MicroRNA-29c prevents pulmonary fibrosis by regulating epithelial cell renewal and apoptosis

American Journal of Respiratory Cell and Molecular Biology

Volumn 57, Issue 6, 2017, Pages 721-732

  Xie, Ting ^a   Liang, Jiurong ^a   Geng, Yan ^a   Liu, Ningshan ^a   Kurkciyan, Adrianne ^a   Kulur, Vrishika ^a   Leng, Dong ^b   Deng, Nan ^a   Liu, Zhenqiu ^a   Song, Jianbo ^a   Chen, Peter ^a   Noble, Paul W ^a   Jiang, Dianhua ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Alveolar epithelial type II cell apoptosis; Alveolar epithelial type II cell renewal; MicroRNA 29c; Pulmonary fibrosis

Indexed keywords

BLEOMYCIN; MICRORNA; MICRORNA 29C; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; MIRN29 MICRORNA, HUMAN; MIRN29 MICRORNA, MOUSE; TLR4 PROTEIN, HUMAN; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL RENEWAL; CELL VIABILITY; ENDOPLASMIC RETICULUM STRESS; FIBROSING ALVEOLITIS; GENE CONTROL; HUMAN; LUNG ALVEOLUS EPITHELIUM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; ANIMAL; CHEMICALLY INDUCED; EPITHELIUM CELL; FEMALE; GENETICS; MALE; METABOLISM; PATHOLOGY; RESPIRATORY MUCOSA;

ANIMALS; APOPTOSIS; EPITHELIAL CELLS; FEMALE; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; MALE; MICE; MICRORNAS; RESPIRATORY MUCOSA; TOLL-LIKE RECEPTOR 4;

EID: 85037132367     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2017-0133OC     Document Type: Article

References (50)

1. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012; 18:1028-1040.
2. Xie T, Liang J, Liu N, Huan C, Zhang Y, Liu W, Kumar M, Xiao R, D'Armiento J, Metzger D, et al. Transcription factor TBX4 regulates myofibroblast accumulation and lung fibrosis. J Clin Invest 2016;126: 3063-3079.
3. Barkauskas CE, Cronce MJ, Rackley CR, Bowie EJ, Keene DR, Stripp BR, Randell SH, Noble PW, Hogan BL. Type 2 alveolar cells are stem cells in adult lung. J Clin Invest 2013;123:3025-3036.
4. Liang J, Zhang Y, Xie T, Liu N, Chen H, Geng Y, Kurkciyan A, Mena JM, Stripp BR, Jiang D, et al. Hyaluronan and TLR4 promote surfactantprotein-C-positive alveolar progenitor cell renewal and prevent severe pulmonary fibrosis in mice. Nat Med 2016;22:1285-1293.
5. Chambers RC, Mercer PF. Mechanisms of alveolar epithelial injury, repair, and fibrosis. Ann Am Thorac Soc 2015;12:S16-S20.
6. Wang Y, Frank DB, Morley MP, Zhou S, Wang X, Lu MM, Lazar MA, Morrisey EE. HDAC3-dependent epigenetic pathway controls lung alveolar epithelial cell remodeling and spreading via miR-17-92 and TGF-b signaling regulation. Dev Cell 2016;36:303-315.
7. Mathis C, Poussin C, Weisensee D, Gebel S, Hengstermann A, Sewer A, Belcastro V, Xiang Y, Ansari S, Wagner S, et al. Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air-liquid interface resemble bronchial epithelium from human smokers. Am J Physiol Lung Cell Mol Physiol 2013;304:L489-L503.
8. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K. microRNAs and epigenetics. FEBS J 2011;278:1598-1609.
9. Huang Y, Crawford M, Higuita-Castro N, Nana-Sinkam P, Ghadiali SN. miR-146a regulates mechanotransduction and pressure-induced inflammation in small airway epithelium. FASEB J 2012;26:3351-3364.
10. Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 2004; 5:396-400.
11. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Ra dmark O, Kim S, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003;425:415-419.
12. Cho JH, Gelinas R,Wang K, Etheridge A, PiperMG, Batte K, Dakhallah D, Price J, Bornman D, Zhang S, et al. Systems biology of interstitial lung diseases: integration of mRNA and microRNA expression changes. BMC Med Genomics 2011;4:8.
13. Li P, Li J, Chen T, Wang H, Chu H, Chang J, Zang W, Wang Y, Ma Y, Du Y, et al. Expression analysis of serum microRNAs in idiopathic pulmonary fibrosis. Int J Mol Med 2014;33:1554-1562.
14. Xie T, Liang J, Guo R, Liu N, Noble PW, Jiang D. Comprehensive microRNA analysis in bleomycin-induced pulmonary fibrosis identifies multiple sites of molecular regulation. Physiol Genomics 2011;43:479-487.
15. Matsushima S, Ishiyama J. microRNA-29c regulates apoptosis sensitivity via modulation of the cell-surface death receptor, Fas, in lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2016;311: L1050-L1061.
16. Liu G, Friggeri A, Yang Y, Milosevic J, Ding Q, Thannickal VJ, Kaminski N, Abraham E. miR-21 mediates fibrogenic activation of pulmonary fibroblasts and lung fibrosis. J Exp Med 2010;207:1589-1597.
17. Cui H, Ge J, Xie N, Banerjee S, Zhou Y, Antony VB, Thannickal VJ, Liu G. miR-34a inhibits lung fibrosis by inducing lung fibroblast senescence. Am J Respir Cell Mol Biol 2017;56:168-178.
18. Cui H, Ge J, Xie N, Banerjee S, Zhou Y, Liu RM, Thannickal VJ, Liu G. miR-34a promotes fibrosis in aged lungs by inducing alveolar epithelial dysfunctions. Am J Physiol Lung Cell Mol Physiol 2016; 312:L415-L424.
19. Zhang Y, Huang XR, Wei LH, Chung AC, Yu CM, Lan HY. miR-29b as a therapeutic agent for angiotensin II-induced cardiac fibrosis by targeting TGF-b/Smad3 signaling. Mol Ther 2014;22:974-985.
20. Wang Y, Liu J, Chen J, Feng T, Guo Q. miR-29 mediates TGFb 1-induced extracellular matrix synthesis through activation of Wnt/bcatenin pathway in human pulmonary fibroblasts. Technol Health Care 2015;23:S119-S125.
21. Robaina MC,Mazzoccoli L, Arruda VO, Reis FR, Apa AG, de Rezende LM, Klumb CE. Deregulation of DNMT1, DNMT3B and miR-29s in Burkitt lymphoma suggests novel contribution for disease pathogenesis. Exp Mol Pathol 2015;98:200-207.
22. Rostas JW III, Pruitt HC, Metge BJ, Mitra A, Bailey SK, Bae S, Singh KP, Devine DJ, Dyess DL, Richards WO, et al. microRNA-29 negatively regulates EMT regulator N-myc interactor in breast cancer. Mol Cancer 2014;13:200.
23. O'Reilly S. microRNAs in fibrosis: opportunities and challenges. Arthritis Res Ther 2016;18:11.
24. Cushing L, Kuang PP, Qian J, Shao F, Wu J, Little F, Thannickal VJ, Cardoso WV, Lü J. miR-29 is a major regulator of genes associated with pulmonary fibrosis. Am J Respir Cell Mol Biol 2011;45:287-294.
25. Parker MW, Rossi D, Peterson M, Smith K, Sikström K, White ES, Connett JE, Henke CA, Larsson O, Bitterman PB. Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J Clin Invest 2014;124:1622-1635.
26. Yang T, Liang Y, Lin Q, Liu J, Luo F, Li X, Zhou H, Zhuang S, Zhang H. miR-29 mediates TGFb1-induced extracellular matrix synthesis through activation of PI3K-AKT pathway in human lung fibroblasts. J Cell Biochem 2013;114:1336-1342.
27. Khalil W, Xia H, Bodempudi V, Kahm J, Hergert P, Smith K, Peterson M, Parker M, Herrera J, Bitterman PB, et al. Pathologic regulation of collagen i by an aberrant protein phosphatase 2A/histone deacetylase C4/microRNA-29 signal axis in idiopathic pulmonary fibrosis fibroblasts. Am J Respir Cell Mol Biol 2015;53:391-399.
28. Guo W, Benlhabib H, Mendelson CR. The microRNA 29 family promotes type II cell differentiation in developing lung. Mol Cell Biol 2016;36:2141.
29. Xie T, Liang J, Liu N, Wang Q, Li Y, Noble PW, Jiang D. microRNA-127 inhibits lung inflammation by targeting IgG Fcg receptor I. J Immunol 2012;188:2437-2444.
30. Ventura A, Meissner A, Dillon CP, McManus M, Sharp PA, Van Parijs L, Jaenisch R, Jacks T. Cre-lox-regulated conditional RNA interference from transgenes. Proc Natl Acad Sci USA 2004;101:10380-10385.
31. 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.
32. Cushing L, Costinean S, Xu W, Jiang Z, Madden L, Kuang P, Huang J, Weisman A, Hata A, Croce CM, et al. Disruption of miR-29 leads to aberrant differentiation of smooth muscle cells selectively associated with distal lung vasculature. PLoS Genet 2015;11:e1005238.
33. Oslowski CM, Urano F. Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol 2011;490:71-92.
34. Shiraishi H, Okamoto H, Yoshimura A, Yoshida H. ER stress-induced apoptosis and caspase-12 activation occurs downstream of mitochondrial apoptosis involving Apaf-1. J Cell Sci 2006;119: 3958-3966.
35. Chen H, Matsumoto K, Brockway BL, Rackley CR, Liang J, Lee JH, Jiang D, Noble PW, Randell SH, Kim CF, et al. Airway epithelial progenitors are region specific and show differential responses to bleomycin-induced lung injury. Stem Cells 2012;30:1948-1960.
36. Fu Z, Tindall DJ. FOXOs, cancer and regulation of apoptosis. Oncogene 2008;27:2312-2319.
37. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-1179.
38. Maegdefessel L, Azuma J, Toh R, Merk DR, Deng A, Chin JT, Raaz U, Schoelmerich AM, Raiesdana A, Leeper NJ, et al. Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Invest 2012;122:497-506.
39. Maurer B, Stanczyk J, Jüngel A, Akhmetshina A, Trenkmann M, Brock M, Kowal-Bielecka O, Gay RE, Michel BA, Distler JH, et al. microRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum 2010;62:1733-1743.
40. Drummond CA, Hill MC, Shi H, Fan X, Xie JX, Haller ST, Kennedy DJ, Liu J, Garrett MR, Xie Z, et al. Na/K-ATPase signaling regulates collagen synthesis through microRNA-29b-3p in cardiac fibroblasts. Physiol Genomics 2016;48:220-229.
41. Adoro S, Cubillos-Ruiz JR, Chen X, Deruaz M, Vrbanac VD, Song M, Park S, Murooka TT, Dudek TE, Luster AD, et al. IL-21 induces antiviral microRNA-29 in CD4 T cells to limit HIV-1 infection. Nat Commun 2015;6:7562.
42. Ma F, Xu S, Liu X, Zhang Q, Xu X, Liu M, Hua M, Li N, Yao H, Cao X. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-g. Nat Immunol 2011;12:861-869.
43. Mundy-Bosse BL, Scoville SD, Chen L, McConnell K, Mao HC, Ahmed EH, Zorko N, Harvey S, Cole J, Zhang X, et al. microRNA-29b mediates altered innate immune development in acute leukemia. J Clin Invest 2016;126:4404-4416.
44. Dong J, Jiang G, Asmann YW, Tomaszek S, Jen J, Kislinger T, Wigle DA. microRNA networks in mouse lung organogenesis. PLoS One 2010;5:e10854.
45. Disayabutr S, Kim EK, Cha SI, Green G, Naikawadi RP, Jones KD, Golden JA, Schroeder A, Matthay MA, Kukreja J, et al. miR-34 miRNAs regulate cellular senescence in type II alveolar epithelial cells of patients with idiopathic pulmonary fibrosis. PLoS One 2016; 11:e0158367.
46. Li S, Geng J, Xu X, Huang X, Leng D, Jiang D, Liang J, Wang C, Jiang D, Dai H. miR-130b-3p modulates epithelial-mesenchymal crosstalk in lung fibrosis by targeting IGF-1. PLoS One 2016;11: e0150418.
47. Ge L, Habiel DM, Hansbro PM, Kim RY, Gharib SA, Edelman JD, Konigshoff M, Parimon T, Brauer R, Huang Y, et al. miR-323a-3p regulates lung fibrosis by targeting multiple profibrotic pathways. JCI Insight 2016;1:e90301.
48. Zhou L, Wang L, Lu L, Jiang P, Sun H, Wang H. Inhibition of miR-29 by TGF-b-Smad3 signaling through dual mechanisms promotes transdifferentiation of mouse myoblasts into myofibroblasts. PLoS One 2012;7:e33766.
49. Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS, et al. NF-kB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 2008;14:369-381.
50. Montgomery RL, Yu G, Latimer PA, Stack C, Robinson K, Dalby CM, Kaminski N, van Rooij E. microRNA mimicry blocks pulmonary fibrosis. EMBO Mol Med 2014;6:1347-1356.