Effect of imatinib on airway smooth muscle thickening in a murine model of chronic asthma

International Archives of Allergy and Immunology

Volumn 155, Issue 3, 2011, Pages 243-251

  Rhee, Chin Kook ^a   Kim, Jin Woo ^a   Park, Chan Kwon ^a   Kim, Joo Sang ^a   Kang, Ji Young ^a   Kim, Seung Joon ^a   Kim, Seok Chan ^a   Kwon, Soon Suk ^a   Kim, Young Kyoon ^a   Park, Sung Hak ^a   Lee, Sook Young ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

Asthma; Imatinib; Remodeling; Smooth muscle; Stem cell factor; Transforming growth factor 1

Indexed keywords

COLLAGEN; IMATINIB; INTERLEUKIN 4; INTERLEUKIN 5; OVALBUMIN; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BREATHING MUSCLE; CONTROLLED STUDY; EOSINOPHIL; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE; SYMPTOMATOLOGY;

AIRWAY REMODELING; ANIMALS; ASTHMA; CHRONIC DISEASE; FEMALE; INTERLEUKINS; MICE; MICE, INBRED BALB C; MUSCLE, SMOOTH; OVALBUMIN; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; SEVERITY OF ILLNESS INDEX; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79551543897     PISSN: 10182438     EISSN: 14230097     Source Type: Journal    
DOI: 10.1159/000321261     Document Type: Article

References (57)

1. Bateman ED, Hurd SS, Barnes PJ, Bousquet J, Drazen JM, FitzGerald M, Gibson P, Ohta K, O'Byrne P, Pedersen SE, Pizzichini E, Sullivan SD, Wenzel SE, Zar HJ: Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J 2008;31:143-178.
2. Wiggs BR, Bosken C, Pare PD, James A, Hogg JC: A model of airway narrowing in asthma and in chronic obstructive pulmonary disease. Am Rev Respir Dis 1992;145:1251-1258.
3. Zuyderduyn S, Sukkar MB, Fust A, Dhaliwal S, Burgess JK: Treating asthma means treating airway smooth muscle cells. Eur Respir J 2008;32:265-274.
4. Chan V, Burgess JK, Ratoff JC, O'Connor BJ, Greenough A, Lee TH, Hirst SJ: Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006;174:379-385. (Pubitemid 44223117)
5. 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. (Pubitemid 40663721)
6. 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. (Pubitemid 43134331)
7. Lazaar AL, Albelda SM, Pilewski JM, Brennan B, Pure E, Panettieri RA: T lymphocytes adhere to airway smooth muscle cells via integrins and CD44 and induce smooth muscle cell DNA synthesis. J Exp Med 1994;180:807-816. (Pubitemid 24256594)
8. Hakonarson H, Kim C, Whelan R, Campbell D, Grunstein MM: Bi-directional activation between human airway smooth muscle cells and T lymphocytes: role in induction of altered airway responsiveness. J Immunol 2001;166:293-303. (Pubitemid 32038445)
9. Sukkar MB, Xie S, Khorasani NM, Kon OM, Stanbridge R, Issa R, Chung KF: Toll-like receptor 2, 3, and 4 expression and function in human airway smooth muscle. J Allergy Clin Immunol 2006;118:641-648.
10. Boxall C, Holgate ST, Davies DE: The contribution of transforming growth factor-beta and epidermal growth factor signalling to airway remodelling in chronic asthma. Eur Respir J 2006;27:208-229. (Pubitemid 43092684)
11. Oliveira SH, Lukacs NW: Stem cell factor: a hemopoietic cytokine with important targets in asthma. Curr Drug Targets Inflamm Allergy 2003;2:313-318.
12. Talpaz M, Silver RT, Druker BJ, Goldman JM, Gambacorti-Passerini C, Guilhot F, Schiffer CA, Fischer T, Deininger MW, Lennard AL, Hochhaus A, Ottmann OG, Gratwohl A, Baccarani M, Stone R, Tura S, Mahon FX, Fernandes-Reese S, Gathmann I, Capdeville R, Kantarjian HM, Sawyers CL: Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 2002;99:1928-1937.
13. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, Sawyers CL: Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001;344:1031-1037. (Pubitemid 32267972)
14. Manley PW, Cowan-Jacob SW, Buchdunger E, Fabbro D, Fendrich G, Furet P, Meyer T, Zimmermann J: Imatinib: a selective tyrosine kinase inhibitor. Eur J Cancer 2002;38(suppl 5):S19-S27.
15. Day E, Waters B, Spiegel K, Alnadaf T, Manley PW, Buchdunger E, Walker C, Jarai G: Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol 2008;599:44-53.
16. Demetri GD, Joensuu H: Systemic treatment of patients with gastrointestinal stromal tumor: current status and future opportunities. Eur J Cancer Suppl 2008;6:1-14. (Pubitemid 351162923)
17. Pardanani A, Reeder T, Porrata LF, Li CY, Tazelaar HD, Baxter EJ, Witzig TE, Cross NC, Tefferi A: Imatinib therapy for hypereosinophilic syndrome and other eosinophilic disorders. Blood 2003;101:3391-3397. (Pubitemid 36857919)
18. Coutre S, Gotlib J: Targeted treatment of hypereosinophilic syndromes and chronic eosinophilic leukemias with imatinib mesylate. Semin Cancer Biol 2004;14:307-315. (Pubitemid 39419476)
19. Griffin JH, Leung J, Bruner RJ, Caligiuri MA, Briesewitz R: Discovery of a fusion kinase in EOL-1 cells and idiopathic hypereosinophilic syndrome. Proc Natl Acad Sci USA 2003;100:7830-7835. (Pubitemid 36760055)
20. Berlin AA, Lukacs NW: Treatment of cockroach allergen asthma model with imatinib attenuates airway responses. Am J Respir Crit Care Med 2005;171:35-39. (Pubitemid 40051692)
21. Berlin AA, Hogaboam CM, Lukacs NW: Inhibition of SCF attenuates peribronchial remodeling in chronic cockroach allergen-induced asthma. Lab Invest 2006;86:557-565. (Pubitemid 43780437)
22. Warner SM, Knight DA: Airway modeling and remodeling in the pathogenesis of asthma. Curr Opin Allergy Clin Immunol 2008;8:44-48.
23. Folli C, Descalzi D, Scordamaglia F, Riccio AM, Gamalero C, Canonica GW: New insights into airway remodelling in asthma and its possible modulation. Curr Opin Allergy Clin Immunol 2008;8:367-375.
24. Bergeron C, Al-Ramli W, Hamid Q: Remodeling in asthma. Proc Am Thorac Soc 2009;6:301-305.
25. Royce SG, Tang ML: The effects of current therapies on airway remodeling in asthma and new possibilities for treatment and prevention. Curr Mol Pharmacol 2009;2:169-181.
26. Devulapalli CS, Lodrup Carlsen KC, Haland G, Munthe-Kaas MC, Pettersen M, Mowinckel P, Carlsen K: No evidence that early use of inhaled corticosteroids reduces current asthma at 10 years of age. Respir Med 2007;101:1625-1632. (Pubitemid 46947881)
27. Hirst SJ: Regulation of airway smooth muscle cell immunomodulatory function: role in asthma. Respir Physiol Neurobiol 2003;137:309-326.
28. Lazaar AL, Panettieri RA: Airway smooth muscle as an immunomodulatory cell: a new target for pharmacotherapy? Curr Opin Pharmacol 2001;1:259-264.
29. Hochhaus A, O'Brien SG, Guilhot F, Druker BJ, Branford S, Foroni L, Goldman JM, Müller MC, Radich JP, Rudoltz M, Mone M, Gathmann I, Hughes TP, Larson RA: Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 2009;23:1054-1061.
30. van Oosterom AT, Judson I, Verweij J, Stroobants S, Donato di Paola E, Dimitrijevic S, Martens M, Webb A, Sciot R, Van Glabbeke M, Silberman S, Nielsen OS: Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumours: a phase I study. Lancet 2001;358:1421-1423. (Pubitemid 33055745)
31. Wynn TA: Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007;117:524-529.
32. Broide DH: Immunologic and inflammatory mechanisms that drive asthma progression to remodeling. J Allergy Clin Immunol 2008;121:560-570.
33. Xie S, Sukkar MB, Issa R, Khorasani NM, Chung KF: Mechanisms of induction of airway smooth muscle hyperplasia by transforming growth factor-beta. Am J Physiol Lung Cell Mol Physiol 2007;293:L245-L253. (Pubitemid 47080733)
34. Bosse Y, Stankova J, Rola-Pleszczynski M: Transforming growth factor-beta1 in asthmatic airway smooth muscle enlargement: is fibroblast growth factor-2 required? Clin Exp Allergy 2010;40:710-724.
35. Chaudhary NI, Schnapp A, Park JE: Pharmacologic differentiation of inflammation and fibrosis in the rat bleomycin model. Am J Respir Crit Care Med 2006;173:769-776.
36. Bizario JC, Cerri DG, Rodrigues LC, Oliveira GL, Nomizo A, de Araujo DD, Fukuhara PS, Ribeiro JC, de Castro FA, Costa MC: Imatinib mesylate ameliorates the dystrophic phenotype in exercised mdx mice. J Neuroimmunol 2009;212:93-101.
37. Zoja C, Corna D, Rottoli D, Zanchi C, Abbate M, Remuzzi G: Imatinib ameliorates renal disease and survival in murine lupus autoimmune disease. Kidney Int 2006;70:97-103. (Pubitemid 44000125)
38. Lukacs NW, Strieter RM, Lincoln PM, Brownell E, Pullen DM, Schock HJ, Chensue SW, Taub DD, Kunkel SL: Stem cell factor (ckit ligand) influences eosinophil recruitment and histamine levels in allergic airway inflammation. J Immunol 1996;156:3945-3951. (Pubitemid 26137682)
39. Campbell E, Hogaboam C, Lincoln P, Lukacs NW: Stem cell factor-induced airway hyperreactivity in allergic and normal mice. Am J Pathol 1999;154:1259-1265. (Pubitemid 29169759)
40. Dolgachev VA, Ullenbruch MR, Lukacs NW, Phan SH: Role of stem cell factor and bone marrow-derived fibroblasts in airway remodeling. Am J Pathol 2009;174:390-400.
41. Miyachi K, Ihara A, Hankins RW, Murai R, Maehiro S, Miyashita H: Efficacy of imatinib mesylate (STI571) treatment for a patient with rheumatoid arthritis developing chronic myelogenous leukemia. Clin Rheumatol 2003;22:329-332. (Pubitemid 37483630)
42. Eklund K, Joensuu H: Treatment of rheumatoid arthritis with imatinib mesylate: clinical improvement in three refractory cases. Ann Med 2003;35:362-367. (Pubitemid 37013677)
43. Eklund K, Lindstedt K, Sandler C, Kovanen PT, Laasonen L, Juurikivi A, Wolff H, Mykknen M, Joensuu H: Maintained efficacy of the tyrosine kinase inhibitor imatinib mesylate in a patient with rheumatoid arthritis. J Clin Rheumatol 2008;14:294-296.
44. Koyama K, Hatsushika K, Ando T, Sakuma M, Wako M, Kato R, Haro H, Sugiyama H, Hamada Y, Ogawa H, Nakao A: Imatinib mesylate both prevents and treats the arthritis induced by type II collagen antibody in mice. Mod Rheumatol 2007;17:306-310. (Pubitemid 47263822)
45. Hjoberg J, Le L, Imrich A, Subramaniam V, Mathew SI, Vallone J, Haley KJ, Green FH, Shore SA, Silverman ES: Induction of early growth-response factor 1 by platelet-derived growth factor in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2004;286:L817-L825. (Pubitemid 38365068)
46. Ushio-Fukai M, Zuo L, Ikeda S, Tojo T, Patrushev NA, Alexander RW: cAbl tyrosine kinase mediates reactive oxygen species- and caveolin-dependent AT1 receptor signaling in vascular smooth muscle: role in vascular hypertrophy. Circ Res 2005;97:829-836. (Pubitemid 41447134)
47. Cho JY, Miller M, McElwain K, McElwain S, Broide DH: Combination of corticosteroid therapy and allergen avoidance reverses allergen-induced airway remodeling in mice. J Allergy Clin Immunol 2005;116:1116-1122. (Pubitemid 41571797)
48. Lee SY, Cho JY, Miller M, McElwain K, McElwain S, Sriramarao P, Raz E, Broide DH: Immunostimulatory DNA inhibits allergen-induced peribronchial angiogenesis in mice. J Allergy Clin Immunol 2006;117:597-603. (Pubitemid 43340224)
49. Ohta S, Oda N, Yokoe T, Tanaka A, Yamamoto Y, Watanabe Y, Minoguchi K, Ohnishi T, Hirose T, Nagase H, Ohta K, Adachi M: Effect of tiotropium bromide on airway inflammation and remodelling in a mouse model of asthma. Clin Exp Allergy 2010;40:1266-1275.
50. Kang JY, Kim JW, Kim JS, Kim SJ, Lee SH, Kwon SS, Kim YK, Moon HS, Song JS, Park SH, Lee SY: Inhibitory effects of anti-immunoglobulin E antibodies on airway remodeling in a murine model of chronic asthma. J Asthma 2010;47:374-380.
51. Ge XN, Bahaie NS, Kang BN, Hosseinkhani MR, Ha SG, Frenzel EM, Liu F, Rao SP, Sriramarao P: Allergen-induced airway remodeling is impaired in galectin-3-deficient mice. J Immunol 2010;185:1205-1214.
52. Lee SY, Kim JS, Lee JM, Kwon SS, Kim KH, Moon HS, Song JS, Park SH, Kim YK: Inhaled corticosteroid prevents the thickening of airway smooth muscle in murine model of chronic asthma. Pulm Pharmacol Ther 2008;21:14-19.
53. Rhee CK, Lee SY, Kang JY, Kim SJ, Kwon SS, Kim YK, Park SH: Effect of peroxisome proliferator-activated receptor-gamma on airway smooth muscle thickening in a murine model of chronic asthma. Int Arch Allergy Immunol 2008;148:289-296.
54. Adcock IM, Chung KF, Caramori G, Ito K: Kinase inhibitors and airway inflammation. Eur J Pharmacol 2006;533:118-132. (Pubitemid 43340009)
55. Sly PD, Turner DJ, Collins RA, Hantos Z: Penh is not a validated technique for measuring airway function in mice. Am J Respir Crit Care Med 2005;172:256-256.
56. Bates J, Irvin C, Brusasco V, Drazen J, Fredberg J, Loring S, Eidelman D, Ludwig M, Macklem P, Martin J, Milic-Emili J, Hantos Z, Hyatt R, Lai-Fook S, Leff A, Solway J, Lutchen K, Suki B, Mitzner W, Par P, Pride N, Sly P: The use and misuse of Penh in animal models of lung disease. Am J Respir Cell Mol Biol 2004;31:373-374. (Pubitemid 39180309)
57. Lundblad LKA, Irvin CG, Hantos Z, Sly P, Mitzner W, Bates JHT: Penh is not a measure of airway resistance! Eur Respir J 2007;30:805-805.