Ca2+-activated K+ channel-3.1 blocker TRAM-34 attenuates airway remodeling and eosinophilia in a murine asthma model

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 2, 2013, Pages 212-219

  Girodet, Pierre Olivier ^a,b   Ozier, Annaig ^a,b   Carvalho, Gabrielle ^a   Ilina, Olga ^a   Ousova, Olga ^a   Gadeau, Alain Pierre ^a   Begueret, Hugues ^b   Wulff, Heike ^c   Marthan, Roger ^a,b   Bradding, Peter ^d   Berger, Patrick ^a,b  

^a CENTRE DE RECHERCHE CARDIO THORACIQUE DE BORDEAUX   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Asthma; Ion channel; KCa3.1; Remodeling; Smooth muscle

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; CALCIUM ACTIVATED POTASSIUM CHANNEL;

AIRWAY REMODELING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; EOSINOPHILIA; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG LAVAGE; MAST CELL; MOUSE; NONHUMAN; PLETHYSMOGRAPHY;

AIRWAY REMODELING; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; PYRAZOLES;

EID: 84873357122     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0103OC     Document Type: Article

References (48)

1. Jeffery PK. Remodeling in asthma and chronic obstructive lung disease. Am J Respir Crit Care Med 2001;164:S28-S38.
2. Girodet PO, Ozier A, Bara I, Tunon de Lara JM, Marthan R, Berger P. Airway remodeling in asthma: new mechanisms and potential for pharmacological intervention. Pharmacol Ther 2011;130:325-337.
3. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745.
4. Pepe C, Foley S, Shannon J, Lemiere C, Olivenstein R, Ernst P, Ludwig MS, Martin JG, Hamid Q. Differences in airway remodeling between subjects with severe and moderate asthma. J Allergy Clin Immunol 2005;116:544-549.
5. Kaminska M, Foley S, Maghni K, Storness-Bliss C, Coxson H, Ghezzo H, Lemiere C, Olivenstein R, Ernst P, Hamid Q, et al. Airway remodeling in subjects with severe asthma with or without chronic persistent airflow obstruction. J Allergy Clin Immunol 2009;124:45-51.
6. Roth M, Johnson PR, Borger P, Bihl MP, Rudiger JJ, King GG, Ge Q, Hostettler K, Burgess JK, Black JL, et al. Dysfunctional interaction of c/EBPalpha and the glucocorticoid receptor in asthmatic bronchial smooth-muscle cells. N Engl J Med 2004;351:560-574.
7. Bara I, Ozier A, Tunon de Lara JM, Marthan R, Berger P. Pathophysiology of bronchial smooth muscle remodelling in asthma. Eur Respir J 2010;36:1174-1184.
8. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID. Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 2002;346:1699-1705.
9. Berger P, Girodet PO, Begueret H, Ousova O, Perng DW, Marthan R, Walls AF, Tunon de Lara JM. Tryptase-stimulated human airway smooth muscle cells induce cytokine synthesis and mast cell chemotaxis. FASEB J 2003;17:2139-2141.
10. Brightling CE, Ammit AJ, Kaur D, Black JL, Wardlaw AJ, Hughes JM, Bradding P. The CXCL10/CXCR3 axis mediates human lung mast cell migration to asthmatic airway smooth muscle. Am J Respir Crit Care Med 2005;171:1103-1108.
11. El-Shazly A, Berger P, Girodet PO, Ousova O, Fayon M, Vernejoux JM, Marthan R, Tunon-de-Lara JM. Fraktalkine produced by airway smooth muscle cells contributes to mast cell recruitment in asthma. J Immunol 2006;176:1860-1868.
12. Begueret H, Berger P, Vernejoux JM, Dubuisson L, Marthan R, Tunon-de-Lara JM. Inflammation of bronchial smooth muscle in allergic asthma. Thorax 2007;62:8-15.
13. Yang W, Kaur D, Okayama Y, Ito A, Wardlaw AJ, Brightling CE, Bradding P. Human lung mast cells adhere to human airway smooth muscle, in part, via tumor suppressor in lung cancer-1. J Immunol 2006;176:1238-1243.
14. Girodet PO, Ozier A, Trian T, Begueret H, Ousova O, Vernejoux JM, Chanez P, Marthan R, Berger P, Tunon de Lara JM. Mast cell adhesion to bronchial smooth muscle in asthma specifically depends on CD51 and CD44 variant 6. Allergy 2010;65:1004-1012.
15. Woodman L, Siddiqui S, Cruse G, Sutcliffe A, Saunders R, Kaur D, Bradding P, Brightling C. Mast cells promote airway smooth muscle cell differentiation via autocrine up-regulation of TGF-beta 1. J Immunol 2008;181:5001-5007.
16. 1 cell compartments in asthma. Am J Respir Crit Care Med 2010;182:317-324.
17. Johnson PR, Roth M, Tamm M, Hughes M, Ge Q, King G, Burgess JK, Black JL. Airway smooth muscle cell proliferation is increased in asthma. Am J Respir Crit Care Med 2001;164:474-477.
18. Trian T, Benard G, Begueret H, Rossignol R, Girodet PO, Ghosh D, Ousova O, Vernejoux JM, Marthan R, Tunon-de-Lara JM, et al. Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med 2007;204: 3173-3181.
19. 2+ ATPase (SERCA) expression contributes to airway remodelling in bronchial asthma. Proc Natl Acad Sci USA 2009;106:10775-10780.
20. McCann JD, Welsh MJ. Calcium-activated potassium channels in canine airway smooth muscle. J Physiol 1986;372:113-127.
21. Marthan R, Martin C, Amédée T, Mironneau J. Calcium channel currents in isolated smooth muscle cells from human bronchus. J Appl Physiol 1989;66:1706-1714.
22. + channels K(Ca)3.1 and K(V)1.3 as novel targets for asthma therapy. Br J Pharmacol 2009;157:1330-1339.
23. Devor DC, Singh AK, Lambert LC, DeLuca A, Frizzell RA, Bridges RJ. Bicarbonate and chloride secretion in CALU-3 human airway epithelial cells. J Gen Physiol 1999;113:743-760.
24. Grunnet M, Rasmussen HB, Hay-Schmidt A, Klaerke DA. The voltagegated potassium channel subunit, KV1.3, is expressed in epithelia. Biochim Biophys Acta 2003;1616:85-94.
25. Pena TL, Rane SG. The fibroblast intermediate conductance K(Ca) channel, FIK, as a prototype for the cell growth regulatory function of the IK channel family. J Membr Biol 1999;172:249-257.
26. 2+ influx and degranulation in human lung mast cells. J Allergy Clin Immunol 2004;114:66-72.
27. + channels regulate human airway smooth muscle proliferation. Am J Respir Cell Mol Biol 2007;37:525-531.
28. + channels are required for human fibrocyte migration. J Allergy Clin Immunol 2011;128:1303-1309.
29. Ca3.1. J Immunol 2008;180:8040-8047.
30. + channels are required for human lung mast cell migration. Thorax 2006;61:880-885.
31. Lederlin M, Ozier A, Montaudon M, Begueret H, Ousova O, Marthan R, Berger P, Laurent F. Airway remodeling in a mouse asthma model assessed by in-vivo respiratory-gated micro-computed tomography. Eur Radiol 2010;20:128-137.
32. Henderson WR Jr, Tang LO, Chu SJ, Tsao SM, Chiang GK, Jones F, Jonas M, Pae C, Wang H, Chi EY. A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am J Respir Crit Care Med 2002;165:108-116.
33. Ca1: a potential immunosuppressant. Proc Natl Acad Sci USA 2000;97:8151-8156.
34. Ca3.1 contributes to atherogenesis in mice and humans. J Clin Invest 2008;118:3025-3037.
35. Lundblad LK, Irvin CG, Adler A, Bates JH. A reevaluation of the validity of unrestrained plethysmography in mice. J Appl Physiol 2002;93:1198-1207.
36. Adler A, Cieslewicz G, Irvin CG. Unrestrained plethysmography is an unreliable measure of airway responsiveness in BALB/c and C57BL/6 mice. J Appl Physiol 2004;97:286-292.
37. Mionnet C, Buatois V, Kanda A, Milcent V, Fleury S, Lair D, Langelot M, Lacoeuille Y, Hessel E, Coffman R, et al. CX3CR1 is required for airway inflammation by promoting T helper cell survival and maintenance in inflamed lung. Nat Med 2010;16:1305-1312.
38. Takeda K, Hamelmann E, Joetham A, Shultz LD, Larsen GL, Irvin CG, Gelfand EW. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J Exp Med 1997;186:449-454.
39. Johnson JR, Pacitto SR, Wong J, Archer EW, Eirefelt S, Miller-Larsson A, Jordana M. Combined budesonide/formoterol therapy in conjunction with allergen avoidance ameliorates house dust mite-induced airway remodeling and dysfunction. Am J Physiol Lung Cell Mol Physiol 2008;295:L780-L788.
40. Woodruff PG, Dolganov GM, Ferrando RE, Donnelly S, Hays SR, Solberg OD, Carter R, Wong HH, Cadbury PS, Fahy JV. Hyperplasia of smooth muscle in mild to moderate asthma without changes in cell size or gene expression. Am J Respir Crit Care Med 2004;169:1001-1006.
41. Siddiqui S, Mistry V, Doe C, Roach K, Morgan A, Wardlaw A, Pavord I, Bradding P, Brightling C. Airway hyperresponsiveness is dissociated from airway wall structural remodeling. J Allergy Clin Immunol 2008; 122:335-341.
42. Berry M, Morgan A, Shaw DE, Parker D, Green R, Brightling C, Bradding P, Wardlaw AJ, Pavord ID. Pathological features and inhaled corticosteroid response of eosinophilic and non-eosinophilic asthma. Thorax 2007;62:1043-1049.
43. Flood-Page P, Menzies-Gow A, Phipps S, Ying S, Wangoo A, Ludwig MS, Barnes N, Robinson D, Kay AB. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 2003;112:1029-1036.
44. Ca3.1 potassium channels. Proc Natl Acad Sci USA 2009;106:14518-14523.
45. Ca3.1 blocker TRAM-34 reduces infarction and neurological deficit in a rat model of ischemia/reperfusion stroke. J Cereb Blood Flow Metab 2011;31:2363-2374.
46. Haldar P, Brightling CE, Hargadon B, Gupta S, Monteiro W, Sousa A, Marshall RP, Bradding P, Green RH, Wardlaw AJ, et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 2009;360:973-984.
47. Ataga KI, Smith WR, De Castro LM, Swerdlow P, Saunthararajah Y, Castro O, Vichinsky E, Kutlar A, Orringer EP, Rigdon GC, et al. Efficacy and safety of the gardos channel blocker, senicapoc (ICA-17043), in patients with sickle cell anemia. Blood 2008;111:3991-3997.
48. Ataga KI, Reid M, Ballas SK, Yasin Z, Bigelow C, James LS, Smith WR, Galacteros F, Kutlar A, Hull JH, et al. Improvements in haemolysis and indicators of erythrocyte survival do not correlate with acute vaso-occlusive crises in patients with sickle cell disease: a Phase III randomized, placebo-controlled, double-blind study of the gardos channel blocker senicapoc (ICA-17043). Br J Haematol 2011;153: 92-104.