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Transient Receptor Potential Channels in the Vasculature

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Earley, Scott, Brayden, Joseph E.·2015·Physiological Reviews

DOI 10.1152/physrev.00026.2014

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Abstract

The mammalian genome encodes 28 distinct members of the transient receptor potential (TRP) superfamily of cation channels, which exhibit varying degrees of selectivity for different ionic species. Multiple TRP channels are present in all cells and are involved in diverse aspects of cellular function, including sensory perception and signal transduction. Notably, TRP channels are involved in regulating vascular function and pathophysiology, the focus of this review. TRP channels in vascular smooth muscle cells participate in regulating contractility and proliferation, whereas endothelial TRP channel activity is an important contributor to endothelium-dependent vasodilation, vascular wall permeability, and angiogenesis. TRP channels are also present in perivascular sensory neurons and astrocytic endfeet proximal to cerebral arterioles, where they participate in the regulation of vascular tone. Almost all of these functions are mediated by changes in global intracellular Ca 2+levels or subcellular Ca 2+signaling events. In addition to directly mediating Ca 2+entry, TRP channels influence intracellular Ca 2+dynamics through membrane depolarization associated with the influx of cations or through receptor- or store-operated mechanisms. Dysregulation of TRP channels is associated with vascular-related pathologies, including hypertension, neointimal injury, ischemia-reperfusion injury, pulmonary edema, and neurogenic inflammation. In this review, we briefly consider general aspects of TRP channel biology and provide an in-depth discussion of the functions of TRP channels in vascular smooth muscle cells, endothelial cells, and perivascular cells under normal and pathophysiological conditions.

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Expression and functional characterization of transient receptor potential vanilloid-related channel 4 (TRPV4) in rat cortical astrocytes
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TRPV4 channels augment macrophage activation and ventilator-induced lung injury
Hamanaka, K., Jian, M.-Y., Townsley, M. I., King, J. A., Liedtke, W., Weber, D. S., Eyal, F. G., Clapp, M. M., & Parker, J. C. (2010) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00315.2009 · Cited by 193
A Functional Single-Nucleotide Polymorphism in the TRPC6 Gene Promoter Associated With Idiopathic Pulmonary Arterial Hypertension
Yu, Y., Keller, S. H., Remillard, C. V., Safrina, O., Nicholson, A., Zhang, S. L., Jiang, W., Vangala, N., Landsberg, J. W., Wang, J.-Y., et al. (2009) · Circulation · doi:10.1161/circulationaha.108.782458 · Cited by 191
Low intravascular pressure activates endothelial cell TRPV4 channels, local Ca 2+ events, and IK Ca channels, reducing arteriolar tone
Bagher, P., Beleznai, T., Kansui, Y., Mitchell, R., Garland, C. J., & Dora, K. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211946109 · Cited by 190
Activation of TRPC6 channels is essential for lung ischaemia–reperfusion induced oedema in mice
Weissmann, N., Sydykov, A., Kalwa, H., Storch, U., Fuchs, B., Mederos y Schnitzler, M., Brandes, R. P., Grimminger, F., Meissner, M., Freichel, M., et al. (2012) · Nature Communications · doi:10.1038/ncomms1660 · Cited by 189
Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues
Petersen, C. C., Berridge, M. J., Borgese, M. F., & Bennett, D. L. (1995) · Biochemical Journal · doi:10.1042/bj3110041 · Cited by 188
The transient receptor potential vanilloid 1: Role in airway inflammation and disease
Geppetti, P., Materazzi, S., & Nicoletti, P. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.12.063 · Cited by 187
Transient Receptor Potential Melastatin 7 Ion Channels Regulate Magnesium Homeostasis in Vascular Smooth Muscle Cells: Role of Angiotensin II
He, Y., Yao, G., Savoia, C., & Touyz, R. M. (2005) · Circulation Research · doi:10.1161/01.res.0000152967.88472.3e · Cited by 186
TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acid-activated actin remodeling
Fiorio Pla, A., Ong, H. L., Cheng, K. T., Brossa, A., Bussolati, B., Lockwich, T., Paria, B., Munaron, L., & Ambudkar, I. S. (2012) · Oncogene · doi:10.1038/onc.2011.231 · Cited by 183
Properties of heterologously expressed hTRP3 channels in bovine pulmonary artery endothelial cells
Kamouchi, M., Philipp, S., Flockerzi, V., Wissenbach, U., Mamin, A., Raeymaekers, L., Eggermont, J., Droogmans, G., & Nilius, B. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0345p.x · Cited by 183
Ca2+ Signaling by TRPC3 Involves Na+ Entry and Local Coupling to the Na+/Ca2+ Exchanger
Rosker, C., Graziani, A., Lukas, M., Eder, P., Zhu, M. X., Romanin, C., & Groschner, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m308108200 · Cited by 183
The TRPM7 Chanzyme Is Cleaved to Release a Chromatin-Modifying Kinase
Krapivinsky, G., Krapivinsky, L., Manasian, Y., & Clapham, D. E. (2014) · Cell · doi:10.1016/j.cell.2014.03.046 · Cited by 183
Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain
Moussaieff, A., Rimmerman, N., Bregman, T., Straiker, A., Felder, C. C., Shoham, S., Kashman, Y., Huang, S. M., Lee, H., Shohami, E., et al. (2008) · The FASEB Journal · doi:10.1096/fj.07-101865 · Cited by 182
TRPM4 controls insulin secretion in pancreatic β-cells
Cheng, H., Beck, A., Launay, P., Gross, S. A., Stokes, A. J., Kinet, J.-P., Fleig, A., & Penner, R. (2007) · Cell Calcium · doi:10.1016/j.ceca.2006.04.032 · Cited by 182
Transient Receptor Potential Channels in Endothelium: Solving the Calcium Entry Puzzle?
Nilius, B., Droogmans, G., & Wondergem, R. (2003) · Endothelium · doi:10.1080/10623320303356 · Cited by 182
AKAP150-dependent cooperative TRPV4 channel gating is central to endothelium-dependent vasodilation and is disrupted in hypertension
Sonkusare, S. K., Dalsgaard, T., Bonev, A. D., Hill-Eubanks, D. C., Kotlikoff, M. I., Scott, J. D., Santana, L. F., & Nelson, M. T. (2014) · Science Signaling · doi:10.1126/scisignal.2005052 · Cited by 180
Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation
Loot, A. E., Popp, R., Fisslthaler, B., Vriens, J., Nilius, B., & Fleming, I. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn207 · Cited by 179
Protein Kinase Cα Phosphorylates the TRPC1 Channel and Regulates Store-operated Ca2+ Entry in Endothelial Cells
Ahmmed, G. U., Mehta, D., Vogel, S., Holinstat, M., Paria, B. C., Tiruppathi, C., & Malik, A. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313975200 · Cited by 177
TRP channels of intracellular membranes
Dong, X., Wang, X., & Xu, H. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06626.x · Cited by 170
Increased catecholamine secretion contributes to hypertension in TRPM4-deficient mice
Mathar, I., Vennekens, R., Meissner, M., Kees, F., Van der Mieren, G., Camacho Londoño, J. E., Uhl, S., Voets, T., Hummel, B., van den Bergh, A., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci41348 · Cited by 170
Protein kinase C regulates vascular myogenic tone through activation of TRPM4
Earley, S., Straub, S. V., & Brayden, J. E. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01286.2006 · Cited by 170
Self-citation
Role of Endogenous TRPC6 Channels in Ca2+ Signal Generation in A7r5 Smooth Muscle Cells
Soboloff, J., Spassova, M., Xu, W., He, L.-P., Cuesta, N., & Gill, D. L. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m506064200 · Cited by 167
Localized TRPA1 channel Ca 2+ signals stimulated by reactive oxygen species promote cerebral artery dilation
Sullivan, M. N., Gonzales, A. L., Pires, P. W., Bruhl, A., Leo, M. D., Li, W., Oulidi, A., Boop, F. A., Feng, Y., Jaggar, J. H., et al. (2015) · Science Signaling · doi:10.1126/scisignal.2005659 · Cited by 167
Self-citation
Roles of TRPM2 in oxidative stress
Takahashi, N., Kozai, D., Kobayashi, R., Ebert, M., & Mori, Y. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.04.006 · Cited by 165
9‐Phenanthrol inhibits human TRPM4 but not TRPM5 cationic channels
Grand, T., Demion, M., Norez, C., Mettey, Y., Launay, P., Becq, F., Bois, P., & Guinamard, R. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.38 · Cited by 164
Synergistic Activation of Vascular TRPC6 Channel by Receptor and Mechanical Stimulation via Phospholipase C/Diacylglycerol and Phospholipase A 2 /ω-Hydroxylase/20-HETE Pathways
Inoue, R., Jensen, L. J., Jian, Z., Shi, J., Hai, L., Lurie, A. I., Henriksen, F. H., Salomonsson, M., Morita, H., Kawarabayashi, Y., et al. (2009) · Circulation Research · doi:10.1161/circresaha.108.193227 · Cited by 163
Functional aspects and mechanisms of TRPV1 involvement in neurogenic inflammation that leads to thermal hyperalgesia
Planells-Cases, R., Garcìa-Sanz, N., Morenilla-Palao, C., & Ferrer-Montiel, A. (2005) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-005-1423-5 · Cited by 162
Plasticity of TRPC expression in arterial smooth muscle: correlation with store-operated Ca2+ entry
Bergdahl, A., Gomez, M. F., Wihlborg, A.-K., Erlinge, D., Eyjolfson, A., Xu, S.-Z., Beech, D. J., Dreja, K., & Hellstrand, P. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00334.2004 · Cited by 162
Transient receptor potential melastatin 6 and 7 channels, magnesium transport, and vascular biology: implications in hypertension
Touyz, R. M. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00903.2007 · Cited by 162
Trp proteins form store‐operated cation channels in human vascular endothelial cells
Groschner, K., Hingel, S., Lintschinger, B., Balzer, M., Romanin, C., Zhu, X., & Schreibmayer, W. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01212-5 · Cited by 161
TRPC3 mediates pyrimidine receptor-induced depolarization of cerebral arteries
Reading, S. A., Earley, S., Waldron, B. J., Welsh, D. G., & Brayden, J. E. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00861.2004 · Cited by 161
Self-citation
VEGF‐Mediated Elevated Intracellular Calcium and Angiogenesis in Human Microvascular Endothelial Cells In Vitro are Inhibited by Dominant Negative TRPC6
ZADEH, M. A. H., GLASS, C. A., MAGNUSSEN, A., HANCOX, J. C., & BATES, D. O. (2008) · Microcirculation · doi:10.1080/10739680802220323 · Cited by 160
Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G
Kwan, H.-Y., Huang, Y., & Yao, X. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0304471101 · Cited by 159
Tumor necrosis factor-α-induced TRPC1 expression amplifies store-operated Ca2+influx and endothelial permeability
Paria, B. C., Vogel, S. M., Ahmmed, G. U., Alamgir, S., Shroff, J., Malik, A. B., & Tiruppathì, C. (2004) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00240.2004 · Cited by 157
Reactive Oxygen Species, NADPH Oxidases, and Hypertension
Datla, S. R., & Griendling, K. K. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.142422 · Cited by 152

Vascular mechanotransduction
Davis, M. J., Earley, S., Li, Y.-S., & Chien, S. (2023) · Physiological Reviews · doi:10.1152/physrev.00053.2021 · Cited by 273
Self-citation
PIP2 depletion promotes TRPV4 channel activity in mouse brain capillary endothelial cells
Harraz, O. F., Longden, T. A., Hill-Eubanks, D., & Nelson, M. T. (2018) · eLife · doi:10.7554/elife.38689 · Cited by 149
Ion channel networks in the control of cerebral blood flow
Longden, T. A., Hill-Eubanks, D. C., & Nelson, M. T. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x15616138 · Cited by 137
Calcium influx through TRPV4 channels modulates the adherens contacts between retinal microvascular endothelial cells
Phuong, T. T. T., Redmon, S. N., Yarishkin, O., Winter, J. M., Li, D. Y., & Križaj, D. (2017) · The Journal of Physiology · doi:10.1113/jp275052 · Cited by 91

See all 420

Authors: Earley, S., & Brayden, J. E.
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2015-04
Volume: 95
Issue: 2
Pages: 645-690
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00026.2014
OpenAlex: W2117597411
Cited by: 420
References: 383
FWCI: 4.38
Type: journal article
Language: en
Open access: green

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Transient Receptor Potential Channels in the Vasculature

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