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Cited by 80Pancreatic function and diabetesConnexins and lens biologyIon channel regulation and function

Cell coupling in mouse pancreatic β-cells measured in intact islets of Langerhans

Zhang, Quan, Galvanovskis, Juris, Abdulkader, Fernando, Partridge, Christopher J, Göpel, Sven O, Eliasson, Lena, Rorsman, Patrik·2008·Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
DOI 10.1098/rsta.2008.0110
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Abstract

The perforated whole-cell configuration of the patch-clamp technique was applied to functionally identified β-cells in intact mouse pancreatic islets to study the extent of cell coupling between adjacent β-cells. Using a combination of current- and voltage-clamp recordings, the total gap junctional conductance between β-cells in an islet was estimated to be 1.22 nS. The analysis of the current waveforms in a voltage-clamped cell (due to the firing of an action potential in a neighbouring cell) suggested that the gap junctional conductance between a pair of β-cells was 0.17 nS. Subthreshold voltage-clamp depolarization (to −55 mV) gave rise to a slow capacitive current indicative of coupling between β-cells, but not in non-β-cells, with a time constant of 13.5 ms and a total charge movement of 0.2 pC. Our data suggest that a superficial β-cell in an islet is in electrical contact with six to seven other β-cells. No evidence for dye coupling was obtained when cells were dialysed with Lucifer yellow even when electrical coupling was apparent. The correction of the measured resting conductance for the contribution of the gap junctional conductance indicated that the whole-cell K ATP channel conductance (GK,ATP) falls from approximately 2.5 nS in the absence of glucose to 0.1 nS at 15 mM glucose with an estimated IC 50 of approximately 4 mM. Theoretical considerations indicate that the coupling between β-cells within the islet is sufficient to allow propagation of [Ca 2+]iwaves to spread with a speed of approximately 80 μm s−1, similar to that observed experimentally in confocal [Ca 2+]iimaging.

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  • The gap junctional conductance between β-cells and δ-cells is estimated to be 23 pS, only about 10% of that between pairs of β-cells.

    “We estimate (Equation 3.2. in ref. 26) the gap junctional conductance between β-cells and δ-cells to be 23 pS.”

    From Loss of electrical β-cell to δ-cell coupling underlies impaired hypoglycaemia-induced glucagon secretion in type-1 diabetes (2024) · cites this paper as [26]

  • Significant KATP channel activity remains at glucose concentrations ≥5 mM in β-cells in intact islets, and whole-cell KATP channel activity falls from ~0.1 nS/pF to <0.02 nS/pF when glucose is varied between 7 and 15 mM.

    “Notably, significant KATP channel activity remains at glucose concentrations ≥5 mM in β-cells in intact islets and whole-cell KATP channel activity falls from ~0.1 nS/pF to <0.02 nS/pF when glucose is varied between 7 and 15 mM (762) (Figure 2C).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [762]

  • Exchange of cytosolic constituents between adjacent β-cells via gap junctions appears unlikely.

    “Another question is whether there is exchange of cytosolic constituents between adjacent β-cells via gap-junctions. However, this appears unlikely given the fact there is little dye-coupling (as measured using low molecular-weight fluorescent probes) in electrically coupled cells (528, 762).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [762]

  • There is little dye-coupling in electrically coupled cells.

    “However, this appears unlikely given the fact there is little dye-coupling (as measured using low molecular-weight fluorescent probes) in electrically coupled cells (528, 762).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [762]

  • Electrical coupling between β-cells in mouse islets is sufficient to explain the propagation of [Ca2+]i waves across the islet, which have a velocity of 80 μm/s.

    “Electrical coupling between β-cells in mouse islets is sufficient to explain the propagation of [Ca2+]i waves across the islet, which have a velocity of 80 μm/s (762).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [762]

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Authors
Zhang, Q., Galvanovskis, J., Abdulkader, F., Partridge, C. J., Göpel, S. O., Eliasson, L., & Rorsman, P.
Affiliations
  • Churchill Hospital (GB)
  • Universidade de São Paulo (BR)
  • AstraZeneca (Sweden) (SE)
  • Lund University (SE)
Corresponding author
Eliasson, Lena
ORCID
Venue
Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
Publisher
The Royal Society
Published
2008-07-16
Volume
366
Issue
1880
Pages
3503-3523
ISSN
  • 1364-503X (ISSN-L)
  • 1471-2962
DOI
10.1098/rsta.2008.0110
OpenAlex
W2168500187
Cited by
80
References
46
Citations by year
2026: 1 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 7 · 2021: 6 · 2020: 7 · 2019: 2 · 2018: 5 · 2017: 8 · 2016: 3 · 2015: 3 · 2014: 5 · 2013: 8 · 2012: 3
FWCI
4.22
Type
journal article
Language
en
Open access
closed
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences (publishedVersion)
  • PubMed (publishedVersion)
  • Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
  • Lund University Publications (Lund University) (submittedVersion)
Funders
Wellcome Trust
Topics
  • Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Keywords
gap junctions, pancreatic islets, electrical coupling, gap junction conductance, ATP-sensitive potassium channels, calcium waves, action potential propagation
MeSH terms
Adenosine Triphosphate, Animals, Calcium, Cells, Cultured, Electrophysiology, Islets of Langerhans, Membrane Potentials, Models, Biological, Potassium, Gap Junctions, Patch-Clamp Techniques, Microscopy, Confocal, Inhibitory Concentration 50, Insulin-Secreting Cells, Mice

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