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Sensory innervation of perivascular adipose tissue: a crucial role in artery vasodilation and leptin release

Baker, Hamidah Abu; Dunn, William R.; Daly, Craig; Ralevic, Vera

Sensory innervation of perivascular adipose tissue: a crucial role in artery vasodilation and leptin release Thumbnail


Authors

Hamidah Abu Baker

William R. Dunn

Craig Daly

VERA RALEVIC vera.ralevic@nottingham.ac.uk
Associate Professor & Reader in Cardiovascular Sciences



Abstract

Aims: Electrical field stimulation (EFS) elicits robust sensory neurogenic relaxation responses in the rat isolated mesenteric arterial bed but these responses are absent or difficult to demonstrate in isolated arteries. We believe that this mismatch is due to the absence of perivascular adipose tissue (PVAT) as it is conventionally removed in studies on isolated vessels. We aimed to determine whether sensory nerves are expressed in PVAT, their physiological roles and their possible interactions with PVAT-derived adipokines.
Methods and Results: Using confocal imaging, enzyme immunoassay (EIA), myography, vascular perfusion and multiplex analysis of rat mesenteric arteries, we show that PVAT is crucial for the roles of sensory nerves in control of vasomotor tone and adipokine release. Immunofluorescence double staining showed co-expression of calcitonin gene-related peptide (CGRP; sensory neurotransmitter) and PGP9.5 (neuronal marker) in PVAT of mesenteric arteries. CGRP release from dissected PVAT, measured using EIA, was increased by capsaicin which activates sensory nerves. EFS in both mesenteric arteries and perfused mesenteric arterial beds, with and without PVAT, demonstrated neurogenic relaxation in the presence of PVAT, which was greatly attenuated in preparations without PVAT. Neurogenic relaxation due to EFS was associated with release of leptin in PVAT-intact mesenteric arterial beds, which was abolished in preparations without PVAT. Exposure to low oxygen was associated with an attenuated leptin and adiponectin release, but an increase in IL-6 release, from mesenteric arterial beds. Exogenous leptin augmented relaxation to CGRP in mesenteric arteries.
Conclusions: These data show, for the first time, expression of sensory nerves within PVAT and that PVAT is crucial for sensory neurogenic vasorelaxation and crosstalk with adipocytes leading to leptin release, which may augment CGRP-mediated relaxation; leptin release is abolished after exposure to conditions of reduced oxygenation.

Citation

Baker, H. A., Dunn, W. R., Daly, C., & Ralevic, V. (2017). Sensory innervation of perivascular adipose tissue: a crucial role in artery vasodilation and leptin release. Cardiovascular Research, 113(8), 962-972. https://doi.org/10.1093/cvr/cvx062

Journal Article Type Article
Acceptance Date Mar 19, 2017
Online Publication Date Mar 23, 2017
Publication Date Jul 1, 2017
Deposit Date Apr 7, 2017
Publicly Available Date Mar 29, 2024
Journal Cardiovascular Research
Print ISSN 0008-6363
Electronic ISSN 1755-3245
Publisher Oxford University Press
Peer Reviewed Peer Reviewed
Volume 113
Issue 8
Pages 962-972
DOI https://doi.org/10.1093/cvr/cvx062
Keywords sensory nerves, perivascular adipose tissue, leptin
Public URL https://nottingham-repository.worktribe.com/output/851656
Publisher URL https://academic.oup.com/cardiovascres/article-lookup/doi/10.1093/cvr/cvx062
Additional Information This is a pre-copyedited, author-produced version of an article accepted for publication in Cardiovascular Research following peer review. The version of record Hamidah Abu Bakar, PhD, William Robert Dunn, PhD, Craig Daly, PhD, Vera Ralevic, PhD; Sensory innervation of perivascular adipose tissue: a crucial role in artery vasodilatation and leptin release. Cardiovascular Research, 2017 cvx062. is available online at: https://academic.oup.com/cardiovascres/article-lookup/doi/10.1093/cvr/cvx062.

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