GPCR-mediated EGF receptor transactivation regulates TRPV4 action in the vasculature

British Journal of Pharmacology

Volumn 172, Issue 10, 2015, Pages 2493-2506

  Saifeddine, Mahmoud ^a   El Daly, Mahmoud ^a,b   Mihara, Koichiro ^a   Bunnett, Nigel W ^c   McIntyre, Peter ^d   Altier, Christophe ^a   Hollenberg, Morley D ^a,e   Ramachandran, Rithwik ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b Minia University   (Egypt)

^c MONASH UNIVERSITY   (Australia)

^d RMIT UNIVERSITY   (Australia)

^e UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; THROMBOXANE; THROMBOXANE A2; THROMBOXANE RECEPTOR; VANILLOID RECEPTOR 4; TRPV4 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL TISSUE; AORTA; ARTICLE; BLOOD VESSEL TONE; CALCIUM SIGNALING; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; MOUSE; MYOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; RECEPTOR TRANSACTIVATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASOCONSTRICTION; VASODILATATION; WIRE MYOGRAPHY; ANIMAL; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; AORTA; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, KNOCKOUT; MYOGRAPHY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TRPV CATION CHANNELS; VASOCONSTRICTION;

EID: 84928324298     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13072     Document Type: Article

References (87)

1. Adams MN, Ramachandran R, Yau MK, Suen JY, Fairlie DP, Hollenberg MD, et al. (2011). Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther 130: 248-282.
2. Alessandri-Haber N, Dina OA, Joseph EK, Reichling D, Levine JD, (2006). A transient receptor potential vanilloid 4-dependent mechanism of hyperalgesia is engaged by concerted action of inflammatory mediators. J Neurosci 26: 3864-3874.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et al. (2013a). The concise guide to PHARMACOLOGY 2013/14: ion channels. Br J Pharmacol 170: 1607-1651.
4. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The concise guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
5. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The concise guide to PHARMACOLOGY 2013/14: catalytic receptors. Br J Pharmacol, 170, 1676-1705.
6. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013d). The concise guide to PHARMACOLOGY 2013/14: enzymes. Br J Pharmacol, 170: 1797-1867.
7. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, et al. (2004). Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312.
8. Awasthi V, Mandal SK, Papanna V, Rao LV, Pendurthi UR, (2007). Modulation of tissue factor-factor VIIa signaling by lipid rafts and caveolae. Arterioscler Thromb Vasc Biol 27: 1447-1455.
9. Bain J, McLauchlan H, Elliott M, Cohen P, (2003). The specificities of protein kinase inhibitors: an update. Biochem J 371 (Pt 1): 199-204.
10. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, et al. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
11. Baylie RL, Brayden JE, (2011). TRPV channels and vascular function. Acta Physiol (Oxf) 203: 99-116.
12. Blobel CP, (2005). ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 6: 32-43.
13. Bubolz AH, Mendoza SA, Zheng X, Zinkevich NS, Li R, Gutterman DD, et al. (2012). Activation of endothelial TRPV4 channels mediates flow-induced dilation in human coronary arterioles: role of Ca2 + entry and mitochondrial ROS signaling. Am J Physiol Heart Circ Physiol 302: H634-H642.
14. Cenac N, Altier C, Motta JP, d'Aldebert E, Galeano S, Zamponi GW, et al. (2010). Potentiation of TRPV4 signalling by histamine and serotonin: an important mechanism for visceral hypersensitivity. Gut 59: 481-488.
15. Clapham DE, (2003). TRP channels as cellular sensors. Nature 426: 517-524.
16. Cohen P, (2010). Guidelines for the effective use of chemical inhibitors of protein function to understand their roles in cell regulation. Biochem J 425: 53-54.
17. Coughlin SR, (2000). Thrombin signalling and protease-activated receptors. Nature 407: 258-264.
18. Damiano BP, Cheung WM, Santulli RJ, Fung-Leung WP, Ngo K, Ye RD, et al. (1999). Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J Pharmacol Exp Ther 288: 671-678.
19. Daub H, Weiss FU, Wallasch C, Ullrich A, (1996). Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379: 557-560.
20. Ducret T, Guibert C, Marthan R, Savineau JP, (2008). Serotonin-induced activation of TRPV4-like current in rat intrapulmonary arterial smooth muscle cells. Cell Calcium 43: 315-323.
21. Earley S, Brayden JE, (2010). Transient receptor potential channels and vascular function. Clin Sci (Lond) 119: 19-36.
22. Earley S, Heppner TJ, Nelson MT, Brayden JE, (2005). TRPV4 forms a novel Ca2 + signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279.
23. Earley S, Pauyo T, Drapp R, Tavares MJ, Liedtke W, Brayden JE, (2009). TRPV4-dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol Heart Circ Physiol 297: H1096-H1102.
24. Eguchi S, Numaguchi K, Iwasaki H, Matsumoto T, Yamakawa T, Utsunomiya H, et al. (1998). Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J Biol Chem 273: 8890-8896.
25. El-Daly M, Saifeddine M, Mihara K, Ramachandran R, Triggle CR, Hollenberg MD, (2014). Proteinase-activated receptors 1 and 2 and the regulation of porcine coronary artery contractility: a role for distinct tyrosine kinase pathways. Br J Pharmacol 171: 2413-2425.
26. Ene FA, Kalmbach A, Kandler K, (2007). Metabotropic glutamate receptors in the lateral superior olive activate TRP-like channels: age- and experience-dependent regulation. J Neurophysiol 97: 3365-3375.
27. Everaerts W, Zhen X, Ghosh D, Vriens J, Gevaert T, Gilbert JP, et al. (2010). Inhibition of the cation channel TRPV4 improves bladder function in mice and rats with cyclophosphamide-induced cystitis. Proc Natl Acad Sci U S A 107: 19084-19089.
28. Fan HC, Zhang X, McNaughton PA, (2009). Activation of the TRPV4 ion channel is enhanced by phosphorylation. J Biol Chem 284: 27884-27891.
29. Gao X, Wu L, O'Neil RG, (2003). Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278: 27129-27137.
30. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T, (2000). International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52: 415-472.
31. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, et al. (2007). Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578 (Pt 3): 715-733.
32. Gschwind A, Zwick E, Prenzel N, Leserer M, Ullrich A, (2001). Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene 20: 1594-1600.
33. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M, (2002). Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22: 6408-6414.
34. Hamberg M, Svensson J, Samuelsson B, (1975). Thromboxanes: a new group of biologically active compounds derived from prostaglandin endoperoxides. Proc Natl Acad Sci U S A 72: 2994-2998.
35. Hartmannsgruber V, Heyken WT, Kacik M, Kaistha A, Grgic I, Harteneck C, et al. (2007). Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS ONE 2: e827.
36. Huang A, Sun D, Koller A, (2000). Shear stress-induced release of prostaglandin H(2) in arterioles of hypertensive rats. Hypertension 35: 925-930.
37. Ingerman-Wojenski C, Silver MJ, Smith JB, Macarak E, (1981). Bovine endothelial cells in culture produce thromboxane as well as prostacyclin. J Clin Invest 67: 1292-1296.
38. Ishizuka T, Kawakami M, Hidaka T, Matsuki Y, Takamizawa M, Suzuki K, et al. (1998). Stimulation with thromboxane A2 (TXA2) receptor agonist enhances ICAM-1, VCAM-1 or ELAM-1 expression by human vascular endothelial cells. Clin Exp Immunol 112: 464-470.
39. Jia Y, Wang X, Varty L, Rizzo CA, Yang R, Correll CC, et al. (2004). Functional TRPV4 channels are expressed in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 287: L272-L278.
40. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
41. Laniyonu AA, Saifeddine M, Yang SG, Hollenberg MD, (1994). Tyrosine kinase inhibitors and the contractile action of G-protein-linked vascular agonists. Can J Physiol Pharmacol 72: 1075-1085.
42. Lee H, Hamilton JR, (2012). Physiology, pharmacology, and therapeutic potential of protease-activated receptors in vascular disease. Pharmacol Ther 134: 246-259.
43. Liedtke W, Friedman JM, (2003). Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci U S A 100: 13698-13703.
44. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, et al. (2000). Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535.
45. Masuyama R, Vriens J, Voets T, Karashima Y, Owsianik G, Vennekens R, et al. (2008). TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts. Cell Metab 8: 257-265.
46. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
47. McGuire JJ, Hollenberg MD, Bennett BM, Triggle CR, (2004). Hyperpolarization of murine small caliber mesenteric arteries by activation of endothelial proteinase-activated receptor 2. Can J Physiol Pharmacol 82: 1103-1112.
48. Mendoza SA, Fang J, Gutterman DD, Wilcox DA, Bubolz AH, Li R, et al. (2009). TRPV4-mediated endothelial Ca2 + influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol 298: H466-H476.
49. Mercado J, Baylie R, Navedo MF, Yuan C, Scott JD, Nelson MT, et al. (2014). Local control of TRPV4 channels by AKAP150-targeted PKC in arterial smooth muscle. J Gen Physiol 143: 559-575.
50. Neri Serneri GG, Abbate R, Gensini GF, Panetta A, Casolo GC, Carini M, (1983). TxA2 production by human arteries and veins. Prostaglandins 25: 753-766.
51. Ohtsu H, Dempsey PJ, Frank GD, Brailoiu E, Higuchi S, Suzuki H, et al. (2006). ADAM17 mediates epidermal growth factor receptor transactivation and vascular smooth muscle cell hypertrophy induced by angiotensin II. Arterioscler Thromb Vasc Biol 26: e133-e137.
52. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
53. Peng H, Lewandrowski U, Muller B, Sickmann A, Walz G, Wegierski T, (2010). Identification of a protein kinase C-dependent phosphorylation site involved in sensitization of TRPV4 channel. Biochem Biophys Res Commun 391: 1721-1725.
54. Peng JB, Hediger MA, (2002). A family of calcium-permeable channels in the kidney: distinct roles in renal calcium handling. Curr Opin Nephrol Hypertens 11: 555-561.
55. Poole DP, Amadesi S, Veldhuis NA, Abogadie FC, Lieu T, Darby W, et al. (2013). Protease-activated receptor 2 (PAR2) protein and transient receptor potential vanilloid 4 (TRPV4) protein coupling is required for sustained inflammatory signaling. J Biol Chem 288: 5790-5802.
56. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, et al. (1999). EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402: 884-888.
57. Ramachandran R, Hollenberg MD, (2008). Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 153 (Suppl. 1): S263-S282.
58. Ramachandran R, Mihara K, Mathur M, Rochdi MD, Bouvier M, Defea K, et al. (2009). Agonist-biased signaling via proteinase activated receptor-2: differential activation of calcium and mitogen-activated protein kinase pathways. Mol Pharmacol 76: 791-801.
59. Ramachandran R, Mihara K, Chung H, Renaux B, Lau CS, Muruve DA, et al. (2011). Neutrophil elastase acts as a biased agonist for proteinase-activated receptor-2 (PAR2). J Biol Chem 286: 24638-24648.
60. Ramachandran R, Noorbakhsh F, Defea K, Hollenberg MD, (2012). Targeting proteinase-activated receptors: therapeutic potential and challenges. Nat Rev Drug Discov 11: 69-86.
61. Russo A, Soh UJ, Paing MM, Arora P, Trejo J, (2009). Caveolae are required for protease-selective signaling by protease-activated receptor-1. Proc Natl Acad Sci U S A 106: 6393-6397.
62. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, et al. (2004). Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164: 769-779.
63. 2+ signals and gap junction function are regulated by caveolin in endothelial cells. Circulation 117: 1065-1074.
64. Song P, Zhang M, Wang S, Xu J, Choi HC, Zou MH, (2009). Thromboxane A2 receptor activates a Rho-associated kinase/LKB1/PTEN pathway to attenuate endothelium insulin signaling. J Biol Chem 284: 17120-17128.
65. 2+ signals through endothelial TRPV4 channels regulate vascular function. Science 336: 597-601.
66. Sukumaran SV, Singh TU, Parida S, Narasimha Reddy CE, Thangamalai R, Kandasamy K, et al. (2013). TRPV4 channel activation leads to endothelium-dependent relaxation mediated by nitric oxide and endothelium-derived hyperpolarizing factor in rat pulmonary artery. Pharmacol Res 78: 18-27.
67. Sullivan MN, Francis M, Pitts NL, Taylor MS, Earley S, (2012). Optical recording reveals novel properties of GSK1016790A-induced vanilloid transient receptor potential channel TRPV4 activity in primary human endothelial cells. Mol Pharmacol 82: 464-472.
68. Suzuki M, Mizuno A, Kodaira K, Imai M, (2003). Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278: 22664-22668.
69. Tabuchi K, Suzuki M, Mizuno A, Hara A, (2005). Hearing impairment in TRPV4 knockout mice. Neurosci Lett 382: 304-308.
70. Takaguri A, Shirai H, Kimura K, Hinoki A, Eguchi K, Carlile-Klusacek M, et al. (2011). Caveolin-1 negatively regulates a metalloprotease-dependent epidermal growth factor receptor transactivation by angiotensin II. J Mol Cell Cardiol 50: 545-551.
71. Tesfamariam B, Jakubowski JA, Cohen RA, (1989). Contraction of diabetic rabbit aorta caused by endothelium-derived PGH2-TxA2. Am J Physiol 257 (5 Pt 2): H1327-H1333.
72. Thorneloe KS, Sulpizio AC, Lin Z, Figueroa DJ, Clouse AK, McCafferty GP, et al. (2008). N-((1S)-1-{[4-((2S)-2-{[(2,4-dichlorophenyl)sulfonyl]amino}-3-hydroxypropanoyl)-1 -piperazinyl]carbonyl}-3-methylbutyl)-1-benzothiophene-2-carboxamide (GSK1016790A), a novel and potent transient receptor potential vanilloid 4 channel agonist induces urinary bladder contraction and hyperactivity: Part I. J Pharmacol Exp Ther 326: 432-442.
73. Thorneloe KS, Cheung M, Bao W, Alsaid H, Lenhard S, Jian MY, et al. (2012). An orally active TRPV4 channel blocker prevents and resolves pulmonary edema induced by heart failure. Science translational medicine 4: 159ra148.
74. Tilley DG, (2011). G protein-dependent and G protein-independent signaling pathways and their impact on cardiac function. Circ Res 109: 217-230.
75. Todaka H, Taniguchi J, Satoh J, Mizuno A, Suzuki M, (2004). Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279: 35133-35138.
76. Touyz RM, Schiffrin EL, (2000). Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. Pharmacol Rev 52: 639-672.
77. Udvardy M, Torok I, Rak K, (1987). Plasma thromboxane and prostacyclin metabolite ratio in atherosclerosis and diabetes mellitus. Thromb Res 47: 479-484.
78. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, et al. (2002a). Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277: 13569-13577.
79. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B, (2002b). Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277: 47044-47051.
80. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B, (2003). Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 434-438.
81. Watanabe H, Murakami M, Ohba T, Takahashi Y, Ito H, (2008). TRP channel and cardiovascular disease. Pharmacol Ther 118: 337-351.
82. Willette RN, Bao W, Nerurkar S, Yue TL, Doe CP, Stankus G, et al. (2008). Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse: part 2. J Pharmacol Exp Ther 326: 443-452.
83. Woodward DF, Jones RL, Narumiya S, (2011). International Union of Basic and Clinical Pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress. Pharmacol Rev 63: 471-538.
84. Wu L, Gao X, Brown RC, Heller S, O'Neil RG, (2007). Dual role of the TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Renal Physiol 293: F1699-F1713.
85. Xia Y, Fu Z, Hu J, Huang C, Paudel O, Cai S, et al. (2013). TRPV4 channel contributes to serotonin-induced pulmonary vasoconstriction and the enhanced vascular reactivity in chronic hypoxic pulmonary hypertension. Am J Physiol Cell Physiol 305: C704-C715.
86. Xu F, Satoh E, Iijima T, (2003). Protein kinase C-mediated Ca2 + entry in HEK 293 cells transiently expressing human TRPV4. Br J Pharmacol 140: 413-421.
87. Zimmerman B, Beautrait A, Aguila B, Charles R, Escher E, Claing A, et al. (2012). Differential beta-arrestin-dependent conformational signaling and cellular responses revealed by angiotensin analogs. Sci Signal 5: ra33.