Prevention of Bleomycin-induced Lung Fibrosis by Aerosolization of Heparin or Urokinase in Rabbits

American Journal of Respiratory and Critical Care Medicine

Volumn 168, Issue 11, 2003, Pages 1358-1365

  Günther, Andreas ^a,b   Lübke, Norbert ^a   Ermert, Monika ^a   Schermuly, Ralph T ^a   Weissmann, Norbert ^a   Breithecker, Andreas ^a   Markart, Philipp ^a   Ruppert, Clemens ^a   Quanz, Karin ^a   Ermert, Leander ^a   Grimminger, Friedrich ^a   Seeger, Werner ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL GIESSEN   (Germany)

Author keywords

Coagulation; Diffuse parenchymal lung disease; Fibrinolysis; Interstitial lung disease; Pulmonary surfactant

Indexed keywords

BLEOMYCIN; COLLAGEN; HEPARIN; HYDROXYPROLINE; UROKINASE;

AEROSOL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN SYNTHESIS; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; FIBRIN FORMATION; FIBRINOGENOLYSIS; FIBROSING ALVEOLITIS; HISTOPATHOLOGY; INFECTION PREVENTION; LUNG COMPLIANCE; LUNG LAVAGE; NEBULIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROVOCATION TEST; TISSUE SECTION;

ADMINISTRATION, INHALATION; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLEOMYCIN; DISEASE MODELS, ANIMAL; FIBRINOLYSIS; HEPARIN; PLASMINOGEN ACTIVATORS; PULMONARY ALVEOLI; PULMONARY FIBROSIS; RABBITS; URINARY PLASMINOGEN ACTIVATOR;

EID: 0344742226     PISSN: 1073449X     EISSN: None     Source Type: Journal    
DOI: 10.1164/rccm.2201082     Document Type: Article

References (56)

1. Coultas DB, Zumwalt RE, Black WC, Sobonya RE. The epidemiology of interstitial lung diseases. Am J Respir Crit Care Med 1994;150:967-972.
2. Phan SH. New strategies for treatment of pulmonary fibrosis. Thorax 1995;50:415-421.
3. Mason RJ, Schwarz MI, Hunninghake GW, Musson RA. Pharmacological therapy for idiopathic pulmonary fibrosis: past, present, and future. Am J Respir Crit Care Med 1999;160:1771-1777.
4. Nakao A, Fujii M, Matsumura R, Kumano K, Saito Y, Miyazono K, Iwamoto T. Transient gene transfer and expression of Smad7 prevents bleomycin induced lung fibrosis in mice. J Clin Invest 1999;104:5-11.
5. Parizada B, Werber MM, Nimrod A. Protective effect of human recombinant MnSOD in adjuvant arthritis and bleomycin-induced lung fibrosis. Free Radic Res Commun 1991;15:297-301.
6. Greco MJ, Kemnitzer JE, Fox JD, Choe JK, Kohn J, Riley DJ, Poiani GJ. Polymer of proline analogue with sustained antifibrotic activity in lung fibrosis. Am J Respir Crit Care Med 1997;155:1391-1397.
7. Zische R, Hofbauer E, Wittnann K, Petkov V, Block LH. A preliminary study of long-term treatment with interferon gamma 1-b and low-dose prednisolon in patients with idiopathic pulmonary fibrosis. N Engl J Med 1999;341:1264-1269.
8. Günther A, Schmidt R, Nix F, Yabut-Perez M, Guth C, Rosseau S, Siebert C, Grimminger F, Morr H, Velcovsky HG. Surfactant abnormalities in idiopathic pulmonary fibrosis, hypersensitivity pneumonitis and sarcoidosis. Eur Respir J 1999;14:565-573.
9. Robinson PC, Watters LC, King TE, Mason RJ. Idiopathic pulmonary fibrosis: abnormalities in bronchoalveolar lavage fluid phospholipids. Am Rev Respir Dis 1988;137:585-591.
10. McCormack FX, King TE, Voelker DR, Robinson PC, Mason RJ. Idiopathic pulmonary fibrosis: abnormalities in bronchoalveolar lavage content of surfactant protein A. Am Rev Respir Dis 1991;144:160-166.
11. Fuchimukai T, Fujiwara T, Takahashi A, Enhorning G. Artificial pulmonary surfactant inhibited by proteins. J Appl Physiol 1987;62:429-437.
12. Kobayashi T, Kitta K, Ganzuka M, Inui S, Grossmann G, Robertson B. Inactivation of exogenous surfactant by pulmonary edema fluid. Pediatr Res 1991;29:353-356.
13. Günther A, Siebert C, Schmidt R, Ziegler S, Grimminger F, Yabut M, Temmesfeld B, Walmrath D, Morr H, Seeger W. Surfactant alterations in severe pneumonia, ARDS and cardiogenic lung edema. Am J Respir Crit Care Med 1996;153:176-184.
14. Seeger W, Elssner A, Günther A, Krämer HJ, Kalinowski HO. Lung surfactant phospholipids associate with polymerizing fibrin: loss of surface activity. Am J Respir Cell Mol Biol 1999;9:213-220.
15. Günther A, Kalinowski M, Elssner A, Seeger W. Clot embedded natural surfactant: kinetics of fibrinolysis and surface activity. Am J Physiol 1994;267:L618-L624.
16. Günther A, Markart P, Kalinowski M, Ruppert C, Grimminger F, Seeger W. Cleavage of surfactant-incorporating fibrin by different fibrinolytic agents: kinetics of lysis and rescue of surface activity. Am J Respir Cell Mol Biol 1999;21:738-745.
17. Idell S, Koenig KB, Fair DS, Martin TR, McLarty J, Maunder RJ. Serial abnormalities of fibrin turnover in evolving adult respiratory distress syndrome. Am J Physiol 1991;261:L240-L248.
18. Günther A, Mosavi P, Heinemann S, Ruppert C, Muth H, Markart P, Grimminger F, Walmrath D, Temmesfeld-Wollbrück B, Seeger W. Alveolar fibrin formation caused by enhanced procoagulant and depressed fibrinolytic capacities in severe pneumonia: comparison with the respiratory distress syndrome. Am J Respir Crit Care Med 2000; 161:454-462.
19. de Moerloose P, de Benedetti E, Nicod L, Vifian C, Reber G. Procoagulant activity in bronchoalveolar lavage fluids: no relationship with tissue factor pathway inhibitor activity. Thromb Res 1992;65:507-518.
20. Günther A, Mosavi P, Ruppert C, Heinemann S, Temmesfeld- Wollbrück B, Velcovsky HG, Morr H, Grimminger F, Walmrath D, Seeger W. Enhanced tissue factor pathway activity and fibrin turnover in the alveolar compartment of patients with interstitial lung disease. Thromb Haemost 2000;83:853-860.
21. Kotani I, Sato A, Hayakaya H, Urano T, Takada Y, Takada A. Increased procoagulant and antifibrinolytic activities in the lungs with idiopathic pulmonary fibrosis. Thromb Res 1995;77:493-504.
22. Griese M. Pulmonary surfactant in health and human lung diseases: state of the art. Eur Respir J 1999;13:1455-1476.
23. Burkhardt A. Alveolitis and collapse in the pathogenesis of pulmonary fibrosis. Am Rev Respir Dis 1989;140:513-524.
24. Ohba T, McDonald JK, Silver RM, Strange C, Carwile LeRoy E, Ludwicka A. Scleroderma bronchoalveolar lavage fluid contains thrombin, a mediator of human lung fibroblast proliferation via induction of platelet-derived growth factor α-receptor. Am J Respir Cell Mol Biol 1994;10:405.
25. Hernandez-Rodriguez NA, Harrison NK, Chambers RC, Gray AJ, Aotuhcott AM, du Bois RM, Black CM, Scully MF, McAnulty RJ. Role of thrombin in pulmonary fibrosis. Lancet 1995;346:1071-1073.
26. Gray AJ, Bishop JE, Reeves JT, Mecham RP, Laurent GJ. Partially degraded fibrin(ogen) stimulates fibroblast proliferation in vitro. Am J Respir Mol Cell Biol 1995;12:684-690.
27. Seeger W, Walmrath D, Grimminger F, Rosseau S, Schütte H, Krämer HJ, Ermert L, Kiss L. Adult respiratory distress syndrome: model systems using isolated perfused rabbit lungs. In: Packer L, editor. Methods in enzymology. Vol. 233: oxygen radicals in biological systems. San Diego: Academic Press; 1994. p. 549-584.
28. Berg RA. Determination of 3-and 4-hydroxyproline. In: Cunnighman LW, Frederiksen DW, editors. Methods in enzymology. Vol. 82: structural and contractile proteins. San Diego: Academic Press; 1982. p. 372-398.
29. Thrall RS, McCormick JR, Jack RM, McReynolds RA, Ward PA. Bleomycin-induced pulmonary fibrosis in the rat: inhibition by indomethacin. Am J Pathol 1979;95:117-130.
30. Jones HA, Schofield JB, Krausz T, Boobis AR, Haslett C. Pulmonary fibrosis correlates with duration of tissue neutrophil activation. Am J Respir Crit Care Med 1998;158:620-628.
31. Piguet PF, Haufman S, Barazzone C, Muller M, Ryffel B, Eugster HP. Resistance of TNF/LT alpha double deficient mice to bleomycininduced fibrosis. Int J Exp Pathol 1997;78:43-48.
32. Zhang K, Gharaee-Kermani M, McGarry B, Remick D, Phan SH. TNF-alpha mediated lung cytokine networking and eosinophil recruitment in pulmonary fibrosis. J Immunol 1997;158:954-959.
33. Lasky JA, Ortiz LA, Tonthat B, Hoyle GW, Corti M, Athas G, Lungarella G, Brody A, Friedman M. Connective tissue growth factor mRNA expression is upregulated in bleomycin-induced lung fibrosis. Am J Physiol 1998;275:L365-L371.
34. Coker RK, Laurent GJ, Shahzeidi S, Lympany PA, du Bois RM, Jefferey PK, McAnulty RJ. Transforming growth factors-beta 1, -beta 2, and -beta 3 stimulate fibroblast procollagen production in vitro but are differentially expressed during bleomycin induced lung fibrosis. Am J Pathol 1997;150:981-991.
35. Temelkovski J, Kumar RK, Maronese SE. Enhanced production of an EGF-like growth factor by parenchymal macrophages following bleomycin-induced pulmonary injury. Exp Lung Res 1997;23:377-391.
36. 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.
37. Robinson PC, Watters LC, King TE, Mason RJ. Idiopathic pulmonary fibrosis: abnormalities in bronchoalveolar lavage fluid phospholipids. Am Rev Respir Dis 1988;137:585-591.
38. McCormack FX, King TE, Voelker DR, Robinson PC, Mason RJ. Idiopathic pulmonary fibrosis: abnormalities in bronchoalveolar lavage content of surfactant protein A. Am Rev Respir Dis 1991;144:160-166.
39. Thrall RS, Swendsen CL, Shannon TH, Kennedy CA, Frederick DS, Grunze MF, Sulavik SB. Correlations of changes in pulmonary surfactant phospholipids with compliance in bleomycin-induced pulmonary fibrosis in the rat. Am Rev Respir Dis 1987;136:113-118.
40. Osanai K, Takahashi K, Sato S, Iwabuchi K, Ohtake K, Sata M, Yasui S. Changes of lung surfactant and pressure-volume curve in bleomycin-induced pulmonary fibrosis. J Appl Physiol 1991;70:1300-1308.
41. Horiuchi T, Mason RJ, Kuroki Y, Cherniack RM. Surface and tissue forces, surfactant protein A, and the phospholipid components of pulmonary surfactant in bleomycin-induced pulmonary fibrosis in the rat. Am Rev Respir Dis 1990;141:1006-1013.
42. Idell S, Gonzales KK, MacArthur CK, Gillies C, Walsh PN, McLarty J, Thrall RS. Bronchoalveolar lavage procoagulant activity in bleomycin-induced lung injury in marmorsets: characterization and relationship to fibrin deposition and fibrosis. Am Rev Respir Dis 1987;136:124-133.
43. Olman MA, Mackman N, Gladson CL, Moser KM, Loskutoff DJ. Changes in procoagulant and fibrinolytic gene expression during bleomycin-induced lung injury in the mouse. J Clin Invest 1995;96:1621-1630.
44. Olman MA, Simmons WL, Pollman DJ, Loftis AY, Bini A, Miller EJ, Fuller GM. Riviera KE. Polymerization of fibrinogen in murine bleomycin-induced lung injury. Am J Physiol 1996;271:L519-L526.
45. Kohler D. Aerosols for systemic treatment. Lung 1990;168:677-684.
46. Schermuly RT, Günther A, Ermert M, Ermert L, Ghofrani HA, Weissmann N, Grimminger F, Seeger W, Walmrath D. Conebulization of surfactant and urokinase restores gas exchange in perfused lungs with alveolar fibrin formation. Am J Physiol Lung Cell Mol Physiol 2001;280:L792-L800.
47. Nieman GF, Goyette D, Paskanik A, Brendenberg CE. Surfactant displacement by plasma lavage results in pulmonary edema. Surgery 1990;107:677-683.
48. Nieman GF, Brendenberg CE. High surface tension pulmonary edema induced by detergent aerosol. J Appl Physiol 1985;58:129-136.
49. Eitzman DT, McCoy RD, Zheng X, Fay WP, Shen T, Ginsburg D, Simon RH. Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest 1996;97:232-237.
50. Howell DC, Goldsack NR, Marshall RP, McAnulty RJ, Starke R, Purdy G, Laurent GJ, Chambers RC. Direct thrombin inhibition reduces lung collagen, accumulation, and connective tissue growth factor mRNA levels in bleomycin-induced pulmonary fibrosis. Am J Pathol 2001;159:1383-1395.
51. Howell DC, Laurent GJ, Chambers RC. Role of thrombin and its major cellular receptor, protease-activated receptor-1, in pulmonary fibrosis. Biochem Soc Trans 2002;30:211-216.
52. Yasui H, Gabazza EC, Taguchi O, Risteli J, Risteli L, Wada H, Yuda H, Kobayashi H, Suzuki K, Adachi Y. Decreased protein C activation is associated with abnormal collagen turnover in the intraalveolar space of patients with interstitial lung disease. Clin Appl Thromb Hemost 2000;6:202-205.
53. Yasui H, Cabazza EC, Tamaki S, Kobayashi T, Hataji O, Yuda H, Shimizu S, Suzuki K, Adachi Y, Taguchi O. Intratracheal administration of activated protein C inhibits bleomycin-induced lung fibrosis in the mouse. Am J Respir Crit Care Med 2001;163:1660-1668.
54. Piguet PF, Van GY, Guo J. Heparin attenuates bleomycin but not silicainduced pulmonary fibrosis in mice: possible relationship with involvement of myofibroblasts in bleomycin, and fibroblasts in silica-induced fibrosis. Int J Exp Pathol 1996;77:155-161.
55. Sisson TH, Hattori N, Xu Y, Simon RH. Treatment of bleomcyin-induced pulmonary fibrosis by transfer of urokinase-type plasminogen activator genes. Hum Gene Ther 1999;10:2315-2323.
56. Hattori N, Degen JL, Sisson TH, Liu H, Moore BB, Pandrangi RG, Simon RH, Drew AF. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J Clin Invest 2000;106:1341-1350.