Glucose dependent K+-channels in pancreatic?-cells are regulated by intracellular ATP
Abstract
The resting conductance of cultured beta-cells from murine pancreases was investigated using the whole-cell, cell-attached and isolated patch modes of the patch-clamp technique. Whole-cell experiments revealed a high input resistance of the cells (greater than 20 G omega per cell or greater than 100 k omega X cm2), if the medium dialysing the cell interior contained 3 mM ATP. The absence of ATP evoked a large additional K+ conductance. In cell-attached patches single K+-channels were observed in the absence of glucose. Addition of glucose (20 mM) to the bath suppressed the channel activity and initiated action potentials. Similar single-channel currents were recorded from isolated patches. In this case the channels were reversibly blocked by adding ATP (3 mM) to the solution at the intracellular side of the membrane. The conductances (51 pS and 56 pS for [K+]0 = 145 mM, T = 21 degrees C) and kinetics (at -70 mV: tau open = 2.2 ms and 1.8 ms, tau closed = 0.38 ms and 0.33 ms) of the glucose- and ATP-dependent channels were found to be very similar. It is concluded that both channels are identical. The result suggests that glucose could depolarize the beta-cell by increasing the cytoplasmic concentration of ATP.
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In ATP-free medium, the KATP channel open probability in inside-out patches is 0.06, and the whole-cell conductance under comparable conditions is ~10 nS.
“In ATP-free medium, the open probability in inside-out patches is 0.06 (366). The whole-cell conductance measured under comparable conditions is ~10 nS (573).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [573]
Glucose metabolism closes the KATP channel, thereby depolarizing the β-cell and initiating β-cell electrical activity, Ca2+ influx and insulin secretion.
“Glucose metabolism closes the KATP channel, thereby depolarizing the β-cell and initiating β-cell electrical activity, Ca2+ influx and insulin secretion (27, 573).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [573]
In whole-cell recordings, the maximum KATP conductance when ATP has washed out is around 2 nS/pF; in perforated patch it is ~1 nS/pF in single β-cells exposed to glucose-free solution; in β-cells within freshly isolated islets it ranges between 0.25 and 0.4 nS/pF.
“In whole-cell recordings, the maximum KATP conductance, measured when ATP has washed out of the cell, is around 2 nS/pF (573). When measured in the perforated patch configuration (where cytosolic ATP levels are undisturbed) it is ~1 nS/pF in single β-cells exposed to glucose-free solution (584, 631). In β-cells within freshly isolated pancreatic islets, it is significantly lower and ranges between”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [573]
Cites
Intracellular ATP directly blocks K+ channels in pancreatic B-cells
Cook, D. L., & Hales, N. (1984) · Nature · doi:10.1038/311271a0 · Cited by 1,208 · cited 2× · see citing works
“These values are similar to those found recently by other investigatiors in rat //-cells (Cook and Hales 1984; Ashcroft et al. 1984).”
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Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men
Rorsman, P., & Ashcroft, F. M. (2018) · Physiological Reviews · doi:10.1152/physrev.00008.2017 · Cited by 793 · see citing works
Self-citationRouth, V. H. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00761-8 · Cited by 237 · see citing works
Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting alpha-cells.
Barg, S., Galvanovskis, J., Göpel, S. O., Rorsman, P., & Eliasson, L. (2000) · Diabetes · doi:10.2337/diabetes.49.9.1500 · Cited by 209 · see citing works
Self-citationKumar, D. P., Rajagopal, S., Mahavadi, S., Mirshahi, F., Grider, J. R., Murthy, K. S., & Sanyal, A. J. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.09.104 · Cited by 206 · see citing works
Miki, T., Nagashima, K., & Seino, S. (1999) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0220113 · Cited by 147 · see citing works
Characterisation of sulphonylurea and ATP-regulated K+ channels in rat pancreatic A-cells
Bokvist, K., Olsen, H. L., Høy, M., Gotfredsen, C. F., Holmes, W. F., Buschard, K., Rorsman, P., & Gromada, J. (1999) · Pflügers Archiv · doi:10.1007/s004249900076 · Cited by 132 · see citing works
Self-citationGlucose-induced changes in cytosolic ATP content in pancreatic islets
Malaisse, W. J., & Sener, A. (1987) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(87)90134-0 · Cited by 116 · see citing works
Rorsman, P., & Hellman, B. (1988) · The Journal of general physiology · doi:10.1085/jgp.91.2.223 · Cited by 97 · see citing works
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- Authors
- Rorsman, P., & Trube, G.
- Affiliations
- Max Planck Institute for Biophysical Chemistry (DE)
- ORCID
- Rorsman, P.
- Venue
- Pfl�gers Archiv European Journal of Physiology
- Published
- 1985-12
- Volume
- 405
- Issue
- 4
- Pages
- 305-309
- ISSN
- 0031-6768 (ISSN-L)
- 1432-2013
- OpenAlex
- W2005150634
- Cited by
- 387
- References
- 1
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 2 · 2023: 5 · 2022: 9 · 2021: 7 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 6 · 2016: 1 · 2015: 9 · 2014: 6 · 2013: 3 · 2012: 10
- FWCI
- 41.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Pflügers Archiv - European Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- 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
- pancreatic beta cells, intracellular ATP, single-channel kinetics, input resistance, action potential
- MeSH terms
- Adenosine Triphosphate, Animals, Body Fluids, Electric Conductivity, Glucose, Intracellular Fluid, Ion Channels, Islets of Langerhans, Mice, Inbred Strains, Potassium, Mice
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