 mM) conditions compared with control α-cells. This resulted in significantly elevated α-cell Ca(2+) influx when TASK-1 channels were inhibited in the presence of high glucose (14 mM). However, there was an insignificant change in α-cell Ca(2+) influx after TASK-1 inhibition in low glucose (1 mM). Glucagon secretion from mouse and human islets was also elevated specifically in high (11 mM) glucose after acute TASK-1 inhibition. Interestingly, mice deficient for α-cell TASK-1 showed improvements in both glucose inhibition of glucagon secretion and glucose tolerance, which resulted from the chronic loss of α-cell TASK-1 currents. Therefore, these data suggest an important role for TASK-1 channels in limiting α-cell excitability and glucagon secretion during glucose stimulation.
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Action potential frequency was paradoxically reduced in β-cells from Knck3-deficient mice.
“Action potential frequency was paradoxically reduced (135), but this may be a consequence of voltage-dependent inactivation of other currents involved in action potential generation.”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
In “TASK-1 currents regulate pancreatic α-cell Δp” (page not available), the paper reports greater action-potential firing in TASK-1-deficient α-cells than in controls under elevated glucose, not reduced firing. The experiment concerns α-cells, whereas the claim specifies β-cells. (LLM, conf=0.85)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredIn 14 mM glucose, blocking TASK1 with the selective inhibitor A1899 depolarizes the human β-cell by about 5 mV and increases action potential frequency.
“In 14 mM glucose, blocking the channel with the selective inhibitor A1899 depolarizes the β-cell by ~5 mV and increases action potential frequency.”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
The section “TASK-1 currents regulate pancreatic α-cell Δp” (page unavailable) reports that A1899 depolarized human α-cells in 14 mM glucose, not human β-cells. The paper describes increased α-cell electrical excitability, but does not give a ~5 mV depolarization or a measured increase in action-potential frequency for A1899-treated human β-cells. (LLM, conf=0.88)
Experimental — accuracy not yet measuredβ-cells from Knck3-deficient mice are slightly more depolarized in the presence of glucose than their wild-type counterparts.
“Despite the small size of the current, β-cells from Knck3-deficient mice were slightly more depolarized in the presence of glucose than their wild-type counterparts.”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
The section “TASK-1 currents regulate pancreatic α-cell Δp” reports that KCNK3/TASK-1-deficient cells were more depolarized than controls under glucose conditions. But the measured cells were α-cells, not β-cells; our copy does not establish the claimed β-cell result. No page number is available in the indexed passage. (LLM, conf=0.89)
Experimental — accuracy not yet measuredAction potential height is also reduced in human β-cells when TASK1 is blocked, presumably due to depolarization-induced inactivation of ion channels involved in action potential firing.
“Action potential height is also reduced, presumably due to depolarization-induced inactivation of ion channels involved in action potential firing (see Section V.B.2.B.2).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
The introductory passage (page unavailable) says TASK-1 inhibition depolarizes the membrane potential in pancreatic β-cells. The Discussion (page unavailable) proposes voltage-dependent channel inactivation after TASK-1 loss, but for α-cells. Our copy does not report reduced action-potential height in human β-cells when TASK-1 is blocked. (LLM, conf=0.78)
Experimental — accuracy not yet measuredTASK1 activates around -30 mV in human β-cells.
“TASK1 activates around -30 mV in human β-cells (135).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
The section ‘TASK-1 channels are functionally expressed in mouse and human α-cells’ reports functional TASK-1-like currents in human α-cells, not β-cells. A search for β-cell activation and −30 mV found no passage establishing the claimed activation voltage in human β-cells; the reported voltage ramp from −120 to 60 mV is not an activation threshold. Page numbers were unavailable in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measured
The contribution of TASK1 to the β-cell membrane conductance is negligible at physiological membrane potentials and even at -10 mV, where the outward current through these channels is only 1 pA/pF.
“As might be predicted from its very low expression, comparison of the membrane currents in wild-type and Knck3 knockout mice indicated its contribution to the β-cell membrane conductance is negligible at physiological membrane potentials and even at -10 mV (the peak of the action potential), the outward current flowing through these channels is only 1 pA/pF (135).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [135]
The section ‘TASK-1 channels are functionally expressed in mouse and human α-cells’ reports currents measured in α-cells, not β-cells. Our copy briefly mentions small TASK-1 currents in β-cells, but the searched passages do not report a β-cell knockout comparison, negligible conductance at physiological potentials, or a 1 pA/pF current at −10 mV. No page numbers are available in the indexed copy. (LLM, conf=0.76)
Experimental — accuracy not yet measured
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- Authors
- Dadi, P. K., Luo, B., Vierra, N. C., & Jacobson, D. A.
- Affiliations
- Vanderbilt University (US)
- University of Oklahoma (US)
- Corresponding author
- Jacobson, David A.
- Venue
- Molecular Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2015-05-01
- Volume
- 29
- Issue
- 5
- Pages
- 777-787
- ISSN
- 0888-8809 (ISSN-L)
- 1944-9917
- PMC
- PMC4415209
- OpenAlex
- W2032445998
- Cited by
- 40
- References
- 52
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 7 · 2020: 7 · 2019: 3 · 2018: 1 · 2017: 7 · 2016: 3
- FWCI
- 3.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Endocrinology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Vanderbilt University (DK20593)
- National Institutes of Health (5p60dk020593-31, DK 20593, P60 DK20593)
- National Institute on Alcohol Abuse and Alcoholism (F31AA021623)
- National Institute of Diabetes and Digestive and Kidney Diseases (P60-DK020593, DK-081666, R03DK096122, R01DK097392, DK096122, K01DK081666, P30DK020593)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Keywords
- TASK-1, potassium channels, alpha cells, glucagon secretion, calcium influx, voltage-gated calcium channels, glucose regulation, glucose tolerance, diabetes mellitus, islets
- MeSH terms
- Animals, Cells, Cultured, Female, Glucagon, Glucose, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Tissue Proteins, Gene Expression, Calcium Signaling, Potassium Channels, Tandem Pore Domain, Glucagon-Secreting Cells, Membrane Potential, Mitochondrial
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