All-transretinoic acid ameliorates bleomycin-induced lung fibrosis by downregulating the TGF-β1/Smad3 signaling pathway in rats

Laboratory Investigation

Volumn 93, Issue 11, 2013, Pages 1219-1231

  Song, Xiaodong ^a   Liu, Weili ^b   Xie, Shuyang ^a   Wang, Meirong ^a   Cao, Guohong ^a,b   Mao, Cuiping ^a   Lv, Changjun ^a,b  

^a BINZHOU MEDICAL UNIVERSITY   (China)

^b The Affiliated Hospital to Binzhou Medical University   (China)

Author keywords

all transretinoic acid; collagen; lung fibrosis; Smad3; TGF b1

Indexed keywords

BLEOMYCIN; COLLAGEN FIBER; HIGH MOBILITY GROUP A2 PROTEIN; RETINOIC ACID; SMAD3 PROTEIN; TRANSCIPTION FACTOR ZEB2; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; COLLAGEN; HOMEODOMAIN PROTEIN; MADH3 PROTEIN, RAT; MESSENGER RNA; TCF8 PROTEIN, RAT; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATORY INFILTRATE; LUNG ALVEOLUS; LUNG FIBROSIS; LUNG PARENCHYMA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DISEASE MODEL; DOWN REGULATION; DRUG EFFECTS; GENETICS; METABOLISM; PULMONARY FIBROSIS; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALS; BIOLOGICAL MARKERS; BLEOMYCIN; COLLAGEN; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HMGA2 PROTEIN; HOMEODOMAIN PROTEINS; PULMONARY FIBROSIS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TRETINOIN;

EID: 84886775810     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.108     Document Type: Article

References (59)

1. du Bois RM. Strategies for treating idiopathic lung fibrosis. Nat Rev Drug Discov 2010;9:129-140.
2. Yang S, Cui H, Xie N, et al. miR-145 regulates myofibroblast differentiation and lung fibrosis. FASEB J 2013;27:2382-2391.
3. Zolak JS, Jagirdar R, Surolia R, et al. Pleural mesothelial cell differentiation and invasion in fibrogenic lung injury. Am J Pathol 2013;182:1239-1247.
4. Liu G, Friggeri A, Yang YP, et al. miR-21 mediates fibrogenic activation of lung fibroblasts and lung fibrosis. J Exp Med 2010;207:1589-1597.
5. Flanders KC. Smad3 as a mediator of the fibrotic response. Int J Exp Pathol 2004;85:47-64. (Pubitemid 38703594)
6. Zhao J, Shi W, Wang YL, et al. Smad3 deficiency attenuates bleomycininduced lung fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2002;282:585-593.
7. Dong XS, Hu XB, Liu W, et al. Effects of RNA interference-induced Smad3 gene silencing on lung fibrosis caused by paraquat in mice. Exp Biol Med 2012;237:548-555.
8. Xiao J, Meng XM, Huang XR, et al. miR-29 inhibits bleomycin-induced lung fibrosis in mice. Mol Ther 2012;20:1251-1260.
9. D'Alessandro-Gabazza CN, Kobayashi T, Boveda-Ruiz D, et al. Development and preclinical efficacy of novel transforming growth factor-b1 short interfering RNAs for lung fibrosis. Am J Respir Cell Mol Biol 2012;46:397-406.
10. Hamasaki T, Suzuki H, Shirohzu H, et al. Efficacy of a novel class of RNA interference therapeutic agents. PloS One 2012;7:e42655.
11. Eldman DR, Patil S, Trinos MJ, et al. Progression-free and overall survival in patients with relapsed/refractory germ cell tumors treated with single-agent chemotherapy: endpoints for clinical trial design. Cancer 2012;118:981-986.
12. Guo P, Chen HJ, Wang QY, et al. Down regulation of N- acetylglucosaminyltransferase V facilitates all-transretinoic acid to induce apoptosis of human hepatocarcinoma cells. Mol Cell Biochem 2006;284: 103-110. (Pubitemid 44404416)
13. Chiharu T, Yoshio K, Rie T, et al. All-trans-retinoic acid prevents radiation-or bleomycin-induced lung fibrosis. Am J Respir Crit Care Med 2006;174, 1352-1360.
14. Dong ZX, Tai WL, Yang YN, et al. The role of all-trans retinoic acid in bleomycin-induced lung fibrosis in mice. Exp Lung Res 2012;38: 82-89.
15. Segel MJ, Or R, Tzurel A, et al. All-trans-retinoic acid (ATRA) is of no benefit in bleomycin-induced lung injury. Pulm Pharmacol Ther 2001;14:403-407. (Pubitemid 32977022)
16. Li ZY, Zhou TB, Qin YH, et al. All-Trans retinoic acid attenuates the renal interstitial fibrosis lesion in rats but not by transforming growth factor-b1/Smad3 signaling pathway. Ren Fail 2013;35:262-267.
17. Zhou TB, Drummen GP, Qin YH. The controversial role of retinoic Acid in fibrotic diseases: analysis of involved signaling pathways. Int J Mol Sci 2012;14:226-243.
18. Wang MR, Zhang JJ, Song XD, et al. Astaxanthin ameliorates lung fibrosis in vivo and in vitro by preventing transdifferentiation, inhibiting proliferation, and promoting apoptosis of activated cells. Food Chem Toxicol 2013;56:450-458.
19. Saadeddin A, Torres-Molina F, Cárcel-Trullols J, et al. Pharmacokinetics of the time-dependent elimination of all-trans-retinoic acid in rats. AAPS Pharm Sci 2004;6:1-9.
20. Szapiel SV, Elson NA, Fulmer JD, et al. Bleomycin-induced interstitial pulmonary disease in the nude, athymic mouse. Am Rev Respir Dis 1979;120:893-899. (Pubitemid 10194957)
21. Loughlin PM, Cooke TG, George WD, et al. Quantifying tumourinfiltrating lymphocyte subsets: a practical immuno-histochemical method. J Immunol Methods 2007;321:32-40. (Pubitemid 46441196)
22. Song XD, Zhang JJ, Wang MR, et al. Astaxanthin induces mitochondria-mediated apoptosis in rat hepatocellular carcinoma CBRH-7919 cells. Biol Pharm Bull 2011;34:839-844.
23. Cao GH, Zhang JJ, Wang MR, et al. Differential expression of long noncoding RNAs in bleomycin-induced lung fibrosis. Int J Mol Med 2013;32:355-364.
24. Hardie WD, Glasser SW, Hagood JS. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 2009;175:3-16.
25. Tomasek JJ, Gabbiani G, Hinz B, et al. Myofibroblasts and mechanoregulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002;3:349-363. (Pubitemid 34619269)
26. Hinz B, Phan SH, Thannickal VJ, et al. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012;180:1340-1355.
27. Pottier N, Maurin T, Chevalier B, et al. Identification of keratinocyte growth factor as a target of microrna-155 in lung fibroblasts: implication in epithelial-mesenchymal interactions. PloS One 2009; 4:e6718.
28. Yu H, Konigshoff M, Jayachandran A, et al. Transgelin is a direct target of tgf-beta/smad3-dependent epithelial cell migration in lung fibrosis. FASEB J 2008;22:1778-1789. (Pubitemid 351811455)
29. Willis BC, Borok Z. Tgf-beta-induced emt: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;293:L525-L534. (Pubitemid 47358808)
30. Brigham C, Willis ZB. TGF-b1-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;293:L525-L534.
31. Jain M, Rivera S, Monclus EA, et al. Mitochondrial reactive oxygen species regulate TGF-beta signaling. J Biol Chem 2013;288:770-777.
32. Meng J, Zou YQ, Hu CP, et al. Fluorofenidone attenuates bleomycininduced lung inflammation and fibrosis in mice via restoring caveolin 1 expression and inhibiting mitogen-activated protein kinase signaling pathway. SHOCK 2012;38:567-573.
33. Salem S, Harris T, Mok JSL, et al. Transforming growth factor-b impairs glucocorticoid activity in the A549 lung adenocarcinoma cell line. Br J Pharmacol 2012;166:2036-2048.
34. Payal K, Naik PD, Bozyk J, et al. Periostinpromotes fibrosis and predicts progression in patients with Idiopathic Lung Fibrosis. Am J Physiol Lung Cell Mol Physiol 2012;303:L1046-L1056.
35. Vincent Jordan N, Prat A, Abell AN, et al. SWI/SNF chromatinremodeling factor Smarcd3/Baf60c controls EMT by inducing Wnt5a signaling. Mol Cell Biol 2013;33:3011-3025.
36. Aparicio LA, Abella V, Valladares M, et al. Posttranscriptional regulation by RNA-binding proteins during epithelial-to-mesenchymal transition. Cell Mol Life Sci 2013 (e-pub ahead of print).
37. Barriga EH, Maxwell PH, Reyes AE, et al. The hypoxia factor Hif-1a controls neural crest chemotaxis and epithelial to mesenchymal transition. J Cell Biol 2013;201:759-776.
38. Lekkerkerker AN, Aarbiou J, van Es T, et al. Cellular players in lung fibrosis. Curr Pharm Des 2012;18:4093-4102.
39. Milara J, Peiró T, Serrano A, et al. Epithelial to mesenchymal transition is increased in patients with COPD and induced by cigarette smoke. Thorax 2013;68:410-420.
40. Wettstein G, Bellaye PS, Kolb M, et al. Inhibition of HSP27 blocks fibrosis development and EMT features by promoting Snail degradation. FASEB J 2013;27:1549-1560.
41. Zheng H, Kang Y. Multilayer control of the EMT master regulators. Oncogene 2013; doi:10.1038/onc.2013.128.
42. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008;14: 818-829. (Pubitemid 351757205)
43. Jayachandran A, Konigshoff M, Yu H, et al. SNAI transcription factors mediate epithelial-mesenchymal transition in lung fibrosis. Thorax 2009;64:1053-1061.
44. Sharma AK, Hubmayr RD. Epithelial to mesenchymal transition: a new twist to biotrauma. Crit Care Med 2012;40:682-683.
45. Boutet A, De Frutos CA, Maxwell PH, et al. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J 2006;25:5603-5613. (Pubitemid 44847200)
46. Galván JA, Astudillo A, Vallina A, et al. Epithelial-mesenchymal transition markers in the differential diagnosis of gastroenteropancreatic neuroendocrine tumors. Am J Clin Pathol 2013;140:61-72.
47. Alexander NR, Tran NL, Rekapally H, et al. N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res 2006;66:3365-3369.
48. Sylvie T, Ulrich V, Maj P, et al. Transforming growth factor-b employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006;174:175-183.
49. Thuault S, Tan EJ, Peinado H, et al. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J Biol Chem 2008;283:33437-33446.
50. Xiong M, Jiang L, Zhou Y, et al. The miR-200 family regulates TGF-1-induced renal tubular epithelial to mesenchymal transition through Smad pathway by targeting ZEB1 and ZEB2 expression. Am J Physiol Renal Physiol 2012;302:F369-F379.
51. Korpal M, Lee ES, Hu G, et al. The miR-200 family inhibits epithelialmesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008;283:14910-14914.
52. Park SM, Gaur AB, Lengyel E, et al. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22:894-907. (Pubitemid 351482843)
53. Xiong M, Jiang L, Zhou Y, et al. The miR-200 family regulates TGF-b1-induced renal tubular epithelial to mesenchymal transition through Smad pathway by targeting ZEB1 and ZEB2 expression. Am J Physiol Renal Physiol 2012;302:F369-F379.
54. Zhu C, Li J, Cheng G, et al. miR-154 inhibits EMT by targeting HMGA2 in prostate cancer cells. Mol Cell Biochem 2013;379:69-75, PMID: 23591597.
55. Tan EJ, Thuault S, Caja L, et al. Regulation of transcription factor Twist expression by the DNA architectural protein high mobility group A2 during epithelial-to-mesenchymal transition. J Biol Chem 2012;287: 7134-7145.
56. Kitase Y, Shuler CF. Microtubule disassembly prevents palatal fusion and alters regulation of the E-cadherin/catenin complex. Int J Dev Biol 2013;57:55-60.
57. Gheldof A, Berx G. Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci 2013;116:317-336.
58. Sánchez-Tilló E, Liu Y, de Barrios O, et al. EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci 2012;69:3429-3456.
59. Nieto MA. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 2011;27:347-376.