DOI: 10.1085/jgp.20028707. SUR1 Regulates PKA-independent cAMP-induced Granule Priming in Mouse Pancreatic B-cells

SUR1 Regulates PKA-independent cAMP-induced Granule Priming in Mouse Pancreatic B-cells

10.1085/jgp.20028707

Crossref journal-article

Rockefeller University Press

The Journal of General Physiology (291)

Abstract

Measurements of membrane capacitance were applied to dissect the cellular mechanisms underlying PKA-dependent and -independent stimulation of insulin secretion by cyclic AMP. Whereas the PKA-independent (Rp-cAMPS–insensitive) component correlated with a rapid increase in membrane capacitance of ∼80 fF that plateaued within ∼200 ms, the PKA-dependent component became prominent during depolarizations &gt;450 ms. The PKA-dependent and -independent components of cAMP-stimulated exocytosis differed with regard to cAMP concentration dependence; the Kd values were 6 and 29 μM for the PKA-dependent and -independent mechanisms, respectively. The ability of cAMP to elicit exocytosis independently of PKA activation was mimicked by the selective cAMP-GEFII agonist 8CPT-2Me-cAMP. Moreover, treatment of B-cells with antisense oligodeoxynucleotides against cAMP-GEFII resulted in partial (50%) suppression of PKA-independent exocytosis. Surprisingly, B-cells in islets isolated from SUR1-deficient mice (SUR1−/− mice) lacked the PKA-independent component of exocytosis. Measurements of insulin release in response to GLP-1 stimulation in isolated islets from SUR1−/− mice confirmed the complete loss of the PKA-independent component. This was not attributable to a reduced capacity of GLP-1 to elevate intracellular cAMP but instead associated with the inability of cAMP to stimulate influx of Cl− into the granules, a step important for granule priming. We conclude that the role of SUR1 in the B cell extends beyond being a subunit of the plasma membrane KATP-channel and that it also plays an unexpected but important role in the cAMP-dependent regulation of Ca2+-induced exocytosis.

Bibliography

Eliasson, L., Ma, X., RenstroÌm, E., Barg, S., Berggren, P.-O., Galvanovskis, J., Gromada, J., Jing, X., Lundquist, I., Salehi, A., Sewing, S., & Rorsman, P. (2003). SUR1 Regulates PKA-independent cAMP-induced Granule Priming in Mouse Pancreatic B-cells. The Journal of General Physiology, 121(3), 181â197.

Authors 12

Lena Eliasson (first)
Xiaosong Ma (additional)
Erik Renström (additional)
Sebastian Barg (additional)
Per-Olof Berggren (additional)
Juris Galvanovskis (additional)
Jesper Gromada (additional)
Xingjun Jing (additional)
Ingmar Lundquist (additional)
Albert Salehi (additional)
Sabine Sewing (additional)
Patrik Rorsman (additional)

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Dates

Type	When
Created	22 years, 6 months ago (Feb. 24, 2003, 2:04 p.m.)
Deposited	2 years, 1 month ago (July 26, 2023, 4:11 p.m.)
Indexed	1 week, 2 days ago (Aug. 27, 2025, 11:53 a.m.)
Issued	22 years, 6 months ago (Feb. 24, 2003)
Published	22 years, 6 months ago (Feb. 24, 2003)
Published Online	22 years, 6 months ago (Feb. 24, 2003)
Published Print	22 years, 6 months ago (March 1, 2003)

Funders 0

None

BibTeX

@article{Eliasson_2003, title={SUR1 Regulates PKA-independent cAMP-induced Granule Priming in Mouse Pancreatic B-cells}, volume={121}, ISSN={0022-1295}, url={http://dx.doi.org/10.1085/jgp.20028707}, DOI={10.1085/jgp.20028707}, number={3}, journal={The Journal of General Physiology}, publisher={Rockefeller University Press}, author={Eliasson, Lena and Ma, Xiaosong and Renström, Erik and Barg, Sebastian and Berggren, Per-Olof and Galvanovskis, Juris and Gromada, Jesper and Jing, Xingjun and Lundquist, Ingmar and Salehi, Albert and Sewing, Sabine and Rorsman, Patrik}, year={2003}, month=feb, pages={181–197} }

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  "abstract": "<jats:p>Measurements of membrane capacitance were applied to dissect the cellular mechanisms underlying PKA-dependent and -independent stimulation of insulin secretion by cyclic AMP. Whereas the PKA-independent (Rp-cAMPS\u2013insensitive) component correlated with a rapid increase in membrane capacitance of \u223c80 fF that plateaued within \u223c200 ms, the PKA-dependent component became prominent during depolarizations &amp;gt;450 ms. The PKA-dependent and -independent components of cAMP-stimulated exocytosis differed with regard to cAMP concentration dependence; the Kd values were 6 and 29 \u03bcM for the PKA-dependent and -independent mechanisms, respectively. The ability of cAMP to elicit exocytosis independently of PKA activation was mimicked by the selective cAMP-GEFII agonist 8CPT-2Me-cAMP. Moreover, treatment of B-cells with antisense oligodeoxynucleotides against cAMP-GEFII resulted in partial (50%) suppression of PKA-independent exocytosis. Surprisingly, B-cells in islets isolated from SUR1-deficient mice (SUR1\u2212/\u2212 mice) lacked the PKA-independent component of exocytosis. Measurements of insulin release in response to GLP-1 stimulation in isolated islets from SUR1\u2212/\u2212 mice confirmed the complete loss of the PKA-independent component. This was not attributable to a reduced capacity of GLP-1 to elevate intracellular cAMP but instead associated with the inability of cAMP to stimulate influx of Cl\u2212 into the granules, a step important for granule priming. We conclude that the role of SUR1 in the B cell extends beyond being a subunit of the plasma membrane KATP-channel and that it also plays an unexpected but important role in the cAMP-dependent regulation of Ca2+-induced exocytosis.</jats:p>",
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