Latent transforming growth factor-β1 protects against bleomycin-induced lung injury in mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 51, Issue 6, 2014, Pages 761-771

  Tang, Yong Jiang ^a   Xiao, Jun ^a,b   Huang, Xiao Ru ^a   Zhang, Yang ^a   Yang, Chen ^a   Meng, Xiao Ming ^a   Feng, Yu Lin ^b   Wang, Xiao Jing ^c   Hui, David S C ^a   Yu, Cheuk Man ^a   Lan, Hui Yao ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b SICHUAN UNIVERSITY   (China)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Fibrosis; Inflammation; Latent transforming growth factor 1; Regulatory T cells; T helper 17

Indexed keywords

BLEOMYCIN; CD4 ANTIGEN; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; CYTOKERATIN 5; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; SMAD3 PROTEIN; SMAD7 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; SMAD7 PROTEIN, MOUSE; TGFB1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CD3+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE OVEREXPRESSION; KERATINOCYTE; LUNG INJURY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PNEUMONIA; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TH17 CELL; UPREGULATION; ANIMAL; BLOOD; CHEMICALLY INDUCED; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; LUNG; LUNG ALVEOLUS MACROPHAGE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; BLEOMYCIN; FEMALE; INFLAMMATION MEDIATORS; LUNG; LUNG INJURY; MACROPHAGES, ALVEOLAR; MICE, INBRED ICR; MICE, TRANSGENIC; PNEUMONIA; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84918838696     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0423OC     Document Type: Article

References (34)

1. Lan HY. Diverse roles of TGF-β/Smads in renal fibrosis and inflammation. Int J Biol Sci 2011;7:1056-1067.
2. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, et al. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 1992;359:693-699.
3. Li MO, Flavell RA. TGF-β: a master of all T cell trades. Cell 2008;134: 392-404.
4. Hoyles RK, Derrett-Smith EC, Khan K, Shiwen X, Howat SL, Wells AU, Abraham DJ, Denton CP. An essential role for resident fibroblasts in experimental lung fibrosis is defined by lineage-specific deletion of high-affinity type II transforming growth factor b receptor. Am J Respir Crit Care Med 2011;183:249-261.
5. Li M, Krishnaveni MS, Li C, Zhou B, Xing Y, Banfalvi A, Li A, Lombardi V, Akbari O, Borok Z, et al. Epithelium-specific deletion of TGF-β receptor type II protects mice from bleomycin-induced pulmonary fibrosis. J Clin Invest 2011;121:277-287.
6. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, Victora GD, Shen Y, Du J, Rubtsov YP, Rudensky AY, et al. TGF-β-induced Foxp3 inhibits Th17 cell differentiation by antagonizing RORgt function. Nature 2008;453:236-240.
7. Oklu R, Hesketh R. The latent transforming growth factor beta binding protein (LTBP) family. Biochem J 2000;352:601-610.
8. Ribeiro SM, Poczatek M, Schultz-Cherry S, Villain M, Murphy-Ullrich JE. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 1999;274: 13586-13593.
9. Jenkins RG, Su X, Su G, Scotton CJ, Camerer E, Laurent GJ, Davis GE, Chambers RC, Matthay MA, Sheppard D. Ligation of protease-activated receptor 1 enhances a vb6 integrin-dependent TGF-β activation and promotes acute lung injury. J Clin Invest 2006;116: 1606-1614.
10. Wakefield LM, Winokur TS, Hollands RS, Christopherson K, Levinson AD, Sporn MB. Recombinant latent transforming growth factor β1 has a longer plasma half-life in rats than active transforming growth factor β1, and a different tissue distribution. J Clin Invest 1990;86: 1976-1984.
11. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 2003;425:577-584.
12. + regulatory T cells. Proc Natl Acad Sci USA 2009;106:13445-13450.
13. Bottinger EP, Factor VM, Tsang ML, Weatherbee JA, Kopp JB, Qian SW, Wakefield LM, Roberts AB, Thorgeirsson SS, Sporn MB. The recombinant proregion of transforming growth factor β1 (latency-associated peptide) inhibits active transforming growth factor β1 in transgenic mice. Proc Natl Acad Sci USA 1996;93: 5877-5882.
14. +Foxp3-regulatory T cells suppress allergic inflammation. J Immunol 2011; 187:6499-6507.
15. Ali NA, Gaughan AA, Orosz CG, Baran CP, McMaken S, Wang Y, Eubank TD, Hunter M, Lichtenberger FJ, Flavahan NA, Lawler J, Marsh CB. Latency associated peptide has in vitro and in vivo immune effects independent of TGF-beta1. PLoS One 2008;3:e1914.
16. + regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respir Res 2011;12:77.
17. Li AG, Wang D, Feng XH, Wang XJ. Latent TGFβ1 overexpression in keratinocytes results in a severe psoriasis-like skin disorder. EMBO J 2004;23:1770-1781.
18. Huang XR, Chung AC, Zhou L, Wang XJ, Lan HY. Latent TGF-β1 protects against crescentic glomerulonephritis. J Am Soc Nephrol 2008;19:233-242.
19. Bottoms SE, Howell JE, Reinhardt AK, Evans IC, McAnulty RJ. TGF-β isoform specific regulation of airway inflammation and remodelling in a murine model of asthma. PLoS ONE 2010;5:e9674.
20. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988;41:467-470.
21. Xiao J, Meng XM, Huang XR, Chung AC, Feng YL, Hui DS, Yu CM, Sung JJ, Lan HY. mIR-29 inhibits bleomycin-induced pulmonary fibrosis in mice. Mol Ther 2012;20:1251-1260.
22. Sisson TH, Mendez M, Choi K, Subbotina N, Courey A, Cunningham A, Dave A, Engelhardt JF, Liu X, White ES, et al. Targeted injury of type II alveolar epithelial cells induces pulmonary fibrosis. Am J Respir Crit Care Med 2010;181:254-263.
23. Chung AC, Huang XR, Zhou L, Heuchel R, Lai KN, Lan HY. Disruption of the Smad7 gene promotes renal fibrosis and inflammation in unilateral ureteral obstruction (UUO) in mice. Nephrol Dial Transplant 2009;24:1443-1454.
24. Wang W, Huang XR, Li AG, Liu F, Li JH, Truong LD, Wang XJ, Lan HY. Signaling mechanism of TGF-β1 in prevention of renal inflammation: role of Smad7. J Am Soc Nephrol 2005;16:1371-1383.
25. Sheppard D. Transforming growth factor b: a central modulator of pulmonary and airway inflammation and fibrosis. Proc Am Thorac Soc 2006;3:413-417.
26. Tatler AL, Jenkins G. TGF-activation and lung fibrosis. Proc Am Thorac Soc 2012;9:130-136.
27. Zhang Y, McCormick LL, Gilliam AC. Latency-associated peptide prevents skin fibrosis in murine sclerodermatous graft-versus-host disease, a model for human scleroderma. J Invest Dermatol 2003; 121:713-719.
28. Lan HY. Smad7 as a therapeutic agent for chronic kidney diseases. Front Biosci 2008;13:4984-4992.
29. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 2000;6: 1365-1375.
30. Venkatesan N, Pini L, Ludwig MS. Changes in Smad expression and subcellular localization in bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2004;287:L1342-L1347.
31. Wong CK, Cao J, Yin YB, Lam CW. Interleukin-17A activation on bronchial epithelium and basophils: a novel inflammatory mechanism. Eur Respir J 2010;35:883-893.
32. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 2006;441: 235-238.
33. Takimoto T, Wakabayashi Y, Sekiya T, Inoue N, Morita R, Ichiyama K, Takahashi R, Asakawa M, Muto G, Mori T, et al. Smad2 and Smad3 are redundantly essential for the TGF-β-mediated regulation of regulatory T plasticity and Th1 development. J Immunol 2010;185:842-855.
34. Probst-Kepper M, Geffers R, Kroger A, Viegas N, Erck C, Hecht HJ, Lunsdorf H, Roubin R, Moharregh-Khiabani D, Wagner K, et al. GARP: a key receptor controlling Foxp3 in human regulatory T cells. J Cell Mol Med 2009;13:3343-3357.