The tyrosine kinase inhibitor bafetinib inhibits PAR2-induced activation of TRPV4 channels in vitro and pain in vivo

British Journal of Pharmacology

Volumn 171, Issue 16, 2014, Pages 3881-3894

  Grace, M S ^a   Lieu, T ^b   Darby, B ^a   Abogadie, F C ^a   Veldhuis, N ^b   Bunnett, N W ^b   Mcintyre, P ^a  

^a RMIT UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE TRIPHOSPHATASE (CALCIUM); BAFETINIB; CALCIUM ION; DASATINIB; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 2; THAPSIGARGIN; TRYPSIN; VANILLOID RECEPTOR 4; VANILLOID RECEPTOR AGONIST; VANILLOID RECEPTOR ANTAGONIST; WORTMANNIN; HC-067047; LEUCINE; MORPHOLINE DERIVATIVE; N-(1-((4-(2-(((2,4-DICHLOROPHENYL)SULFONYL)AMINO)-3-HYDROXYPROPANOYL)-1-PIPERAZINYL)CARBONYL)-3-METHYLBUTYL)-1-BENZOTHIOPHENE-2-CARBOXAMIDE; OLIGOPEPTIDE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE; SERYL-LEUCYL-ISOLEUCYL-GLYCYL-ARGINYL-LEUCINE; SULFONAMIDE; TRPV4 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYPERALGESIA; IMAGING SYSTEM; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; GENETICS; METABOLISM; PAIN;

ANIMALS; HEK293 CELLS; HUMANS; HYPERALGESIA; LEUCINE; MALE; MICE, INBRED C57BL; MORPHOLINES; OLIGOPEPTIDES; PAIN; PROTEIN KINASE INHIBITORS; PYRIMIDINES; PYRROLES; RECEPTOR, PAR-2; SULFONAMIDES; TRPV CATION CHANNELS; TRYPSIN;

EID: 84905024930     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12750     Document Type: Article

References (54)

1. Alemi F, Kwon E, Poole DP, Lieu T, Lyo V, Cattaruzza F, et-al. (2013). The TGR5 receptor mediates bile acid-induced itch and analgesia. J Clin Invest 123: 1513-1530.
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. 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.
7. Bautista DM, Jordt S-E, Nikai T, Tsuruda PR, Read AJ, Poblete J, et-al. (2006). TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282.
8. Capodici C, Hanft S, Feoktistov M, Pillinger MH, (1998). Phosphatidylinositol 3-kinase mediates chemoattractant-stimulated, CD11b/CD18-dependent cell-cell adhesion of human neutrophils: evidence for an ERK-independent pathway. J Immunol 160: 1901-1909.
9. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
10. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL, (1994). Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53: 55-63.
11. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, et-al. (2004). Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24: 4293-4299.
12. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, et-al. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117: 1979-1987.
13. 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.
14. Fecto F, Shi Y, Huda R, Martina M, Siddique T, Deng H-X, (2011). Mutant TRPV4-mediated toxicity is linked to increased constitutive function in axonal neuropathies. J Biol Chem 286: 17281-17291.
15. Fu Y, Subramanya A, Rozansky D, Cohen DM, (2006). WNK kinases influence TRPV4 channel function and localization. Am J Physiol Renal Physiol 290: F1305-F1314.
16. Gavva NR, Treanor JJS, Garami A, Fang L, Surapaneni S, Akrami A, et-al. (2008). Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136: 202-210.
17. 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: 715-733.
18. Güler 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.
19. Imam SZ, Trickler W, Kimura S, Binienda ZK, Paule MG, Slikker W, et-al. (2013). Neuroprotective efficacy of a new brain-penetrating C-Abl inhibitor in a murine Parkinson's disease model. PLoS ONE 8: e65129.
20. Jacobsen SE, Nørskov-Lauritsen L, Thomsen ARB, Smajilovic S, Wellendorph P, Larsson NHP, et-al. (2013). Delineation of the GPRC6A receptor signaling pathways using a mammalian cell line stably expressing the receptor. J Pharmacol Exp Ther 347: 298-309.
21. Karim SA, Creedon H, Patel H, Carragher NO, Morton JP, Muller WJ, et-al. (2013). Dasatinib inhibits mammary tumour development in a genetically engineered mouse model. J Pathol 230: 430-440.
22. Lamandé SR, Yuan Y, Gresshoff IL, Rowley L, Belluoccio D, Kaluarachchi K, et-al. (2011). Mutations in TRPV4 cause an inherited arthropathy of hands and feet. Nat Genet 43: 1142-1146.
23. Lee EJ, Shin SH, Chun J, Hyun S, Kim Y, Kang SS, (2010). The modulation of TRPV4 channel activity through its Ser 824 residue phosphorylation by SGK1. Anim Cells Syst 14: 99-114.
24. Li J, Kanju P, Patterson M, Chew W-L, Cho S-H, Gilmour I, et-al. (2011). TRPV4-mediated calcium influx into human bronchial epithelia upon exposure to diesel exhaust particles. Environ Health Perspect 119: 784-793.
25. Liedtke W, Friedman JM, (2003). Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci U S A 100: 13698-13703.
26. Liedtke W, Choe Y, Martí-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.
27. Minke B, Selinger Z, (1996). Role of Drosophila TRP in inositide-mediated Ca2+ entry. Mol Neurobiol 12: 163-180.
28. Montell C, Rubin GM, (1989). Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2: 1313-1323.
29. Moore C, Cevikbas F, Pasolli HA, Chen Y, Kong W, Kempkes C, et-al. (2013). Correction for Moore et-al., UVB radiation generates sunburn pain and affects skin by activating epidermal TRPV4 ion channels and triggering endothelin-1 signaling. Proc. Natl. Acad. Sci. U S A 110: 15502-15502.
30. Ossovskaya VS, Bunnett NW, (2004). Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84: 579-621.
31. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, et-al. (2002). A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
32. Peng H, Lewandrowski U, Müller 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.
33. 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.
34. 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.
35. Ramachandran R, Noorbakhsh F, Defea K, Hollenberg MD, (2012). Targeting proteinase-activated receptors: therapeutic potential and challenges. Nat Rev Drug Discov 11: 69-86.
36. Santos FPS, Kantarjian H, Cortes J, Quintas-Cardama A, (2010). Bafetinib, a dual Bcr-Abl/Lyn tyrosine kinase inhibitor for the potential treatment of leukemia. Curr Opin Investig Drugs 11: 1450-1465.
37. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL, (2004). Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305: 399-401.
38. Sipe WEB, Brierley SM, Martin CM, Phillis BD, Cruz FB, Grady EF, et-al. (2008). Transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol 294: G1288-G1298.
39. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, et-al. (2000). Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6: 151-158.
40. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD, (2000). OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2: 695-702.
41. Suzuki M, Mizuno A, Kodaira K, Imai M, (2003). Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278: 22664-22668.
42. Takeuchi M, Kimura S, Ashihara E, Maekawa T, Castañer R, Bolõs J, (2009). Bafetinib. Dual BCR/ABL and Lyn tyrosine kinase inhibitor treatment of chronic myeloid leukaemia. Drugs Future 34: 261.
43. 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 urin. J Pharmacol Exp Ther 326: 432-442.
44. Veldhuis NA, Lew MJ, Abogadie FC, Poole DP, Jennings EA, Ivanusic JJ, et-al. (2012). N-glycosylation determines ionic permeability and desensitization of the TRPV1 capsaicin receptor. J Biol Chem 287: 21765-21772.
45. Vergnolle N, Bunnett NW, Sharkey KA, Brussee V, Compton SJ, Grady EF, et-al. (2001). Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat Med 7: 821-826.
46. Vincent F, Acevedo A, Nguyen MT, Dourado M, DeFalco J, Gustafson A, et-al. (2009). Identification and characterization of novel TRPV4 modulators. Biochem Biophys Res Commun 389: 490-494.
47. Vogt-Eisele AK, Weber K, Sherkheli MA, Vielhaber G, Panten J, Gisselmann G, et-al. (2007). Monoterpenoid agonists of TRPV3. Br J Pharmacol 151: 530-540.
48. Vriens J, Owsianik G, Janssens A, Voets T, Nilius B, (2007). Determinants of 4 alpha-phorbol sensitivity in transmembrane domains 3 and 4 of the cation channel TRPV4. J Biol Chem 282: 12796-12803.
49. 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.
50. 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.
51. Watanabe H, Vriens J, Prenen J, (2003). Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 4-8.
52. Wegierski T, Lewandrowski U, Müller B, Sickmann A, Walz G, (2009). Tyrosine phosphorylation modulates the activity of TRPV4 in response to defined stimuli. J Biol Chem 284: 2923-2933.
53. Wong F, Schaefer EL, Roop BC, Lamendola JN, Johnson-Seaton D, Shao D, (1989). Proper function of the drosophila trp gene product during pupal development is important for normal visual transduction in the adult. Neuron 3: 81-94.
54. Xu H, Zhao H, Tian W, Yoshida K, Roullet J-B, Cohen DM, (2003). Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J Biol Chem 278: 11520-11527.