The antifibrotic effects of plasminogen activation occur via prostaglandin E2 synthesis in humans and mice

Journal of Clinical Investigation

Volumn 120, Issue 6, 2010, Pages 1950-1960

  Bauman, Kristy A ^a   Wettlaufer, Scott H ^a   Okunishi, Katsuhide ^a   Vannella, Kevin M ^b   Stoolman, Joshua S ^a   Huang, Steven K ^a   Courey, Anthony J ^a   White, Eric S ^a   Hogaboam, Cory M ^a   Simon, Richard H ^a   Toews, Galen B ^a   Sisson, Thomas H ^a   Moore, Bethany B ^a   Peters Golden, Marc ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; COLLAGEN; CYCLOOXYGENASE 2; PLASMIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROSTAGLANDIN E2; PROTEINASE ACTIVATED RECEPTOR 1; SCATTER FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FIBRINOLYSIS; FIBROSING ALVEOLITIS; HUMAN; HUMAN CELL; LUNG FIBROBLAST; LUNG FIBROSIS; MOUSE; NONHUMAN; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UPREGULATION;

ADULT; ANIMALS; BLEOMYCIN; COLLAGEN; CYCLOOXYGENASE 2; DINOPROSTONE; EXTRACELLULAR MATRIX; FIBRINOLYSIN; FIBROBLASTS; FIBROSIS; HUMANS; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMINOGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PULMONARY FIBROSIS; RECEPTOR, PAR-1;

EID: 77953189863     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI38369     Document Type: Article

References (69)

1. Bertozzi P, et al. Depressed bronchoalveolar urokinase activity in patients with adult respiratory distress syndrome. N Engl J Med. 1990;322(13):890-897. (Pubitemid 20108378)
2. Chapman HA, Allen CL, Stone OL. Abnormalities in pathways of alveolar fibrin turnover among patients with interstitial lung disease. Am Rev Respir Dis. 1986;133(3):437-443. (Pubitemid 16126278)
3. Idell S, et al. Local abnormalities in coagulation and fibrinolytic pathways predispose to alveolar fibrin deposition in the adult respiratory distress syndrome. J Clin Invest. 1989;84(2):695-705. (Pubitemid 19197006)
4. Eitzman DT, et al. Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest. 1996;97(1):232-237.
5. Swaisgood CM, French EL, Noga C, Simon RH, Ploplis VA. The development of bleomycin-induced pulmonary fibrosis in mice deficient for components of the fibrinolytic system. Am J Pathol. 2000;157(1):177-187. (Pubitemid 30641735)
6. Hattori N, et al. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J Clin Invest. 2000;106(11):1341-1350.
7. Sisson TH, Hanson KE, Subbotina N, Patwardhan A, Hattori N, Simon RH. Inducible lung-specific urokinase expression reduces fibrosis and mortality after lung injury in mice. Am J Physiol Lung Cell Mol Physiol. 2002;283(5):L1023-L1032.
8. Sisson TH, Hattori N, Xu Y, Simon RH. Treatment of bleomycin-induced pulmonary fibrosis by transfer of urokinase-type plasminogen activator genes. Hum Gene Ther. 1999;10(14):2315-2323. (Pubitemid 29459842)
9. Gunther A, et al. Prevention of bleomycin-induced lung fibrosis by aerosolization of heparin or urokinase in rabbits. Am J Respir Crit Care Med. 2003;168(11):1358-1365. (Pubitemid 37487332)
10. Ploplis VA, et al. A total fibrinogen deficiency is compatible with the development of pulmonary fibrosis in mice. Am J Pathol. 2000;157(3):703-708. (Pubitemid 32109361)
11. Matsuoka H, Sisson TH, Nishiuma T, Simon RH. Plasminogen-mediated activation and release of hepatocyte growth factor from extracellular matrix. Am J Respir Cell Mol Biol. 2006;35(6):705-713. (Pubitemid 44901860)
12. Baum B, Moss S, Breul R, Crystal R. Effect of cyclic AMP on the intracellular degradation of newly synthesized collagen. J Biol Chem. 1980;255(7):2843-2847. (Pubitemid 10089301)
13. Goldstein R, Polgar P. The effect and interaction of bradykinin and prostaglandins on protein and collagen production by lung fibroblasts. J Biol Chem. 1982;257(15):8630-8633. (Pubitemid 12004184)
14. Korn J, Halushka P, Leroy E. Mononuclear cell modulation of connective tissue function: suppression of fibroblast growth by stimulation of endogenous prostaglandin production. J Clin Invest. 1980;65(2):543-554. (Pubitemid 10159885)
15. 2 inhibits collagen expression and proliferation in patient-derived normal lung fibroblasts via E prostanoid 2 receptor and cAMP signaling. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L405-L413.
16. 2 on fibronectin release from human alveolar macrophages. Am Rev Respir Dis. 1990;141(4 pt 1):965-969.
17. Borok Z, et al. Augmentation of functional prostaglandin E levels on the respiratory epithelial surface by aerosol administration of prostaglandin E. Am Rev Respir Dis. 1991;144(5):1080-1084.
18. 2 and to express cyclooxygenase-2. J Clin Invest. 1995;95(4):1861-1868.
19. 2 production in normal and fibrotic lung fibroblasts: potential implications for the evolution of the inflammatory process. Am J Respir Cell Mol Biol. 2000;22(5):628-634.
20. McAnulty RJ, Hernandez-Rodriguez NA, Mutsaers S, Coker R, Laurent G. Indomethacin suppresses the anti-proliferative effects of transforming growth factor-beta isoforms on fibroblast cell cultures. Biochem J. 1997;321(pt 3):639-643. (Pubitemid 27084870)
21. Coward WR, Watts K, Feghali-Bostwick CA, Knox A, Pang L. Defective histone acetylation is responsible for the diminished expression of cyclooxygenase 2 in idiopathic pulmonary fibrosis. Mol Cell Biol. 2009;29(15):4325-4339.
22. Moore BB, et al. GM-CSF regulates bleomycin-induced pulmonary fibrosis via a prostaglandin-dependent mechanism. J Immunol. 2000;165(7):4032-4039.
23. Keerthisingam C, et al. Cyclooxygenase-2 deficiency results in a loss of the anti-proliferative response to transforming growth factor-β in human fibrotic lung fibroblasts and promotes bleomycin-induced fibrosis in mice. Am J Pathol. 2001;158(4):1411-1422. (Pubitemid 32281305)
24. 2. J Immunol. 2005;174(9):5644-5649.
25. Arras M, et al. IL-9 protects against bleomycin-induced lung injury: involvement of prostaglandins. Am J Pathol. 2005;166(1):107-115. (Pubitemid 40051664)
26. 2. Am J Physiol Lung Cell Mol Physiol. 2003;284(2):L342-L349.
27. 2 efficacy on prevention and protection from bleomycin-induced lung injury and fibrosis. Am J Respir Cell Mol Biol. 2009;41(1):50-58.
28. 2 resistance in fibroblasts from patients with usual interstitial pneumonia. Am J Respir Crit Care Med. 2008;177(1):66-74.
29. Allan EH, Martin TJ. Prostaglandin E2 regulates production of plasminogen activator isoenzymes, urokinase receptor, and plasminogen activator inhibitor-1 in primary cultures of rat calvarial osteoblasts. J Cell Physiol. 1995;165(3):521-529. (Pubitemid 3008503)
30. Iwamoto J, et al. Expression of urokinase-type plasminogen activator and its receptor in gastric fibroblasts and effects of nonsteroidal antiinflammatory drugs and prostaglandin. Dig Dis Sci. 2003;48(12):2247-2256. (Pubitemid 38021727)
31. Pai R, Nakamura T, Moon WS, Tarnawski AS. Prostaglandins promote colon cancer cell invasion; signaling by cross-talk between two distinct growth factor receptors. FASEB J. 2003;17(12):1640-1647. (Pubitemid 37100065)
32. Hattori N, et al. The plasminogen activation system reduces fibrosis in the lung by a hepatocyte growth factor-dependent mechanism. Am J Pathol. 2004;164(3):1091-1098. (Pubitemid 38235490)
33. Peters-Golden M, et al. Protection from pulmonary fibrosis in leukotriene-deficient mice. Am J Respir Crit Care Med. 2002;165(2):229-235. (Pubitemid 34084463)
34. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med. 1994;1(1):71-81.
35. Moore BB, Murray L, Das A, Wilke CA, Herrygers AB, Toews GB. The role of CCL12 in the recruitment of fibrocytes and lung fibrosis. Am J Respir Cell Mol Biol. 2006;35(2):175-181. (Pubitemid 44175316)
36. Kolodsick JE, Peters-Golden M, Larios J, Toews GB, Thannickal VJ, Moore BB. Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am J Respir Cell Mol Biol. 2003;29(5):537-544. (Pubitemid 37357704)
37. -/- mice: implications for fibroproliferation. Am J Physiol Lung Cell Mol Physiol. 2003;284(6):L1103-L1111.
38. Jenkins RG, et al. Ligation of protease-activated receptor 1 enhances alpha(v)beta6 integrin-dependent TGF-beta activation and promotes acute lung injury. J Clin Invest. 2006;116(6):1606-1614. (Pubitemid 43911014)
39. Syeda F, et al. Cyclooxygenase-2 induction and prostacyclin release by protease-activated receptors in endothelial cells require cooperation between mitogen-activated protein kinase and NF-kappaB pathways. J Biol Chem. 2006;281(17):11792-11804.
40. Lyon M, Deakin J, Mizuno K, Nakamura T, Gallagher J. Interaction of hepatocyte growth factor with heparin sulfate. Elucidation of the major heparan sulfate structural determinants. J Biol Chem. 1994;269(15):11216-11223.
41. Mizuno K, Nakamura T. Proteolytic activation of a single chain precursor of hepatocyte growth factor by extracellular serine-protease. Biochem Biophys Res Commun. 1992;189(3):1631-1638.
42. Shanmukhappa K, Matte U, Degen JL, Bezerra JA. Plasmin-mediated proteolysis is required for hepatocyte growth factor activation during liver repair. J Biol Chem. 2009;284(19):12917-12923.
43. 2 is a potent inhibitor of epithelial-to-mesenchymal transition: interaction with hepatocyte growth factor. Am J Physiol Renal Physiol. 2006;291(6):F1323-F1331.
44. Lee YH, Suzuki YJ, Griffin AJ, Day RM. Hepatocyte growth factor regulates cyclooxygenase-2 expression via beta-catenin, AKT, and p42/p44 MAPK in human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2008;294(4):L778-L786.
45. Christensen JG, et al. A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res. 2003;63(21):7345-7355.
46. 2. Am J Physiol Lung Cell Mol Physiol. 2005;288(5):L793-L802.
47. Trejo J. Protease-activated receptors: new concepts in regulation of G protein-coupled receptor signaling and trafficking. J Pharmacol Exp Ther. 2003;307(2):437-442. (Pubitemid 37310654)
48. 2 and selective EP agonists on chemotaxis of human neutrophils. Br J Pharmacol. 1995;116(7):2903-2908.
49. 2 regulates wound closure in airway epithelium. Am J Physiol Lung Cell Mol Physiol. 2001;280(3):L421-L431.
50. 2 inhibits fibroblast chemotaxis. Am J Physiol Lung Cell Mol Physiol. 2001;281(5):L1257-L1263.
51. 2 inhibits fibroblast migration by E-prostanoid 2 receptor-mediated increase in PTEN activity. Am J Respir Cell Mol Biol. 2005;32(2):135-141.
52. 2 inhibition of TGF-beta1-induced myofibroblast differentiation is SMAD-independent but involves cell shape and adhesion-dependent signaling. Am J Physiol Lung Cell Mol Physiol. 2007;293(2):L417-L428.
53. Mandal SK, Rao LV, Tran TT, Pendurthi UR. A novel mechanism of plasmin-induced mitogenesis in fibroblasts. J Thromb Haemost. 2005;3(1):163-169.
54. Horowitz JC, Rogers DS, Simon RH, Sisson TH, Thannickal VJ. Plasminogen activation-induced pericellular fibronectin proteolysis promotes fibroblast apoptosis. Am J Respir Cell Mol Biol. 2007;38(1):78-87.
55. Lama V, Moore B, Christensen P, Toews G, Peters-Golden M. Prostaglandin E2 synthesis and suppression of fibroblast proliferation by alveolar epithelial cells is cyclooxygenase-2-dependent. Am J Respir Cell Mol Biol. 2002;27(6):752-758. (Pubitemid 35381185)
56. Bogatkevich GS, et al. Down-regulation of collagen and connective tissue growth factor expression with hepatocyte growth factor in lung fibroblasts from white scleroderma patients via two signaling pathways. Arthritis Rheum. 2007;56(10):3468-3477.
57. Gong R, Rifai A, Tolbert EM, Centracchio JN, Dworkin LD. Hepatocyte growth factor modulates matrix metalloproteinases and plasminogen activator/plasmin proteolytic pathways in progressive renal interstitial fibrosis. J Am Soc Nephrol. 2003;14(12):3047-3060. (Pubitemid 37509283)
58. Marchand-Adam S, et al. Defect of pro-hepatocyte growth factor activation by fibroblasts in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2006;174(1):58-66. (Pubitemid 43955245)
59. Dohi M, Hasegawa T, Yamamoto K, Marshall BC. Hepatocyte growth factor attenuates collagen accumulation in a murine model of pulmonary fibrosis. Am J Respir Crit Care Med. 2000;162(6):2302-2307. (Pubitemid 32051704)
60. Gazdhar A, et al. Gene transfer of hepatocyte growth factor by electroporation reduces bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L529-L536. (Pubitemid 46271606)
61. Watanabe M, et al. Hepatocyte growth factor gene transfer to alveolar septa for effective suppression of lung fibrosis. Mol Ther. 2005;12(1):58-67.
62. Sherriff-Tadano R, et al. Antifibrotic effects of hepatocyte growth factor on scleroderma fibroblasts and analysis of its mechanism. Mod Rheumatol. 2006;16(6):364-371.
63. Matsumoto-Taniura N, Matsumoto K, Nakamura T. Prostaglandin production in mouse mammary tumour cells confers invasive growth potential by inducing hepatocyte growth factor in stromal fibroblasts. Br J Cancer. 1999;81(2):194-202.
64. Fan S, et al. The cytokine hepatocyte growth factor/scatter factor inhibits apoptosis and enhances DNA repair by a common mechanism involving signaling through phosphatidyl inositol 3′ kinase. Oncogene. 2000;19(18):2212-2223.
65. Shukla MN, Rose JL, Ray R, Lathrop KL, Ray A, Ray P. Hepatocyte growth factor inhibits epithelial to myofibroblast transition in lung cells via SMAD7. Am J Respir Cell Mol Biol. 2009;40(6):643-653.
66. Carmeliet P, et al. Plasminogen activator inhibitor-1 gene-deficient mice. I. Generation by homologous recombination and characterization. J Clin Invest. 1993;92(6):2746-2755.
67. Corti M, Brody AR, Harrison JH. Isolation and primary culture of murine alveolar type II cells. Am J Respir Cell Mol Biol. 1996;14(4):309-315.
68. 2 resistance in fibroblasts from patients with usual interstitial pneumonia. Am J Respir Crit Care Med. 2008;177(1):66-74.
69. Powell-Jones CH. Rapid SDS-PAGE zymography of plasminogen activators. Thromb Res. 1988;49(2):299-302.