miR-31 is a negative regulator of fibrogenesis and pulmonary fibrosis

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3790-3799

  Yang, Shanzhong ^a   Xie, Na ^a   Cui, Huachun ^a   Banerjee, Sami ^a   Abraham, Edward ^b   Thannickal, Victor J ^a   Liu, Gang ^a  

^a University of Alabama at Birmingham   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Contraction; Fibroblasts; Integrin 5; Migration; RhoA

Indexed keywords

ALPHA5 INTEGRIN; BLEOMYCIN; MICRORNA 31; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CONTROLLED STUDY; EX VIVO STUDY; FIBROGENESIS; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG FIBROBLAST; LUNG FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE; DNA PRIMERS; FIBROBLASTS; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; INTEGRIN ALPHA5; LUNG; MICE; MICRORNAS; REAL-TIME POLYMERASE CHAIN REACTION; RHOA GTP-BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

MUS;

EID: 84865763591     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-202366     Document Type: Article

References (45)

1. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R. A. (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363
2. Thannickal, V. J., Toews, G. B., White, E. S., Lynch, J. P., 3rd, and Martinez, F. J. (2004) Mechanisms of pulmonary fibrosis. Annu. Rev. Med. 55, 395-417
3. Cutroneo, K. R., White, S. L., Phan, S. H., and Ehrlich, H. P. (2007) Therapies for bleomycin-induced lung fibrosis through regulation of TGF-β1 induced collagen gene expression. J. Cell. Physiol. 211, 585-589
4. Lee, C. G., Cho, S., Homer, R. J., and Elias, J. A. (2006) Genetic control of transforming growth factor-β1-induced emphysema and fibrosis in the murine lung. Proc. Am. Thorac. Soc. 3, 476-477
5. Ramos, C., Montano, M., Garcia-Alvarez, J., Ruiz, V., Uhal, B. D., Selman, M., and Pardo, A. (2001) Fibroblasts from idiopathic pulmonary fibrosis and normal lungs differ in growth rate, apoptosis, and tissue inhibitor of metalloproteinases expression. Am. J. Respir. Cell Mol. Biol. 24, 591-598
6. Xia, H., Diebold, D., Nho, R., Perlman, D., Kleidon, J., Kahm, J., Avdulov, S., Peterson, M., Nerva, J., Bitterman, P., and Henke, C. (2008) Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J. Exp. Med. 205, 1659-1672
7. Vuga, L. J., Ben-Yehudah, A., Kovkarova-Naumovski, E., Oriss, T., Gibson, K. F., Feghali-Bostwick, C., and Kaminski, N. (2009) WNT5A is a regulator of fibroblast proliferation and resistance to apoptosis. Am. J. Respir. Cell Mol. Biol. 41, 583-589
8. Cai, G. Q., Zheng, A., Tang, Q., White, E. S., Chou, C. F., Gladson, C. L., Olman, M. A., and Ding, Q. (2010) Downregulation of FAK-related non-kinase mediates the migratory phenotype of human fibrotic lung fibroblasts. Exp. Cell Res. 316, 1600-1609
9. Zhou, Y., Hagood, J. S., Lu, B., Merryman, W. D., and Murphy-Ullrich, J. E. (2010) Thy-1-integrin alphav beta5 interactions inhibit lung fibroblast contraction-induced latent transforming growth factor-beta1 activation and myofibroblast differentiation. J. Biol. Chem. 285, 22382-22393
10. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
11. Zeng, Y. (2006) Principles of micro-RNA production and maturation. Oncogene 25, 6156-6162
12. Engels, B. M., and Hutvagner, G. (2006) Principles and effects of microRNA-mediated post-transcriptional gene regulation. Oncogene 25, 6163-6169
13. Bushati, N., and Cohen, S. M. (2007) microRNA functions. Annu. Rev. Cell Dev. Biol. 23, 175-205
14. Ambros, V. (2001) microRNAs: tiny regulators with great potential. Cell 107, 823-826
15. Croce, C. M. (2009) Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10, 704-714
16. Croce, C. M., and Calin, G. A. (2005) miRNAs, cancer, and stem cell division. Cell 122, 6-7
17. Pandey, A. K., Agarwal, P., Kaur, K., and Datta, M. (2009) MicroRNAs in diabetes: tiny players in big disease. Cell. Physiol. Biochem. 23, 221-232
18. Latronico, M. V., and Condorelli, G. (2009) MicroRNAs and cardiac pathology. Nat. Rev. Cardiol. 6, 419-429
19. Thum, T., Catalucci, D., and Bauersachs, J. (2008) MicroRNAs: novel regulators in cardiac development and disease. Cardiovasc. Res. 79, 562-570
20. Mishra, P. K., Tyagi, N., Kumar, M., and Tyagi, S. C. (2009) MicroRNAs as a therapeutic target for cardiovascular diseases. J. Cell. Mol. Med. 13, 778-789
21. Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., Galuppo, P., Just, S., Rottbauer, W., Frantz, S., Castoldi, M., Soutschek, J., Koteliansky, V., Rosenwald, A., Basson, M. A., Licht, J. D., Pena, J. T., Rouhanifard, S. H., Muckenthaler, M. U., Tuschl, T., Martin, G. R., Bauersachs, J., and Engelhardt, S. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456, 980-984
22. Liu, G., Friggeri, A., Yang, Y., Milosevic, J., Ding, Q., Thannickal, V. J., Kaminski, N., and Abraham, E. (2010) miR-21 mediates fibrogenic activation of pulmonary fibroblasts and lung fibrosis. J. Exp. Med. 207, 1589-1597
23. Patel, S., Takagi, K. I., Suzuki, J., Imaizumi, A., Kimura, T., Mason, R. M., Kamimura, T., and Zhang, Z. (2005) RhoGTPase activation is a key step in renal epithelial mesenchymal transdifferentiation. J. Am. Soc. Nephrol. 16, 1977-1984
24. Watts, K. L., Cottrell, E., Hoban, P. R., and Spiteri, M. A. (2006) RhoA signaling modulates cyclin D1 expression in human lung fibroblasts; implications for idiopathic pulmonary fibrosis. Respir. Res. 7, 88
25. Tsapara, A., Luthert, P., Greenwood, J., Hill, C. S., Matter, K., and Balda, M. S. (2010) The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration. Mol. Biol. Cell 21, 860-870
26. Kondrikov, D., Caldwell, R. B., Dong, Z., and Su, Y. (2010) Reactive oxygen species-dependent RhoA activation mediates collagen synthesis in hyperoxic lung fibrosis. Free Radic. Biol. Med. 50, 1689-1698
27. White, L. R., Blanchette, J. B., Ren, L., Awn, A., Trpkov, K., and Muruve, D. A. (2007) The characterization of alpha5-integrin expression on tubular epithelium during renal injury. Am. J. Physiol. Renal Physiol. 292, F567-F576
28. Konigshoff, M., Kramer, M., Balsara, N., Wilhelm, J., Amarie, O. V., Jahn, A., Rose, F., Fink, L., Seeger, W., Schaefer, L., Gunther, A., and Eickelberg, O. (2009) WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J. Clin. Invest. 119, 772-787
29. Liu, G., Park, Y. J., and Abraham, E. (2008) Interleukin-1 receptor-associated kinase (IRAK) -1-mediated NF-κB activation requires cytosolic and nuclear activity. FASEB J. 22, 2285-2296
30. Moore, B. B., and Hogaboam, C. M. (2008) Murine models of pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L152-L160
31. Pandit, K. V., Corcoran, D., Yousef, H., Yarlagadda, M., Tzouvelekis, A., Gibson, K. F., Konishi, K., Yousem, S. A., Singh, M., Handley, D., Richards, T., Selman, M., Watkins, S. C., Pardo, A., Ben-Yehudah, A., Bouros, D., Eickelberg, O., Ray, P., Benos, P. V., and Kaminski, N. (2010) Inhibition and role of Let-7d in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 182, 220-229
32. Kang, H. R., Cho, S. J., Lee, C. G., Homer, R. J., and Elias, J. A. (2007) Transforming growth factor (TGF)-beta1 stimulates pulmonary fibrosis and inflammation via a Bax-dependent, bid-activated pathway that involves matrix metalloproteinase-12. J. Biol. Chem. 282, 7723-7732
33. Finlay, G. A., Thannickal, V. J., Fanburg, B. L., and Paulson, K. E. (2000) Transforming growth factor-β 1-induced activation of the ERK pathway/activator protein-1 in human lung fibroblasts requires the autocrine induction of basic fibroblast growth factor. J. Biol. Chem. 275, 27650-27656
34. Sheppard, D. (2006) Transforming growth factor beta: a central modulator of pulmonary and airway inflammation and fibrosis. Proc. Am. Thorac. Soc. 3, 413-417
35. Gharaee-Kermani, M., Hu, B., Phan, S. H., and Gyetko, M. R. (2009) Recent advances in molecular targets and treatment of idiopathic pulmonary fibrosis: focus on TGFβ signaling and the myofibroblast. Curr. Med. Chem. 16, 1400-1417
36. Thannickal, V. J., Lee, D. Y., White, E. S., Cui, Z., Larios, J. M., Chacon, R., Horowitz, J. C., Day, R. M., and Thomas, P. E. (2003) Myofibroblast differentiation by transforming growth factor-β1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J. Biol. Chem. 278, 12384-12389
37. Munger, J. S., Huang, X., Kawakatsu, H., Griffiths, M. J., Dalton, S. L., Wu, J., Pittet, J. F., Kaminski, N., Garat, C., Matthay, M. A., Rifkin, D. B., and Sheppard, D. (1999) The integrin alpha v beta 6 binds and activates latent TGF-β1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319-328
38. Yao, H. W., Xie, Q. M., Chen, J. Q., Deng, Y. M., and Tang, H. F. (2004) TGF-β1 induces alveolar epithelial to mesenchymal transition in vitro. Life Sci. 76, 29-37
39. Xu, J., Lamouille, S., and Derynck, R. (2009) TGF-β-induced epithelial to mesenchymal transition. Cell Res. 19, 156-172
40. Willis, B. C., and Borok, Z. (2007) TGF-β-induced EMT: mechanisms and implications for fibrotic lung disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L525-L534
41. Willis, B. C., Liebler, J. M., Luby-Phelps, K., Nicholson, A. G., Crandall, E. D., du Bois, R. M., and Borok, Z. (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-β1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol. 166, 1321-1332
42. Kasai, H., Allen, J. T., Mason, R. M., Kamimura, T., and Zhang, Z. (2005) TGF-β1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir. Res. 6, 56
43. Kim, K. K., Kugler, M. C., Wolters, P. J., Robillard, L., Galvez, M. G., Brumwell, A. N., Sheppard, D., and Chapman, H. A. (2006) Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc. Natl. Acad. Sci. U. S. A. 103, 13180-13185
44. Wu, Z., Yang, L., Cai, L., Zhang, M., Cheng, X., Yang, X., and Xu, J. (2007) Detection of epithelial to mesenchymal transition in airways of a bleomycin induced pulmonary fibrosis model derived from an alpha-smooth muscle actin-Cre transgenic mouse. Respir. Res. 8, 1
45. Degryse, A. L., Tanjore, H., Xu, X. C., Polosukhin, V. V., Jones, B. R., Boomershine, C. S., Ortiz, C., Sherrill, T. P., McMahon, F. B., Gleaves, L. A., Blackwell, T. S., and Lawson, W. E. (2011) TGFβ signaling in lung epithelium regulates bleomycin-induced alveolar injury and fibroblast recruitment. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L887-L897