Mitogen-activated protein kinase (MAPK)-regulated interactions between osterix and Runx2 are critical for the transcriptional osteogenic program

Journal of Biological Chemistry

Volumn 289, Issue 39, 2014, Pages 27105-27117

  Artigas, Natalia ^a   Ureña, Carlos ^a   Rodríguez Carballo, Edgardo ^a   Rosa, José Luis ^a   Ventura, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DNA SEQUENCES; ENZYMES; PHOSPHORYLATION; TRANSCRIPTION;

FUNCTIONAL INTERACTION; MITOGEN ACTIVATED PROTEIN KINASE; MOLECULAR DESCRIPTIONS; OSTEOBLAST DIFFERENTIATION; PHOSPHORYLATION SITES; PHYSICAL INTERACTIONS; PROTEIN-PROTEIN INTERACTIONS; TRANSCRIPTIONAL COMPLEXES;

BINDING SITES;

BONE SIALOPROTEIN; COLLAGEN TYPE 1; FIBROMODULIN; MITOGEN ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; OSTERIX PROTEIN, MOUSE; RUNX2 PROTEIN, HUMAN; RUNX2 PROTEIN, MOUSE; SP7 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; COL1A1 GENE; FMOD GENE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IBSP GENE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OSTEOBLAST; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ANIMAL; BONE DEVELOPMENT; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CORE BINDING FACTOR ALPHA 1 SUBUNIT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; OSTEOGENESIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84907581200     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.576793     Document Type: Article

References (53)

1. Sinha, K. M., Yasuda, H., Zhou, X., and de Crombrugghe, B. (2014) Osterix and NO66 histone demethylase control the chromatin architecture of Osterix target genes during osteoblast differentiation. J. Bone Miner. Res. 29, 855-865
2. Karsenty, G., Kronenberg, H. M., and Settembre, C. (2009) Genetic control of bone formation. Annu. Rev. Cell Dev. Biol. 25, 629-648
3. Liu, T. M., and Lee, E. H. (2013) Transcriptional regulatory cascades in Runx2-dependent bone development. Tissue Eng. Part B Rev. 19, 254-263
4. Ducy, P., Zhang, R., Geoffroy, V., Ridall, A. L., and Karsenty, G. (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89, 747-754
5. 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
6. Baek, W. Y., de Crombrugghe, B., and Kim, J. E. (2010) Postnatally induced inactivation of Osterix in osteoblasts results in the reduction of bone formation and maintenance. Bone 46, 920-928
7. 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
8. Lee, B., Thirunavukkarasu, K., Zhou, L., Pastore, L., Baldini, A., Hecht, J., Geoffroy, V., Ducy, P., and Karsenty, G. (1997) Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat. Genet. 16, 307-310
9. Timpson, N. J., Tobias, J. H., Richards, J. B., Soranzo, N., Duncan, E. L., Sims, A. M., Whittaker, P., Kumanduri, V., Zhai, G., Glaser, B., Eisman, J., Jones, G., Nicholson, G., Prince, R., Seeman, E., Spector, T. D., Brown, M. A., Peltonen, L., Smith, G. D., Deloukas, P., and Evans, D. M. (2009) Common variants in the region around Osterix are associated with bone mineral density and growth in childhood. Hum. Mol. Genet. 18, 1510-1517
10. Lapunzina, P., Aglan, M., Temtamy, S., Caparrós-Martín, J. A., Valencia, M., Letón, R., Martínez-Glez, V., Elhossini, R., Amr, K., Vilaboa, N., and Ruiz-Perez, V. L. (2010) Identification of a frameshift mutation in Osterix in a patient with recessive osteogenesis imperfecta. Am. J. Hum. Genet. 87, 110-114
11. Lee, K. E., Seymen, F., Ko, J., Yildirim, M., Tuna, E. B., Gencay, K., and Kim, J. W. (2013) RUNX2 mutations in cleidocranial dysplasia. Genet. Mol. Res. 12, 4567-4574
12. Mundlos, S., Otto, F., Mundlos, C., Mulliken, J. B., Aylsworth, A. S., Albright, S., Lindhout, D., Cole, W. G., Henn, W., Knoll, J. H., Owen, M. J., Mertelsmann, R., Zabel, B. U., and Olsen, B. R. (1997) Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89, 773-779
13. Liu, T., Gao, Y., Sakamoto, K., Minamizato, T., Furukawa, K., Tsukazaki, T., Shibata, Y., Bessho, K., Komori, T., and Yamaguchi, A. (2007) BMP-2 promotes differentiation of osteoblasts and chondroblasts in Runx2-deficient cell lines. J. Cell. Physiol. 211, 728-735
14. Lee, M. H., Kwon, T. G., Park, H. S., Wozney, J. M., and Ryoo, H. M. (2003) BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem. Biophys. Res. Commun. 309, 689-694
15. 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
16. Ulsamer, A., Ortuño, M. J., Ruiz, S., Susperregui, A. R., Osses, N., Rosa, J. L., and Ventura, F. (2008) BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J. Biol. Chem. 283, 3816-3826
17. Nishio, Y., Dong, Y., Paris, M., O'Keefe, R. J., Schwarz, E. M., and Drissi, H. (2006) Runx2-mediated regulation of the zinc finger Osterix/Sp7 gene. Gene 372, 62-70
18. Kern, B., Shen, J., Starbuck, M., and Karsenty, G. (2001) Cbfa1 contributes to the osteoblast-specific expression of type I collagen genes. J. Biol. Chem. 276, 7101-7107
19. Nishimura, R., Wakabayashi, M., Hata, K., Matsubara, T., Honma, S., Wakisaka, S., Kiyonari, H., Shioi, G., Yamaguchi, A., Tsumaki, N., Akiyama, H., and Yoneda, T. (2012) Osterix regulates calcification and degradation of chondrogenic matrices through matrix metalloproteinase 13 (MMP13) expression in association with transcription factor Runx2 during endochondral ossification. J. Biol. Chem. 287, 33179-33190
20. Lee, K. N., Jang, W. G., Kim, E. J., Oh, S. H., Son, H. J., Kim, S. H., Franceschi, R., Zhang, X. K., Lee, S. E., and Koh, J. T. (2012) Orphan nuclear receptor chicken ovalbumin upstream promoter-transcription factor II (COUP-TFII) protein negatively regulates bone morphogenetic protein 2-induced osteoblast differentiation through suppressing runt-related gene 2 (Runx2) activity. J. Biol. Chem. 287, 18888-18899
21. Ortuño, M. J., Susperregui, A. R., Artigas, N., Rosa, J. L., and Ventura, F. (2013) Osterix induces Col1a1 gene expression through binding to Sp1 sites in the bone enhancer and proximal promoter regions. Bone 52, 548-556
22. Niger, C., Lima, F., Yoo, D. J., Gupta, R. R., Buo, A. M., Hebert, C., and Stains, J. P. (2011) The transcriptional activity of osterix requires the recruitment of Sp1 to the osteocalcin proximal promoter. Bone 49, 683-692
23. Chen, F., Zhang, X., Sun, S., Zara, J. N., Zou, X., Chiu, R., Culiat, C. T., Ting, K., and Soo, C. (2011) NELL-1, an osteoinductive factor, is a direct transcriptional target of Osterix. PLoS ONE 6, e24638
24. Bialek, P., Kern, B., Yang, X., Schrock, M., Sosic, D., Hong, N., Wu, H., Yu, K., Ornitz, D. M., Olson, E. N., Justice, M. J., and Karsenty, G. (2004) A twist code determines the onset of osteoblast differentiation. Dev. Cell 6, 423-435
25. Hinoi, E., Fujimori, S., Wang, L., Hojo, H., Uno, K., and Yoneda, Y. (2006) Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activation. J. Biol. Chem. 281, 18015-18024
26. Hong, J. H., Hwang, E. S., McManus, M. T., Amsterdam, A., Tian, Y., Kalmukova, R., Mueller, E., Benjamin, T., Spiegelman, B. M., Sharp, P. A., Hopkins, N., and Yaffe, M. B. (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309, 1074-1078
27. Javed, A., Bae, J. S., Afzal, F., Gutierrez, S., Pratap, J., Zaidi, S. K., Lou, Y., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2008) Structural coupling of Smad and Runx2 for execution of the BMP2 osteogenic signal. J. Biol. Chem. 283, 8412-8422
28. Roca, H., Phimphilai, M., Gopalakrishnan, R., Xiao, G., and Franceschi, R. T. (2005) Cooperative interactions between RUNX2 and homeodomain protein-binding sites are critical for the osteoblast-specific expression of the bone sialoprotein gene. J. Biol. Chem. 280, 30845-30855
29. Shimoyama, A., Wada, M., Ikeda, F., Hata, K., Matsubara, T., Nifuji, A., Noda, M., Amano, K., Yamaguchi, A., Nishimura, R., and Yoneda, T. (2007) Ihh/Gli2 signaling promotes osteoblast differentiation by regulating Runx2 expression and function. Mol. Biol. Cell 18, 2411-2418
30. Zhang, Y. W., Yasui, N., Ito, K., Huang, G., Fujii, M., Hanai, J., Nogami, H., Ochi, T., Miyazono, K., and Ito, Y. (2000) A RUNX2/PEBP2αA/CBFA1 mutation displaying impaired transactivation and Smad interaction in cleidocranial dysplasia. Proc. Natl. Acad. Sci. U.S.A. 97, 10549-10554
31. Koga, T., Matsui, Y., Asagiri, M., Kodama, T., de Crombrugghe, B., Nakashima, K., and Takayanagi, H. (2005) NFAT and Osterix cooperatively regulate bone formation. Nat. Med. 11, 880-885
32. Greenblatt, M. B., Shim, J. H., and Glimcher, L. H. (2013) Mitogen-activated protein kinase pathways in osteoblasts. Annu. Rev. Cell Dev. Biol. 29, 63-79
33. Ortuño, M. J., Ruiz-Gaspà, S., Rodríguez-Carballo, E., Susperregui, A. R., Bartrons, R., Rosa, J. L., and Ventura, F. (2010) p38 regulates expression of osteoblast-specific genes by phosphorylation of Osterix. J. Biol. Chem. 285, 31985-31994
34. Choi, Y. H., Gu, Y. M., Oh, J. W., and Lee, K. Y. (2011) Osterix is regulated by Erk1/2 during osteoblast differentiation. Biochem. Biophys. Res. Commun. 415, 472-478
35. Celil, A. B., and Campbell, P. G. (2005) BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via theMAPKand protein kinaseDsignaling pathways. J. Biol. Chem. 280, 31353-31359
36. Ducy, P., and Karsenty, G. (1995) Two distinct osteoblast-specific cisacting elements control expression of a mouse osteocalcin gene. Mol. Cell. Biol. 15, 1858-1869
37. Jin, H., van't Hof, R. J., Albagha, O. M., and Ralston, S. H. (2009) Promoter and intron 1 polymorphisms of COL1A1 interact to regulate transcription and susceptibility to osteoporosis. Hum. Mol. Genet. 18, 2729-2738
38. Paredes, R., Arriagada, G., Cruzat, F., Villagra, A., Olate, J., Zaidi, K., van Wijnen, A., Lian, J. B., Stein, G. S., Stein, J. L., and Montecino, M. (2004) Bone-specific transcription factor Runx2 interacts with the 1α,25-dihydroxyvitamin D3 receptor to up-regulate rat osteocalcin gene expression in osteoblastic cells. Mol. Cell. Biol. 24, 8847-8861
39. Pelletier, N., Champagne, N., Stifani, S., and Yang, X. J. (2002) MOZ and MORF histone acetyltransferases interact with the Runt-domain transcription factor Runx2. Oncogene 21, 2729-2740
40. Kawate, H., Wu, Y., Ohnaka, K., and Takayanagi, R. (2007) Mutual transactivational repression of Runx2 and the androgen receptor by an impairment of their normal compartmentalization. J. Steroid Biochem. Mol. Biol. 105, 46-56
41. Kim, S., Koga, T., Isobe, M., Kern, B. E., Yokochi, T., Chin, Y. E., Karsenty, G., Taniguchi, T., and Takayanagi, H. (2003) Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Dev. 17, 1979-1991
42. Greenblatt, M. B., Shim, J. H., Zou, W., Sitara, D., Schweitzer, M., Hu, D., Lotinun, S., Sano, Y., Baron, R., Park, J. M., Arthur, S., Xie, M., Schneider, M. D., Zhai, B., Gygi, S., Davis, R., and Glimcher, L. H. (2010) The p38 MAPK pathway is essential for skeletogenesis and bone homeostasis in mice. J. Clin. Invest. 120, 2457-2473
43. Ge, C., Yang, Q., Zhao, G., Yu, H., Kirkwood, K. L., and Franceschi, R. T. (2012) Interactions between extracellular signal-regulated kinase 1/2 and p38 MAP kinase pathways in the control of RUNX2 phosphorylation and transcriptional activity. J. Bone Miner. Res. 27, 538-551
44. Xiao, G., Jiang, D., Gopalakrishnan, R., and Franceschi, R. T. (2002) Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/ Runx2. J. Biol. Chem. 277, 36181-36187
45. Xiao, G., Jiang, D., Thomas, P., Benson, M. D., Guan, K., Karsenty, G., and Franceschi, R. T. (2000) MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J. Biol. Chem. 275, 4453-4459
46. Cheng, A., and Genever, P. G. (2010) SOX9 determines RUNX2 transactivity by directing intracellular degradation. J. Bone Miner. Res. 25, 2680-2689
47. Zhou, G., Zheng, Q., Engin, F., Munivez, E., Chen, Y., Sebald, E., Krakow, D., and Lee, B. (2006) Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc. Natl. Acad. Sci. U.S.A. 103, 19004-19009
48. Thirunavukkarasu, K., Mahajan, M., McLarren, K. W., Stifani, S., and Karsenty, G. (1998) Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbfβ. Mol. Cell. Biol. 18, 4197-4208
49. Kim, Y. J., Kim, B. G., Lee, S. J., Lee, H. K., Lee, S. H., Ryoo, H. M., and Cho, J. Y. (2007) The suppressive effect of myeloid Elf-1-like factor (MEF) in osteogenic differentiation. J. Cell. Physiol. 211, 253-260
50. Sierra, J., Villagra, A., Paredes, R., Cruzat, F., Gutierrez, S., Javed, A., Arriagada, G., Olate, J., Imschenetzky, M., Van Wijnen, A. J., Lian, J. B., Stein, G. S., Stein, J. L., and Montecino, M. (2003) Regulation of the bone-specific osteocalcin gene by p300 requires Runx2/Cbfa1 and the vitaminD3 receptor but not p300 intrinsic histone acetyltransferase activity. Mol. Cell. Biol. 23, 3339-3351
51. Guicheux, J., Lemonnier, J., Ghayor, C., Suzuki, A., Palmer, G., and Caverzasio, J. (2003) Activation of p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation. J. Bone Miner. Res. 18, 2060-2068
52. Franceschi, R. T., Xiao, G., Jiang, D., Gopalakrishnan, R., Yang, S., and Reith, E. (2003) Multiple signaling pathways converge on the Cbfa1/ Runx2 transcription factor to regulate osteoblast differentiation. Connect. Tissue Res. 44, Suppl. 1, 109-116
53. Lee, H. W., Suh, J. H., Kim, H. N., Kim, A. Y., Park, S. Y., Shin, C. S., Choi, J. Y., and Kim, J. B. (2008) Berberine promotes osteoblast differentiation by Runx2 activation with p38 MAPK. J. Bone Miner. Res. 23, 1227-1237