Wilms' tumor 1 (Wt1) regulates pleural mesothelial cell plasticity and transition into myofibroblasts in idiopathic pulmonary fibrosis

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1122-1131

  Karki, Suman ^a   Surolia, Ranu ^a   Hock, Thomas David ^a   Guroji, Purusotham ^a   Zolak, Jason S ^b   Duggal, Ryan ^a   Ye, Tong ^b   Thannickal, Victor J ^a   Antony, Veena B ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Matrix remodeling; Mesothelial to mesenchymal transition; Smooth muscle actin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN GEL; FIBRONECTIN; SHORT HAIRPIN RNA; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; WT1 PROTEIN; COLLAGEN; PRIMER DNA; SMOOTH MUSCLE ACTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LINEAGE; CELL MIGRATION; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; FIBROSING ALVEOLITIS; GENE LOCUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MESOTHELIAL TO MESENCHYMAL TRANSITION; MESOTHELIUM CELL; MOUSE; MUSCLE CONTRACTILITY; MYOFIBROBLAST; NONHUMAN; PHASE CONTRAST MICROSCOPY; PHENOTYPIC PLASTICITY; PLEURAL MESOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THREE DIMENSIONAL IMAGING; TRANSGENIC MOUSE; UPREGULATION; WESTERN BLOTTING; CELL DIFFERENTIATION; EPITHELIUM; GENETICS; MATRIX REMODELING; MESOTHELIAL-TO-MESENCHYMAL TRANSITION; METABOLISM; NEPHROBLASTOMA; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; PLEURA; POLYMERASE CHAIN REACTION;

MATRIX REMODELING; MESOTHELIAL-TO-MESENCHYMAL TRANSITION; SMOOTH MUSCLE ACTIN;

BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINEAGE; COLLAGEN; DNA PRIMERS; EPITHELIUM; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; MYOFIBROBLASTS; PLEURA; POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA1; WILMS TUMOR;

EID: 84899575746     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-236828     Document Type: Article

References (49)

1. Khalil, N., and O'Connor, R. (2004) Idiopathic pulmonary fibrosis: current understanding of the pathogenesis and the status of treatment. CMAJ 171, 153-160
2. Bjoraker, J. A., Ryu, J. H., Edwin, M. K., Myers, J. L., Tazelaar, H. D., Schroeder, D. R., and Offord, K. P. (1998) Prognostic significance of histopathologic subsets in idiopathic pulmonary fibrosis. Am. J. Resp. Crit. Care Med. 157, 199-203
3. Hinz, B., and Gabbiani, G. (2010) Fibrosis: recent advances in myofibroblast biology and new therapeutic perspectives. F1000 Biol. Rep. 2, 78
4. Lansley, S. M., Searles, R. G., Hoi, A., Thomas, C., Moneta, H., Herrick, S. E., Thompson, P. J., Newman, M., Sterrett, G. F., Prele, C. M., and Mutsaers, S. E. (2011) Mesothelial cell differentiation into osteoblast-And adipocyte-like cells. J. Cell. Mol. Med. 15, 2095-2105
5. Misumi, S., and Lynch, D. A. (2006) Idiopathic pulmonary fibrosis/usual interstitial pneumonia: imaging diagnosis, spectrum of abnormalities, and temporal progression. Proc. Am. Thorac. Soc. 3, 307-314
6. Cool, C. D., Groshong, S. D., Rai, P. R., Henson, P. M., Stewart, J. S., and Brown, K. K. (2006) Fibroblast foci are not discrete sites of lung injury or repair: the fibroblast reticulum. Am. J. Respir. Crit. Care Med. 174, 654-658
7. Bostrom, H., Willetts, K., Pekny, M., Leveen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellstrom, M., Gebre-Medhin, S., Schalling, M., Nilsson, M., Kurland, S., Tornell, J., Heath, J. K., and Betsholtz, C. (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873
8. Borok, Z. (2009) Role for alpha3 integrin in EMT and pulmonary fibrosis. J. Clin. Invest. 119, 7-10
9. Willis, B. C., duBois, R. M., and Borok, Z. (2006) Epithelial origin of myofibroblasts during fibrosis in the lung. Proc. Am. Thorac. Soc. 3, 377-382
10. Chilosi, M., Poletti, V., Zamo, A., Lestani, M., Montagna, L., Piccoli, P., Pedron, S., Bertaso, M., Scarpa, A., Murer, B., Cancellieri, A., Maestro, R., Semenzato, G., and Doglioni, C. (2003) Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am. J. Pathol. 162, 1495-1502
11. Rock, J. R., Barkauskas, C. E., Cronce, M. J., Xue, Y., Harris, J. R., Liang, J., Noble, P. W., and Hogan, B. L. (2011) Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc. Natl. Acad. Sci. U. S. A. 108, E1475-E1483
12. Nasreen, N., Mohammed, K. A., Mubarak, K. K., Baz, M. A., Akindipe, O. A., Fernandez-Bussy, S., and Antony, V. B. (2009) Pleural mesothelial cell transformation into myofibroblasts and haptotactic migration in response to TGF-beta1 in vitro. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L115-L124
13. Mubarak, K. K., Montes-Worboys, A., Regev, D., Nasreen, N., Mohammed, K. A., Faruqi, I., Hensel, E., Baz, M. A., Akindipe, O. A., Fernandez-Bussy, S., Nathan, S. D., and Antony, V. B. (2012) Parenchymal trafficking of pleural mesothelial cells in idiopathic pulmonary fibrosis. Eur. Respir. J. 39, 133-140
14. Antony, V. B. (2003) Immunological mechanisms in pleural disease. Eur. Respir. J. 21, 539-544
15. Antony, V. B., Hott, J. W., Kunkel, S. L., Godbey, S. W., Burdick, M. D., and Strieter, R. M. (1995) Pleural mesothelial cell expression of C-C (monocyte chemotactic peptide) and C-X-C (interleukin 8) chemokines. Am. J. Respir. Cell Mol. Biol. 12, 581-588
16. Pace, E., Ferraro, M., Mody, C. H., Melis, M. R., Scafidi, V., Bonanno, A., Profita, M., Giarratano, A., and Gjomarkaj, M. (2008) Pleural mesothelial cells express both BLT2 and PPARalpha and mount an integrated response to pleural leukotriene B4. J. Immunol. 181, 7292-7299
17. Glista-Baker, E. E., Taylor, A. J., Sayers, B. C., Thompson, E. A., and Bonner, J. C. (2012) Nickel nanoparticles enhance plateletderived growth factor-induced chemokine expression by mesothelial cells via prolonged mitogen-Activated protein kinase activation. Am. J. Respir. Cell Mol. Biol. 47, 552-561
18. Mutsaers, S. E. (2002) Mesothelial cells: their structure, function and role in serosal repair. Respirology 7, 171-191
19. Humphreys, B. D., Lin, S. L., Kobayashi, A., Hudson, T. E., Nowlin, B. T., Bonventre, J. V., Valerius, M. T., McMahon, A. P., and Duffield, J. S. (2010) Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 176, 85-97
20. Scholz, H., and Kirschner, K. M. (2011) Oxygen-Dependent Gene Expression in development and cancer: lessons learned from the Wilms' tumor gene, WT1. Front. Mol. Neurosci. 4, 4
21. Miller-Hodges, E., and Hohenstein, P. (2012) WT1 in disease: shifting the epithelial-mesenchymal balance. J. Pathol. 226, 229-240
22. Zolak, J. S., Jagirdar, R., Surolia, R., Karki, S., Oliva, O., Hock, T., Guroji, P., Ding, Q., Liu, R. M., Bolisetty, S., Agarwal, A., Thannickal, V. J., and Antony, V. B. (2013) Pleural mesothelial cell differentiation and invasion in fibrogenic lung injury. Am J. Pathol. 182, 1239-1247
23. Debnath, J., Muthuswamy, S. K., and Bruggea, J. S. (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268
24. Zhou, B., Ma, Q., Rajagopal, S., Wu, S. M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K. R., and Pu, W. T. (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454, 109-113
25. Arlt, M. J., Born, W., and Fuchs, B. (2012) Improved visualization of lung metastases at single cell resolution in mice by combined in-situ perfusion of lung tissue and X-Gal staining of lacZ-Tagged tumor cells. J. Vis. Exp. 66, e4162
26. Walters, D. M., and Kleeberger, S. R. (2008) Mouse models of bleomycin-induced pulmonary fibrosis. Curr. Protoc. Pharmacol. Chapter 5, Unit 5.46
27. Thornton, E. E., Krummel, M. F., and Looney, M. R. (2012) Live imaging of the lung. Curr. Protoc. Cytom. Chapter 12, Unit 12.28
28. Que, J., Wilm, B., Hasegawa, H., Wang, F., Bader, D., and Hogan, B. L. (2008) Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc. Natl. Acad. Sci. U. S. A. 105, 16626-16630
29. Sakairi, T., Abe, Y., and Kopp, J. B. (2011) TGF-beta1 reduces Wilms' tumor suppressor gene expression in podocytes. Nephrol. Dial. Transplant. 26, 2746-2752
30. Parenti, R., Perris, R., Vecchio, G. M., Salvatorelli, L., Torrisi, A., Gravina, L., and Magro, G. (2013) Immunohistochemical expression of Wilms' tumor protein (WT1) in developing human epithelial and mesenchymal tissues. Acta Histochem. 115, 70-75
31. Gauldie, J., Bonniaud, P., Sime, P., Ask, K., and Kolb, M. (2007) TGF-beta, Smad3 and the process of progressive fibrosis. Biochem. Soc. Trans. 35, 661-664
32. Ju, W., Ogawa, A., Heyer, J., Nierhof, D., Yu, L., Kucherlapati, R., Shafritz, D. A., and Bottinger, E. P. (2006) Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation. Mol. Cell. Biol. 26, 654-667
33. Phanish, M. K., Wahab, N. A., Colville-Nash, P., Hendry, B. M., and Dockrell, M. E. (2006) The differential role of Smad2 and Smad3 in the regulation of pro-fibrotic TGFbeta1 responses in human proximal-Tubule epithelial cells. Biochem. J. 393, 601-607
34. Thuault, S., Valcourt, U., Petersen, M., Manfioletti, G., Heldin, C. H., and Moustakas, A. (2006) Transforming growth factorbeta employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol. 174, 175-183
35. Come, C., Arnoux, V., Bibeau, F., and Savagner, P. (2004) Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J. Mammary Gland Biol. Neoplasia 9, 183-193
36. Takeichi, M., Nimura, K., Mori, M., Nakagami, H., and Kaneda, Y. (2013) The transcription factors Tbx18 and Wt1 control the epicardial epithelial-mesenchymal transition through bi-directional regulation of Slug in murine primary epicardial cells. PloS ONE 8, e57829
37. Morita, T., Mayanagi, T., and Sobue, K. (2007) Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via Slug induction and actin remodeling. J. Cell Biol. 179, 1027-1042
38. Sato, M., Muragaki, Y., Saika, S., Roberts, A. B., and Ooshima, A. (2003) Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J. Clin. Invest. 112, 1486-1494
39. Decologne, N., Kolb, M., Margetts, P. J., Menetrier, F., Artur, Y., Garrido, C., Gauldie, J., Camus, P., and Bonniaud, P. (2007) TGF-beta1 induces progressive pleural scarring and subpleural fibrosis. J. Immunol. 179, 6043-6051
40. Jomgeow, T., Oji, Y., Tsuji, N., Ikeda, Y., Ito, K., Tsuda, A., Nakazawa, T., Tatsumi, N., Sakaguchi, N., Takashima, S., Shirakata, T., Nishida, S., Hosen, N., Kawakami, M., Tsuboi, A., Oka, Y., Itoh, K., and Sugiyama, H. (2006) Wilms' tumor gene WT1 17AA()/KTS() isoform induces morphological changes and promotes cell migration and invasion in vitro. Cancer Sci. 97, 259-270
41. Burwell, E. A., McCarty, G. P., Simpson, L. A., Thompson, K. A., and Loeb, D. M. (2007) Isoforms of Wilms' tumor suppressor gene (WT1) have distinct effects on mammary epithelial cells. Oncogene 26, 3423-3430
42. Chapman, H. A. (2012) Epithelial responses to lung injury: role of the extracellular matrix. Proc. Am. Thorac. Soc. 9, 89-95
43. Zavadil, J., and Bottinger, E. P. (2005) TGF-beta and epithelialto-mesenchymal transitions. Oncogene 24, 5764-5774
44. Nakamura, Y., Sagara, T., Seki, K., Hirano, S., and Nishida, T. (2003) Permissive effect of fibronectin on collagen gel contraction mediated by bovine trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 44, 4331-4336
45. Kalluri, R., and Neilson, E. G. (2003) Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 112, 1776-1784
46. Hosono, S., Gross, I., English, M. A., Hajra, K. M., Fearon, E. R., and Licht, J. D. (2000) E-cadherin is a WT1 target gene. J. Biol. Chem. 275, 10943-10953
47. Chen, H., Paradies, N. E., Fedor-Chaiken, M., and Brackenbury, R. (1997) E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms. J. Cell Sci. 110, 345-356
48. Fransvea, E., Angelotti, U., Antonaci, S., and Giannelli, G. (2008) Blocking transforming growth factor-beta up-regulates E-cadherin and reduces migration and invasion of hepatocellular carcinoma cells. Hepatology 47, 1557-1566
49. Zhou, B., and Pu, W. T. (2012) Genetic Cre-loxP assessment of epicardial cell fate using Wt1-driven Cre alleles. Circulation Res. 111, e276-e280