Glucose‐dependent regulation of rhythmic action potential firing in pancreatic β‐cells by kATP‐channel modulation
Open accessAbstract
The regulation of a K+ current activating during oscillatory electrical activity (IK,slow) in an insulin‐releasing β‐cell was studied by applying the perforated patch whole‐cell technique to intact mouse pancreatic islets. The resting whole‐cell conductance in the presence of 10 m m glucose amounted to 1.3 nS, which rose by 50 % during a series of 26 simulated action potentials. Application of the K ATP‐channel blocker tolbutamide produced uninterrupted action potential firing and reduced IK,slow by ≈50 %. Increasing glucose from 15 to 30 m m, which likewise converted oscillatory electrical activity into continuous action potential firing, reduced IK,slow by ≈30 % whilst not affecting the resting conductance. Action potential firing may culminate in opening of K ATP channels by activation of ATP‐dependent Ca 2+ pumping as suggested by the observation that the sarco‐endoplasmic reticulum Ca 2+‐ATPase (SERCA) inhibitor thapsigargin (4 μ m) inhibited IK,slow by 25 % and abolished bursting electrical activity. We conclude that oscillatory glucose‐induced electrical activity in the β‐cell involves the opening of K ATP‐channel activity and that these channels, in addition to constituting the glucose‐regulated K+ conductance, also play a role in the graded response to supra‐threshold glucose concentrations.
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Glucose and tolbutamide influence KATP-channel activity also at supra-threshold glucose concentrations.
“These data indicate, consistent with conclusions based on membrane potential measurements (261, 335), that glucose and tolbutamide influence KATP-channel activity also at supra-threshold glucose concentrations.”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [335]
Cites
Santos, R. M., Rosario, L. M., Nadal, A., Garcia-Sancho, J., Soria, B., & Valdeolmillos, M. (1991) · Pfl�gers Archiv European Journal of Physiology · doi:10.1007/bf00550880 · Cited by 350 · cited 1× · see citing works
“The oscillations in electrical activity are accompanied by changes in the cytoplasmic Ca2+ concentration (Santos et al. 1991), which in turn give rise to brief pulses (~10 s) of insulin secretion (Gilon & Henquin, 1992; Bergsten, 1995; Barbosa et al. 1998).”
BackgroundVoltage‐gated and resting membrane currents recorded from B‐cells in intact mouse pancreatic islets
Göpel, S., Kanno, T., Barg, S., Galvanovskis, J., & Rorsman, P. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00717.x · Cited by 226 · see citing works
Self-citationGöpel, S. O., Kanno, T., Barg, S., Eliasson, L., Galvanovskis, J., Renström, E., & Rorsman, P. (1999) · The Journal of General Physiology · doi:10.1085/jgp.114.6.759 · Cited by 137 · see citing works
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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-citationRegulation of Insulin Secretion in Human Pancreatic Islets
Rorsman, P., & Braun, M. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183754 · Cited by 599 · see citing works
Self-citationMicroRNA-7a regulates pancreatic β cell function
Latreille, M., Hausser, J., Stützer, I., Zhang, Q., Hastoy, B., Gargani, S., Kerr-Conte, J., Pattou, F., Zavolan, M., Esguerra, J. L. S., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73066 · Cited by 281 · see citing works
Self-citationGöpel, S., Zhang, Q., Eliasson, L., Ma, X., Galvanovskis, J., Kanno, T., Salehi, A., & Rorsman, P. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.059675 · Cited by 160 · see citing works
Self-citationZhang, Q., Chibalina, M. V., Bengtsson, M., Groschner, L. N., Ramracheya, R., Rorsman, N. J. G., Leiss, V., Nassar, M. A., Welling, A., Gribble, F. M., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.274209 · Cited by 90 · see citing works
Self-citationCell coupling in mouse pancreatic β-cells measured in intact islets of Langerhans
Zhang, Q., Galvanovskis, J., Abdulkader, F., Partridge, C. J., Göpel, S. O., Eliasson, L., & Rorsman, P. (2008) · Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rsta.2008.0110 · Cited by 80 · see citing works
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- Authors
- Kanno, T., Rorsman, P., & Göpel, S. O.
- Affiliations
- Hirosaki University (JP)
- Lund University (SE)
- Corresponding author
- Göpel, S. O.
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2002-12
- Volume
- 545
- Issue
- 2
- Pages
- 501-507
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC2290696
- OpenAlex
- W2164983923
- Cited by
- 89
- References
- 3
- Citations by year
- 2025: 2 · 2022: 2 · 2021: 4 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 4 · 2016: 1 · 2015: 3 · 2014: 10 · 2013: 3 · 2012: 7
- FWCI
- 5.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- pancreatic beta cells, ATP-sensitive potassium channels, action potential firing, insulin secretion, tolbutamide, thapsigargin, SERCA, pancreatic islets
- MeSH terms
- Action Potentials, Animals, Calcium, Electrophysiology, Enzyme Inhibitors, Glucose, Hypoglycemic Agents, Islets of Langerhans, Membrane Potentials, Tolbutamide, Calcium Channels, Potassium Channels, ATP-Binding Cassette Transporters, Thapsigargin, Potassium Channels, Inwardly Rectifying, Mice, KATP Channels, In Vitro Techniques
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