Activation of Wnt5a-Ror2 signaling associated with epithelial-to-mesenchymal transition of tubular epithelial cells during renal fibrosis

Genes to Cells

Volumn 18, Issue 7, 2013, Pages 608-619

  Li, Xin ^a   Yamagata, Kaoru ^a   Nishita, Michiru ^a   Endo, Mitsuharu ^a   Arfian, Nur ^a   Rikitake, Yoshiyuki ^a   Emoto, Noriaki ^a,b   Hirata, Ken ichi ^a   Tanaka, Yoshiya ^c   Minami, Yasuhiro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE ROR2; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; VIMENTIN; WNT5A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; IMMUNOFLUORESCENCE TEST; KIDNEY FIBROSIS; KIDNEY TUBULE BASEMENT MEMBRANE; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; KIDNEY DISEASES; MALE; MICE; MICE, INBRED C57BL; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; SIGNAL TRANSDUCTION; WNT PROTEINS;

GASTROPODA; MUS;

EID: 84879415865     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12064     Document Type: Article

References (43)

1. Asada, N., Takase, M., Nakamura, J. et al. (2011) Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J. Clin. Invest. 121, 3981-3990.
2. du Bois, R.M. (2010) Strategies for treating idiopathic pulmonary fibrosis. Nat. Rev. Drug. Discov. 9, 129-140.
3. Boor, P., Ostendorf, T. & Floege, J. (2010) Renal fibrosis: novel insights into mechanisms and therapeutic targets. Nat. Rev. Nephrol. 6, 643-656.
4. Böttinger, E.P. & Bitzer, M. (2002) TGF-signaling in renal disease. J. Am. Soc. Nephrol. 13, 2600-2610.
5. Cheng, S. & Lovett, D.H. (2003) Gelatinase A (MMP-2) is necessary and sufficient for renal tubular cell epithelial-mesenchymal transformation. Am. J. Pathol. 162, 1937-1949.
6. Cheng, S., Pollock, A.S., Mahimkar, R., Olson, J.L. & Lovett, D.H. (2006) Matrix metalloproteinase 2 and basement membrane integrity: a unifying mechanism for progressive renal injury. FASEB J. 20, 1898-1900.
7. Du, X., Shimizu, A., Masuda, Y., Kuwahara, N., Arai, T., Kataoka, M., Uchiyama, M., Kaneko, T., Akimoto, T., Iino, Y. & Fukuda, Y. (2012) Involvement of matrix metalloproteinase-2 in the development of renal interstitial fibrosis in mouse obstructive nephropathy. Lab. Invest. 92, 1149-1160.
8. Endo, M., Doi, R., Nishita, M. & Minami, Y. (2012) Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J. Cell Sci. 125, 2017-2029.
9. Enomoto, M., Hayakawa, S., Itsukushima, S., Ren, D.Y., Matsuo, M., Tamada, K., Oneyama, C., Okada, M., Takumi, T., Nishita, M. & Minami, Y. (2009) Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 28, 3197-3208.
10. Guarino, M., Tosoni, A. & Nebuloni, M. (2009) Direct contribution of epithelium to organ fibrosis: epithelial-mesenchymal transition. Hum. Pathol. 40, 1365-1376.
11. He, W., Dai, C., Li, Y., Zeng, G., Monga, S.P. & Liu, Y. (2009) Wnt/beta-catenin signaling promotes renal interstitial fibrosis. J. Am. Soc. Nephrol. 20, 765-776.
12. Hu, B. & Phan, S.H. (2013) Myofibroblasts. Curr. Opin. Rheumatol. 254, 71-77.
13. Jayachandran, A., Königshoff, M., Yu, H., Rupniewska, E., Hecker, M., Klepetko, W., Seeger, W. & Eickelberg, O. (2009) SNAI transcription factors mediate epithelial-mesenchymal transition in lung fibrosis. Thorax 64, 1053-1061.
14. Kani, S., Oishi, I., Yamamoto, H., Yoda, A., Suzuki, H., Nomachi, A., Iozumi, K., Nishita, M., Kikuchi, A., Takumi, T. & Minami, Y. (2004) The receptor-tyrosine kinase Ror2 associates with and is activated by casein kinase Iε. J. Biol. Chem. 279, 50102-50109.
15. Klahr, S. & Morrissey, J. (2002) Obstructive nephropathy and renal fibrosis. Am. J. Physiol. Renal Physiol. 283, F861-F875.
16. Lange-Sperandio, B., Trautmann, A., Eickelberg, O., Jayachandran, A., Oberle, S., Schmidutz, F., Rodenbeck, B., Hömme, M., Horuk, R. & Schaefer, F. (2007) Leukocytes induce epithelial to mesenchymal transition after unilateral ureteral obstruction in neonatal mice. Am. J. Pathol. 171, 861-871.
17. Levänen, B., Wheelock, A.M., Eklund, A., Grunewald, J. & Nord, M. (2011) Increased pulmonary Wnt (wingless/integrated)-signaling in patients with sarcoidosis. Respir. Med. 105, 282-291.
18. Lian, Y.G., Zhou, Q.G., Zhang, Y.J. & Zheng, F.L. (2011) VEGF ameliorates tubulointerstitial fibrosis in unilateral ureteral obstruction mice via inhibition of epithelial-mesenchymal transition. Acta Pharmacol. Sin. 32, 1513-1521.
19. Liu, Y. (2004) Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J. Am. Soc. Nephrol. 15, 1-12.
20. Logan, C.Y. & Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
21. Maeda, K., Kobayashi, Y., Udagawa, N., Uehara, S., Ishihara, A., Mizoguchi, T., Kikuchi, Y., Takada, I., Kato, S., Kani, S., Nishita, M., Marumo, K., Martin, T.J., Minami, Y. & Takahashi, N. (2012) Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat. Med. 18, 405-412.
22. Matsuda, T., Nomi, M., Ikeya, M., Kani, S., Oishi, I., Terashima, T., Takada, S. & Minami, Y. (2001) Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech. Dev. 105, 153-156.
23. Meran, S. & Steadman, R. (2011) Fibroblasts and myofibroblasts in renal fibrosis. Int. J. Exp. Pathol. 92, 158-167.
24. Miyoshi, H., Ajima, R., Luo, C.T., Yamaguchi, T.P. & Stappenbeck, T.S. (2012) Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Science 338, 108-113.
25. Nishita, M., Enomoto, M., Yamagata, K. & Minami, Y. (2010a) Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 20, 346-354.
26. Nishita, M., Itsukushima, S., Nomachi, A., Endo, M., Wang, Z., Inaba, D., Qiao, S., Takada, S., Kikuchi, A. & Minami, Y. (2010b) Ror2/Frizzled complex mediates Wnt5a-induced AP1 activation by regulating Dishevelled polymerization. Mol. Cell. Biol. 30, 3610-3619.
27. Nishita, M., Yoo, S.K., Nomachi, A., Kani, S., Sougawa, N., Ohta, Y., Takada, S., Kikuchi, A. & Minami, Y. (2006) Filopodia formation mediated by receptor-tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J. Cell Biol. 175, 555-562.
28. Nomachi, A., Nishita, M., Inaba, D., Enomoto, M., Hamasaki, M. & Minami, Y. (2008) Receptor-tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J. Biol. Chem. 283, 27973-27981.
29. O'Connell, M.P., Fiori, J.L., Xu, M., Carter, A.D., Frank, B.P., Camilli, T.C., French, A.D., Dissanayake, S.K., Indig, F.E., Bernier, M., Taub, D.D., Hewitt, S.M. & Weeraratna, A.T. (2010) The orphan tyrosine kinase receptor, ROR2, mediates Wnt5A signaling in metastatic melanoma. Oncogene 29, 34-44.
30. Oishi, I., Suzuki, H., Onishi, N., Takada, R., Kani, S., Ohkawara, B., Koshida, I., Suzuki, K., Yamada, G., Schwabe, G.C., Mundlos, S., Shibuya, H., Takada, S. & Minami, Y. (2003) The receptor-tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signaling pathway. Genes Cells 8, 645-654.
31. Pozharskaya, V., Torres-González, E., Rojas, M., Gal, A., Amin, M., Dollard, S., Roman, J., Stecenko, A.A. & Mora, A.L. (2009) Twist: a regulator of epithelial-mesenchymal transition in lung fibrosis. PLoS ONE 4, e7559.
32. Qian, D., Jones, C., Rzadzinska, A., Mark, S., Zhang, X., Steel, K.P., Dai, X. & Chen, P. (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306, 121-133.
33. Ren, D., Minami, Y. & Nishita, M. (2011) Critical role of Wnt5a-Ror2 signaling in motility and invasiveness of carcinoma cells following Snail-mediated epithelial-mesenchymal transition. Genes Cells 16, 304-315.
34. Takeuchi, S., Takeda, K., Oishi, I., Nomi, M., Ikeya, M., Itoh, K., Tamura, S., Ueda, T., Hatta, T., Otani, H., Terashima, T., Takada, S., Yamamura, H., Akira, S. & Minami, Y. (2000) Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 5, 71-78.
35. Tsai, J.P., Liou, J.H., Kao, W.T., Wang, S.C., Lian, J.D. & Chang, H.R. (2012) Increased expression of intranuclear matrix metalloproteinase 9 in atrophic renal tubules is associated with renal fibrosis. PLoS ONE 7, e48164.
36. Vuga, L.J., Ben-Yehudah, A., Kovkarova-Naumovski, E., Oriss, T., Gibson, K.F., Feghali-Bostwick, C. & Kaminski, N. (2009) WNT5A is a regulator of fibroblast proliferation and resistance to apoptosis. Am. J. Respir. Cell Mol. Biol. 41, 583-589.
37. Wang, X., Zhou, Y., Tan, R., Xiong, M., He, W., Fang, L., Wen, P., Jiang, L. & Yang, J. (2010) Mice lacking the matrix metalloproteinase-9 gene reduce renal interstitial fibrosis in obstructive nephropathy. Am. J. Physiol. Renal Physiol. 299, F973-F982.
38. Wodarz, A. & Nusse, R. (1998) Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88.
39. Wright, T.M., Brannon, A.R., Gordan, J.D., Mikels, A.J., Mitchell, C., Chen, S., Espinosa, I., van de Rijn, M., Pruthi, R., Wallen, E., Edwards, L., Nusse, R. & Rathmell, W.K. (2009) Ror2, a developmentally regulated kinase, promotes tumor growth potential in renal cell carcinoma. Oncogene 28, 2513-2523.
40. Yamagata, K., Fujiyama, S., Ito, S., Ueda, T., Murata, T., Naitou, M., Takeyama, K., Minami, Y., O'Malley, B.W. & Kato, S. (2009) Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell 36, 340-347.
41. Yamagata, K., Li, X., Ikegaki, S., Oneyama, C., Okada, M., Nishita, M. & Minami, Y. (2012) Dissection of Wnt5a-Ror2 signaling leading to matrix metalloproteinase (MMP-13) expression. J. Biol. Chem. 287, 1588-1599.
42. Yamamoto, H., Oue, N., Sato, A., Hasegawa, Y., Yamamoto, H., Matsubara, A., Yasui, W. & Kikuchi, A. (2010) Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29, 2036-2046.
43. Zhang, P., Cai, Y., Soofi, A. & Dressler, G.R. (2012) Activation of Wnt11 by transforming growth factor-β drives mesenchymal gene expression through non-canonical Wnt protein signaling in renal epithelial cells. J. Biol. Chem. 287, 21290-21302.