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Differential distribution and functional impact of BK channel beta1 subunits across mesenteric, coronary, and different cerebral arteries of the rat

  • Ion channels, receptors and transporters
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Abstract

Large conductance, Ca2+ i- and voltage-gated K+ (BK) channels regulate myogenic tone and, thus, arterial diameter. In smooth muscle (SM), BK channels include channel-forming α and auxiliary β1 subunits. BK β1 increases the channel’s Ca2+ sensitivity, allowing BK channels to negatively feedback on depolarization-induced Ca2+ entry, oppose SM contraction and favor vasodilation. Thus, endothelial-independent vasodilation can be evoked though targeting of SM BK β1 by endogenous ligands, including lithocholate (LCA). Here, we investigated the expression of BK β1 across arteries of the cerebral and peripheral circulations, and the contribution of such expression to channel function and BK β1-mediated vasodilation. Data demonstrate that endothelium-independent, BK β1-mediated vasodilation by LCA is larger in coronary (CA) and basilar (BA) arteries than in anterior cerebral (ACA), middle cerebral (MCA), posterior cerebral (PCA), and mesenteric (MA) arteries, all arterial segments having a similar diameter. Thus, differential dilation occurs in extracranial arteries which are subjected to similar vascular pressure (CA vs. MA) and in arteries that irrigate different brain regions (BA vs. ACA, MCA, and PCA). SM BK channels from BA and CA displayed increased basal activity and LCA responses, indicating increased BK β1 functional presence. Indeed, in the absence of detectable changes in BK α, BA and CA myocytes showed an increased location of BK β1 in the plasmalemma/subplasmalemma. Moreover, these myocytes distinctly showed increased BK β1 messenger RNA (mRNA) levels. Supporting a major role of enhanced BK β1 transcripts in artery dilation, LCA-induced dilation of MCA transfected with BK β1 complementary DNA (cDNA) was as high as LCA-induced dilation of untransfected BA or CA.

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Acknowledgements

The authors thank Bangalore Shivakumar and Maria T. Asuncion-Chin for their excellent technical assistance. This work was supported by an American Heart Association Predoctoral Fellowship (to G.K.) and the National Institutes of Health grants R37AA11560 and R01HL104631 (to A.M.D).

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Authors and Affiliations

  1. Department of Pharmacology, College of Medicine, The University of Tennessee Health Science Center, 71 South Manassas St, Memphis, TN, 38103, USA

    Guruprasad Kuntamallappanavar, Shivantika Bisen, Anna N. Bukiya & Alex M. Dopico

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  1. Guruprasad Kuntamallappanavar
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  2. Shivantika Bisen
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  3. Anna N. Bukiya
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  4. Alex M. Dopico
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Corresponding author

Correspondence to Alex M. Dopico.

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This procedure was approved by the Institutional Animal Care and Use Committee from the University of Tennessee Health Science Center (UTHSC), an AAALAC accredited institution.

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The authors declare that they have no conflict of interest.

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Kuntamallappanavar, G., Bisen, S., Bukiya, A.N. et al. Differential distribution and functional impact of BK channel beta1 subunits across mesenteric, coronary, and different cerebral arteries of the rat. Pflugers Arch - Eur J Physiol 469, 263–277 (2017). https://doi.org/10.1007/s00424-016-1929-z

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  • DOI: https://doi.org/10.1007/s00424-016-1929-z

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