SnoN suppresses maturation of chondrocytes by mediating signal cross-talk between transforming growth factor-β and bone morphogenetic protein pathways

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 29101-29113

  Kawamura, Ichiro ^a   Maeda, Shingo ^a   Imamura, Katsuyuki ^a   Setoguchi, Takao ^a   Yokouchi, Masahiro ^a   Ishidou, Yasuhiro ^a   Komiya, Setsuro ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION STEPS; ADULT MICE; ARTICULAR CARTILAGES; ATDC5 CELLS; BONE MORPHOGENETIC PROTEINS; CELLULAR PROCESS; CHONDROCYTE MATURATION; CHONDROCYTES; ENDOCHONDRAL OSSIFICATION; GROWTH PLATE; HYPERTROPHIC CHONDROCYTES; MOUSE EMBRYOS; NEGATIVE FEEDBACK MECHANISM; OVER-EXPRESSION; SIGNALING PATHWAYS; TRANSFORMING GROWTH FACTORS;

BONE; CARTILAGE; CELLS; CROSSTALK; CYTOLOGY; PHOSPHORYLATION; PLANTS (BOTANY); SIGNALING;

BODY FLUIDS;

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; BONE MORPHOGENETIC PROTEIN; COLLAGEN TYPE 10; COLLAGEN TYPE 10A1; COLLAGEN TYPE 2; COLLAGEN TYPE 2A1; INHIBITOR OF DIFFERENTIATION 1; SKI RELATED NOVEL PROTEIN N; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; ID1 GENE; INHIBITION KINETICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; BENZAMIDES; BONE MORPHOGENETIC PROTEIN 2; CARTILAGE, ARTICULAR; CERCOPITHECUS AETHIOPS; CHONDROCYTES; COS CELLS; DIOXOLES; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OSTEOARTHRITIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84865242186     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349415     Document Type: Article

References (53)

1. 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
2. Provot, S., and Schipani, E. (2005) Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328, 658-665
3. 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
4. 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
5. 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
6. Takeda, S., Bonnamy, J. P., Owen, M. J., Ducy, P., and Karsenty, G. (2001) Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 15, 467-481
7. Scotti, C., Tonnarelli, B., Papadimitropoulos, A., Scherberich, A., Schaeren, S., Schauerte, A., Lopez-Rios, J., Zeller, R., Barbero, A., and Martin, I. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc. Natl. Acad. Sci. U.S.A. 107, 7251-7256
8. Pullig, O., Weseloh, G., Ronneberger, D., Käkönen, S., and Swoboda, B. (2000) Chondrocyte differentiation in human osteoarthritis. Expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif. Tissue Int. 67, 230-240
9. Sandell, L. J., and Aigner, T. (2001) Articular cartilage and changes in arthritis. An introduction. Cell biology of osteoarthritis. Arthritis Res. 3, 107-113
10. Dreier, R. (2010) Hypertrophic differentiation of chondrocytes in osteoarthritis. The developmental aspect of degenerative joint disorders. Arthritis Res. Ther. 12, 216
11. Nelea, V., Luo, L., Demers, C. N., Antoniou, J., Petit, A., Lerouge, S., R Wertheimer, M., and Mwale, F. (2005) Selective inhibition of type X collagen expression in human mesenchymal stem cell differentiation on polymer substrates surface-modified by glow discharge plasma. J. Biomed. Mater. Res. A 75, 216-223
12. Sekiya, I., Vuoristo, J. T., Larson, B. L., and Prockop, D. J. (2002) In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 4397-4402
13. Miyazono, K., Kamiya, Y., and Morikawa, M. (2010) Bone morphogenetic protein receptors and signal transduction. J. Biochem. 147, 35-51
14. Tsumaki, N., Nakase, T., Miyaji, T., Kakiuchi, M., Kimura, T., Ochi, T., and Yoshikawa, H. (2002) Bone morphogenetic protein signals are required for cartilage formation and differently regulate joint development during skeletogenesis. J. Bone Miner. Res. 17, 898-906
15. Yoon, B. S., Ovchinnikov, D. A., Yoshii, I., Mishina, Y., Behringer, R. R., and Lyons, K. M. (2005) Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc. Natl. Acad. Sci. U.S.A. 102, 5062-5067
16. Retting, K. N., Song, B., Yoon, B. S., and Lyons, K. M. (2009) BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development 136, 1093-1104
17. Furumatsu, T., Tsuda, M., Taniguchi, N., Tajima, Y., and Asahara, H. (2005) Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. J. Biol. Chem. 280, 8343-8350
18. Volk, S. W., Luvalle, P., Leask, T., and Leboy, P. S. (1998) A BMP-responsive transcriptional region in the chicken type X collagen gene. J. Bone Miner. Res. 13, 1521-1529
19. 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-A, Suppl. 1, S15-S22
20. Kempf, H., Ionescu, A., Udager, A. M., and Lassar, A. B. (2007) Prochondrogenic signals induce a competence for Runx2 to activate hypertrophic chondrocyte gene expression. Dev. Dyn. 236, 1954-1962
21. Kobayashi, T., Lyons, K. M., McMahon, A. P., and Kronenberg, H. M. (2005) BMP signaling stimulates cellular differentiation at multiple steps during cartilage development. Proc. Natl. Acad. Sci. U.S.A. 102, 18023-18027
22. van Beuningen, H. M., Glansbeek, H. L., van der Kraan, P. M., and van den Berg, W. B. (1998) Differential effects of local application of BMP-2 or TGF-β1 on both articular cartilage composition and osteophyte formation. Osteoarthr. Cartil. 6, 306-317
23. Yang, X., Chen, L., Xu, X., Li, C., Huang, C., and Deng, C. X. (2001) TGF-β/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J. Cell Biol. 153, 35-46
24. Serra, R., Johnson, M., Filvaroff, E. H., LaBorde, J., Sheehan, D. M., Derynck, R., and Moses, H. L. (1997) Expression of a truncated, kinase-defective TGF-β type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J. Cell Biol. 139, 541-552
25. Wu, Q., Kim, K. O., Sampson, E. R., Chen, D., Awad, H., O'Brien, T., Puzas, J. E., Drissi, H., Schwarz, E. M., O'Keefe, R. J., Zuscik, M. J., and Rosier, R. N. (2008) Induction of an osteoarthritis-like phenotype and degradation of phosphorylated Smad3 by Smurf2 in transgenic mice. Arthritis Rheum. 58, 3132-3144
26. Li, T. F., Darowish, M., Zuscik, M. J., Chen, D., Schwarz, E. M., Rosier, R. N., Drissi, H., and O'Keefe, R. J. (2006) Smad3-deficient chondrocytes have enhanced BMP signaling and accelerated differentiation. J. Bone Miner. Res. 21, 4-16
27. Bobick, B. E., and Kulyk, W. M. (2004) The MEK-ERK signaling pathway is a negative regulator of cartilage-specific gene expression in embryonic limb mesenchyme. J. Biol. Chem. 279, 4588-4595
28. Gosset, M., Berenbaum, F., Thirion, S., and Jacques, C. (2008) Primary culture and phenotyping of murine chondrocytes. Nat. Protoc. 3, 1253-1260
29. Alvarez, J., Sohn, P., Zeng, X., Doetschman, T., Robbins, D. J., and Serra, R. (2002) TGFβ2 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression. Development 129, 1913-1924
30. Tominaga, H., Maeda, S., Hayashi, M., Takeda, S., Akira, S., Komiya, S., Nakamura, T., Akiyama, H., and Imamura, T. (2008) CCAAT/enhancer-binding protein β promotes osteoblast differentiation by enhancing Runx2 activity with ATF4. Mol. Biol. Cell 19, 5373-5386
31. Ahrens, P. B., Solursh, M., and Reiter, R. S. (1977) Stage-related capacity for limb chondrogenesis in cell culture. Dev. Biol. 60, 69-82
32. Shukunami, C., Ohta, Y., Sakuda, M., and Hiraki, Y. (1998) Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp. Cell Res. 241, 1-11
33. Korchynskyi, O., and ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891
34. Canalis, E., Economides, A. N., and Gazzerro, E. (2003) Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev. 24, 218-235
35. Miyazono, K., Maeda, S., and Imamura, T. (2005) BMP receptor signaling. Transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 16, 251-263
36. Stroschein, S. L., Wang, W., Zhou, S., Zhou, Q., and Luo, K. (1999) Negative feedback regulation of TGF-β signaling by the SnoN oncoprotein. Science 286, 771-774
37. Sun, Y., Liu, X., Ng-Eaton, E., Lodish, H. F., and Weinberg, R. A. (1999) SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor β signaling. Proc. Natl. Acad. Sci. U.S.A. 96, 12442-12447
38. Pearson-White, S., and Crittenden, R. (1997) Proto-oncogene Sno expression, alternative isoforms and immediate early serum response. Nucleic Acids Res. 25, 2930-2937
39. Shinagawa, T., Dong, H. D., Xu, M., Maekawa, T., and Ishii, S. (2000) The sno gene, which encodes a component of the histone deacetylase complex, acts as a tumor suppressor in mice. EMBO J. 19, 2280-2291
40. Jahchan, N. S., You, Y. H., Muller, W. J., and Luo, K. (2010) Transforming growth factor-β regulator SnoN modulates mammary gland branching morphogenesis, postlactational involution, and mammary tumorigenesis. Cancer Res. 70, 4204-4213
41. Krakowski, A. R., Laboureau, J., Mauviel, A., Bissell, M. J., and Luo, K. (2005) Cytoplasmic SnoN in normal tissues and nonmalignant cells antagonizes TGF-β signaling by sequestration of the Smad proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 12437-12442
42. Takeda, M., Mizuide, M., Oka, M., Watabe, T., Inoue, H., Suzuki, H., Fujita, T., Imamura, T., Miyazono, K., and Miyazawa, K. (2004) Interaction with Smad4 is indispensable for suppression of BMP signaling by c-Ski. Mol. Biol. Cell 15, 963-972
43. Wang, W., Mariani, F. V., Harland, R. M., and Luo, K. (2000) Ski represses bone morphogenic protein signaling in Xenopus and mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 97, 14394-14399
44. Dennler, S., Itoh, S., Vivien, D., ten Dijke, P., Huet, S., and Gauthier, J. M. (1998) Direct binding of Smad3 and Smad4 to critical TGF β-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17, 3091-3100
45. Mankin, H. J., Dorfman, H., Lippiello, L., and Zarins, A. (1971) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J. Bone Joint Surg. Am. 53, 523-537
46. Kuroki, H., Nakagawa, Y., Mori, K., Ohba, M., Suzuki, T., Mizuno, Y., Ando, K., Takenaka, M., Ikeuchi, K., and Nakamura, T. (2004) Acoustic stiffness and change in plug cartilage over time after autologous osteochondral grafting. Correlation between ultrasound signal intensity and histological score in a rabbit model. Arthritis Res. Ther. 6, R492-R504
47. Li, T. F., Gao, L., Sheu, T. J., Sampson, E. R., Flick, L. M., Konttinen, Y. T., Chen, D., Schwarz, E. M., Zuscik, M. J., Jonason, J. H., and O'Keefe, R. J. (2010) Aberrant hypertrophy in Smad3-deficient murine chondrocytes is rescued by restoring transforming growth factor β-activated kinase 1/activating transcription factor 2 signaling. A potential clinical implication for osteoarthritis. Arthritis Rheum. 62, 2359-2369
48. Zhu, Q., Pearson-White, S., and Luo, K. (2005) Requirement for the SnoN oncoprotein in transforming growth factor β-induced oncogenic transformation of fibroblast cells. Mol. Cell Biol. 25, 10731-10744
49. Maeda, S., Hayashi, M., Komiya, S., Imamura, T., and Miyazono, K. (2004) Endogenous TGF-β signaling suppresses maturation of osteoblastic mesenchymal cells. EMBO J. 23, 552-563
50. Valdes, A. M., Spector, T. D., Tamm, A., Kisand, K., Doherty, S. A., Dennison, E. M., Mangino, M., Tamm, A., Kerna, I., Hart, D. J., Wheeler, M., Cooper, C., Lories, R. J., Arden, N. K., and Doherty, M. (2010) Genetic variation in the SMAD3 gene is associated with hip and knee osteoarthritis. Arthritis Rheum. 62, 2347-2352
51. Kizawa, H., Kou, I., Iida, A., Sudo, A., Miyamoto, Y., Fukuda, A., Mabuchi, A., Kotani, A., Kawakami, A., Yamamoto, S., Uchida, A., Nakamura, K., Notoya, K., Nakamura, Y., and Ikegawa, S. (2005) An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat. Genet. 37, 138-144
52. Nakajima, M., Kizawa, H., Saitoh, M., Kou, I., Miyazono, K., and Ikegawa, S. (2007) Mechanisms for asporin function and regulation in articular cartilage. J. Biol. Chem. 282, 32185-32192
53. Blaney Davidson, E. N., Scharstuhl, A., Vitters, E. L., van der Kraan, P. M., and van den Berg, W. B. (2005) Reduced transforming growth factor-β signaling in cartilage of old mice. Role in impaired repair capacity. Arthritis Res. Ther. 7, R1338-R1347