Hydrogen sulfide protects against bleomycin-induced pulmonary fibrosis in rats by inhibiting NF-κB expression and regulating Th1/Th2 balance

Toxicology Letters

Volumn 224, Issue 3, 2014, Pages 387-394

  Cao, Hua ^a   Zhou, Xiaohong ^a   Zhang, Jianping ^a   Huang, Xinli ^a   Zhai, Yu ^a   Zhang, Xuejing ^a   Chu, Li ^a  

^a HEBEI UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Bleomycin; Cytokine; Hydrogen sulfide; Nuclear factor kappa B; Pulmonary fibrosis

Indexed keywords

BLEOMYCIN; GAMMA INTERFERON; HYDROGEN SULFIDE; HYDROXYPROLINE; INTERLEUKIN 4; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EOSINOPHIL COUNT; LUNG FIBROSIS; LUNG LAVAGE; LYMPHOCYTE COUNT; MACROPHAGE; MALE; NEUTROPHIL COUNT; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RAT; TH1 CELL; TH1 TH2 BALANCE; TH2 CELL;

EID: 84890153660     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.11.008     Document Type: Article

References (40)

1. Cooper J.A.D. Pulmonary fibrosis pathways are slowly coming into light. Am. J. Respir. Cell Mol. Biol. 2000, 22:520-523. (PubMed: 10783121).
2. Bjoraker J.A., Ryu J.H., Edwin M.K., Myers J.L., Tazelaar H.D., Schroeder D.R., Offord K.P. Prognostic significance of histopathologic subsets in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 1998, 157:199-203. (PubMed: 9445300).
3. Braga P.C., Dal Sasso M., Culici M., Spallino A., Marabini L., Bianchi T., Nappi G. Effects of sulphurous water on human neutrophil elastase release. Ther. Adv. Respir. Dis. 2010, 4:333-340. (PubMed: 20650977).
4. Cortijo J., Cerda-Nicolas M., Serrano A., Bioque G., Estrela J.M., Santangelo F., Esteras A., Llombart-Bosch A., Morcillo E.J. Attenuation by oral N-acetylcysteine of bleomycin-induced lung injury in rats. Eur. Respir. J. 2001, 17:1228-1235. (PubMed: 11491169).
5. Cowburn A.S., Deighton J., Walmsley S.R., Chilvers E.R. The survival effect of TNF-α in human neutrophils is mediated via NF-κB-dependent IL-8 release. Eur. J. Immunol. 2004, 34:1733-1743. (PubMed: 15162444).
6. Fan H.N., Wang H.J., Yang-Dan C.R., Ren L., Wang C., Li Y.F., Deng Y. Protective effects of hydrogen sulfide on oxidative stress and fibrosis in hepatic stellate cells. Mol. Med. Rep. 2013, 7:247-253. (PubMed: 23129058).
7. Fang L.P., Li H., Tang C.S., Geng B., Qi Y.F., Liu X.M. Hydrogen sulfide attenuates the pathogenesis of pulmonary fibrosis induced by bleomycin in rats. Can. J. Physiol. Pharmacol. 2009, 87:531-538. (PubMed: 19767876).
8. Fang L.P., Lin Q., Tang C.S., Liu X.M. Hydrogen sulfide suppresses migration, proliferation and myofibroblast transdifferentiation of human lung fibroblasts. Pulm. Pharmacol. Ther. 2009, 22:554-561. (PubMed: 19651225).
9. Fang L.P., Lin Q., Tang C.S., Liu X.M. Hydrogen sulfide attenuates epithelial-mesenchymal transition of human alveolar epithelial cells. Pharmacol. Res. 2010, 61:298-305. (PubMed: 19913099).
10. Furuie H., Yamasaki H., Suga M., Ando M. Altered accessory cell function of alveolar macrophages: a possible mechanism for induction of Th2 secretory profile in idiopathic pulmonary fibrosis. Eur. Respir. J. 1997, 10:787-794. (PubMed: 9150314).
11. Gurujeylakshmi G., Wang Y., Giri S.N. Taurine and niacin block lung injury and fibrosis by down-regulating bleomycin-induced activation of transcription nuclear factor-κB in mice. J. Pharmacol. Exp. Ther. 2000, 293:82-90. (PubMed: 10734156).
12. Huang X.L., Ma H.J., Zhou X.H., Fan Y.M., Xian X.H., Cao H. Effect of exogenous hydrogen sulfide on polymorphonuclear neutrophil accumulation in acute lung injury rat induced by lipopolysaccharides and its mechanism. Zhongguo Ying Yong Sheng Li Xue Za Zhi 2010, 26:477-480. (PubMed: 21328993).
13. Inayama M., Nishioka Y., Azuma M., Muto S., Aono Y., Makino H., Tani K., Uehara H., Izumi K., Itai A., Sone S. A novel IκB kinase-β inhibitor ameliorates bleomycin-induced pulmonary fibrosis in mice. Am. J. Respir. Crit. Care Med. 2006, 173:1016-1022. (PubMed: 16456147).
14. Ishii H., Takada K. Bleomycin induces E-selectin expression in cultured umbilical vein endothelial cells by increasing its mRNA levels through activation of NF-κB/Rel. Toxicol. Appl. Pharmacol. 2002, 184:88-97. (PubMed: 12408953).
15. Jiang D., Liang J., Hodge J., Lu B., Zhu Z., Yu S., Fan J., Gao Y., Yin Z., Homer R., Gerard C., Noble P.W. Regulation of pulmonary fibrosis by chemokine receptor CXCR3. J. Clin. Invest. 2004, 114:291-299. (PubMed: 15254596).
16. Kalayarasan S., Sriram N., Sudhandiran G. Diallyl sulfide attenuates bleomycin-induced pulmonary fibrosis: critical role of iNOS, NF-κB, TNF-α and IL-1β. Life Sci. 2008, 82:1142-1153. (PubMed: 18462759).
17. Kawai K., Akaza H. Bleomycin-induced pulmonary toxicity in chemotherapy for testicular cancer. Expert. Opin. Drug. Saf. 2003, 2:587-596. (PubMed: 14585067).
18. Keane M.P., Belperio J.A., Arenberg D.A., Burdick M.D., Xu Z.J., Xue Y.Y., Strieter R.M. IFN-γ-inducible protein-10 attenuates bleomycin-induced pulmonary fibrosis via inhibition of angiogenesis. J. Immunol. 1999, 163:5686-5692. (PubMed: 10553099).
19. Kikuchi N., Ishii Y., Morishima Y., Yageta Y., Haraguchi N., Itoh K., Yamamoto M., Hizawa N. Nrf2 protects against pulmonary fibrosis by regulating the lung oxidant level and Th1/Th2 balance. Respir. Res. 2010, 11:31. (PubMed: 20298567).
20. Kimura Y., Goto Y., Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox Signal. 2010, 12:1-13. (PubMed: 19852698).
21. Kroegel C., Mock B., Hengst U., Reissig A. Interferon-γ-1b: therapeutic option in advanced idiopathic pulmonary fibrosis?. Respiration 2004, 71:656-657. (PubMed: 15627882).
22. Kunkel S.L., Lukacs N.W., Strieter R.M., Chensue S.W. Th1 and Th2 responses regulate experimental lung granuloma development. Sarcoidosis Vasc. Diffuse Lung Dis. 1996, 13:120-128. (PubMed: 8893380).
23. Liu X., Kohyama T., Wang H., Zhu Y.K., Wen F.Q., Kim H.J., Romberger D.J., Rennard S.I. Th2 cytokine regulation of type I collagen gel contraction mediated by human lung mesenchymal cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2002, 282:L1049-L1056. (PubMed: 11943670).
24. Lou L.X., Geng B., Du J.B., Tang C.S. Hydrogen sulphide-induced hypothermia attenuates stress-related ulceration in rats. Clin. Exp. Pharmacol. Physiol. 2008, 35:223-228. (PubMed: 17941893).
25. Moore B.B., Hogaboam C.M. Murine models of pulmonary fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 2008, 294:L152-L160. (PubMed: 17993587).
26. Pociask D.A., Chen K., Choi S.M., Oury T.D., Steele C., Kolls J.K. γδ T cells attenuate bleomycin-induced fibrosis through the production of CXCL10. Am. J. Pathol. 2010, 178:1167-1176. (PubMed: 21356368).
27. Postlethwaite A.E., Holness M.A., Katai H., Raghow R. Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J. Clin. Invest. 1992, 90:1479-1485. (PubMed: 1401080).
28. Schwaiblmair M., Behr W., Haeckel T., Märkl B., Foerg W., Berghaus T. Drug induced interstitial lung disease. Open Respir. Med. J. 2012, 6:63-74. (PubMed: 22896776).
29. Segel M.J., Izbicki G., Cohen P.Y., Or R., Christensen T.G., Wallach-Dayan S.B., Breuer R. Role of interferon-γ in the evolution of murine bleomycin lung fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 2003, 285:L1255-L1262. (PubMed: 12857673).
30. Sempowski G.D., Derdak S., Phipps R.P. Interleukin-4 and interferon-γ discordantly regulate collagen biosynthesis by functionally distinct lung fibroblast subsets. J. Cell Physiol. 1996, 167:290-296. (PubMed: 8613470).
31. Sen C.K., Traber K.E., Packer L. Inhibition of NF-κ B activation in human T-cell lines by anetholdithiolthione. Biochem. Biophys. Res. Commun. 1996, 218:148-153. (PubMed: 8573121).
32. Shen Q., Qin Z., Lu A. Preventive effect of exogenous hydrogen sulfide on hepatic fibrosis in rats. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2012, 37:911-915. (PubMed: 23000765).
33. Smith R.E., Strieter R.M., Phan S.H., Lukacs N., Kunkel S.L. TNF and IL-6 mediate MIP-1α expression in bleomycin-induced lung injury. J. Leukoc. Biol. 1998, 64:528-536. (PubMed: 9766634).
34. Strieter R.M., Starko K.M., Enelow R.I., Noth I., Valentine V.G., Idiopathic Pulmonary Fibrosis Biomarkers Study Group Effects of interferon-gamma 1b on biomarker expression in patients with idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care. Med. 2004, 170:133-140. (PubMed: 15044205).
35. Szapiel S.V., Elson N.A., Fulmer J.D., Hunninghake G.W., Crystal R.G. Bleomyein-induced interstitial pulmonary disease in the nude, athymic mouse. Am. Rev. Respir. Dis. 1979, 120:893-899. (PubMed: 92208).
36. Ulloa L., Doody J., Massagué J. Inhibition of transforming growth factor-β/SMAD signalling by the interferon-γ/STAT pathway. Nature 1999, 397:710-713. (PubMed: 10067896).
37. White E.S., Lazar M.H., Thannickal V.J. Pathogenetic mechanisms in usual interstitial pneumonia/idiopathic pulmonary fibrosis. J. Pathol. 2003, 201:343-354. (PubMed: 14595745).
38. Woessner J.F. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch. Biochem. Biophys. 1961, 93:440-447. (PubMed: 13786180).
39. Zhong G.Z., Li Y.B., Liu X.L., Guo L.S., Chen M.L., Yang X.C. Hydrogen sulfide opens the KATP channel on rat atrial and ventricular myocytes. Cardiology 2010, 115:120-126. (PubMed: 19940474).
40. Ziesche R., Hofbauer E., Wittmann K., Petkov V., Block L.H. A preliminary study of long-term treatment with interferon gamma-1b and low-dose prednisolone in patients with idiopathic pulmonary fibrosis. N. Engl. J. Med. 1999, 341:1264-1269. (PubMed: 10528036).