The role of tyrosine kinases in the pathogenesis of idiopathic pulmonary fibrosis

European Respiratory Journal

Volumn 45, Issue 5, 2015, Pages 1426-1433

  Grimminger, Friedrich ^a,c   Günther, Andreas ^a   Vancheri, Carlo ^b  

^a UNIVERSITY HOSPITAL MARBURG   (Germany)

^b UNIVERSITY OF CATANIA   (Italy)

^c JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR 4; GEFITINIB; IMATINIB; NILOTINIB; NINTEDANIB; PLATELET DERIVED GROWTH FACTOR A; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR C; PLATELET DERIVED GROWTH FACTOR D; PROTEIN TYROSINE KINASE; SU 11657; SU 5918; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR;

ANTIFIBROTIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; CELL PROLIFERATION; DISEASE COURSE; DISEASE EXACERBATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG SAFETY; ENZYME ACTIVATION; ENZYME INHIBITION; FIBROSING ALVEOLITIS; HUMAN; IN VITRO STUDY; LUNG FIBROBLAST; NONHUMAN; PATHOGENESIS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PULMONARY HYPERTENSION; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CLINICAL TRIAL (TOPIC); ENZYMOLOGY; HOMEOSTASIS; LUNG DISEASE; LUNG FIBROSIS; METABOLISM; MORTALITY; PHOSPHORYLATION;

ANIMALS; CLINICAL TRIALS AS TOPIC; DISEASE PROGRESSION; FIBROBLAST GROWTH FACTORS; HOMEOSTASIS; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; LUNG DISEASES; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN-TYROSINE KINASES; PULMONARY FIBROSIS; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84928309315     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00149614     Document Type: Review

References (84)

1. American Thoracic Society, European Respiratory Society. American Thoracic Society/European Respiratory Society international multidisciplinary consensus classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med 2002; 165: 277-304.
2. Coultas DB, Zumwalt RE, Black WC, et al. The epidemiology of interstitial lung diseases. Am J Respir Crit Care Med 1994; 150: 967-972.
3. Raghu G, Weycker D, Edelsberg J, et al. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006; 174: 810-816.
4. Kaunisto J, Salomaa ER, Hodgson U, et al. Idiopathic pulmonary fibrosis - A systematic review on methodology for the collection of epidemiological data. BMC Pulm Med 2013; 13: 53.
5. Raghu G, Collard HR, Egan JJ, et al. An official ATS/ERS/JRS/ALAT statement: Idiopathic pulmonary fibrosis: Evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011; 183: 788-824.
6. King TE Jr, Bradford WZ, Castro-Bernardini S, et al. A Phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N Engl J Med 2014; 370: 2083-2092.
7. Molyneaux PL, Maher TM. The role of infection in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir Rev 2013; 22: 376-381.
8. Katzenstein ALA, Myers JL. Idiopathic pulmonary fibrosis: Clinical relevance of pathologic classification. Am J Respir Crit Care Med 1998; 157: 1301-1315.
9. Hardie WD, Hagood JS, Dave V, et al. Signaling pathways in the epithelial origins of pulmonary fibrosis. Cell Cycle 2010; 9: 2769-2776.
10. King TE Jr, Pardo A, Selman M. Idiopathic pulmonary fibrosis. Lancet 2011; 378: 1949-1961.
11. Wuyts WA, Agostini C, Antoniou KM, et al. The pathogenesis of pulmonary fibrosis: A moving target. Eur Respir J 2013; 41: 1207-1218.
12. Cronkhite JT, Xing C, Raghu G, et al. Telomere shortening in familial and sporadic pulmonary fibrosis. Am J Respir Crit Care Med 2008; 178: 729-737.
13. Fernandez IE, Eickelberg O. New cellular and molecular mechanisms of lung injury and fibrosis in idiopathic pulmonary fibrosis. Lancet 2012; 380: 680-688.
14. Allen JT, Spiteri MA. Growth factors in idiopathic pulmonary fibrosis: relative roles. Respir Res 2002; 3: 13.
15. Bauman KA, Wettlaufer SH, Okunishi K, et al. The antifibrotic effects of plasminogen activation occur via prostaglandin E2 synthesis in humans and mice. J Clin Invest 2010; 120: 1950-1960.
16. Pfaff EM, Becker S, Günther A, et al. Dickkopf proteins influence lung epithelial cell proliferation in idiopathic pulmonary fibrosis. Eur Respir J 2011; 37: 79-87.
17. Willis BC, Borok Z. TGF-β-induced EMT: Mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007; 293: L525-L534.
18. Hung C, Linn G, Chow YH, et al. Role of lung pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2013; 188: 820-830.
19. Hunter T. The Croonian Lecture 1997. The phosphorylation of proteins on tyrosine: Its role in cell growth and disease. Philos Trans R Soc Lond B Biol Sci 1998; 353: 583-605.
20. Manning G, Whyte DB, Martinez R, et al. The protein kinase complement of the human genome. Science 2002; 298: 1912-1934.
21. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000; 103: 211-225.
22. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010; 141: 1117-1134.
23. Almendro V, García-Recio S, Gascón P. Tyrosine kinase receptor transactivation associated to G protein-coupled receptors. Curr Drug Targets 2010; 11: 1169-1180.
24. Miller WT. Determinants of substrate recognition in nonreceptor tyrosine kinases. Acc Chem Res 2003; 36: 393-400.
25. Chen H, Ma J, Li W, et al. A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol Cell 2007; 27: 717-730.
26. Grimminger F, Schermuly RT, Ghofrani HA. Targeting non-malignant disorders with tyrosine kinase inhibitors. Nat Rev Drug Discov 2010; 9: 956-970.
27. Beyer C, Distler JH. Tyrosine kinase signaling in fibrotic disorders: Translation of basic research to human disease. Biochim Biophys Acta 2013; 1832: 897-904.
28. Olson LE, Soriano P. PDGFRβ signaling regulates mural cell plasticity and inhibits fat development. Dev Cell 2011; 20: 815-826.
29. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008; 22: 1276-1312.
30. Olsson AK, Dimberg A, Kreuger J, et al. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006; 7: 359-371.
31. Holmes DI, Zachary I. The vascular endothelial growth factor (VEGF) family: Angiogenic factors in health and disease. Genome Biol 2005; 6: 209.
32. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006; 290: L209-L221.
33. Kaner RJ, Crystal RG. Compartmentalization of vascular endothelial growth factor to the epithelial surface of the human lung. Mol Med 2001; 7: 240-246.
34. Del Moral PM, Sala FG, Tefft D, et al. VEGF-A signaling through Flk-1 is a critical facilitator of early embryonic lung epithelial to endothelial crosstalk and branching morphogenesis. Dev Biol 2006; 290: 177-188.
35. Roberts JR, Perkins GD, Fujisawa T, et al. Vascular endothelial growth factor promotes physical wound repair and is anti-apoptotic in primary distal lung epithelial and A549 cells. Crit Care Med 2007; 35: 2164-2170.
36. Compernolle V, Brusselmans K, Acker T, et al. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002; 8: 702-710.
37. Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem 2011; 149: 121-130.
38. Dosanjh A. The fibroblast growth factor pathway and its role in the pathogenesis of lung disease. J Interferon Cytokine Res 2012; 32: 111-114.
39. Vallath S, Hynds RE, Succony L, et al. Targeting EGFR signalling in chronic lung disease: Therapeutic challenges and opportunities. Eur Respir J 2014; 44: 513-522.
40. Holbro T, Hynes NE. ErbB receptors: Directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 2004; 44: 195-217.
41. Zhuo Y, Zhang J, Laboy M, et al. Modulation of PDGF-C and PDGF-D expression during bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2004; 286: L182-L188.
42. Gurujeyalakshmi G, Hollinger MA, Giri SN. Pirfenidone inhibits PDGF isoforms in bleomycin hamster model of lung fibrosis at the translational level. Am J Physiol 1999; 276: L311-L318.
43. Rice AB, Moomaw CR, Morgan DL, et al. Specific inhibitors of platelet-derived growth factor or epidermal growth factor receptor tyrosine kinase reduce pulmonary fibrosis in rats. Am J Pathol 1999; 155: 213-221.
44. Trojanowska M. Role of PDGF in fibrotic diseases and systemic sclerosis. Rheumatology 2008; 47: Suppl. 5, v2-v4.
45. Martinet Y, Rom WN, Grotendorst GR, et al. Exaggerated spontaneous release of platelet-derived growth factor by alveolar macrophages from patients with idiopathic pulmonary fibrosis. N Engl J Med 1987; 317: 202-209.
46. Hetzel M, Bachem M, Anders D, et al. Different effects of growth factors on proliferation and matrix production of normal and fibrotic human lung fibroblasts. Lung 2005; 183: 225-237.
47. Hostettler KE, Papakonstantinou E, Klagas I, et al. Anti-fibrotic effects of nintedanib (BIBF 1120) in primary human lung fibroblasts derived from idiopathic pulmonary fibrosis and from non-fibrotic controls. Am J Respir Crit Care Med 2013; 187: A3374.
48. Xiao L, Du Y, Shen Y, et al. TGF-β 1 induced fibroblast proliferation is mediated by the FGF-2/ERK pathway. Front Biosci 2012; 17: 2667-2674.
49. Yu ZH, Wang DD, Zhou ZY, et al. Mutant soluble ectodomain of fibroblast growth factor receptor-2 IIIc attenuates bleomycin-induced pulmonary fibrosis in mice. Biol Pharm Bull 2012; 35: 731-736.
50. Wygrecka M, Dahal BK, Kosanovic D, et al. Mast cells and fibroblasts work in concert to aggravate pulmonary fibrosis: role of transmembrane SCF and the PAR-2/PKC-α/Raf-1/p44/42 signaling pathway. Am J Pathol 2013; 182: 2094-2108.
51. Inoue Y, King TE Jr, Tinkle SS, et al. Human mast cell basic fibroblast growth factor in pulmonary fibrotic disorders. Am J Pathol 1996; 149: 2037-2054.
52. Rubin JS, Osada H, Finch PW, et al. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 1989; 86: 802-806.
53. Gupte VV, Ramasamy SK, Reddy R, et al. Overexpression of fibroblast growth factor-10 during both inflammatory and fibrotic phases attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Respir Crit Care Med 2009; 180: 424-436.
54. MacKenzie B, El Agha E, Al Alam D, et al. The role of fibroblast growth factors in idiopathic lung fibrosis. Pneumologie 2012; 66: A514.
55. Farkas L, Kolb M. Pulmonary microcirculation in interstitial lung disease. Proc Am Thorac Soc 2011; 8: 516-521.
56. Hamada N, Kuwano K, Yamada M, et al. Anti-vascular endothelial growth factor gene therapy attenuates lung injury and fibrosis in mice. J Immunol 2005; 175: 1224-1231.
57. Lee CG, Link H, Baluk P, et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 2004; 10: 1095-1103.
58. McKeown S, Richter AG, O'Kane C, et al. MMP expression and abnormal lung permeability are important determinants of outcome in IPF. Eur Respir J 2009; 33: 77-84.
59. Ando M, Miyazaki E, Ito T, et al. Significance of serum vascular endothelial growth factor level in patients with idiopathic pulmonary fibrosis. Lung 2010; 188: 247-252.
60. Andrianifahanana M, Wilkes MC, Gupta SK, et al. Profibrotic TGFβ responses require the cooperative action of PDGF and ErbB receptor tyrosine kinases. FASEB J 2013; 27: 4444-4454.
61. Madtes DK, Busby HK, Strandjord TP, et al. Expression of transforming growth factor-α and epidermal growth factor receptor is increased following bleomycin-induced lung injury in rats. Am J Respir Cell Mol Biol 1994; 11: 540-551.
62. Hardie WD, Le Cras TD, Jiang K, et al. Conditional expression of transforming growth factor-α in adult mouse lung causes pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2004; 286: L741-L749.
63. Nethery DE, Moore BB, Minowada G, et al. Expression of mutant human epidermal receptor 3 attenuates lung fibrosis and improves survival in mice. J Appl Physiol 2005; 99: 298-307.
64. Baughman RP, Lower EE, Miller MA, et al. Overexpression of transforming growth factor-α and epidermal growth factor-receptor in idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 1999; 16: 57-61.
65. Tatosyan AG, Mizenina OA. Kinases of the Src family: structure and functions. Biochemistry (Mosc) 2000; 65: 49-58.
66. Ulsamer A, Wei Y, Kim KK, et al. Axin pathway activity regulates in vivo pY654-β-catenin accumulation and pulmonary fibrosis. J Biol Chem 2012; 287: 5164-5172.
67. Schermuly RT, Dony E, Ghofrani HA, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 2005; 115: 2811-2821.
68. Hoeper MM, Barst RJ, Bourge RC, et al. Imatinib mesylate as add-on therapy for pulmonary arterial hypertension: results of the randomized IMPRES study. Circulation 2013; 127: 1128-1138.
69. Schaefer CJ, Ruhrmund DW, Pan L, et al. Antifibrotic activities of pirfenidone in animal models. Eur Respir Rev 2011; 20: 85-97.
70. Abdollahi A, Li M, Ping G, et al. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J Exp Med 2005; 201: 925-935.
71. Aono Y, Nishioka Y, Inayama M, et al. Imatinib as a novel antifibrotic agent in bleomycin-induced pulmonary fibrosis in mice. Am J Respir Crit Care Med 2005; 171: 1279-1285.
72. Ishii Y, Fujimoto S, Fukuda T. Gefitinib prevents bleomycin-induced lung fibrosis in mice. Am J Respir Crit Care Med 2006; 174: 550-556.
73. Li M, Abdollahi A, Gröne HJ, et al. Late treatment with imatinib mesylate ameliorates radiation-induced lung fibrosis in a mouse model. Radiat Oncol 2009; 4: 66.
74. Rhee CK, Lee SH, Yoon HK, et al. Effect of nilotinib on bleomycin-induced acute lung injury and pulmonary fibrosis in mice. Respiration 2011; 82: 273-287.
75. Chung L, Fiorentino DF, Benbarak MJ, et al. Molecular framework for response to imatinib mesylate in systemic sclerosis. Arthritis Rheum 2009; 60: 584-591.
76. Akhmetshina A, Venalis P, Dees C, et al. Treatment with imatinib prevents fibrosis in different preclinical models of systemic sclerosis and induces regression of established fibrosis. Arthritis Rheum 2009; 60: 219-224.
77. Ding L, Dolgachev V, Wu Z, et al. Essential role of stem cell factor-c-Kit signalling pathway in bleomycin-induced pulmonary fibrosis. J Pathol 2013; 230: 205-214.
78. Daniels CE, Lasky JA, Limper AH, et al. Imatinib treatment for idiopathic pulmonary fibrosis: randomized placebo-controlled trial results. Am J Respir Crit Care Med 2010; 181: 604-610.
79. Hilberg F, Roth GJ, Krssak M, et al. BIBF 1120: Triple angiokinase inhibitor with sustained receptor blockade and good antitumor efficacy. Cancer Res 2008; 68: 4774-4782.
80. Wollin L, Maillet I, Quesniaux V, et al. Antifibrotic and anti-inflammatory activity of the tyrosine kinase inhibitor nintedanib in experimental models of lung fibrosis. J Pharmacol Exp Ther 2014; 349: 209-220.
81. Chaudhary NI, Roth GJ, Hilberg F, et al. Inhibition of PDGF, VEGF and FGF signalling attenuates fibrosis. Eur Respir J 2007; 29: 976-985.
82. Daniels CE, Wilkes MC, Edens M, et al. Imatinib mesylate inhibits the profibrogenic activity of TGF-β and prevents bleomycin-mediated lung fibrosis. J Clin Invest 2004; 114: 1308-1316.
83. Richeldi L, Costabel U, Selman M, et al. Efficacy of a tyrosine kinase inhibitor in idiopathic pulmonary fibrosis. N Engl J Med 2011; 365: 1079-1087.
84. Richeldi L, du Bois RM, Raghu G, et al. Efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N Engl J Med 2014; 370: 2071-2082.