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PMID: 26392222 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

TRPC6 is the endothelial calcium channel that regulates leukocyte transendothelial migration during the inflammatory response.

The Journal of experimental medicine ·Vol. 212 ·No. 11 ·2015-10-19 ·Pages 1883-99

Weber EW, Han F, Tauseef M, Birnbaumer L, Mehta D, Muller WA

Abstract

Leukocyte transendothelial migration (TEM) is a tightly regulated, multistep process that is critical to the inflammatory response. A transient increase in endothelial cytosolic free calcium ion concentration (↑[Ca(2+)]i) is required for TEM. However, the mechanism by which endothelial ↑[Ca(2+)]i regulates TEM and the channels mediating this ↑[Ca(2+)]i are unknown. Buffering ↑[Ca(2+)]i in endothelial cells does not affect leukocyte adhesion or locomotion but selectively blocks TEM, suggesting a role for ↑[Ca(2+)]i specifically for this step. Transient receptor potential canonical 6 (TRPC6), a Ca(2+) channel expressed in endothelial cells, colocalizes with platelet/endothelial cell adhesion molecule-1 (PECAM) to surround leukocytes during TEM and clusters when endothelial PECAM is engaged. Expression of dominant-negative TRPC6 or shRNA knockdown in endothelial cells arrests neutrophils apically over the junction, similar to when PECAM is blocked. Selectively activating endothelial TRPC6 rescues TEM during an ongoing PECAM blockade, indicating that TRPC6 functions downstream of PECAM. Furthermore, endothelial TRPC6 is required for trafficking of lateral border recycling compartment membrane, which facilitates TEM. Finally, mice lacking TRPC6 in the nonmyeloid compartment (i.e., endothelium) exhibit a profound defect in neutrophil TEM with no effect on leukocyte trafficking. Our findings identify endothelial TRPC6 as the calcium channel mediating the ↑[Ca(2+)]i required for TEM at a step downstream of PECAM homophilic interactions.

MeSH Terms
Animals Calcium/metabolism Cell Movement Cytosol/metabolism Egtazic Acid/analogs & derivatives,pharmacology Endothelial Cells/physiology Humans Inflammation/metabolism Leukocytes/physiology Mice Mice, Inbred C57BL Platelet Endothelial Cell Adhesion Molecule-1/physiology TRPC Cation Channels/physiology TRPC6 Cation Channel
Chemicals
Platelet Endothelial Cell Adhesion Molecule-1 TRPC Cation Channels TRPC6 Cation Channel TRPC6 protein, human Trpc6 protein, mouse 1,2-bis(2-aminophenoxy)ethane N,N,N',N'-tetraacetic acid acetoxymethyl ester Egtazic Acid Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Weber Evan W
Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611.
Han Fei
Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611.
Tauseef Mohammad
Department of Pharmacology, Center for Lung and Vascular Biology, University of Illinois in Chicago College of Medicine, Chicago, IL 60612.
Birnbaumer Lutz
Neurobiology Laboratory, National Institute of Environmental Health Sciences, Research Triangle Park, NC 27709.
Mehta Dolly
Department of Pharmacology, Center for Lung and Vascular Biology, University of Illinois in Chicago College of Medicine, Chicago, IL 60612.
Muller William A
Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611 wamuller@northwestern.edu.
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Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
1540-9538
Published
2015-10-19
Epub
2015-00-21
Pages
1883-99
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC4612081
Subset
IM
Grants
NHLBI NIH HHS · R01 HL046849 · United States
NIEHS NIH HHS · Z01-ES-101684 · United States
NHLBI NIH HHS · R37HL064774 · United States
NHLBI NIH HHS · P01 HL077806 · United States
NHLBI NIH HHS · R37 HL064774 · United States
NHLBI NIH HHS · R01HL046849 · United States
NHLBI NIH HHS · R01 HL071794 · United States
NHLBI NIH HHS · R01 HL084153 · United States
NHLBI NIH HHS · P01 HL060678 · United States
Intramural NIH HHS · Z01 ES101684 · United States
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