Osterix regulates calcification and degradation of chondrogenic matrices through matrix metalloproteinase 13 (MMP13) expression in association with transcription factor Runx2 during endochondral ossification

Journal of Biological Chemistry

Volumn 287, Issue 40, 2012, Pages 33179-33190

  Nishimura, Riko ^a   Wakabayashi, Makoto ^a   Hata, Kenji ^a   Matsubara, Takuma ^a   Honma, Shiho ^a   Wakisaka, Satoshi ^a   Kiyonari, Hiroshi ^b   Shioi, Go ^b   Yamaguchi, Akira ^c   Tsumaki, Noriyuki ^d   Akiyama, Haruhiko ^e   Yoneda, Toshiyuki ^a  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; MAMMALS; TRANSCRIPTION; TRANSCRIPTION FACTORS;

CHONDROCYTE DIFFERENTIATION; ENDOCHONDRAL OSSIFICATION; FUNCTIONAL INTERACTION; MATRIX METALLOPROTEINASE 13; MICROARRAY ANALYSIS; MOLECULAR MECHANISM; PHYSICAL INTERACTIONS; REGULATORY MECHANISM;

BIOMINERALIZATION;

COLLAGENASE 3; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIFICATION; CARTILAGE MATRIX; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ENCHONDRAL OSSIFICATION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OSSIFICATION; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; UPREGULATION;

MUS;

EID: 84866920548     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.337063     Document Type: Article

References (38)

1. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
2. de Crombrugghe, B., Lefebvre, V., Behringer, R. R., Bi, W., Murakami, S., and Huang, W. (2000) Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol. 19, 389-394
3. Komori, T. (2011) Signaling networks in RUNX2-dependent bone development. J. Cell. Biochem. 112, 750-755
4. Nishimura, R., Hata, K., Ikeda, F., Ichida, F., Shimoyama, A., Matsubara, T., Wada, M., Amano, K., and Yoneda, T. (2008) Signal transduction and transcriptional regulation during mesenchymal cell differentiation. J. Bone Miner. Metab. 26, 203-212 (Pubitemid 351677844)
5. Ornitz, D. M., and Marie, P. J. (2002) FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 16, 1446-1465 (Pubitemid 34686327)
6. Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F.D., Keutel, J., Hustert, E., Wolf, U., Tommerup, N., Schempp, W., and Scherer, G. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120
7. Foster, J. W., Dominguez-Steglich, M. A., Guioli, S., Kwok, C., Weller, P. A., Stevanović, M., Weissenbach, J., Mansour, S., Young, I. D., and Goodfellow, P. N. (1994) Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372, 525-530 (Pubitemid 24368528)
8. Akiyama, H., Chaboissier, M. C., Martin, J. F., Schedl, A., and de Crombrugghe, B. (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 16, 2813-2828 (Pubitemid 35253149)
9. Ng, L. J., Wheatley, S., Muscat, G. E., Conway-Campbell, J., Bowles, J., Wright, E., Bell, D. M., Tam, P. P., Cheah, K. S., and Koopman, P. (1997) SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 183, 108-121 (Pubitemid 27157837)
10. Lefebvre, V., Huang, W., Harley, V. R., Goodfellow, P. N., and de Crombrugghe, B. (1997) SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro-α1(II) collagen gene. Mol. Cell. Biol. 17, 2336-2346 (Pubitemid 27133320)
11. Liu, Y., Li, H., Tanaka, K., Tsumaki, N., and Yamada, Y. (2000) Identification of an enhancer sequence within the first intron required for cartilage-specific transcription of the α2(XI) collagen gene. J. Biol. Chem. 275, 12712-12718 (Pubitemid 30241422)
12. Takahashi, I., Nuckolls, G. H., Takahashi, K., Tanaka, O., Semba, I., Dashner, R., Shum, L., and Slavkin, H. C. (1998) Compressive force promotes sox9, type II collagen, and aggrecan and inhibits IL-1β expression resulting in chondrogenesis in mouse embryonic limb bud mesenchymal cells. J. Cell Sci. 111, 2067-2076 (Pubitemid 28391071)
13. Takigawa, Y., Hata, K., Muramatsu, S., Amano, K., Ono, K., Wakabayashi, M., Matsuda, A., Takada, K., Nishimura, R., and Yoneda, T. (2010) The transcription factor Znf219 regulates chondrocyte differentiation by assembling a transcription factory with Sox9. J. Cell Sci. 123, 3780-3788
14. Amano, K., Hata, K., Sugita, A., Takigawa, Y., Ono, K., Wakabayashi, M., Kogo, M., Nishimura, R., and Yoneda, T. (2009) Sox9 family members negatively regulate maturation and calcification of chondrocytes through up-regulation of parathyroid hormone-related protein. Mol. Biol. Cell 20, 4541-4551
15. Hattori, T., Müller, C., Gebhard, S., Bauer, E., Pausch, F., Schlund, B., Bösl, M. R., Hess, A., Surmann-Schmitt, C., von der Mark, H., de Crombrugghe, B., and von der Mark, K. (2010) SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation, and endochondral ossification. Development 137, 901-911
16. Enomoto, H., Enomoto-Iwamoto, M., Iwamoto, M., Nomura, S., Himeno, M., Kitamura, Y., Kishimoto, T., and Komori, T. (2000) Cbfa1 is a positive regulatory factor in chondrocyte maturation. J. Biol. Chem. 275, 8695-8702 (Pubitemid 30180221)
17. Yoshida, C. A., Yamamoto, H., Fujita, T., Furuichi, T., Ito, K., Inoue, K., Yamana, K., Zanma, A., Takada, K., Ito, Y., and Komori, T. (2004) Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 18, 952-963 (Pubitemid 38529663)
18. Zheng, Q., Zhou, G., Morello, R., Chen, Y., Garcia-Rojas, X., and Lee, B. (2003) Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J. Cell Biol. 162, 833-842 (Pubitemid 37087723)
19. Kwon, T. G., Zhao, X., Yang, Q., Li, Y., Ge, C., Zhao, G., and Franceschi, R. T. (2011) Physical and functional interactions between Runx2 and HIF-1α induce vascular endothelial growth factor gene expression. J. Cell. Biochem. 112, 3582-3593
20. Komori, T. (2010) Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res. 339, 189-195
21. Rutges, J. P., Duit, R. A., Kummer, J. A., Oner, F. C., van Rijen, M. H., Verbout, A. J., Castelein, R. M., Dhert, W. J., and Creemers, L. B. (2010) Hypertrophic differentiation and calcification during intervertebral disc degeneration. Osteoarthritis Cartilage 18, 1487-1495
22. Kawaguchi, H. (2008) Endochondral ossification signals in cartilage degradation during osteoarthritis progression in experimental mouse models. Mol. Cells 25, 1-6
23. Matsubara, T., Kida, K., Yamaguchi, A., Hata, K., Ichida, F., Meguro, H., Aburatani, H., Nishimura, R., and Yoneda, T. (2008) BMP2 regulates Osterix through Msx2 and Runx2 during osteoblast differentiation. J. Biol. Chem. 283, 29119-29125
24. Hata, K., Nishimura, R., Muramatsu, S., Matsuda, A., Matsubara, T., Amano, K., Ikeda, F., Harley, V. R., and Yoneda, T. (2008) Paraspeckle protein p54nrb links Sox9-mediated transcription with RNA processing during chondrogenesis in mice. J. Clin. Invest. 118, 3098-3108
25. Suzuki, Y., Yoshitomo-Nakagawa, K., Maruyama, K., Suyama, A., and Sugano, S. (1997) Construction and characterization of a full-length-enriched and a 5′-end-enriched cDNA library. Gene 200, 149-156 (Pubitemid 27460481)
26. Ikegami, D., Akiyama, H., Suzuki, A., Nakamura, T., Nakano, T., Yoshikawa, H., and Tsumaki, N. (2011) Sox9 sustains chondrocyte survival and hypertrophy in part through Pik3ca-Akt pathways. Development 138, 1507-1519
27. Yagi, T., Tokunaga, T., Furuta, Y., Nada, S., Yoshida, M., Tsukada, T., Saga, Y., Takeda, N., Ikawa, Y., and Aizawa, S. (1993) A novel ES cell line, TT2, with high germ line-differentiating potency. Anal. Biochem. 214, 70-76 (Pubitemid 23300355)
28. Nishimura, R., Moriyama, K., Yasukawa, K., Mundy, G. R., and Yoneda, T. (1998) Combination of interleukin-6 and soluble interleukin-6 receptors induces differentiation and activation of JAK-STAT and MAP kinase pathways in MG-63 human osteoblastic cells. J. Bone Miner. Res. 13, 777-785 (Pubitemid 28224193)
29. Nakashima, K., Zhou, X., Kunkel, G., Zhang, Z., Deng, J. M., Behringer, R. R., and de Crombrugghe, B. (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108, 17-29 (Pubitemid 34137009)
30. Kaback, L. A., Soung do, Y., Naik, A., Smith, N., Schwarz, E. M., O'Keefe, R. J., Drissi, H. (2008) Osterix/Sp7 regulates mesenchymal stem cell mediated endochondral ossification. J. Cell. Physiol. 214, 173-182
31. Zhou, X., Zhang, Z., Feng, J. Q., Dusevich, V.M., Sinha, K., Zhang, H., Darnay, B. G., and de Crombrugghe, B. (2010) Multiple functions of Osterix are required for bone growth and homeostasis in postnatal mice. Proc. Natl. Acad. Sci. U.S.A. 107, 12919-12924
32. Kirsch, T., and Wuthier, R. E. (1994) Stimulation of calcification of growth plate cartilage matrix vesicles by binding to type II and X collagens. J. Biol. Chem. 269, 11462-11469 (Pubitemid 24200363)
33. Mengshol, J. A, Vincenti, M. P., and Brinckerhoff, C. E. (2001) IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 29, 4361-4372 (Pubitemid 33064776)
34. Tang, W., Li, Y., Osimiri, L., and Zhang, C. (2011) Osteoblast-specific transcription factor Osterix (Osx) is an upstream regulator of Satb2 during bone formation. J. Biol. Chem. 286, 32995-33002
35. 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 (Pubitemid 39627796)
36. Stickens, D., Behonick, D. J., Ortega, N., Heyer, B., Hartenstein, B., Yu, Y., Fosang, A.J., Schorpp-Kistner, M., Angel, P., and Werb, Z. (2004) Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131, 5883-5895 (Pubitemid 40123905)
37. von der Mark, K., Kirsch, T., Nerlich, A., Kuss, A., Weseloh, G., Glückert, K., and Stöss, H. (1992) Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum. 35, 806-811
38. Fuerst, M., Bertrand, J., Lammers, L., Dreier, R., Echtermeyer, F., Nitschke, Y., Rutsch, F., Schäfer, F. K., Niggemeyer, O., Steinhagen, J., Lohmann, C.H., Pap, T., Rüther, W. (2009) Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum. 60, 2694-2703