Dissection of Wnt5a-Ror2 signaling leading to matrix metalloproteinase (MMP-13) expression

Journal of Biological Chemistry

Volumn 287, Issue 2, 2012, Pages 1588-1599

  Yamagata, Kaoru ^a   Li, Xin ^a   Ikegaki, Shunkichi ^a   Oneyama, Chitose ^b   Okada, Masato ^b   Nishita, Michiru ^a   Minami, Yasuhiro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATOR PROTEIN-1; C-JUN N-TERMINAL KINASE; CARTILAGINOUS TISSUES; CHROMATIN IMMUNOPRECIPITATION ASSAY; CONSTITUTIVELY ACTIVES; GENE INDUCTION; GENE PROMOTER; INTRACELLULAR SIGNALING; INVASIVENESS; MATRIX; MATRIX METALLOPROTEINASES; MOLECULAR BASIS; OSTEOSARCOMA CELLS; PROMOTER REGION; REPORTER ASSAY; SAOS-2 CELLS; SPECIFIC INHIBITORS; TRANSCRIPTIONAL ACTIVATIONS;

ASSAYS; CELL CULTURE; CELLS; CHEMICAL ACTIVATION; ENZYME ACTIVITY; GENES; MACHINERY; PHOSPHORYLATION; TISSUE; TRANSCRIPTION; TRANSCRIPTION FACTORS;

SIGNALING;

COLLAGENASE 3; DISHEVELLED 2; MEMBRANE PROTEIN; PROTEIN ROR2; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MATRIX METALLOPROTEINASE 13; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; TRANSCRIPTION FACTOR AP-1; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84862956461     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.315127     Document Type: Article

References (44)

1. Wodarz, A., and Nusse, R. (1998) Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88
2. Logan, C. Y., and Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810
3. Mikels, A. J., and Nusse, R. (2006) Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol. 4, e115
4. Iozzo, R. V., Eichstetter, I., and Danielson, K. G. (1995) Aberrant expression of the growth factor Wnt-5A in human malignancy. Cancer Res. 55, 3495-3499
5. Weeraratna, A. T., Jiang, Y., Hostetter, G., Rosenblatt, K., Duray, P., Bittner, M., and Trent, J. M. (2002) Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1, 279-288
6. Kurayoshi, M., Oue, N., Yamamoto, H., Kishida, M., Inoue, A., Asahara, T., Yasui, W., and Kikuchi, A. (2006) Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 66, 10439-10448
7. Pukrop, T., Klemm, F., Hagemann, T., Gradl, D., Schulz, M., Siemes, S., Trümper, L., and Binder, C. (2006) Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc. Natl. Acad. Sci. U.S.A. 103, 5454-5459
8. Enomoto, M., Hayakawa, S., Itsukushima, S., Ren, D. Y., Matsuo, M., Tamada, K., Oneyama, C., Okada, M., Takumi, T., Nishita, M., and Minami, Y. (2009) Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 28, 3197-3208
9. Yamamoto, H., Oue, N., Sato, A., Hasegawa, Y., Yamamoto, H., Matsubara, A., Yasui, W., and Kikuchi, A. (2010) Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29, 2036-2046
10. Nishita, M., Yoo, S. K., Nomachi, A., Kani, S., Sougawa, N., Ohta, Y., Takada, S., Kikuchi, A., and Minami, Y. (2006) Filopodia formation mediated by receptor-tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J. Cell Biol. 175, 555-562
11. Nomachi, A., Nishita, M., Inaba, D., Enomoto, M., Hamasaki, M., and 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
12. 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., and Minami, Y. (2003) The receptor-tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signaling pathway. Genes Cells 8, 645-654
13. Yamamoto, S., Nishimura, O., Misaki, K., Nishita, M., Minami, Y., Yonemura, S., Tarui, H., and Sasaki, H. (2008) Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev. Cell 15, 23-36
14. 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., and Rathmell, W. K. (2009) Ror2, a developmentally regulated kinase, promotes tumor growth potential in renal cell carcinoma. Oncogene 28, 2513-2523
15. Ren, D., Minami, Y., and 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
16. Inada, M., Wang, Y., Byrne, M. H., Rahman, M. U., Miyaura, C., López-Otín, C., and Krane, S. M. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc. Natl. Acad. Sci. U.S.A. 101, 17192-17197
17. Ståhle-Bäckdahl, M., Sandstedt, B., Bruce, K., Lindahl, A., Jiménez, M. G., Vega, J. A., and López-Otín, C. (1997) Collagenase-3 (MMP-13) is expressed during human fetal ossification and re-expressed in postnatal bone remodeling and in rheumatoid arthritis. Lab. Invest. 76, 717-728
18. Freije, J. M., Díez-Itza, I., Balbín, M., Sánchez, L. M., Blasco, R., Tolivia, J., and López-Otín, C. (1994) Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J. Biol. Chem. 269, 16766-16773
19. Uría, J. A., Balbín, M., López, J. M., Alvarez, J., Vizoso, F., Takigawa, M., and López-Otín, C. (1998) Collagenase-3 (MMP-13) expression in chondrosarcoma cells and its regulation by basic fibroblast growth factor. Am. J. Pathol. 153, 91-101
20. Airola, K., Karonen, T., Vaalamo, M., Lehti, K., Lohi, J., Kariniemi, A. L., Keski-Oja, J., and Saarialho-Kere, U. K. (1999) Expression of collagenases-1 and -3 and their inhibitors TIMP-1 and -3 correlates with the level of invasion in malignant melanomas. Br. J. Cancer 80, 733-743
21. Etoh, T., Inoue, H., Yoshikawa, Y., Barnard, G. F., Kitano, S., and Mori, M. (2000) Increased expression of collagenase-3 (MMP-13) and MT1-MMP in esophageal cancer is related to cancer aggressiveness. Gut 47, 50-56
22. Yamada, T., Oshima, T., Yoshihara, K., Tamura, S., Kanazawa, A., Inagaki, D., Yamamoto, N., Sato, T., Fujii, S., Numata, K., Kunisaki, C., Shiozawa, M., Morinaga, S., Akaike, M., Rino, Y., Tanaka, K., Masuda, M., and Imada, T. (2010) Overexpression of MMP-13 gene in colorectal cancer with liver metastasis. Anticancer Res. 30, 2693-2699
23. Airola, K., Johansson, N., Kariniemi, A. L., Kähäri, V. M., and Saarialho-Kere, U. (1997) Human collagenase-3 is expressed in malignant squamous epithelium of the skin. J. Invest. Dermatol. 109, 225-231
24. Johansson, N., Airola, K., Grénman, R., Kariniemi, A. L., Saarialho-Kere, U., and Kähäri, V. M. (1997) Expression of collagenase-3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am. J. Pathol. 151, 499-508
25. Johansson, N., Vaalamo, M., Grénman, S., Hietanen, S., Klemi, P., Saarialho-Kere, U., and Kähäri, V. M. (1999) Collagenase-3 (MMP-13) is expressed by tumor cells in invasive vulvar squamous cell carcinomas. Am. J. Pathol. 154, 469-480
26. Nishita, M., Enomoto, M., Yamagata, K., and Minami, Y. (2010) Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 20, 346-354
27. Borden, P., Solymar, D., Sucharczuk, A., Lindman, B., Cannon, P., and Heller, R. A. (1996) Cytokine control of interstitial collagenase and collagenase- 3 gene expression in human chondrocytes. J. Biol. Chem. 271, 23577-23581
28. Kobayashi, M., Squires, G. R., Mousa, A., Tanzer, M., Zukor, D. J., Antoniou, J., Feige, U., and Poole, A. R. (2005) Role of interleukin-1 and tumor necrosis factor α in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum. 52, 128-135
29. Solís-Herruzo, J. A., Rippe, R. A., Schrum, L. W., de La Torre, P., García, I., Jeffrey, J. J., Muñoz-Yagüe, T., and Brenner, D. A. (1999) Interleukin-6 increases rat metalloproteinase-13 gene expression through stimulation of activator protein 1 transcription factor in cultured fibroblasts. J. Biol. Chem. 274, 30919-30926
30. Uría, J. A., Jiménez, M. G., Balbín, M., Freije, J. M., and López-Otín, C. (1998) Differential effects of transforming growth factor-β on the expression of collagenase-1 and collagenase-3 in human fibroblasts. J. Biol. Chem. 273, 9769-9777
31. Uría, J. A., Ståhle-Bäckdahl, M., Seiki, M., Fueyo, A., and López-Otín, C. (1997) Regulation of collagenase-3 expression in human breast carcinomas is mediated by stromal-epithelial cell interactions. Cancer Res. 57, 4882-4888
32. Ala-aho, R., and Kähäri, V. M. (2005) Collagenases in cancer. Biochimie 87, 273-286
33. Masckauchán, T. N., Agalliu, D., Vorontchikhina, M., Ahn, A., Parmalee, N. L., Li, C. M., Khoo, A., Tycko, B., Brown A. M., and Kitajewski, J. (2006) Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2. Mol. Biol. Cell 17, 5163-5172
34. Kani, S., Oishi, I., Yamamoto, H., Yoda, A., Suzuki, H., Nomachi, A., Iozumi, K., Nishita, M., Kikuchi, A., Takumi, T., and Minami, Y. (2004) The receptor-tyrosine kinase Ror2 associates with and is activated by casein kinase I∈. J. Biol. Chem. 279, 50102-50109
35. Nishita, M., Itsukushima, S., Nomachi, A., Endo, M., Wang, Z., Inaba, D., Qiao, S., Takada, S., Kikuchi, A., and Minami, Y. (2010) Ror2/Frizzled complex mediates Wnt5a-induced AP1 activation by regulating Dishevelled polymerization. Mol. Cell. Biol. 30, 3610-3619
36. Yamagata, K., Fujiyama, S., Ito, S., Ueda, T., Murata, T., Naitou, M., Takeyama, K., Minami, Y., O'Malley, B. W., and Kato, S. (2009) Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell 36, 340-347
37. Gupta, S., Campbell, D., Dérijard, B., and Davis, R. J. (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267, 389-393
38. González-Sancho, J. M., Brennan, K. R., Castelo-Soccio, L. A., and Brown, A. M. (2004) Wnt proteins induce Dishevelled phosphorylation via anLRP5/6- independent mechanism, irrespective of their ability to stabilize β-catenin. Mol. Cell. Biol. 24, 4757-4768
39. Witte, F., Bernatik, O., Kirchner, K., Masek, J., Mahl, A., Krejci, P., Mundlos, S., Schambony, A., Bryja, V., and Stricker, S. (2010) Negative regulation of Wnt signaling mediated by CK1-phosphorylated Dishevelled via Ror2. FASEB J. 24, 2417-2426
40. Kanazawa, S., Fujiwara, T., Matsuzaki, S., Shingaki, K., Taniguchi, M., Miyata, S., Tohyama, M., Sakai, Y., Yano, K., Hosokawa, K., and Kubo, T. (2010) bFGF regulates PI 3-kinase-Rac1-JNK pathway and promotes fibroblast migration in wound healing. PLoS One 5, e12228
41. Morioka, K., Tanikawa, C., Ochi, K., Daigo, Y., Katagiri, T., Kawano, H., Kawaguchi, H., Myoui, A., Yoshikawa, H., Naka, N., Araki, N., Kudawara, I., Ieguchi, M., Nakamura, K., Nakamura, Y., and Matsuda, K. (2009) Orphan receptor-tyrosine kinase ROR2 as a potential therapeutic target for osteosarcoma. Cancer Sci. 100, 1227-1233
42. Nomi, M., Oishi, I., Kani, S., Suzuki, H., Matsuda, T., Yoda, A., Kitamura, M., Itoh, K., Takeuchi, S., Takeda, K., Akira, S., Ikeya, M., Takada, S., and Minami, Y. (2001) Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice. Redundant and pleiotropic functions of mRor1 and mRor2 receptor-tyrosine kinases. Mol. Cell. Biol. 21, 8329-8335
43. Boumah, C. E., Lee, M., Selvamurugan, N., Shimizu, E., and Partridge, N. C. (2009) Runx2 recruits p300 to mediate parathyroid hormone effects on histone acetylation and transcriptional activation of the matrix metalloproteinase-13 gene. Mol. Endocrinol. 23, 1255-1263
44. Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R. T., Gao, Y. H., Inada, M., Sato, M., Okamoto, R., Kitamura, Y., Yoshiki, S., and Kishimoto, T. (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764