Effects of the protein kinase inhibitor, imatinib mesylate, on epithelial/mesenchymal phenotypes: Implications for treatment of fibrotic diseases

Journal of Pharmacology and Experimental Therapeutics

Volumn 321, Issue 1, 2007, Pages 35-44

  Vittal, Ragini ^a   Zhang, Hengmin ^a   Han, MeiLan K ^a   Moore, Bethany B ^a   Horowitz, Jeffrey C ^a   Thannickal, Victor J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; COLLAGEN; IMATINIB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; EPITHELIUM; FEMALE; FIBROBLAST; FIBROBLAST CULTURE; FIBROGENESIS; FIBROSIS; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; LUNG INJURY; MESENCHYME; MOUSE; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TISSUE REPAIR;

ADMINISTRATION, ORAL; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BLEOMYCIN; BLOTTING, WESTERN; BROMODEOXYURIDINE; CASPASE 3; CELL LINE, TUMOR; CELLS, CULTURED; COLLAGEN; DNA, SINGLE-STRANDED; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FIBROBLASTS; FIBROSIS; GASTROINTESTINAL STROMAL TUMORS; HUMANS; IMMUNOHISTOCHEMISTRY; INDICATORS AND REAGENTS; INJECTIONS, INTRAPERITONEAL; LEUKEMIA, MYELOID, CHRONIC; LUNG DISEASES; MESENCHYMAL STEM CELLS; MICE; PHENOTYPE; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; SIGNAL TRANSDUCTION;

EID: 33947411686     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.106.113407     Document Type: Article

References (40)

1. Aono Y, Nishioka Y, Inayama M, Ugai M, Kishi J, Uehara H, Izumi K, and Sone S (2005) Imatinib as a novel antifibrotic agent in bleomycin-induced pulmonary fibrosis in mice. Am J Respir Crit Care Med 171:1279-1285.
2. Bergeron A, Bergot E, Vilela G, Ades L, Devergie A, Esperou H, Socie G, Calvo F, Gluckman E, Ribaud P, et al. (2002) Hypersensitivity pneumonitis related to imatinib mesylate. J Clin Oncol 20:4271-4272.
3. Borzone G, Moreno R, Urrea R, Meneses M, Oyarzun M, and Lisboa C (2001) Bleomycin-induced chronic lung damage does not resemble human idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 163:1648-1653.
4. Buchdunger E, Cioffi CL, Law N, Stover D, Ohno-Jones S, Druker BJ, and Lydon NB (2000) Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 295:139-145.
5. Chaudhary NI, Schnapp A, and Park JE (2006) Pharmacological differentiation of inflammation and fibrosis in the rat bleomycin model. Am J Respir Crit Care Med 173:769-776.
6. Cohen P (2002) Protein kinases: the major drug targets of the twenty-first century? Nat Rev Drug Discov 1:309-315.
7. Daniels CE, Wilkes MC, Edens M, Kottom TJ, Murphy SJ, Limper AH, and Leof EB (2004) Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Investig 114:1308-1316.
8. Desmouliere A, Geinoz A, Gabbiani F, and Gabbiani G (1993) Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122:103-111.
9. Desmouliere A, Redard M, Darby I, and Gabbiani G (1995) Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 146:56-66.
10. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, et al. (2001) Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 344:1031-1037.
11. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, and Lydon NB (1996) Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 2:561-566.
12. Flanders KC, Sullivan CD, Fujii M, Sowers A, Anzano MA, Arabshahi A, Major C, Deng C, Russo A, Mitchell JB, et al. (2002) Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am J Pathol 160:1057-1068.
13. Gilbert RE, Kelly DJ, McKay T, Chadban S, Hill PA, Cooper ME, Atkins RC, and Nikolic-Paterson DJ (2001) PDGF signal transduction inhibition ameliorates experimental mesangial proliferative glomerulonephritis. Kidney Int 59:1324-1332.
14. Havrilesky LJ, Hurteau JA, Whitaker RS, Elbendary A, Wu S, Rodriguez GC, Bast RC Jr, and Berchuck A (1995) Regulation of apoptosis in normal and malignant ovarian epithelial cells by transforming growth factor beta. Cancer Res 55:944-948.
15. Horowitz JC, Cui Z, Moore TA, Meier TR, Reddy RC, Toews GB, Standiford TJ, and Thannickal VJ (2006a) Constitutive activation of prosurvival signaling in alveolar mesenchymal cells isolated from patients with nonresolving acute respiratory distress syndrome. Am J Physiol 290:L415-L425.
16. Horowitz JC, Lee DY, Waghray M, Keshamouni VG, Thomas PE, Zhang H, Cui Z, and Thannickal VJ (2004) Activation of the pro-survival phosphatidylinositol 3-kinase/AKT pathway by transforming growth factor-beta1 in mesenchymal cells is mediated by p38 MAPK-dependent induction of an autocrine growth factor. J Biol Chem 279:1359-1367.
17. Horowitz JC, Rogers DS, Sharma V, Vittal R, White ES, Cui Z, and Thannickal VJ (2006b) Combinatorial activation of FAK and AKT by transforming growth factor-beta1 confers an anoikis-resistant phenotype to myofibroblasts. Cell Signal, in press.
18. Hu B, Wu Z, and Phan SH (2003) Smad3 mediates transforming growth factor-beta-induced alpha-smooth muscle actin expression. Am J Respir Cell Mol Biol 29:397-404.
19. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, and Chapman HA (2006) Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 103:13180-13185.
20. Liu JY, Morris GF, Lei WH, Hart CE, Lasky JA, and Brody AR (1997) Rapid activation of PDGF-A and -B expression at sites of lung injury in asbestos-exposed rats. Am J Respir Cell Mol Biol 17:129-140.
21. Ma CX, Hobday TJ, and Jett JR (2003) Imatinib mesylate-induced interstitial pneumonitis. Mayo Clin Proc 78:1578-1579.
22. Ohnishi K, Sakai F, Kudoh S, and Ohno R (2006) Twenty-seven cases of drug-induced interstitial lung disease associated with imatinib mesylate. Leukemia 20:1162-1164.
23. Pietras K, Rubin K, Sjoblom T, Buchdunger E, Sjoquist M, Heldin CH, and Ostman A (2002) Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy. Cancer Res 62:5476-5484.
24. Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu CY, et al. (2004) Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 164:651-663.
25. Selman M, King TE, and Pardo A (2001) Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 134:136-151.
26. Thannickal V, Toews GB, White ES, Lynch JP III, and Martinez FJ (2004) Mechanisms of pulmonary fibrosis. Annu Rev Med 55:19.11-19.23.
27. Thannickal VJ, Flaherty KR, Hyzy RC, and Lynch JP 3rd (2005) Emerging drugs for idiopathic pulmonary fibrosis. Expert Opin Emerg Drugs 10:707-727.
28. Thannickal VJ and Horowitz JC (2006) Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 3:350-356.
29. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM, Chacon R, Horowitz JC, Day RM, and Thomas PE (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.
30. Thrall RS, Barton RW, D'Amato DA, and Sulavik SB (1982) Differential cellular analysis of bronchoalveolar lavage fluid obtained at various stages during the development of bleomycin-induced pulmonary fibrosis in the rat. Am Rev Respir Dis 126:488-492.
31. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, and Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3:349-363.
32. Tuveson DA, Willis NA, Jacks T, Griffin JD, Singer S, Fletcher CD, Fletcher JA, and Demetri GD (2001) STI571 inactivation of the gastrointestinal stromal tumor c-KIT oncoprotein: biological and clinical implications. Oncogene 20:5054-5058.
33. Vittal R, Horowitz JC, Moore BB, Zhang H, Martinez FJ, Toews GB, Standiford TJ, and Thannickal VJ (2005) Modulation of prosurvival signaling in fibroblasts by a protein kinase inhibitor protects against fibrotic tissue injury. Am J Pathol 166:367-375.
34. Waghray M, Cui Z, Horowitz JC, Subramanian IM, Martinez FJ, Toews GB, and Thannickal VJ (2005) Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. FASEB J 19:854-856.
35. Wang S, Wilkes MC, Leof EB, and Hirschberg R (2005) Imatinib mesylate blocks a non-Smad TGF-beta pathway and reduces renal fibrogenesis in vivo. FASEB J 19:1-11.
36. Wang WL, Healy ME, Sattler M, Verma S, Lin J, Maulik G, Stiles CD, Griffin JD, Johnson BE, and Salgia R (2000) Growth inhibition and modulation of kinase pathways of small cell lung cancer cell lines by the novel tyrosine kinase inhibitor STI 571. Oncogene 19:3521-3528.
37. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, and Borok Z (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 166:1321-1332.
38. Yokoyama T, Miyazawa K, Kurakawa E, Nagate A, Shimamoto T, Iwaya K, Akata S, Aoshima M, Serizawa H, and Ohyashiki K (2004) Interstitial pneumonia induced by imatinib mesylate: pathologic study demonstrates alveolar destruction and fibrosis with eosinophilic infiltration. Leukemia 18:645-646.
39. Yoshiji H, Kuriyama S, Noguchi R, Ikenaka Y, Yoshii J, Yanase K, Namisaki T, Kitade M, Yamazaki M, Asada K, et al. (2006) Amelioration of liver fibrogenesis by dual inhibition of PDGF and TGF-beta with a combination of imatinib mesylate and ACE inhibitor in rats. Int J Mol Med 17:899-904.
40. Zhang K, Rekhter MD, Gordon D, and Phan SH (1994) Myofibroblasts and their role in lung collagen gene expression during pulmonary fibrosis: a combined immunohistochemical and in situ hybridization study. Am J Pathol 145:114-125.