The K+ channel KCa3.1 as a novel target for idiopathic pulmonary fibrosis

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Roach, Katy Morgan ^a   Duffy, Stephen Mark ^a   Coward, William ^b   Feghali Bostwick, Carol ^c   Wulff, Heike ^d   Bradding, Peter ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ACTIVATED POTASSIUM CHANNEL K CA 3.1; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CURRENT; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ELECTROPHYSIOLOGY; FEMALE; FIBROSING ALVEOLITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; LUNG PARENCHYMA; MALE; MOLECULAR PATHOLOGY; MYOFIBROBLAST; PATCH CLAMP TECHNIQUE; POTASSIUM CURRENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; WOUND HEALING;

EID: 84894087084     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085244     Document Type: Article

References (40)

1. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J et al. (2011) An official ATS/ERS/JRS/ALAT statement: Idiopathic pulmonary fibrosis: Evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 183: 788-824. doi:10.1164/rccm.2009-040GL. PubMed: 21471066.
2. Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G (2006) Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 174: 810-816. doi:10.1164/rccm.200602-163OC. PubMed: 16809633. (Pubitemid 44511663)
3. Gribbin J, Hubbard RB, Le Jeune I, Smith CJ, West J et al. (2006) Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax 61: 980-985. doi:10.1136/thx.2006.062836. PubMed: 16844727. (Pubitemid 44787169)
4. Strieter RM (2005) Pathogenesis and natural history of usual interstitial pneumonia: The whole story or the last chapter of a long novel. Chest 128: 526S-532S. doi:10.1378/chest.128.5-suppl-1.526S. PubMed: 16304243.
5. Grinnell F (1994) Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 124: 401-404. doi:10.1083/jcb.124.4.401. PubMed: 8106541.
6. McAnulty RJ (2007) Fibroblasts and myofibroblasts: Their source, function and role in disease. Int J Biochem Cell Biol 39: 666-671. doi:10.1016/j.biocel. 2006.11.005. PubMed: 17196874.
7. Phan SH (2002) The myofibroblast in pulmonary fibrosis. Chest 122: 286S-289S. doi:10.1378/chest.122.6-suppl.286S. PubMed: 12475801.
8. Fanger CM, Rauer H, Neben AL, Miller MJ, Rauer H et al. (2001) Calcium-activated potassium channels sustain calcium signaling in T lymphocytes - selective blockers and manipulated channel expression levels. J Biol Chem 276: 12249-12256. doi:10.1074/jbc.M011342200. PubMed: 11278890.
9. Ghanshani S, Wulff H, Miller MJ, Rohm H, Neben A et al. (2000) Up-regulation of the IKCa1 potassium channel during T-cell activation. molecular mechanism and functional consequences. J Biol Chem 275: 37137-37149. doi:10.1074/jbc.M003941200. PubMed: 10961988. (Pubitemid 32002132)
10. Cruse G, Duffy SM, Brightling CE, Bradding P (2006) Functional KCa3.1 K+ channels are required for human lung mast cell migration. Thorax 61: 880-885. doi:10.1136/thx.2006.060319. PubMed: 16809411. (Pubitemid 44570309)
11. Shepherd MC, Duffy SM, Harris T, Cruse G, Schuliga M et al. (2007) K(ca)3.1 Ca2+-activated K+ channels regulate human airway smooth muscle proliferation. Am J Respir Cell Mol Biol 37: 525-531. doi:10.1165/rcmb.2006- 0358OC. PubMed: 17585114. (Pubitemid 350058183)
12. Duffy S, Berger P, Cruse G, Yang W, Bolton SJ et al. (2004) The K+ channel iKCA1 potentiates Ca2+ influx and degranulation in human lung mast cells. J Allergy Clin Immunol 114: 66-72. doi:10.1016/j.jaci.2004.04.005. PubMed: 15241346. (Pubitemid 39005119)
13. Grgic I, Kiss E, Kaistha BP, Busch C, Kloss M et al. (2009) Renal fibrosis is attenuated by targeted disruption of KCa3.1 potassium channels. Proc Natl Acad Sci U S A 106: 14518-14523. doi:10.1073/pnas.0903458106. PubMed: 19706538.
14. Keira SM, Ferreira LM, Gragnani A, Duarte Ids Santos, Anunciação Isabel Neves dos (2004) Experimental model for fibroblast culture. Acta Cirurgica Bras 19: 11-16.
15. Pilewski JM, Liu LX, Henry AC, Knauer AV, Feghali-Bostwick CA (2005) Insulin-like growth factor binding proteins 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am J Pathol 166: 399-407. doi:10.1016/S0002-9440(10)62263-8. PubMed: 15681824. (Pubitemid 40189037)
16. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391: 85-100. doi:10.1007/BF00656997. PubMed: 6270629. (Pubitemid 11012976)
17. Duffy SM, Lawley WJ, Conley EC, Bradding P (2001) Resting and activation-dependent ion channels in human mast cells. J Immunol 167: 4261-4270. PubMed: 11591748. (Pubitemid 32954300)
18. Wulff H, Miller MJ, Hansel W, Grissmer S, Cahalan MD et al. (2000) Design of a potent and selective inhibitor of the intermediate-conductance Ca2+-activated K+ channel, IKCa1: A potential immunosuppressant. Proc Natl Acad Sci U S A 97: 8151-8156. doi:10.1073/pnas.97.14.8151. PubMed: 10884437. (Pubitemid 30460788)
19. Stocker JW, De Franceschi L, McNaughton-Smith GA, Corrocher R, Beuzard Y et al. (2003) ICA-17043, a novel gardos channel blocker, prevents sickled red blood cell dehydration in vitro and in vivo in SAD mice. Blood 101: 2412-2418. doi:10.1182/blood-2002-05-1433. PubMed: 12433690. (Pubitemid 36302090)
20. Huang M, Sharma S, Zhu LX, Keane MP, Luo J et al. (2002) IL-7 inhibits fibroblast TGF-beta production and signaling in pulmonary fibrosis. J Clin Invest 109: 931-937. doi:10.1172/JCI14685. PubMed: 11927620.
21. Distler JHW, Jüngel A, Huber LC, Schulze-Horsel U, Zwerina J et al. (2007) Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis Rheum 56: 311-322. doi:10.1002/art.22314. PubMed: 17195235. (Pubitemid 46106205)
22. Woodman L, Siddiqui S, Cruse G, Sutcliffe A, Saunders R et al. (2008) Mast cells promote airway smooth muscle cell differentiation via autocrine up-regulation of TGF-β1. Journal of Immunology 181: 5001-5007. PubMed: 18802103.
23. Duffy SM, Lawley WJ, Kaur D, Yang W, Bradding P (2003) Inhibition of human mast cell proliferation and survival by tamoxifen in association with ion channel modulation. J Allergy Clin Immunol 112: 965-972. doi:10.1016/j.jaci. 2003.07.004. PubMed: 14610489. (Pubitemid 37412067)
24. + channels confer distinctive patterns of distribution in human tissues and differential cellular localisation in the colon and corpus cavernosum. Naunyn Schmiedebergs Arch Pharmacol 369: 602-615. doi:10.1007/s00210-004-0934-5. PubMed: 15127180.
25. Ohya S, Niwa S, Yanagi A, Fukuyo Y, Yamamura H et al. (2011) Involvement of dominant-negative spliced variants of the intermediate conductance Ca2+-activated K+ channel, KCa3.1, in immune function of lymphoid cells. J Biol Chem 286: 16940-16952. doi:10.1074/jbc.M110.184192. PubMed: 21345794.
26. Cruse G, Singh SR, Duffy SM, Doe C, Saunders R, et al. (2011) Functional KCa3.1 K+ channels are required for human fibrocyte migration. J Allergy Clin Immunol 128: 1303-1309.e2
27. Pedersen KA, Schrøder RL, Skaaning-Jensen B, Strøbaek D, Olesen SP et al. (1999) Activation of the human intermediate-conductance ca(2+)-activated K(+) channel by 1-ethyl-2-benzimidazolinone is strongly ca(2+)-dependent. Biochim Biophys Acta 1420: 231-240. doi:10.1016/S0005-2736(99) 00110-8. PubMed: 10446306. (Pubitemid 29369034)
28. Köhler R, Wulff H, Eichler I, Kneifel M, Neumann D et al. (2003) Blockade of the intermediate-conductance calcium-activated potassium channel as a new therapeutic strategy for restenosis. Circulation 108: 1119-1125. doi:10.1161/01.CIR.0000086464.04719.DD. PubMed: 12939222. (Pubitemid 37071524)
29. Zhou X, Wu W, Hu H, Milosevic J, Konishi K et al. (2011) Genomic differences distinguish the myofibroblast phenotype of distal lung from airway fibroblasts. Am J Respir Cell Mol Biol.
30. Kotaru C, Schoonover KJ, Trudeau JB, Huynh ML, Zhou X et al. (2006) Regional fibroblast heterogeneity in the lung: Implications for remodeling. Am J Respir Crit Care Med 173: 1208-1215. doi:10.1164/rccm.200508-1218OC. PubMed: 16543551. (Pubitemid 43848390)
31. Koegel H, Kaesler S, Burgstahler R, Werner S, Alzheimer C (2003) Unexpected down-regulation of the hIK1 Ca2+-activated K+ channel by its opener 1-ethyl-2-benzimidazolinone in HaCaT keratinocytes. J Biol Chem 278: 3323-3330. PubMed: 12421833.
32. Bi D, Toyama K, Lemaître V, Takai J, Fan F et al. (2013) The intermediate conductance calcium-activated potassium channel KCa3.1 regulates vascular smooth muscle cell proliferation via controlling calcium-dependent signaling. J Biol Chem 288: 15843-15853. doi:10.1074/jbc.M112.427187. PubMed: 23609438.
33. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM et al. (2003) Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 278: 12384-12389. doi:10.1074/jbc.M208544200. PubMed: 12531888. (Pubitemid 36800223)
34. Raghu G, Masta S, Meyers D, Narayanan AS (1989) Collagen synthesis by normal and fibrotic human lung fibroblasts and the effect of transforming growth factor-beta. Am Rev Respir Dis 140: 95-100. doi:10.1164/ajrccm/140.1.95. PubMed: 2751176. (Pubitemid 19177088)
35. Willis BC, Borok Z (2007) TGF-beta-induced EMT: Mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293: L525-L534. doi:10.1152/ajplung.00163.2007. PubMed: 17631612. (Pubitemid 47358808)
36. Grgic I, Eichler I, Heinau P, Si H, Brakemeier S et al. (2005) Selective blockade of the intermediate-conductance Ca2+-activated K+ channel suppresses proliferation of microvascular and macrovascular endothelial cells and angiogenesis in vivo. Arterioscler Thromb Vasc Biol 25: 704-709. doi:10.1161/01.ATV.0000156399.12787.5c. PubMed: 15662023. (Pubitemid 40463857)
37. Wulff H, Castle NA (2010) Therapeutic potential of KCa3.1 blockers: Recent advances and promising trends. Expert Rev Clin Pharmacol 3: 385-396. doi:10.1586/ecp.10.11. PubMed: 22111618.
38. Stankevicius E, Dalsgaard T, Kroigaard C, Beck L, Boedtkjer E et al. (2011) Opening of small and intermediate calcium-activated potassium channels induces relaxation mainly mediated by nitric-oxide release in large arteries and endothelium-derived hyperpolarizing factor in small arteries from rat. J Pharmacol Exp Ther 339: 842-850. doi:10.1124/jpet.111.179242. PubMed: 21880870.
39. Kroigaard C, Dalsgaard T, Nielsen G, Laursen BE, Pilegaard H et al. (2012) Activation of endothelial and epithelial KCa2.3 calcium-activated potassium channels by NS309 relaxes human small pulmonary arteries and bronchioles. Br J Pharmacol 167: 37-47. doi:10.1111/j.1476-5381.2012.01986.x. PubMed: 22506557.
40. Ataga KI, Smith WR, De Castro LM, Swerdlow P, Saunthararajah Y et al. (2008) Efficacy and safety of the gardos channel blocker, senicapoc (ICA-17043), in patients with sickle cell anemia. Blood 111: 3991-3997. doi:10.1182/blood- 2007-08-110098. PubMed: 18192510.