Long-term treatment with fasudil improves bleomycin-induced pulmonary fibrosis and pulmonary hypertension via inhibition of Smad2/3 phosphorylation

Pulmonary Pharmacology and Therapeutics

Volumn 26, Issue 6, 2013, Pages 635-643

  Bei, Yihua ^a,b   Hua Huy, ThÔng ^a   Duong Quy, Sy ^a   Nguyen, Viet Ha ^a   Chen, Weihua ^a,b   Nicco, Carole ^a   Batteux, Frédéric ^a   Dinh Xuan, Anh Tuan ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Bleomycin; Pulmonary fibrosis; Pulmonary hypertension; Rho kinases; RhoA

Indexed keywords

BLEOMYCIN; COLLAGEN; FASUDIL; RHO KINASE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTICLE; B LYMPHOCYTE; COMPETITIVE INHIBITION; CONTROLLED STUDY; HEART VENTRICLE HYPERTROPHY; HEMODYNAMIC MONITORING; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; LUNG FIBROSIS; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY HYPERTENSION; PULMONARY VASCULAR DISEASE; STAINING; SYSTOLIC BLOOD PRESSURE; T LYMPHOCYTE; TREATMENT DURATION;

BALF; BLEOMYCIN; BLM; BRONCHOALVEOLAR LAVAGE FLUID; CONNECTIVE TISSUE DISEASE; CTD; IDIOPATHIC PULMONARY FIBROSIS; ILD; INTERSTITIAL LUNG DISEASE; IPF; MEDIAL WALL THICKNESS; MWT; PF; PH; PULMONARY FIBROSIS; PULMONARY HYPERTENSION; PULMONARY VASCULAR RESISTANCE; PVR; RHO-KINASE; RHO-KINASES; RHOA; RIGHT VENTRICULAR SYSTOLIC PRESSURE; ROCK; RVSP;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANIMALS; BLEOMYCIN; DISEASE MODELS, ANIMAL; HUMANS; HYPERTENSION, PULMONARY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INJECTIONS, INTRAPERITONEAL; MALE; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PULMONARY FIBROSIS; SEVERITY OF ILLNESS INDEX; SMAD2 PROTEIN; SMAD3 PROTEIN; TIME FACTORS;

EID: 84887997600     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2013.07.008     Document Type: Article

References (48)

1. Behr J., Ryu J.H. Pulmonary hypertension in interstitial lung disease. Eur Respir J 2008, 31:1357-1367.
2. Duong-Quy S., Bei Y., Liu Z., Dinh-Xuan A.T. Role of Rho-kinase and its inhibitors in pulmonary hypertension. Pharmacol Ther 2013, 137:352-364.
3. Loirand G., Guérin P., Pacaud P. Rho kinases in cardiovascular physiology and pathophysiology. Circ Res 2006, 98:322-334.
4. Barman S.A., Zhu S., White R.E. RhoA/Rho-kinase signaling: a therapeutic target in pulmonary hypertension. Vasc Health Risk Manag 2009, 5:663-671.
5. Guilluy C., Sauzeau V., Rolli-Derkinderen M., Guérin P., Sagan C., Pacaud P., et al. Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension. Br J Pharmacol 2005, 146:1010-1018.
6. Abe K., Tawara S., Oi K., Hizume T., Uwatoku T., Fukumoto Y., et al. Long-term inhibition of Rho-kinase ameliorates hypoxia-induced pulmonary hypertension in mice. JCardiovasc Pharmacol 2006, 48:280-285.
7. Tawara S., Fukumoto Y., Shimokawa H. Effects of combined therapy with a Rho-kinase inhibitor and prostacyclin on monocrotaline-induced pulmonary hypertension in rats. JCardiovasc Pharmacol 2007, 50:195-200.
8. Jiang B.H., Tawara S., Abe K., Takaki A., Fukumoto Y., Shimokawa H. Acute vasodilator effect of fasudil, a Rho-kinase inhibitor, in monocrotaline-induced pulmonary hypertension in rats. JCardiovasc Pharmacol 2007, 49:85-89.
9. Mouchaers K.T.B., Schalij I., de Boer M.A., Postmus P.E., van Hinsbergh V.W.M., van Nieuw Amerongen G.P., et al. Fasudil reduces monocrotaline-induced pulmonary arterial hypertension: comparison with bosentan and sildenafil. Eur Respir J 2010, 36:800-807.
10. Fukumoto Y., Matoba T., Ito A., Tanaka H., Kishi T., Hayashidani S., et al. Acute vasodilator effects of a Rho-kinase inhibitor, fasudil, in patients with severe pulmonary hypertension. Heart 2005, 91:391-392.
11. Ishikura K., Yamada N., Ito M., Ota S., Nakamura M., Isaka N., et al. Beneficial acute effects of rho-kinase inhibitor in patients with pulmonary arterial hypertension. Circ J 2006, 70:174-178.
12. Li F., Xia W., Yuan S., Sun R. Acute inhibition of Rho-kinase attenuates pulmonary hypertension in patients with congenital heart disease. Pediatr Cardiol 2009, 30:363-366.
13. Fujita H., Fukumoto Y., Saji K., Sugimura K., Demachi J., Nawata J., et al. Acute vasodilator effects of inhaled fasudil, a specific Rho-kinase inhibitor, in patients with pulmonary arterial hypertension. Heart Vessels 2010, 25:144-149.
14. Moeller A., Ask K., Warburton D., Gauldie J., Kolb M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis?. Int J Biochem Cell Biol 2008, 40:362-382.
15. Shimizu Y., Dobashi K., Iizuka K., Horie T., Suzuki K., Tukagoshi H., et al. Contribution of small GTPase Rho and its target protein rock in a murine model of lung fibrosis. Am J Respir Crit Care Med 2001, 163:210-217.
16. Ou X., Feng Y., Wen F., Huang X., Xiao J., Wang K., et al. Simvastatin attenuates bleomycin-induced pulmonary fibrosis in mice. Chin Med J 2008, 121:1821-1829.
17. Hemnes A.R., Zaiman A., Champion H.C. PDE5A inhibition attenuates bleomycin-induced pulmonary fibrosis and pulmonary hypertension through inhibition of ROS generation and RhoA/Rho kinase activation. Am J Physiol Lung Cell Mol Physiol 2008, 294:L24-L33.
18. Schroll S., Arzt M., Sebah D., Nüchterlein M., Blumberg F., Pfeifer M. Improvement of bleomycin-induced pulmonary hypertension and pulmonary fibrosis by the endothelin receptor antagonist Bosentan. Respir Physiol Neurobiol 2010, 170:32-36.
19. Ortiz L.A., Champion H.C., Lasky J.A., Gambelli F., Gozal E., Hoyle G.W., et al. Enalapril protects mice from pulmonary hypertension by inhibiting TNF-mediated activation of NF-kappaB and AP-1. Am J Physiol Lung Cell Mol Physiol 2002, 282:L1209-L1221.
20. McNamara P.J., Murthy P., Kantores C., Teixeira L., Engelberts D., van Vliet T., et al. Acute vasodilator effects of Rho-kinase inhibitors in neonatal rats with pulmonary hypertension unresponsive to nitric oxide. Am J Physiol Lung Cell Mol Physiol 2008, 294:L205-L213.
21. Jiang C., Huang H., Liu J., Wang Y., Lu Z., Xu Z. Fasudil, a rho-kinase inhibitor, attenuates bleomycin-induced pulmonary fibrosis in mice. Int J Mol Sci 2012, 13:8293-8307.
22. Biernacka A., Dobaczewski M., Frangogiannis N.G. TGF-β signaling in fibrosis. Growth Factors 2011, 29:196-202.
23. Kamaraju A.K., Roberts A.B. Role of Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-beta-mediated Smad-dependent growth inhibition of human breast carcinoma cells invivo. JBiol Chem 2005, 280:1024-1036.
24. Chen S., Crawford M., Day R.M., Briones V.R., Leader J.E., Jose P.A., et al. RhoA modulates Smad signaling during transforming growth factor-beta-induced smooth muscle differentiation. JBiol Chem 2006, 281:1765-1770.
25. Nozik-Grayck E., Suliman H.B., Majka S., Albietz J., Van Rheen Z., Roush K., et al. Lung EC-SOD overexpression attenuates hypoxic induction of Egr-1 and chronic hypoxic pulmonary vascular remodeling. Am J Physiol Lung Cell Mol Physiol 2008, 295:L422-L430.
26. Sur S., Wild J.S., Choudhury B.K., Sur N., Alam R., Klinman D.M. Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. JImmunol 1999, 162:6284-6293.
27. Servettaz A., Goulvestre C., Kavian N., Nicco C., Guilpain P., Chéreau C., et al. Selective oxidation of DNA topoisomerase 1 induces systemic sclerosis in the mouse. JImmunol 2009, 182:5855-5864.
28. Bringardner B.D., Baran C.P., Eubank T.D., Marsh C.B. The role of inflammation in the pathogenesis of idiopathic pulmonary fibrosis. Antioxid Redox Signaling 2008, 10:287-302.
29. Kamata H., Tasaka S., Inoue K., Miyamoto K., Nakano Y., Shinoda H., et al. Carbon black nanoparticles enhance bleomycin-induced lung inflammatory and fibrotic changes in mice. Exp Biol Med (Maywood) 2011, 236:315-324.
30. Izbicki G., Segel M.J., Christensen T.G., Conner M.W., Breuer R. Time course of bleomycin-induced lung fibrosis. Int J Exp Pathol 2002, 83:111-119.
31. Nagatoya K., Moriyama T., Kawada N., Takeji M., Oseto S., Murozono T., et al. Y-27632 prevents tubulointerstitial fibrosis in mouse kidneys with unilateral ureteral obstruction. Kidney Int 2002, 61:1684-1695.
32. He Y., Xu H., Liang L., Zhan Z., Yang X., Yu X., et al. Antiinflammatory effect of Rho kinase blockade via inhibition of NF-kappaB activation in rheumatoid arthritis. Arthritis Rheum 2008, 58:3366-3376.
33. Okamoto H., Yoshio T., Kaneko H., Yamanaka H. Inhibition of NF-kappaB signaling by fasudil as a potential therapeutic strategy for rheumatoid arthritis. Arthritis Rheum 2010, 62:82-92.
34. Montaner S., Perona R., Saniger L., Lacal J.C. Multiple signalling pathways lead to the activation of the nuclear factor kappaB by the Rho family of GTPases. JBiol Chem 1998, 273:12779-12785.
35. Gurujeyalakshmi G., Wang Y., Giri S.N. Taurine and niacin block lung injury and fibrosis by down-regulating bleomycin-induced activation of transcription nuclear factor-kappaB in mice. JPharmacol Exp Ther 2000, 293:82-90.
36. Wipff P.-J., Rifkin D.B., Meister J.-J., Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. JCell Biol 2007, 179:1311-1323.
37. Huang X., Gai Y., Yang N., Lu B., Samuel C.S., Thannickal V.J., et al. Relaxin regulates myofibroblast contractility and protects against lung fibrosis. Am J Pathol 2011, 179:2751-2765.
38. Tomasek J.J., Vaughan M.B., Kropp B.P., Gabbiani G., Martin M.D., Haaksma C.J., et al. Contraction of myofibroblasts in granulation tissue is dependent on Rho/Rho kinase/myosin light chain phosphatase activity. Wound Repair Regen 2006, 14:313-320.
39. Parizi M., Howard E.W., Tomasek J.J. Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Exp Cell Res 2000, 254:210-220.
40. Zhao J., Shi W., Wang Y.-L., Chen H., Bringas P., Datto M.B., et al. Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2002, 282:L585-L593.
41. Bujak M., Ren G., Kweon H.J., Dobaczewski M., Reddy A., Taffet G., et al. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation 2007, 116:2127-2138.
42. Sato M., Muragaki Y., Saika S., Roberts A.B., Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. JClin Invest 2003, 112:1486-1494.
43. Flanders K.C., Sullivan C.D., Fujii M., Sowers A., Anzano M.A., Arabshahi A., et al. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am J Pathol 2002, 160:1057-1068.
44. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
45. Bhowmick N.A., Ghiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E., et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001, 12:27-36.
46. Xu J., Lamouille S., Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res 2009, 19:156-172.
47. Engel M.E., McDonnell M.A., Law B.K., Moses H.L. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. JBiol Chem 1999, 274:37413-37420.
48. Renzoni E.A., Walsh D.A., Salmon M., Wells A.U., Sestini P., Nicholson A.G., et al. Interstitial vascularity in fibrosing alveolitis. Am J Respir Crit Care Med 2003, 167:438-443.