TRPV4 inhibition counteracts edema and inflammation and improves pulmonary function and oxygen saturation in chemically induced acute lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 2, 2014, Pages

  Balakrishna, Shrilatha ^a   Song, Weifeng ^b   Achanta, Satyanarayana ^a   Doran, Stephen F ^b   Liu, Boyi ^a   Kaelberer, Melanie M ^a   Yu, Zhihong ^b   Sui, Aiwei ^a   Cheung, Mui ^c   Leishman, Emma ^d   Eidam, Hilary S ^c   Ye, Guosen ^c   Willette, Robert N ^c   Thorneloe, Kevin S ^c   Bradshaw, Heather B ^d   Matalon, Sadis ^b   Jordt, Sven Eric ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c GLAXOSMITHKLINE   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Acute lung injury; Chlorine; TRPV4

Indexed keywords

ACUTE LUNG INJURY; CHLORINE; TRPV4;

ACUTE LUNG INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS; BRONCHOALVEOLAR LAVAGE FLUID; CHLORINE; HEK293 CELLS; HUMANS; HYDROCHLORIC ACID; MALE; MICE; PNEUMONIA; RATS; TRPV CATION CHANNELS;

EID: 84904359102     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00065.2014     Document Type: Article

References (42)

1. 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 99: 988-995, 2006.
2. Becker M, Forrester M. Pattern of chlorine gas exposures reported to Texas poison control centers, 2000 through 2005. Tex Med 104: 52-57, 51, 2008.
3. Bessac BF, Jordt SE. Sensory detection and responses to toxic gases: mechanisms, health effects, and countermeasures. Proc Am Thorac Soc 7: 269-277, 2010.
4. Bessac BF, Sivula M, von Hehn CA, Escalera J, Cohn L, Jordt SE. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J Clin Invest 118: 1899-1910, 2008.
5. Bice T, Li G, Malinchoc M, Lee AS, Gajic O. Incidence and risk factors of recurrent acute lung injury. Crit Care Med 39: 1069-1073, 2011.
6. Bradshaw HB, Raboune S, Hollis JL. Opportunistic activation of TRP receptors by endogenous lipids: exploiting lipidomics to understand TRP receptor cellular communication. Life Sci 92: 404-409, 2013.
7. Bradshaw HB, Rimmerman N, Hu SS, Burstein S, Walker JM. Novel endogenous N-acyl glycines identification and characterization. Vitam Horm 81: 191-205, 2009.
8. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D'Amours M, Witek JS, Fanger CM, Chong JA, Hayward NJ, Homer RJ, Cohn L, Huang X, Moran MM, Jordt SE. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci USA 106: 9099-9104, 2009.
9. Catravas JD, Snead C, Dimitropoulou C, Chang AS, Lucas R, Verin AD, Black SM. Harvesting, identification and barrier function of human lung microvascular endothelial cells. Vascul Pharmacol 52: 175-181, 2010.
10. + channel blockers reduce functional bladder capacity in the conscious spontaneously hypertensive rat. Urology 79: 1410. e1-e6, 2012.
11. Dries DJ, Endorf FW. Inhalation injury: epidemiology, pathology, treatment strategies. Scand J Trauma Resusc Emerg Med 21: 31, 2013.
12. 2+ release in astrocytic endfeet and amplify neurovascular coupling responses. Proc Natl Acad Sci USA 110: 6157-6162, 2013.
13. Germann PG, Hafner D. A rat model of acute respiratory distress syndrome (ARDS): part 1. Time dependency of histological and pathological changes. J Pharmacol Toxicol Methods 40: 101-107, 1998.
14. Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol Med 17: 293-307, 2011.
15. Groot-Kormelink PJ, Fawcett L, Wright PD, Gosling M, Kent TC. Quantitative GPCR and ion channel transcriptomics in primary alveolar macrophages and macrophage surrogates. BMC Immunol 13: 57, 2012.
16. 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 299: L353-L362, 2010.
17. Hamanaka K, Jian MY, Weber DS, Alvarez DF, Townsley MI, Al-Mehdi AB, King JA, Liedtke W, Parker JC. TRPV4 initiates the acute calcium-dependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol Lung Cell Mol Physiol 293: L923-L932, 2007.
18. Heiner I, Eisfeld J, Halaszovich CR, Wehage E, Jungling E, Zitt C, Luckhoff A. Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem J 371: 1045-1053, 2003.
19. Honavar J, Samal AA, Bradley KM, Brandon A, Balanay J, Squadrito GL, MohanKumar K, Maheshwari A, Postlethwait EM, Matalon S, Patel RP. Chlorine gas exposure causes systemic endothelial dysfunction by inhibiting endothelial nitric oxide synthase-dependent signaling. Am J Respir Cell Mol Biol 45: 419-425, 2011.
20. Huh D, Leslie DC, Matthews BD, Fraser JP, Jurek S, Hamilton GA, Thorneloe KS, McAlexander MA, Ingber DE. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci Transl Med 4: 159ra147, 2012.
21. Jian MY, King JA, Al-Mehdi AB, Liedtke W, Townsley MI. High vascular pressure-induced lung injury requires P450 epoxygenase-dependent activation of TRPV4. Am J Respir Cell Mol Biol 38: 386-392, 2008.
22. Johnston LK, Rims CR, Gill SE, McGuire JK, Manicone AM. Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol 47: 417-426, 2012.
23. Jonasson S, Wigenstam E, Koch B, Bucht A. Early treatment of chlorine-induced airway hyperresponsiveness and inflammation with corticosteroids. Toxicol Appl Pharmacol 271: 168-174, 2013.
24. Jordt SE, Tominaga M, Julius D. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA 97: 8134-8139, 2000.
25. Li J, Kanju P, Patterson M, Chew WL, Cho SH, Gilmour I, Oliver T, Yasuda R, Ghio A, Simon SA, Liedtke W. TRPV4-mediated calcium influx into human bronchial epithelia upon exposure to diesel exhaust particles. Environ Health Perspect 119: 784-793, 2011.
26. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535, 2000.
27. Lorenzo IM, Liedtke W, Sanderson MJ, Valverde MA. TRPV4 channel participates in receptor-operated calcium entry and ciliary beat frequency regulation in mouse airway epithelial cells. Proc Natl Acad Sci USA 105: 12611-12616, 2008.
28. Luhr OR, Antonsen K, Karlsson M, Aardal S, Thorsteinsson A, Frostell CG, Bonde J. Incidence and mortality after acute respiratory failure and acute respiratory distress syndrome in Sweden, Denmark, and Iceland. The ARF Study Group. Am J Respir Crit Care Med 159: 1849-1861, 1999.
29. Saghatelian A, McKinney MK, Bandell M, Patapoutian A, Cravatt BF. A FAAH-regulated class of N-acyl taurines that activates TRP ion channels. Biochemistry 45: 9007-9015, 2006.
30. Smoum R, Bar A, Tan B, Milman G, Attar-Namdar M, Ofek O, Stuart JM, Bajayo A, Tam J, Kram V, O'Dell D, Walker MJ, Bradshaw HB, Bab I, Mechoulam R. Oleoyl serine, an endogenous N-acyl amide, modulates bone remodeling and mass. Proc Natl Acad Sci USA 107: 17710-17715, 2010.
31. Song W, Wei S, Liu G, Yu Z, Estell K, Yadav AK, Schwiebert LM, Matalon S. Postexposure administration of a β2-agonist decreases chlorine-induced airway hyperreactivity in mice. Am J Respir Cell Mol Biol 45: 88-94, 2011.
32. 2+ signals through endothelial TRPV4 channels regulate vascular function. Science 336: 597-601, 2012.
33. Thorneloe KS, Cheung M, Bao W, Alsaid H, Lenhard S, Jian MY, Costell M, Maniscalco-Hauk K, Krawiec JA, Olzinski A, Gordon E, Lozinskaya I, Elefante L, Qin P, Matasic DS, James C, Tunstead J, Donovan B, Kallal L, Waszkiewicz A, Vaidya K, Davenport EA, Larkin J, Burgert M, Casillas LN, Marquis RW, Ye G, Eidam HS, Goodman KB, Toomey JR, Roethke TJ, Jucker BM, Schnackenberg CG, Townsley MI, Lepore JJ, Willette RN. An orally active TRPV4 channel blocker prevents and resolves pulmonary edema induced by heart failure. Sci Transl Med 4: 159ra148, 2012.
34. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111, 2009.
35. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578, 2012.
36. Van Sickle D, Wenck MA, Belflower A, Drociuk D, Ferdinands J, Holguin F, Svendsen E, Bretous L, Jankelevich S, Gibson JJ, Garbe P, Moolenaar RL. Acute health effects after exposure to chlorine gas released after a train derailment. Am J Emerg Med 27: 1-7, 2009.
37. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
38. White CW, Martin JG. Chlorine gas inhalation: human clinical evidence of toxicity and experience in animal models. Proc Am Thorac Soc 7: 257-263, 2010.
39. Willette RN, Bao W, Nerurkar S, Yue TL, Doe CP, Stankus G, Turner GH, Ju H, Thomas H, Fishman CE, Sulpizio A, Behm DJ, Hoffman S, Lin Z, Lozinskaya I, Casillas LN, Lin M, Trout RE, Votta BJ, Thorneloe K, Lashinger ES, Figueroa DJ, Marquis R, Xu X. 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, 2008.
40. Wright HL, Thomas HB, Moots RJ, Edwards SW. RNA-seq reveals activation of both common and cytokine-specific pathways following neutrophil priming. PLoS One 8: e58598, 2013.
41. Yadav AK, Bracher A, Doran SF, Leustik M, Squadrito GL, Postlethwait EM, Matalon S. Mechanisms and modification of chlorine-induced lung injury in animals. Proc Am Thorac Soc 7: 278-283, 2010.
42. Yang XR, Lin AH, Hughes JM, Flavahan NA, Cao YN, Liedtke W, Sham JS. Upregulation of osmo-mechanosensitive TRPV4 channel facilitates chronic hypoxia-induced myogenic tone and pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 302: L555-L568, 2012.