Indian hedgehog signaling regulates transcription and expression of collagen type X via Runx2/Smads interactions

Journal of Biological Chemistry

Volumn 289, Issue 36, 2014, Pages 24898-24910

  Amano, Katsuhiko ^a,b   Densmore, Michael ^a   Nishimura, Riko ^b   Lanske, Beate ^a  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMINERALIZATION; BONE; COLLAGEN; FEEDBACK; KRYPTON; MINERALOGY; TRANSCRIPTION;

CHONDROCYTE DIFFERENTIATION; CHONDROCYTE MATURATION; ENDOCHONDRAL OSSIFICATION; MATRIX MINERALIZATION; MOLECULAR MECHANISM; NEGATIVE FEEDBACK LOOP; PARATHYROID HORMONES; PROMOTER ACTIVITIES;

BODY FLUIDS;

COLLAGEN TYPE 10; SMAD PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX2; COL10A1 PROTEIN, MOUSE; GLI PROTEIN; IHH PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; ONCOPROTEIN; PROTEIN BINDING; SMAD1 PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR GLI2;

ANIMAL CELL; ARTICLE; BINDING ASSAY; BONE MINERALIZATION; CALCIFICATION; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; COL10A1 GENE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FOXA2 GENE; FOXA3 GENE; GENE; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC TRANSCRIPTION; GLI1 GENE; GLI2 GENE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MEF2C GENE; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; REGULATORY MECHANISM; RUNX2 GENE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; CONFOCAL MICROSCOPY; COS 1 CELL LINE; CYTOLOGY; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CHONDROCYTES; COLLAGEN TYPE X; CORE BINDING FACTOR ALPHA 1 SUBUNIT; COS CELLS; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; TRANS-ACTIVATORS;

EID: 84906987335     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570507     Document Type: Article

References (46)

1. de Crombrugghe, B., Lefebvre, V., and Nakashima, K. (2001) Regulatory mechanisms in the pathways of cartilage and bone formation. Curr. Opin. Cell Biol. 13, 721-727
2. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
3. Gao, B., Guo, J., She, C., Shu, A., Yang, M., Tan, Z., Yang, X., Guo, S., Feng, G., and He, L. (2001) Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat. Genet. 28, 386-388
4. Hellemans, J., Coucke, P. J., Giedion, A., De Paepe, A., Kramer, P., Beemer, F., and Mortier, G. R. (2003) Homozygous mutations in IHH cause acrocapitofemoral dysplasia, an autosomal recessive disorder with coneshaped epiphyses in hands and hips. Am. J. Hum. Genet. 72, 1040-1046
5. Lanske, B., Karaplis, A. C., Lee, K., Luz, A., Vortkamp, A., Pirro, A., Karperien, M., Defize, L. H., Ho, C., Mulligan, R. C., Abou-Samra, A. B., Jüppner, H., Segre, G. V., and Kronenberg, H. M. (1996) PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 273, 663-666
6. Vortkamp, A., Lee, K., Lanske, B., Segre, G. V., Kronenberg, H. M., and Tabin, C. J. (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622
7. Karp, S. J., Schipani, E., St-Jacques, B., Hunzelman, J., Kronenberg, H., and McMahon, A. P. (2000) Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone-related protein-dependent and -independent pathways. Development 127, 543-548
8. Kobayashi, T., Soegiarto, D. W., Yang, Y., Lanske, B., Schipani, E., McMahon, A. P., and Kronenberg, H. M. (2005) Indian hedgehog stimulates periarticular chondrocyte differentiation to regulate growth plate length independently of PTHrP. J. Clin. Invest. 115, 1734-1742
9. Maeda, Y., Schipani, E., Densmore, M. J., and Lanske, B. (2010) Partial rescue of postnatal growth plate abnormalities in Ihh mutants by expression of a constitutively active PTH/PTHrP receptor. Bone 46, 472-478
10. Amano, K., Ichida, F., Sugita, A., Hata, K., Wada, M., Takigawa, Y., Nakanishi, M., Kogo, M., Nishimura, R., and Yoneda, T. (2008) MSX2 stimulates chondrocyte maturation by controlling Ihh expression. J. Biol. Chem. 283, 29513-29521
11. Mak, K. K., Kronenberg, H. M., Chuang, P. T., Mackem, S., and Yang, Y. (2008) Indian hedgehog signals independently of PTHrP to promote chondrocyte hypertrophy. Development 135, 1947-1956
12. Higashikawa, A., Saito, T., Ikeda, T., Kamekura, S., Kawamura, N., Kan, A., Oshima, Y., Ohba, S., Ogata, N., Takeshita, K., Nakamura, K., Chung, U. I., and Kawaguchi, H. (2009) Identification of the core element responsive to runt-related transcription factor 2 in the promoter of human type X collagen gene. Arthritis Rheum. 60, 166-178
13. Li, F., Lu, Y., Ding, M., Napierala, D., Abbassi, S., Chen, Y., Duan, X., Wang, S., Lee, B., and Zheng, Q. (2011) Runx2 contributes to murine Col10a1 gene regulation through direct interaction with its cis-enhancer. J. Bone Miner. Res. 26, 2899-2910
14. Ueta, C., Iwamoto, M., Kanatani, N., Yoshida, C., Liu, Y., Enomoto-Iwamoto, M., Ohmori, T., Enomoto, H., Nakata, K., Takada, K., Kurisu, K., and Komori, T. (2001) Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J. Cell Biol. 153, 87-100
15. 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
16. Arnold, M. A., Kim, Y., Czubryt, M. P., Phan, D., McAnally, J., Qi, X., Shelton, J. M., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2007) MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev. Cell 12, 377-389
17. Kozhemyakina, E., Cohen, T., Yao, T. P., and Lassar, A. B. (2009) Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway. Mol. Cell. Biol. 29, 5751-5762
18. Ionescu, A., Kozhemyakina, E., Nicolae, C., Kaestner, K. H., Olsen, B. R., and Lassar, A. B. (2012) FoxA family members are crucial regulators of the hypertrophic chondrocyte differentiation program. Dev. Cell 22, 927-939
19. Gebhard, S., Pöschl, E., Riemer, S., Bauer, E., Hattori, T., Eberspaecher, H., Zhang, Z., Lefebvre, V., de Crombrugghe, B., and von der Mark, K. (2004) A highly conserved enhancer in mammalian type X collagen genes drives high levels of tissue-specific expression in hypertrophic cartilage in vitro and in vivo. Matrix Biol. 23, 309-322
20. 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
21. Sasaki, H., Hui, C., Nakafuku, M., and Kondoh, H. (1997)Abinding site for Gli proteins is essential for HNF-3β floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322
22. Morikawa, M., Koinuma, D., Miyazono, K., and Heldin, C. H. (2013) Genome-wide mechanisms of Smad binding. Oncogene 32, 1609-1615
23. 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
24. Hesse, E., Saito, H., Kiviranta, R., Correa, D., Yamana, K., Neff, L., Toben, D., Duda, G., Atfi, A., Geoffroy, V., Horne, W. C., and Baron, R. (2010) Zfp521 controls bone mass by HDAC3-dependent attenuation of Runx2 activity. J. Cell Biol. 191, 1271-1283
25. 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
26. Minina, E., Kreschel, C., Naski, M. C., Ornitz, D. M., and Vortkamp, A. (2002) Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev. Cell 3, 439-449
27. Minina, E., Wenzel, H. M., Kreschel, C., Karp, S., Gaffield, W., McMahon, A. P., and Vortkamp, A. (2001) BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128, 4523-4534
28. Lee, K. S., Kim, H. J., Li, Q. L., Chi, X. Z., Ueta, C., Komori, T., Wozney, J. M., Kim, E. G., Choi, J. Y., Ryoo, H. M., and Bae, S. C. (2000) Runx2 is a common target of transforming growth factor β1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol. Cell. Biol. 20, 8783-8792
29. Drissi, M. H., Li, X., Sheu, T. J., Zuscik, M. J., Schwarz, E. M., Puzas, J. E., Rosier, R. N., and O'Keefe, R. J. (2003) Runx2/Cbfa1 stimulation by retinoic acid is potentiated by BMP2 signaling through interaction with Smad1 on the collagen X promoter in chondrocytes. J. Cell. Biochem. 90, 1287-1298
30. Leboy, P., Grasso-Knight, G., D'Angelo, M., Volk, S. W., Lian, J. V., Drissi, H., Stein, G. S., and Adams, S. L. (2001) Smad-Runx interactions during chondrocyte maturation. J. Bone Joint Surg. Am. 83, S15-S22
31. Nishimura, R., Hata, K., Harris, S. E., Ikeda, F., and Yoneda, T. (2002) Core-binding factor α1 (Cbfa1) induces osteoblastic differentiation of C2C12 cells without interactions with Smad1 and Smad5. Bone 31, 303-312
32. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D., and Peterson, R. T. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41
33. Jiang, J., and Hui, C. C. (2008) Hedgehog signaling in development and cancer. Dev. Cell 15, 801-812
34. Hojo, H., Ohba, S., Taniguchi, K., Shirai, M., Yano, F., Saito, T., Ikeda, T., Nakajima, K., Komiyama, Y., Nakagata, N., Suzuki, K., Mishina, Y., Yamada, M., Konno, T., Takato, T., Kawaguchi, H., Kambara, H., and Chung, U. I. (2013) Hedgehog-Gli activators direct osteo-chondrogenic function of bone morphogenetic protein toward osteogenesis in the perichondrium. J. Biol. Chem. 288, 9924-9932
35. Hojo, H., Ohba, S., Yano, F., Saito, T., Ikeda, T., Nakajima, K., Komiyama, Y., Nakagata, N., Suzuki, K., Takato, T., Kawaguchi, H., and Chung, U. I. (2012) Gli1 protein participates in Hedgehog-mediated specification of osteoblast lineage during endochondral ossification. J. Biol. Chem. 287, 17860-17869
36. Park, H. L., Bai, C., Platt, K. A., Matise, M. P., Beeghly, A., Hui, C. C., Nakashima, M., and Joyner, A. L. (2000) Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127, 1593-1605
37. Miao, D., Liu, H., Plut, P., Niu, M., Huo, R., Goltzman, D., and Henderson, J. E. (2004) Impaired endochondral bone development and osteopenia in Gli2-deficient mice. Exp. Cell Res. 294, 210-222
38. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H., Joyner, A. L., and Hui, C. (1997) Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123
39. Joeng, K. S., and Long, F. (2009) The Gli2 transcriptional activator is a crucial effector for Ihh signaling in osteoblast development and cartilage vascularization. Development 136, 4177-4185
40. Hilton, M. J., Tu, X., Cook, J., Hu, H., and Long, F. (2005) Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 132, 4339-4351
41. Koziel, L., Wuelling, M., Schneider, S., and Vortkamp, A. (2005) Gli3 acts as a repressor downstream of Ihh in regulating two distinct steps of chondrocyte differentiation. Development 132, 5249-5260
42. Leung, V. Y., Gao, B., Leung, K. K., Melhado, I. G., Wynn, S. L., Au, T. Y., Dung, N. W., Lau, J. Y., Mak, A. C., Chan, D., and Cheah, K. S. (2011) SOX9 governs differentiation stage-specific gene expression in growth plate chondrocytes via direct concomitant transactivation and repression. PLoS Genet. 7, e1002356
43. 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
44. Zheng, Q., Keller, B., Zhou, G., Napierala, D., Chen, Y., Zabel, B., Parker, A. E., and Lee, B. (2009) Localization of the cis-enhancer element for mouse type X collagen expression in hypertrophic chondrocytes in vivo. J. Bone Miner. Res. 24, 1022-1032
45. Seriwatanachai, D., Densmore, M. J., Sato, T., Correa, D., Neff, L., Baron, R., and Lanske, B. (2011) Deletion of Zfp521 rescues the growth plate phenotype in a mouse model of Jansen metaphyseal chondrodysplasia. FASEB J. 25, 3057-3067
46. 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