Evidence of a Role for Fibroblast Transient Receptor Potential Canonical 3 Ca2+ Channel in Renal Fibrosis
Transient receptor potential canonical (TRPC) Ca(2+)-permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the possible role of fibroblast TRPC3 in the development of renal fibrosis. In vitro, a macromolecular complex formed by TRPC1/TRPC3/TRPC6 existed...
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Published in | Journal of the American Society of Nephrology Vol. 26; no. 8; pp. 1855 - 1876 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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American Society of Nephrology
01.08.2015
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Abstract | Transient receptor potential canonical (TRPC) Ca(2+)-permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the possible role of fibroblast TRPC3 in the development of renal fibrosis. In vitro, a macromolecular complex formed by TRPC1/TRPC3/TRPC6 existed in isolated cultured rat renal fibroblasts. However, specific blockade of TRPC3 with the pharmacologic inhibitor pyr3 was sufficient to inhibit both angiotensin II- and 1-oleoyl-2-acetyl-sn-glycerol-induced Ca(2+) entry in these cells, which was detected by fura-2 Ca(2+) imaging. TRPC3 blockade or Ca(2+) removal inhibited fibroblast proliferation and myofibroblast differentiation by suppressing the phosphorylation of extracellular signal-regulated kinase (ERK1/2). In addition, pyr3 inhibited fibrosis and inflammation-associated markers in a noncytotoxic manner. Furthermore, TRPC3 knockdown by siRNA confirmed these pharmacologic findings. In adult male Wistar rats or wild-type mice subjected to unilateral ureteral obstruction, TRPC3 expression increased in the fibroblasts of obstructed kidneys and was associated with increased Ca(2+) entry, ERK1/2 phosphorylation, and fibroblast proliferation. Both TRPC3 blockade in rats and TRPC3 knockout in mice inhibited ERK1/2 phosphorylation and fibroblast activation as well as myofibroblast differentiation and extracellular matrix remodeling in obstructed kidneys, thus ameliorating tubulointerstitial damage and renal fibrosis. In conclusion, TRPC3 channels are present in renal fibroblasts and control fibroblast proliferation, differentiation, and activation through Ca(2+)-mediated ERK signaling. TRPC3 channels might constitute important therapeutic targets for improving renal remodeling in kidney disease. |
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AbstractList | Transient receptor potential canonical (TRPC) Ca
2+
-permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the possible role of fibroblast TRPC3 in the development of renal fibrosis.
In vitro
, a macromolecular complex formed by TRPC1/TRPC3/TRPC6 existed in isolated cultured rat renal fibroblasts. However, specific blockade of TRPC3 with the pharmacologic inhibitor pyr3 was sufficient to inhibit both angiotensin II- and 1-oleoyl-2-acetyl-
sn
-glycerol–induced Ca
2+
entry in these cells, which was detected by fura-2 Ca
2+
imaging. TRPC3 blockade or Ca
2+
removal inhibited fibroblast proliferation and myofibroblast differentiation by suppressing the phosphorylation of extracellular signal-regulated kinase (ERK1/2). In addition, pyr3 inhibited fibrosis and inflammation-associated markers in a noncytotoxic manner. Furthermore, TRPC3 knockdown by siRNA confirmed these pharmacologic findings. In adult male Wistar rats or wild-type mice subjected to unilateral ureteral obstruction, TRPC3 expression increased in the fibroblasts of obstructed kidneys and was associated with increased Ca
2+
entry, ERK1/2 phosphorylation, and fibroblast proliferation. Both TRPC3 blockade in rats and TRPC3 knockout in mice inhibited ERK1/2 phosphorylation and fibroblast activation as well as myofibroblast differentiation and extracellular matrix remodeling in obstructed kidneys, thus ameliorating tubulointerstitial damage and renal fibrosis. In conclusion, TRPC3 channels are present in renal fibroblasts and control fibroblast proliferation, differentiation, and activation through Ca
2+
-mediated ERK signaling. TRPC3 channels might constitute important therapeutic targets for improving renal remodeling in kidney disease. Transient receptor potential canonical (TRPC) Ca(2+)-permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the possible role of fibroblast TRPC3 in the development of renal fibrosis. In vitro, a macromolecular complex formed by TRPC1/TRPC3/TRPC6 existed in isolated cultured rat renal fibroblasts. However, specific blockade of TRPC3 with the pharmacologic inhibitor pyr3 was sufficient to inhibit both angiotensin II- and 1-oleoyl-2-acetyl-sn-glycerol-induced Ca(2+) entry in these cells, which was detected by fura-2 Ca(2+) imaging. TRPC3 blockade or Ca(2+) removal inhibited fibroblast proliferation and myofibroblast differentiation by suppressing the phosphorylation of extracellular signal-regulated kinase (ERK1/2). In addition, pyr3 inhibited fibrosis and inflammation-associated markers in a noncytotoxic manner. Furthermore, TRPC3 knockdown by siRNA confirmed these pharmacologic findings. In adult male Wistar rats or wild-type mice subjected to unilateral ureteral obstruction, TRPC3 expression increased in the fibroblasts of obstructed kidneys and was associated with increased Ca(2+) entry, ERK1/2 phosphorylation, and fibroblast proliferation. Both TRPC3 blockade in rats and TRPC3 knockout in mice inhibited ERK1/2 phosphorylation and fibroblast activation as well as myofibroblast differentiation and extracellular matrix remodeling in obstructed kidneys, thus ameliorating tubulointerstitial damage and renal fibrosis. In conclusion, TRPC3 channels are present in renal fibroblasts and control fibroblast proliferation, differentiation, and activation through Ca(2+)-mediated ERK signaling. TRPC3 channels might constitute important therapeutic targets for improving renal remodeling in kidney disease. |
Author | Aftimos, Georges Saliba, Youakim Farès, Nassim Abramowitz, Joel Smayra, Viviane Birnbaumer, Lutz Karam, Ralph |
Author_xml | – sequence: 1 givenname: Youakim surname: Saliba fullname: Saliba, Youakim organization: Physiology and Pathophysiology Research Laboratory, Pole of Technology and Health, Faculty of Medicine and – sequence: 2 givenname: Ralph surname: Karam fullname: Karam, Ralph organization: Physiology and Pathophysiology Research Laboratory, Pole of Technology and Health, Faculty of Medicine and – sequence: 3 givenname: Viviane surname: Smayra fullname: Smayra, Viviane organization: Faculty of Medicine, Saint Joseph University, Beirut, Lebanon – sequence: 4 givenname: Georges surname: Aftimos fullname: Aftimos, Georges organization: Department of Anatomopathology, National Institute of Pathology, Baabda, Lebanon; and – sequence: 5 givenname: Joel surname: Abramowitz fullname: Abramowitz, Joel organization: Laboratory of Neurobiology, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina – sequence: 6 givenname: Lutz surname: Birnbaumer fullname: Birnbaumer, Lutz organization: Laboratory of Neurobiology, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina – sequence: 7 givenname: Nassim surname: Farès fullname: Farès, Nassim email: nassim.fares@usj.edu.lb organization: Physiology and Pathophysiology Research Laboratory, Pole of Technology and Health, Faculty of Medicine and nassim.fares@usj.edu.lb |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25479966$$D View this record in MEDLINE/PubMed |
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Copyright | Copyright © 2015 by the American Society of Nephrology. Copyright © 2015 by the American Society of Nephrology 2015 |
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Keywords | calcium fibroblast signaling ion channel kidney disease cell renal fibrosis |
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Notes | V.S. and G.A. contributed equally to this work. |
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Snippet | Transient receptor potential canonical (TRPC) Ca(2+)-permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the... Transient receptor potential canonical (TRPC) Ca 2+ -permeant channels, especially TRPC3, are increasingly implicated in cardiorenal diseases. We studied the... |
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SubjectTerms | Animals Basic Research Calcium - metabolism Cell Differentiation Cell Proliferation Cells, Cultured Extracellular Matrix - metabolism Fibroblasts - cytology Fibroblasts - metabolism Fibrosis Kidney - pathology Male MAP Kinase Signaling System Mice Mice, Knockout Myofibroblasts - cytology Phenotype Protein Isoforms - metabolism Rats, Wistar Renal Insufficiency, Chronic - etiology Renal Insufficiency, Chronic - metabolism Renal Insufficiency, Chronic - pathology TRPC Cation Channels - metabolism Up-Regulation Ureteral Obstruction |
Title | Evidence of a Role for Fibroblast Transient Receptor Potential Canonical 3 Ca2+ Channel in Renal Fibrosis |
URI | https://www.ncbi.nlm.nih.gov/pubmed/25479966 https://pubmed.ncbi.nlm.nih.gov/PMC4520158 |
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