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Cited by 55Calcium signaling and nucleotide metabolismIon channel regulation and functionPhosphodiesterase function and regulation

Vasodilation by the calcium-mobilizing messenger cyclic ADP-ribose

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Boittin, François-Xavier, Dipp, Michelle, Kinnear, Nicholas P., Galione, Antony, Evans, A. Mark·2003·Journal of Biological Chemistry
DOI 10.1074/jbc.m204891200
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Abstract

In artery smooth muscle, adenylyl cyclase-coupled receptors such as beta-adrenoceptors evoke Ca(2+) signals, which open Ca(2+)-activated potassium (BK(Ca)) channels in the plasma membrane. Thus, blood pressure may be lowered, in part, through vasodilation due to membrane hyperpolarization. The Ca(2+) signal is evoked via ryanodine receptors (RyRs) in sarcoplasmic reticulum proximal to the plasma membrane. We show here that cyclic adenosine diphosphate-ribose (cADPR), by activating RyRs, mediates, in part, hyperpolarization and vasodilation by beta-adrenoceptors. Thus, intracellular dialysis of cADPR increased the cytoplasmic Ca(2+) concentration proximal to the plasma membrane in isolated arterial smooth muscle cells and induced a concomitant membrane hyperpolarization. Smooth muscle hyperpolarization mediated by cADPR, by beta-adrenoceptors, and by cAMP, respectively, was abolished by chelating intracellular Ca(2+) and by blocking RyRs, cADPR, and BK(Ca) channels with ryanodine, 8-amino-cADPR, and iberiotoxin, respectively. The cAMP-dependent protein kinase A antagonist N-(2-[p-bromocinnamylamino]ethyl)-5-isoquinolinesulfonamide hydrochloride (H89) blocked hyperpolarization by isoprenaline and cAMP, respectively, but not hyperpolarization by cADPR. Thus, cADPR acts as a downstream element in this signaling cascade. Importantly, antagonists of cADPR and BK(Ca) channels, respectively, inhibited beta-adrenoreceptor-induced artery dilation. We conclude, therefore, that relaxation of arterial smooth muscle by adenylyl cyclase-coupled receptors results, in part, from a cAMP-dependent and protein kinase A-dependent increase in cADPR synthesis, and subsequent activation of sarcoplasmic reticulum Ca(2+) release via RyRs, which leads to activation of BK(Ca) channels and membrane hyperpolarization.

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  • CD38 possesses ADP-ribosyl cyclase activity that produces cyclic ADP-ribose (cADPR) from β-NAD+.

    “CD38 possesses ADP-ribosyl cyclase activity (Lee, 2001;Higashida et al., 2001a and2007;Boittin et al., 2003;Guse, 2005) that produces cyclic ADP-ribose (cADPR) from β-NAD + , also known as Vitamin B3, an abundant substrate in the brain (Denu, 2005).”

    From CD38 and its role in oxytocin secretion and social behavior (2012) · cites this paper as Boittin et al., 2003

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Authors
Boittin, F.-X., Dipp, M., Kinnear, N. P., Galione, A., & Evans, A. M.
Affiliations
University of St Andrews (GB)
Corresponding author
Evans, A. Mark
ORCID
Boittin, François-Xavier
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2003-03
Volume
278
Issue
11
Pages
9602-9608
ISSN
0021-9258 (ISSN-L)
DOI
10.1074/jbc.m204891200
OpenAlex
W1984873108
Cited by
55
References
50
Citations by year
2024: 1 · 2023: 1 · 2020: 1 · 2019: 2 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 3 · 2013: 4 · 2012: 1
FWCI
3.74
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Phosphodiesterase function and regulation
Keywords
cyclic ADP-ribose, vasodilation, beta-adrenergic receptors, calcium mobilization, ryanodine receptor, sarcoplasmic reticulum calcium release, BKCa channels, membrane hyperpolarization, cAMP signaling, protein kinase A
MeSH terms
Cyclic AMP, Animals, Arteries, Calcium, Cell Membrane, Cells, Cultured, Dose-Response Relationship, Drug, Electrophysiology, Enzyme Inhibitors, Isoproterenol, Isoquinolines, Peptides, Ryanodine, Sarcoplasmic Reticulum, Sulfonamides, Time Factors, Vasodilator Agents, Potassium Channels, Cyclic AMP-Dependent Protein Kinases, Ryanodine Receptor Calcium Release Channel, Cyclic ADP-Ribose, Rats

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