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Cited by 160Pancreatic function and diabetesCellular transport and secretionCalcium signaling and nucleotide metabolism

Capacitance measurements of exocytosis in mouse pancreatic α‐, β‐ and δ‐cells within intact islets of Langerhans

Göpel, Sven, Zhang, Quan, Eliasson, Lena, Ma, Xiao‐Song, Galvanovskis, Juris, Kanno, Takahiro, Salehi, Albert, Rorsman, Patrik·2004·The Journal of Physiology
DOI 10.1113/jphysiol.2003.059675
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Abstract

Capacitance measurements of exocytosis were applied to functionally identified α‐, β‐ and δ‐cells in intact mouse pancreatic islets. The maximum rate of capacitance increase in β‐cells during a depolarization to 0 mV was equivalent to 14 granules s−1, <5% of that observed in isolated β‐cells. β‐Cell secretion exhibited bell‐shaped voltage dependence and peaked at +20 mV. At physiological membrane potentials (up to ∼−20 mV) the maximum rate of release was ∼4 granules s−1. Both exocytosis (measured by capacitance measurements) and insulin release (detected by radioimmunoassay) were strongly inhibited by the L‐type Ca 2+ channel blocker nifedipine (25 μ m) but only marginally (<20%) affected by the R‐type Ca 2+ channel blocker SNX482 (100 n m). Exocytosis in the glucagon‐producing α‐cells peaked at +20 mV. The capacitance increases elicited by pulses to 0 mV exhibited biphasic kinetics and consisted of an initial transient (150 granules s−1) and a sustained late component (30 granules s−1). Whereas addition of the N‐type Ca 2+ channel blocker ω‐conotoxin GVIA (0.1 μ m) inhibited glucagon secretion measured in the presence of 1 m m glucose to the same extent as an elevation of glucose to 20 m m, the L‐type Ca 2+ channel blocker nifedipine (25 μ m) had no effect. Thus, glucagon release during hyperglycaemic conditions depends principally on Ca 2+‐influx through N‐type rather than L‐type Ca 2+ channels. Exocytosis in the somatostatin‐secreting δ‐cells likewise exhibited two kinetically separable phases of capacitance increase and consisted of an early rapid (600 granules s−1) component followed by a sustained slower (60 granules s−1) component. We conclude that (1) capacitance measurements in intact pancreatic islets are feasible; (2) exocytosis measured in β‐cells in situ is significantly slower than that of isolated cells; and (3) the different types of islet cells exhibit distinct exocytotic features.

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Crossref · 10.1113/jphysiol.2003.059675

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  • At 20 mM glucose, the time spent above -20 mV (the voltage where insulin granule exocytosis first becomes detectable) is ~30 ms.

    “Its width is somewhat variable but, at 20 mM glucose, the time spent above -20 mV (the voltage where insulin granule exocytosis first becomes detectable (222)) is ~30 ms (288).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [222]

  • Mouse β-cells express L-type Ca2+ channels (Cacna1c and Cacna1d) and smaller amounts of N- and P/Q-type Ca2+ channels.

    “Mouse β-cells express L-type Ca2+ channels (Cacna1c and Cacna1d) and smaller amounts of N- (Cacna1b) and P/Q-type (Cacna1a) Ca2+ channels (211, 222, 603) (seem Appendix Figure 3A).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [222]

  • The lower rate of capacitance increase observed for β-cells in intact islets agrees well with that of insulin secretion measured biochemically.

    “The lower rate of capacitance increase observed for β-cells in intact islets agrees well with that of insulin secretion measured biochemically (222).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [222]

  • It is unlikely that the low rate of β-cell secretion in intact islets is due to paracrine inhibition, as pre-treatment with pertussis toxin only marginally increased the rate of exocytosis.

    “It is unlikely that the low rate of β-cell secretion in intact islets is due to paracrine inhibition (for example, exerted by somatostatin released from neighboring δ-cells) as pre-treatment with pertussis toxin (which blocks inhibitory G proteins) only marginally increased the rate of exocytosis (222).”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [222]

  • When measured in β-cells within intact islets, exocytosis becomes detectable during a 40-ms depolarization, does not plateau and operates at a maximum rate of 50 fF/s, only ~10% of that seen in isolated β-cells.

    “When measured in β-cells within intact islets, exocytosis becomes detectable during a 40-ms depolarization, does not plateau and operates at a maximum rate of 50 fF/s (222), only ~10% of that seen in isolated β-cells.”

    From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [222]

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Authors
Göpel, S., Zhang, Q., Eliasson, L., Ma, X., Galvanovskis, J., Kanno, T., Salehi, A., & Rorsman, P.
Affiliations
Lund University (SE)
ORCID
Venue
The Journal of Physiology
Publisher
Wiley
Published
2004-04-21
Volume
556
Issue
3
Pages
711-726
ISSN
  • 0022-3751 (ISSN-L)
  • 1469-7793
DOI
10.1113/jphysiol.2003.059675
OpenAlex
W1562853684
Cited by
160
References
55
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 9 · 2019: 3 · 2018: 2 · 2017: 3 · 2016: 3 · 2015: 9 · 2014: 18 · 2013: 11 · 2012: 14
FWCI
9.47
Type
journal article
Language
en
Open access
closed
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • The Journal of Physiology (publishedVersion)
  • PubMed (publishedVersion)
  • Lund University Publications (Lund University) (submittedVersion)
Funders
  • Göran Gustafssons Stiftelser
  • Lunds Universitet
  • Svenska Sällskapet för Medicinsk Forskning
  • Hirosaki University
  • Novo Nordisk Fonden
Topics
  • Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords
exocytosis, capacitance measurement, pancreatic islets, alpha cells, pancreatic beta cells, delta cells, insulin secretion, glucagon secretion, somatostatin, L-type calcium channels, N-type calcium channels, nifedipine, omega-conotoxin GVIA, membrane potential
MeSH terms
Insulin Secretion, Action Potentials, Animals, Cells, Cultured, Electrophysiology, Exocytosis, Glucagon, Glucose, Insulin, Islets of Langerhans, Kinetics, Membrane Potentials, Mice, Inbred Strains, Nifedipine, Spider Venoms, Patch-Clamp Techniques, Somatostatin-Secreting Cells, Calcium Channels, L-Type, Calcium Channels, N-Type, omega-Conotoxin GVIA, Calcium Channels, R-Type, Secretory Vesicles, Electric Capacitance, Pertussis Toxin, Microscopy, Electron, Transmission, Mice

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