Role of transient receptor potential vanilloid 4 in neutrophil activation and acute lung injury

American Journal of Respiratory Cell and Molecular Biology

Volumn 54, Issue 3, 2016, Pages 370-383

  Yin, Jun ^a,b   Michalick, Laura ^c   Tang, Christine ^b,d   Tabuchi, Arata ^b   Goldenberg, Neil ^b   Dan, Qinghong ^b   Awwad, Khader ^e   Wang, Liming ^a,b   Erfinanda, Lasti ^c   Nouailles, Geraldine ^c   Witzenrath, Martin ^c   Vogelzang, Alexis ^f   Lv, Lu ^a   Lee, Warren L ^b   Zhang, Haibo ^b   Rotstein, Ori ^b,d   Kapus, Andras ^b,d   Szaszi, Katalin ^b,d   Fleming, Ingrid ^e   Liedtke, Wolfgang B ^g   Kuppe, Hermann ^h   Kuebler, Wolfgang M ^b,c,d,h   more..

^a AFFILIATED PEOPLE S HOSPITAL OF JIANGSU UNIVERSITY   (China)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

^e GOETHE UNIVERSITY   (Germany)

^f MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

^h DEUTSCHES HERZZENTRUM BERLIN   (Germany)

Author keywords

Acute lung injury; Calcium; Neutrophil; Reactive oxygen sepsis; Transient receptor potential vanilloid 4

Indexed keywords

CALCIUM ION; EPOXYICOSATRIENOIC ACID; GSK 2193874; HC 067047; HYDROCHLORIC ACID; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOPEROXIDASE; RAC PROTEIN; RANTES; REACTIVE OXYGEN METABOLITE; RECEPTOR BLOCKING AGENT; THROMBOCYTE ACTIVATING FACTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 4; HC-067047; MORPHOLINE DERIVATIVE; PYRROLE DERIVATIVE; TRPV4 PROTEIN, HUMAN; TRPV4 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BLOOD VESSEL PERMEABILITY; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRAVASATION; GENOTYPE; HISTOLOGY; IN VIVO STUDY; INFLAMMATION; ISOLATED LUNG; LEUKOCYTE ACTIVATION; LEUKOCYTE ADHERENCE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROPHYLAXIS; PROTECTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE MARROW TRANSPLANTATION; CALCIUM SIGNALING; CAPILLARY PERMEABILITY; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HUMAN; KNOCKOUT MOUSE; LUNG; LUNG EDEMA; METABOLISM; NEUTROPHIL; PNEUMONIA; VASCULARIZATION;

ACUTE LUNG INJURY; ANIMALS; BONE MARROW TRANSPLANTATION; CALCIUM SIGNALING; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; HUMANS; HYDROCHLORIC ACID; LUNG; MALE; MICE, KNOCKOUT; MORPHOLINES; NEUTROPHIL ACTIVATION; NEUTROPHILS; PNEUMONIA; PULMONARY EDEMA; PYRROLES; TRPV CATION CHANNELS;

EID: 84963830297     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0225OC     Document Type: Article

References (50)

1. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, Camporota L, Slutsky AS; ARDS Definition Task Force. Acute respiratory distress syndrome: The Berlin definition. JAMA 2012;307:2526-2533.
2. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 2005;353:1685-1693.
3. Diaz JV, Brower R, Calfee CS, Matthay MA. Therapeutic strategies for severe acute lung injury. Crit Care Med 2010;38:1644-1650.
4. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 2000;342:1301-1308.
5. Guérin C, Reignier J, Richard JC, Beuret P, Gacouin A, Boulain T, Mercier E, Badet M, Mercat A, Baudin O, et al.; PROSEVA Study Group. Prone positioning in severe acute respiratory distress syndrome. N Engl J Med 2013;368:2159-2168.
6. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349.
7. Yin J, Kuebler WM. Mechanotransduction by TRP channels: general concepts and specific role in the vasculature. Cell Biochem Biophys 2010;56:1-18.
8. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI. 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.
9. Damann N, Owsianik G, Li S, Poll C, Nilius B. The calcium-conducting ion channel transient receptor potential canonical 6 is involved in macrophage inflammatory protein-2-induced migration of mouse neutrophils. Acta Physiol (Oxf) 2009;195:3-11.
10. Hamanaka K, Jian MY, Townsley MI, King JA, Liedtke W, Weber DS, Eyal FG, Clapp MM, Parker JC. TRPV4 channels augment macrophage activation and ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 2010;299:L353-L362.
11. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 2003;424:434-438.
12. Jian MY, King JA, Al-Mehdi AB, Liedtke W, Townsley MI. High vascular pressure-induced lung injury requires P450 epoxygenasedependent activation of TRPV4. Am J Respir Cell Mol Biol 2008;38: 386-392.
13. Yin J, Hoffmann J, Kaestle SM, Neye N, Wang L, Baeurle J, Liedtke W, Wu S, Kuppe H, Pries AR, et al. Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4. Circ Res 2008;102:966-974.
14. Spinsanti G, Zannolli R, Panti C, Ceccarelli I, Marsili L, Bachiocco V, Frati F, Aloisi AM. Quantitative Real-Time PCR detection of TRPV1-4 gene expression in human leukocytes from healthy and hyposensitive subjects. Mol Pain 2008;4:51.
15. Link TM, Park U, Vonakis BM, Raben DM, Soloski MJ, Caterina MJ. TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat Immunol 2010;11:232-239.
16. Michalick L, Mertens M, Liedtke W, Kuebler WM.Transient receptor potential cation channel vanilloid (TRPV) 4 in ventilator-induced lung injury (VILI) [abstract]. FASEB J 2013;27:914.12.
17. Luo Y, Dorf ME. Isolation of mouse neutrophils. Curr Protoc Immunol 2001;Chapter 3:Unit 3.20.
18. Malam Z, Parodo J, Waheed F, Szaszi K, Kapus A, Marshall JC. Pre-B cell colony-enhancing factor (PBEF/Nampt/visfatin) primes neutrophils for augmented respiratory burst activity through partial assembly of the NADPH oxidase. J Immunol 2011;186: 6474-6484.
19. Waheed F, Dan Q, Amoozadeh Y, Zhang Y, Tanimura S, Speight P, Kapus A, Szászi K. Central role of the exchange factor GEF-H1 in TNF-a-induced sequential activation of Rac, ADAM17/TACE, and RhoA in tubular epithelial cells. Mol Biol Cell 2013;24: 1068-1082.
20. Frömel T, Jungblut B, Hu J, Trouvain C, Barbosa-Sicard E, Popp R, Liebner S, Dimmeler S, Hammock BD, Fleming I. Soluble epoxide hydrolase regulates hematopoietic progenitor cell function via generation of fatty acid diols. Proc Natl Acad Sci USA 2012;109: 9995-10000.
21. Balakrishna S, Song W, Achanta S, Doran SF, Liu B, Kaelberer MM, Yu Z, Sui A, Cheung M, Leishman E, et al. TRPV4 inhibition counteracts edema and inflammation and improves pulmonary function and oxygen saturation in chemically induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 2014;307:L158-L172.
22. Samapati R, Yang Y, Yin J, Stoerger C, Arenz C, Dietrich A, Gudermann T, Adam D, Wu S, Freichel M, et al. Lung endothelial Ca21 and permeability response to platelet-activating factor is mediated by acid sphingomyelinase and transient receptor potential classical 6. Am J Respir Crit Care Med 2012;185:160-170.
23. Stephens CJ, Graham RM, Yadava OP, Leong LL, Sturm MJ, Taylor RR. Plasma platelet activating factor degradation and serum lipids after coronary bypass surgery. Cardiovasc Res 1992;26: 25-31.
24. Futosi K, Fodor S, Mócsai A. Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol 2013;17:638-650.
25. Everaerts W, Zhen X, Ghosh D, Vriens J, Gevaert T, Gilbert JP, Hayward NJ, McNamara CR, Xue F, Moran MM, et al. Inhibition of the cation channel TRPV4 improves bladder function in mice and rats with cyclophosphamide-induced cystitis. Proc Natl Acad Sci USA 2010;107:19084-19089.
26. Vriens J, Owsianik G, Fisslthaler B, Suzuki M, Janssens A, Voets T, Morisseau C, Hammock BD, Fleming I, Busse R, et al. Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 2005;97: 908-915.
27. Kao YY, Gianni D, Bohl B, Taylor RM, Bokoch GM. Identification of a conserved Rac-binding site on NADPH oxidases supports a direct GTPase regulatory mechanism. J Biol Chem 2008;283: 12736-12746.
28. D'Souza-Schorey C, Boettner B, Van Aelst L. Rac regulates integrinmediated spreading and increased adhesion of T lymphocytes. Mol Cell Biol 1998;18:3936-3946.
29. Kuiper JW, Sun C, Magalhães MA, Glogauer M. Rac regulates PtdInsP3 signaling and the chemotactic compass through a redox-mediated feedback loop. Blood 2011;118:6164-6171.
30. Price LS, Langeslag M, ten Klooster JP, Hordijk PL, Jalink K, Collard JG. Calcium signaling regulates translocation and activation of Rac. J Biol Chem 2003;278:39413-39421.
31. Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2008;295: L379-L399.
32. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM; Acute Lung Injury in Animals Study Group. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol 2011;44:725-738.
33. Uhlig S, Goggel R, Engel S. Mechanisms of platelet-activating factor (PAF)-mediated responses in the lung. Pharmacol Rep 2005;57 (suppl):206-221.
34. Uhlig S, Yang Y, Waade J, Wittenberg C, Babendreyer A, Kuebler WM. Differential regulation of lung endothelial permeability in vitro and in situ. Cell Physiol Biochem 2014;34:1-19.
35. Garcia-Elias A, Mrkonjić S, Jung C, Pardo-Pastor C, Vicente R, Valverde MA. The TRPV4 channel. Handbook Exp Pharmacol 2014;222:293-319.
36. Nilius B, Owsianik G. Channelopathies converge on TRPV4. Nat Genet 2010;42:98-100.
37. Morty RE, Kuebler WM. TRPV4: An exciting new target to promote alveolocapillary barrier function. Am J Physiol Lung Cell Mol Physiol 2014;307:L817-L821.
38. Thorneloe KS, Cheung M, Bao W, Alsaid H, Lenhard S, Jian MY, Costell M, Maniscalco-Hauk K, Krawiec JA, Olzinski A, et al. An orally active trpv4 channel blocker prevents and resolves pulmonary edema induced by heart failure. Science Transl Med 2012;4:159ra148.
39. Wu S, Jian MY, Xu YC, Zhou C, Al-Mehdi AB, Liedtke W, Shin HS, Townsley MI. Ca21 entry via alpha1G and TRPV4 channels differentially regulates surface expression of P-selectin and barrier integrity in pulmonary capillary endothelium. Am J Physiol Lung Cell Mol Physiol 2009;297:L650-L657.
40. Looney MR, Su X, Van Ziffle JA, Lowell CA, Matthay MA. Neutrophils and their Fc gamma receptors are essential in a mouse model of transfusion-related acute lung injury. J Clin Invest 2006;116: 1615-1623.
41. Till GO, Johnson KJ, Kunkel R, Ward PA. Intravascular activation of complement and acute lung injury: dependency on neutrophils and toxic oxygen metabolites. J Clin Invest 1982;69:1126-1135.
42. Hauser CJ, Fekete Z, Adams JM, Garced M, Livingston DH, Deitch EA. PAF-mediated Ca21 influx in human neutrophils occurs via storeoperated mechanisms. J Leukoc Biol 2001;69:63-68.
43. Goldenberg NM, Wang L, Ranke H, Liedtke W, Tabuchi A, Kuebler WM. TRPV4 is required for hypoxic pulmonary vasoconstriction. Anesthesiology 2015;122:1338-1348.
44. Zhu Y, Schieber EB, McGiff JC, Balazy M. Identification of arachidonate P-450 metabolites in human platelet phospholipids. Hypertension 1995;25:854-859.
45. Montero M, Garcia-Sancho J, Alvarez J. Comparative effects of cytochrome P-450 inhibitors on Ca21 and Mn21 entry induced by agonists or by emptying the Ca21 stores of human neutrophils. Biochim Biophys Acta 1993;1177:127-133.
46. Garcia-Elias A, Lorenzo IM, Vicente R, Valverde MA. IP3 receptor binds to and sensitizes TRPV4 channel to osmotic stimuli via a calmodulinbinding site. J Biol Chem 2008;283:31284-31288.
47. Yao HY, Chen L, Xu C, Wang J, Chen J, Xie QM, Wu X, Yan XF. Inhibition of Rac activity alleviates lipopolysaccharide-induced acute pulmonary injury in mice. Biochimt Biophys Acta 2011;1810:666-674.
48. Fichna J, Mokrowiecka A, Cygankiewicz AI, Zakrzewski PK, Malecka- Panas E, Janecka A, Krajewska WM, Storr MA. Transient receptor potential vanilloid 4 blockade protects against experimental colitis in mice: A new strategy for inflammatory bowel diseases treatment? Neurogastroenterol Motil 2012;24:e557-e560.
49. Denadai-Souza A, Martin L, de Paula MA, de Avellar MC, Muscará MN, Vergnolle N, Cenac N. Role of transient receptor potential vanilloid 4 in rat joint inflammation. Arthritis Rheum 2012;64:1848-1858.
50. Tintinger GR, Steel HC, Theron AJ, Anderson R. Pharmacological control of neutrophil-mediated inflammation: strategies targeting calcium handling by activated polymorphonuclear leukocytes. Drug Des Devel Ther 2009;2:95-104.