Regulation of BMP-dependent chondrogenesis in early limb mesenchyme by TGFβ signals

Journal of Cell Science

Volumn 123, Issue 12, 2010, Pages 2068-2076

  Karamboulas, Konstantina ^a   Dranse, Helen J ^a   Underhill, T Michael ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Chondroblast differentiation; Chondrogenic program; GATA factors; Skeletogenesis

Indexed keywords

ACTIN; BONE MORPHOGENETIC PROTEIN; LIGAND; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL FATE; CELL MATURATION; CELL POPULATION; CHONDROGENESIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FORELIMB; GATA3 GENE; GATA5 GENE; GATA6 GENE; GENE; GENE INDUCTION; HINDLIMB; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARTILAGE; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROGENESIS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIMB BUDS; MALE; MESODERM; MICE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

ERINACEIDAE; MURINAE;

EID: 77953557018     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.062901     Document Type: Article

References (39)

1. Bandyopadhyay, A., Tsuji, K., Cox, K., Harfe, B. D., Rosen, V. and Tabin, C. J. (2006). Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2, e216.
2. Barna, M. and Niswander, L. (2007). Visualization of cartilage formation: insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev. Cell 12, 931-941.
3. Duprez, D., Bell, E. J., Richardson, M. K., Archer, C. W., Wolpert, L., Brickell, P. M. and Francis-West, P. H. (1996). Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech. Dev. 57, 145-157.
4. Feijen, A., Goumans, M. J. and van den Eijnden-van Raaij, A. J. (1994). Expression of activin subunits, activin receptors and follistatin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 120, 3621-3637.
5. 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.
6. Ganan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M. A. and Hurle, J. M. (1996). Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122, 2349-2357.
7. Hoffman, L. M., Garcha, K., Karamboulas, K., Cowan, M. F., Drysdale, L. M., Horton, W. A. and Underhill, T. M. (2006). BMP action in skeletogenesis involves attenuation of retinoid signaling. J. Cell Biol. 174, 101-113.
8. Jiang, T. X., Yi, J. R., Ying, S. Y. and Chuong, C. M. (1993). Activin enhances chondrogenesis of limb bud cells: stimulation of precartilaginous mesenchymal condensations and expression of NCAM. Dev. Biol. 155, 545-557.
9. Kulyk, W. M., Rodgers, B. J., Greer, K. and Kosher, R. A. (1989). Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-beta. Dev. Biol. 135, 424-430.
10. Laping, N. J., Grygielko, E., Mathur, A., Butter, S., Bomberger, J., Tweed, C., Martin, W., Fornwald, J., Lehr, R., Harling, J. et al. (2002). Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol. Pharmacol. 62, 58-64.
11. 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 alpha1(II) collagen gene. Mol. Cell. Biol. 17, 2336-2346.
12. Lefebvre, V., Li, P. and de Crombrugghe, B. (1998). A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J. 17, 5718-5733. (Pubitemid 28445983)
13. Leonard, C. M., Fuld, H. M., Frenz, D. A., Downie, S. A., Massague, J. and Newman, S. A. (1991). Role of transforming growth factor-beta in chondrogenic pattern formation in the embryonic limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenous TGF-beta and evidence for endogenous TGF-beta-like activity. Dev. Biol. 145, 99-109.
14. Lin, T., Ambasudhan, R., Yuan, X., Li, W., Hilcove, S., Abujarour, R., Lin, X., Hahm, H. S., Hao, E., Hayek, A. et al. (2009). A chemical platform for improved induction of human iPSCs. Nat. Methods 6, 805-808.
15. Lorda-Diez, C. I., Montero, J. A., Martinez-Cue, C., Garcia-Porrero, J. A. and Hurle, J. M. (2009). Transforming growth factors {beta} (TGF{beta}S) coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J. Biol. Chem. 284, 29988-29996
16. Maeda, S., Hayashi, M., Komiya, S., Imamura, T. and Miyazono, K. (2004). Endogenous TGF-beta signaling suppresses maturation of osteoblastic mesenchymal cells. EMBO J. 23, 552-563. (Pubitemid 38282387)
17. Massague, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
18. Merino, R., Macias, D., Ganan, Y., Rodriguez-Leon, J., Economides, A. N., Rodriguez-Esteban, C., Izpisua-Belmonte, J. C. and Hurle, J. M. (1999). Control of digit formation by activin signalling. Development 126, 2161-2170. (Pubitemid 29271701)
19. Muramatsu, S., Wakabayashi, M., Ohno, T., Amano, K., Ooishi, R., Sugahara, T., Shiojiri, S., Tashiro, K., Suzuki, Y., Nishimura, R. et al. (2007). Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J. Biol. Chem. 282, 32158-32167.
20. Murtaugh, L. C., Chyung, J. H. and Lassar, A. B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev. 13, 225-237.
21. Murtaugh, L. C., Zeng, L., Chyung, J. H. and Lassar, A. B. (2001). The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMP-dependent axial chondrogenesis. Dev. Cell 1, 411-422. (Pubitemid 33586090)
22. Nohno, T., Noji, S., Koyama, E., Myokai, F., Ohuchi, H., Nishikawa, K., Sumitomo, S., Taniguchi, S. and Saito, T. (1993). Expression patterns of the activin receptor IIA and IIB genes during chick limb development. Prog. Clin. Biol. Res. 383B, 705-714.
23. Pearse, R. V., 2nd, Scherz, P. J., Campbell, J. K. and Tabin, C. J. (2007). A cellular lineage analysis of the chick limb bud. Dev. Biol. 310, 388-400.
24. Peterkin, T., Gibson, A., Loose, M. and Patient, R. (2005). The roles of GATA-4, -5 and -6 in vertebrate heart development. Semin. Cell Dev. Biol. 16, 83-94.
25. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S. and Marshak, D. R. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147.
26. Pryce, B. A., Watson, S. S., Murchison, N. D., Staverosky, J. A., Dunker, N. and Schweitzer, R. (2009). Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development 136, 1351-1361.
27. 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.
28. Roark, E. F. and Greer, K. (1994). Transforming growth factor-beta and bone morphogenetic protein-2 act by distinct mechanisms to promote chick limb cartilage differentiation in vitro. Dev. Dyn. 200, 103-116.
29. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L. and Doetschman, T. (1997). TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124, 2659-2670. (Pubitemid 27341765)
30. Schofield, J. N. and Wolpert, L. (1990). Effect of TGF-beta 1, TGF-beta 2, and bFGF on chick cartilage and muscle cell differentiation. Exp. Cell Res. 191, 144-148.
31. Semba, I., Nonaka, K., Takahashi, I., Takahashi, K., Dashner, R., Shum, L., Nuckolls, G. H. and Slavkin, H. C. (2000). Positionally-dependent chondrogenesis induced by BMP4 is co-regulated by Sox9 and Msx2. Dev. Dyn. 217, 401-414.
32. Seo, H. S. and Serra, R. (2007). Deletion of Tgfbr2 in Prx1-cre expressing mesenchyme results in defects in development of the long bones and joints. Dev. Biol. 310, 304-316.
33. Tribioli, C. and Lufkin, T. (1999). The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126, 5699-5711. (Pubitemid 30035018)
34. Watabe, T., Nishihara, A., Mishima, K., Yamashita, J., Shimizu, K., Miyazawa, K., Nishikawa, S. and Miyazono, K. (2003). TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 163, 1303-1311. (Pubitemid 38032091)
35. Weston, A. D., Rosen, V., Chandraratna, R. A. and Underhill, T. M. (2000). Regulation of skeletal progenitor differentiation by the BMP and retinoid signaling pathways. J. Cell Biol. 148, 679-690.
36. Weston, A. D., Chandraratna, R. A., Torchia, J. and Underhill, T. M. (2002). Requirement for RAR-mediated gene repression in skeletal progenitor differentiation. J. Cell Biol. 158, 39-51.
37. Weston, A. D., Sampaio, A. V., Ridgeway, A. G. and Underhill, T. M. (2003). Inhibition of p38 MAPK signaling promotes late stages of myogenesis. J. Cell Sci. 116, 2885-2893.
38. Xu, S. C., Harris, M. A., Rubenstein, J. L., Mundy, G. R. and Harris, S. E. (2001). Bone morphogenetic protein-2 (BMP-2) signaling to the Col2alpha1 gene in chondroblasts requires the homeobox gene Dlx-2. DNA Cell Biol. 20, 359-365.
39. 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. USA 102, 5062-5067.