TRPV4 and the regulation of vascular tone

Journal of Cardiovascular Pharmacology

Volumn 61, Issue 2, 2013, Pages 113-119

  Filosa, Jessica A ^a   Yao, Xiaoqiang ^b   Rath, Geraldine ^c  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

astrocytes; endothelium; TRPV4; vascular smooth muscle cells; vasodilation

Indexed keywords

AQUAPORIN 4; CALCITONIN GENE RELATED PEPTIDE; CAVEOLIN 1; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; VANILLOID RECEPTOR 4;

ARTICLE; ASTROCYTE; BLOOD PRESSURE REGULATION; BLOOD VESSEL TONE; BRAIN CIRCULATION; CALCIUM SIGNALING; CELL COMMUNICATION; CELLS; ENDOTHELIUM CELL; HUMAN; MICROGLIA; NEGATIVE FEEDBACK; NONHUMAN; PERIPHERAL CIRCULATION; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SHEAR STRESS; SMOOTH MUSCLE FIBER; SPINAL GANGLION; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION; VASODILATATION;

ANIMALS; ASTROCYTES; BRAIN; CAVEOLINS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HEMODYNAMICS; HUMANS; MYOCYTES, SMOOTH MUSCLE; TRPV CATION CHANNELS; VASODILATION;

EID: 84873408820     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e318279ba42     Document Type: Article

References (90)

1. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol. 2006;68:619-647.
2. Plant TD, Strotmann R. Trpv4. Handb Exp Pharmacol. 2007;(179): 189-205.
3. Kunert-Keil C, Bisping F, Kruger J, et al. Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics. 2006;7:159.
4. Nilius B, Vriens J, Prenen J, et al. TRPV4 calcium entry channel: A paradigm for gating diversity. Am J Physiol Cell Physiol. 2004;286: C195-C205.
5. Vriens J, Watanabe H, Janssens A, et al. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA. 2004;101:396-401.
6. Voets T, Prenen J, Vriens J, et al. Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem. 2002;277:33704-33710.
7. Watanabe H, Davis JB, Smart D, et al. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem. 2002;277: 13569-13577.
8. Watanabe H, Vriens J, Janssens A, et al. Modulation of TRPV4 gating by intra- and extracellular Ca2+. Cell Calcium. 2003;33:489-495.
9. Watanabe H, Vriens J, Suh SH, et al. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem. 2002;277:47044-47051.
10. Everaerts W, Nilius B, Owsianik G. The vanilloid transient receptor potential channel TRPV4: from structure to disease. Prog Biophys Mol Biol. 2010;103:2-17.
11. Verma P, Kumar A, Goswami C. TRPV4-mediated channelopathies. Channels (Austin). 2010;4:319-328.
12. Garcia-Elias A, Lorenzo IM, Vicente R, et al. IP3 receptor binds to and sensitizes TRPV4 channel to osmotic stimuli via a calmodulin-binding site. J Biol Chem. 2008;283:31284-31288.
13. Becker D, Muller M, Leuner K, et al. The C-terminal domain of TRPV4 is essential for plasma membrane localization. Mol Membr Biol. 2008;25: 139-151.
14. Ramadass R, Becker D, Jendrach M, et al. Spectrally and spatially resolved fluorescence lifetime imaging in living cells: TRPV4-microfilament interactions. Arch Biochem Biophys. 2007;463:27-36.
15. Suzuki M, Mizuno A, Kodaira K, et al. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem. 2003;278:22664-22668.
16. Liu X, Bandyopadhyay BC, Nakamoto T, et al. A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem. 2006; 281:15485-15495.
17. Benfenati V, Caprini M, Dovizio M, et al. An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci USA. 2011;108: 2563-2568.
18. Wang Y, Fu X, Gaiser S, et al. OS-9 regulates the transit and polyubiquitination of TRPV4 in the endoplasmic reticulum. J Biol Chem. 2007; 282:36561-36570.
19. Kottgen M, Buchholz B, Garcia-Gonzalez MA, et al. TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol. 2008;182:437-447.
20. Saliez J, Bouzin C, Rath G, et al. Role of caveolar compartmentation in endothelium-derived hyperpolarizing factor-mediated relaxation: Ca2+ signals and gap junction function are regulated by caveolin in endothelial cells. Circulation. 2008;117:1065-1074.
21. Arniges M, Vazquez E, Fernandez-Fernandez JM, et al. Swellingactivated Ca2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J Biol Chem. 2004;279:54062-54068.
22. Earley S, Heppner TJ, Nelson MT, et al. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res. 2005;97:1270-1279.
23. Fernandez-Fernandez JM, Andrade YN, Arniges M, et al. Functional coupling of TRPV4 cationic channel and large conductance, calciumdependent potassium channel in human bronchial epithelial cell lines. Pflugers Arch. 2008;457:149-159.
24. Guler AD, Lee H, Iida T, et al. Heat-evoked activation of the ion channel, TRPV4. J Neurosci. 2002;22:6408-6414.
25. O'Neil RG, Heller S. The mechanosensitive nature of TRPV channels. Pflugers Arch. 2005;451:193-203.
26. Alvarez DF, King JA, Weber D, et al. Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: A novel mechanism of acute lung injury. Circ Res. 2006;99:988-995.
27. Campbell WB, Fleming I. Epoxyeicosatrienoic acids and endotheliumdependent responses. Pflugers Arch. 2010;459:881-895.
28. Vincent F, Duncton MA. TRPV4 agonists and antagonists. Curr Top Med Chem. 2011;11:2216-2226.
29. Alexander SP, Mathie A, Peters JA. Guide to Receptors and Channels (gRAC), 5th edition. Br J Pharmacol. 2011;164(suppl 1):S1-S324.
30. Watanabe H, Vriens J, Prenen J, et al. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature. 2003; 424:434-438.
31. Loot AE, Popp R, Fisslthaler B, et al. Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res. 2008;80:445-452.
32. Vriens J, Owsianik G, Fisslthaler B, et al. Modulation of the Ca2+ permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res. 2005;97:908-915.
33. Earley S, Pauyo T, Drapp R, et al. TRPV4-dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol Heart Circ Physiol. 2009;297:H1096-H1102.
34. Feletou M, Vanhoutte PM. EDHF: An update. Clin Sci (Lond). 2009;117: 139-155.
35. Marrelli SP, O'Neil R G, Brown RC, et al. PLA2 and TRPV4 channels regulate endothelial calcium in cerebral arteries. Am J Physiol Heart Circ Physiol. 2007;292:H1390-H1397.
36. Martin E, Dahan D, Cardouat G, et al. Involvement of TRPV1 and TRPV4 channels in migration of rat pulmonary arterial smooth muscle cells. Pflugers Arch. 2012;464:261-272.
37. Yang XR, Lin AH, Hughes JM, et al. Upregulation of osmo-mechanosensitive TRPV4 channel facilitates chronic hypoxia-induced myogenic tone and pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2012;302: L555-L568.
38. Gao F, Wang DH. Hypotension induced by activation of the transient receptor potential vanilloid 4 channels: Role of Ca2+-activated K+ channels and sensory nerves. J Hypertens. 2010;28:102-110.
39. Watanabe H, Murakami M, Ohba T, et al. TRP channel and cardiovascular disease. Pharmacol Ther. 2008;118:337-351.
40. Du J, Wong WY, Sun L, et al. Protein kinase G inhibits flow-induced Ca2+ entry into collecting duct cells. J Am Soc Nephrol. 2012;23:1172-1180.
41. Ma X, Qiu S, Luo J, et al. Functional role of vanilloid transient receptor potential 4-canonical transient receptor potential 1 complex in flowinduced Ca2+ influx. Arterioscler Thromb Vasc Biol. 2010;30:851-858.
42. Kwan HY, Shen B, Ma X, et al. TRPC1 associates with BK(Ca) channel to form a signal complex in vascular smooth muscle cells. Circ Res. 2009;104:670-678.
43. Köhler R, Heyken WT, Heinau P, et al. Evidence for a functional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler Thromb Vasc Biol. 2006;26:1495-1502.
44. Willette RN, Bao W, Nerurkar S, et al. Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse: Part 2. J Pharmacol Exp Ther. 2008;326: 443-452.
45. Zhang DX, Mendoza SA, Bubolz AH, et al. Transient receptor potential vanilloid type 4-deficient mice exhibit impaired endothelium-dependent relaxation induced by acetylcholine in vitro and in vivo. Hypertension. 2009;53:532-538.
46. Köhler R, Hoyer J. Role of TRPV4 in the Mechanotransduction of shear stress in endothelial cells. Chap 27. In: Liedtke WB, Heller S, eds. TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades. Boca Raton:CRC Press;2007, Chapter 27.
47. Sonkusare SK, Bonev AD, Ledoux J, et al. Elementary Ca2+ signals through endothelial TRPV4 channels regulate vascular function. Science. 2012;336:597-601.
48. AbsiM, BurnhamMP, Weston AH, et al. Effects of methyl beta-cyclodextrin on EDHF responses in pig and rat arteries; association between SK(Ca) channels and caveolin-rich domains. Br J Pharmacol. 2007;151:332-340.
49. Riddle MA, Hughes JM, Walker BR. Role of caveolin-1 in endothelial BKCa channel regulation of vasoreactivity. Am J Physiol Cell Physiol. 2011;301:C1404-C1414.
50. Isshiki M, Anderson RG. Function of caveolae in Ca2+ entry and Ca2+-dependent signal transduction. Traffic. 2003;4:717-723.
51. Brazer SC, Singh BB, Liu X, et al. Caveolin-1 contributes to assembly of store-operated Ca2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem. 2003;278:27208-27215.
52. Graziani A, Bricko V, Carmignani M, et al. Cholesterol- and caveolinrich membrane domains are essential for phospholipase A2-dependent EDHF formation. Cardiovasc Res. 2004;64:234-242.
53. Everaerts W, Nilius B, Owsianik G. The vanilloid transient receptor potential channel Trpv4: from structure to disease. Prog Biophys Mol Biol. 2009;103:2-17.
54. Cohen DM. The transient receptor potential vanilloid-responsive 1 and 4 cation channels: Role in neuronal osmosensing and renal physiology. Curr Opin Nephrol Hypertens. 2007;16:451-458.
55. Konno M, Shirakawa H, Iida S, et al. Stimulation of transient receptor potential vanilloid 4 channel suppresses abnormal activation of microglia induced by lipopolysaccharide. Glia. 2012;60:761-770.
56. Shirakawa H, Nakagawa T, Kaneko S. [Pathophysiological roles of transient receptor potential channels in glial cells]. Yakugaku Zasshi. 2010; 130:281-287.
57. Benfenati V, Amiry-Moghaddam M, Caprini M, et al. Expression and functional characterization of transient receptor potential vanilloidrelated channel 4 (TRPV4) in rat cortical astrocytes. Neuroscience. 2007;148:876-892.
58. Butenko O, Dzamba D, Benesova J, et al. The increased activity of TRPV4 channel in the astrocytes of the adult rat hippocampus after cerebral hypoxia/ischemia. PLoS One. 2012;7:e39959.
59. Filosa JA, Bonev AD, Straub SV, et al. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci. 2006;9: 1397-1403.
60. Amruthesh SC, Boerschel MF, McKinney JS, et al. Metabolism of arachidonic acid to epoxyeicosatrienoic acids, hydroxyeicosatetraenoic acids, and prostaglandins in cultured rat hippocampal astrocytes. J Neurochem. 1993;61:150-159.
61. Alkayed NJ, Narayanan J, Gebremedhin D, et al. Molecular characterization of an arachidonic acid epoxygenase in rat brain astrocytes. Stroke. 1996;27:971-979.
62. Metea MR, Newman EA. Glial cells dilate and constrict blood vessels: A mechanism of neurovascular coupling. J Neurosci. 2006;26:2862-2870.
63. Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature. 2004;431:195-199.
64. Takano T, Tian GF, Peng W, et al. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci. 2006;9:260-267.
65. Zonta M, Angulo MC, Gobbo S, et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci. 2003;6:43-50.
66. Attwell D, Buchan AM, Charpak S, et al. Glial and neuronal control of brain blood flow. Nature. 2010;468:232-243.
67. Blanco VM, Stern JE, Filosa JA. Tone-dependent vascular responses to astrocyte-derived signals. Am J Physiol Heart Circ Physiol. 2008;294: H2855-H2863.
68. Girouard H, Bonev AD, Hannah RM, et al. Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA. 2010;107:3811-3816.
69. Simard M, Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience. 2004;129:877-896.
70. Amiry-Moghaddam M, Frydenlund DS, Ottersen OP. Anchoring of aquaporin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience. 2004;129:999-1010.
71. Amiry-Moghaddam M, Xue R, Haug FM, et al. Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. FASEB J. 2004;18:542-544.
72. Price DL, Ludwig JW, Mi H, et al. Distribution of rSlo Ca2+-activated K+ channels in rat astrocyte perivascular endfeet. Brain Res. 2002;956: 183-193.
73. Higashimori H, Blanco VM, Tuniki VR, et al. Role of epoxyeicosatrienoic acids as autocrine metabolites in glutamate-mediated K+ signaling in perivascular astrocytes. Am J Physiol Cell Physiol. 2010;299:C1068-C1078.
74. Ding XL, Wang YH, Ning LP, et al. Involvement of TRPV4-NO-cGMPPKG pathways in the development of thermal hyperalgesia following chronic compression of the dorsal root ganglion in rats. Behav Brain Res. 2010;208:194-201.
75. Bal-Price A, Moneer Z, Brown GC. Nitric oxide induces rapid, calciumdependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia. 2002;40:312-323.
76. Ferraro G, Sardo P. Nitric oxide and brain hyperexcitability. In Vivo. 2004;18:357-366.
77. Grant AD, Cottrell GS, Amadesi S, et al. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol. 2007;578(Pt 3):715-733.
78. Koltzenburg M. The role of TRP channels in sensory neurons. Novartis Found Symp. 2004;260:206-213; discussion 213-220, 277-209.
79. McHugh J, Keller NR, Appalsamy M, et al. Portal osmopressor mechanism linked to transient receptor potential vanilloid 4 and blood pressure control. Hypertension. 2010;55:1438-1443.
80. Liu TT, Bi HS, Lv SY, et al. Inhibition of the expression and function of TRPV4 by RNA interference in dorsal root ganglion. Neurol Res. 2010; 32:466-471.
81. Cenac N, Altier C, Chapman K, et al. Transient receptor potential vanilloid-4 has a major role in visceral hypersensitivity symptoms. Gastroenterology. 2008;135:937-946; 946 e931-932.
82. Gao F, Sui D, Garavito RM, et al. Salt intake augments hypotensive effects of transient receptor potential vanilloid 4: functional significance and implication. Hypertension. 2009;53:228-235.
83. Ryskamp DA, Witkovsky P, Barabas P, et al. The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci. 2011;31: 7089-7101.
84. Troidl C, Troidl K, Schierling W, et al. Trpv4 induces collateral vessel growth during regeneration of the arterial circulation. J Cell Mol Med. 2009;13:2613-2621.
85. Schierling W, Troidl K, Apfelbeck H, et al. Cerebral arteriogenesis is enhanced by pharmacological as well as fluid-shear-stress activation of the Trpv4 calcium channel. Eur J Vasc Endovasc Surg. 2011;41:589-596.
86. Ducret T, Guibert C, Marthan R, et al. Serotonin-induced activation of TRPV4-like current in rat intrapulmonary arterial smooth muscle cells. Cell Calcium. 2008;43:315-323.
87. Mizoguchi F, Mizuno A, Hayata T, et al. Transient receptor potential vanilloid 4 deficiency suppresses unloading-induced bone loss. J Cell Physiol. 2008;216:47-53.
88. Auer-Grumbach M, Olschewski A, Papic L, et al. Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C. Nat Genet. 2010;42:160-164.
89. Carreno FR, Ji LL, Cunningham JT. Altered central TRPV4 expression and lipid raft association related to inappropriate vasopressin secretion in cirrhotic rats. Am J Physiol Regul Integr Comp Physiol. 2009;296:R454-R466.
90. Tian W, Fu Y, Garcia-Elias A, et al. A loss-of-function nonsynonymous polymorphism in the osmoregulatory TRPV4 gene is associated with human hyponatremia. Proc Natl Acad Sci USA. 2009;106: 14034-14039.