Cited by 307Ion Channels and ReceptorsNitric Oxide and Endothelin EffectsCalcium signaling and nucleotide metabolism

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Systemic Activation of the Transient Receptor Potential Vanilloid Subtype 4 Channel Causes Endothelial Failure and Circulatory Collapse: Part 2

Willette, Robert N., Bao, Weike, Nerurkar, Sandhya, Yue, Tian-li, Doe, Chris P., Stankus, Gerald, Turner, Gregory H., Ju, Haisong, Thomas, Heath, Fishman, Cindy E., Sulpizio, Anthony, Behm, David J., Hoffman, Sandra, Lin, Zuojun, Lozinskaya, Irina, Casillas, Linda N., Lin, Min, Lee Trout, Robert E., Votta, Bartholomew J., Thorneloe, Kevin, Lashinger, Erin S.R., Figueroa, David J., Marquis, Robert, Xu, Xiaoping·2008·The Journal of Pharmacology and Experimental Therapeutics

DOI 10.1124/jpet.107.134551

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Abstract

The transient receptor potential (TRP) vanilloid subtype 4 (V4) is a nonselective cation channel that exhibits polymodal activation and is expressed in the endothelium, where it contributes to intracellular Ca2+ homeostasis and regulation of cell volume. The purpose of the present study was to evaluate the systemic cardiovascular effects of GSK1016790A, a novel TRPV4 activator, and to examine its mechanism of action. In three species (mouse, rat, and dog), the i.v. administration of GSK1016790A induced a dose-dependent reduction in blood pressure, followed by profound circulatory collapse. In contrast, GSK1016790A had no acute cardiovascular effects in the TRPV4-/- null mouse. Hemodynamic analyses in the dog and rat demonstrate a profound reduction in cardiac output. However, GSK1016790A had no effect on rate or contractility in the isolated, buffer-perfused rat heart, and it produced potent endothelial-dependent relaxation of rodent-isolated vascular ring segments that were abolished by nitric-oxide synthase (NOS) inhibition (N-nitro-L-arginine methyl ester; L-NAME), ruthenium red, and endothelial NOS (eNOS) gene deletion. However, the in vivo circulatory collapse was not altered by NOS inhibition (L-NAME) or eNOS gene deletion but was associated with (concentration and time appropriate) profound vascular leakage and tissue hemorrhage in the lung, intestine, and kidney. TRPV4 immunoreactivity was localized in the endothelium and epithelium in the affected organs. GSK1016790A potently induced rapid electrophysiological and morphological changes (retraction/condensation) in cultured endothelial cells. In summary, inappropriate activation of TRPV4 produces acute circulatory collapse associated with endothelial activation/injury and failure of the pulmonary microvascular permeability barrier. It will be important to determine the role of TRPV4 in disorders associated with edema and microvascular congestion.

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Authors: Willette, R. N., Bao, W., Nerurkar, S., Yue, T.-L., Doe, C. P., Stankus, G., Turner, G. H., Ju, H., Thomas, H., Fishman, C. E., Sulpizio, A., Behm, D. J., Hoffman, S., Lin, Z., Lozinskaya, I., Casillas, L. N., Lin, M., Lee Trout, R. E., Votta, B. J., Thorneloe, K., Lashinger, E. S. R., Figueroa, D. J., Marquis, R., & Xu, X.
Affiliations: GlaxoSmithKline (United States) (US)
ORCID: Bao, Weike
Turner, Gregory H.
Thomas, Heath
Fishman, Cindy E.
Casillas, Linda N.
Lin, Min
Thorneloe, Kevin
Figueroa, David J.
Xu, Xiaoping
Venue: The Journal of Pharmacology and Experimental Therapeutics
Publisher: Elsevier BV
Published: 2008-08
Volume: 326
Issue: 2
Pages: 443-452
ISSN: 0022-3565 (ISSN-L)
DOI: 10.1124/jpet.107.134551
OpenAlex: W2161804336
Cited by: 300
References: 21
Citations by year: 2026: 12 · 2025: 8 · 2024: 8 · 2023: 20 · 2022: 16 · 2021: 14 · 2020: 24 · 2019: 21 · 2018: 16 · 2017: 22 · 2016: 17 · 2015: 19 · 2014: 22 · 2013: 14 · 2012: 20
FWCI: 7.46
Type: journal article
Language: en
Update notices: erratum (2011-07-01)
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords: TRPV4, GSK1016790A, cardiovascular collapse, endothelial permeability, endothelial injury, endothelial cell retraction, nitric oxide synthase, endothelium-dependent relaxation, blood pressure reduction, cardiac output, TRPV4 knockout mice, edema
MeSH terms: Animals, Aorta, Thoracic, Capillary Permeability, Cell Adhesion, Cell Line, Dogs, Dose-Response Relationship, Drug, Endothelium, Vascular, Female, Hemodynamics, Humans, Immunohistochemistry, Leucine, Male, Sulfonamides, Vasoconstriction, Molecular Structure, Ventricular Function, Left, Rats, Sprague-Dawley, Mice, Knockout, Patch-Clamp Techniques, TRPV Cation Channels, Mice, Rats

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Systemic Activation of the Transient Receptor Potential Vanilloid Subtype 4 Channel Causes Endothelial Failure and Circulatory Collapse: Part 2

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