Co-ordination of TGF-β and FGF signaling pathways in bone organ cultures

Mechanisms of Development

Volumn 122, Issue 4, 2005, Pages 557-571

  Mukherjee, Aditi ^a,b   Dong, Sai Sai ^c   Clemens, Thomas ^a   Alvarez, Jesus ^c,d   Serra, Rosa ^c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

Author keywords

Cartilage; Endochondral bone; FGF18; FGFR3; IGF; Perichondrium

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; BONE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO; METATARSAL BONE; MOUSE; NONHUMAN; OSSIFICATION; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 15944388991     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2004.11.006     Document Type: Article

References (65)

1. J. Alvarez, J. Horton, P. Sohn, and R. Serra The perichondrium plays an important role in mediating the effects of TGF-beta1 on endochondral bone formation Dev. Dyn. 221 2001 311 321
2. J. Alvarez, P. Sohn, X. Zeng, T. Doetschman, D.J. Robbins, and R. Serra TGFbeta2 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression Development 129 2002 1913 1924
3. R.T. Ballock, A. Heydemann, L.M. Wakefield, K.C. Flanders, A.B. Roberts, and M.B. Sporn TGF-β1 prevents hypertrophy of epipheseal chondrocytes: Regulation of gene expression for cartilage matrix proteins and metalloproteases Dev. Biol. 158 1993 414 429
4. F. Beck, N.J. Samani, S. Byrne, K. Morgan, R. Gebhard, and W.J. Brammar Histochemical localization of IGF-I and IGF-II mRNA in the rat between birth and adulthood Development 104 1988 29 39
5. K. Bohme, K.H. Winterhalter, and P. Bruckner Terminal differentiation of chondrocytes in culture is a spontaneous process and is arrested by TGF-β2 and basic fibroblast growth factoe in synergy Exp. Cell Res. 216 1995 191 198
6. D. Burke, D. Wilkes, T.L. Blundell, and S. Malcolm Fibroblast growth factor receptors: lessons from the genes Trends Biochem. Sci. 23 1998 59 62
7. R. Cancedda, F.D. Cancedda, and P. Castagnola Chondrocyte differentiation Int. Rev. Cytol. 159 1995 265 358
8. A. Cerra, K.J. Mansfield, and C.G. Chamberlain Exacerbation of TGF-beta-induced cataract by FGF-2 in cultured rat lenses Mol. Vis. 9 2003 689 700
9. L. Chen, R. Adar, X. Yang, E.O. Monsonego, C. Li, and P.V. Hauschka Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis J. Clin. Invest. 104 1999 1517 1525
10. L. Chen, C. Li, W. Qiao, X. Xu, and C. Deng A Ser(365)→Cys mutation of fibroblast growth factor receptor 3 in mouse downregulates Ihh/PTHrP signals and causes severe achondroplasia Hum. Mol. Genet. 10 2001 457 465
11. J.D. Coffin, R.Z. Florkiewicz, J. Neumann, T. Mort-Hopkins, G.W. Dorn 2nd, and P. Lightfoot Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice Mol. Biol. Cell 6 1995 1861 1873
12. J.S. Colvin, B.A. Bohne, G.W. Harding, D.G. McEwen, and D.M. Ornitz Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3 Nat. Genet. 12 1996 390 397
13. I. Cosic, A.E. Drummond, J.R. Underwood, and M.T. Hearn In vitro inhibition of the actions of basic FGF by a novel 16 amino acid peptide Mol. Cell Biochem. 130 1994 1 9
14. X. Coumoul, and C. Deng Roles of FGFRs in mammalian development and congenital disease Birth Defects Res. (Part C) 69 2003 286 304
15. V. Coxam, M.A. Miller, B.M. Bowman, D. Qi, and S.C. Miller Insulin-like growth factor 1 and parathyroid hormone effects on the growth of fetal rat metatarsal bones cultured in serum-free medium Biol. Neonate 68 1995 368 376
16. V. Coxam, M.A. Miller, M.B. Bowman, and S.C. Miller Ontogenesis of IGF regulation of longitudinal bone growth in rat metatarsal rudiments cultured in serum-free medium Arch. Physiol. Biochem. 104 1996 173 179
17. P. de Los Rios, and D.J. Hill Expression and release of insulin-like growth factor binding proteins in isolated epiphyseal growth plate chondrocytes from the ovine fetus J. Cell Physiol. 183 2000 172 181
18. A.L. Delezoide, C. Benoist-Lasselin, L. Legeai-Mallet, M. le Merrer, A. Munnich, M. Vekemans, and J. Bonaventure Spatio-temporal expression of FGFR 1, 2 and 3 genes during human embryo-fetal ossification Mech. Dev. 77 1998 19 30
19. C. Deng, A. Wynshaw-Boris, F. Zhou, A. Kuo, and P. Leder Fibroblast growth factor receptor 3 is a negative regulator of bone growth Cell 84 1996 911 921
20. A.E. Denker, S.B. Nicoll, and R.S. Tuan Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with TGF-β1 Differentiation 59 1994 25 34
21. D.L. Di Nino, F. Long, and T.F. Linsenmayer Regulation of endochondral cartilage growth in the developing avian limb: cooperative involvement of perichondrium and periosteum Dev. Biol. 240 2001 433 442
22. S.C. Dieudonne, C.M. Semeins, S.W. Goei, S. Vukicevic, J.K. Nulend, and T.K. Sampath Opposite effects of osteogenic protein and TGF-β on chondrogenesis in cultured long bone rudiments J. Bone Miner. Res. 9 1994 771 780
23. J. Dupont, and M. Holzenberger Biology of insulin-like growth factors in development Birth Defects Res. (Part C) 69 2003 257 271
24. S. Garofalo, M. Kliger-Spatz, J.L. Cooke, O. Wolstin, G.P. Lunstrum, and S.M. Moshkovitz Skeletal dysplasia and defective chondrocyte differentiation by targeted overexpression of fibroblast growth factor 9 in transgenic mice J. Bone Miner. Res. 14 1999 1909 1915
25. D. Gatherer, P. ten Dijke, D.T. Baird, and R.J. Akhurst Expression of TGF-β isoforms during first trimester human embryogenesis Development 110 1990 445 460
26. A. Haaijman, M. Karperien, B. Lanske, J. Hendriks, C. Lowik, A. Bronckers, and E. Burger Inhibition of terminal chondrocyte differentiation by bone morphogenetic protein 7 (OP-1) in vitro depends on the periarticular region but is independent of parathyroid hormone-related peptide Bone 25 1999 397 404
27. V.K.M. Han, A.J. D'Ercole, and P.K. Lund Cellular localization of somatomedin (insulin-like growth factor) messenger RNA in the human fetus Science 236 1987 193 197
28. U.I. Heine, E.F. Munoz, K.C. Flanders, L.R. Ellingsworth, H.-Y.P. Lam, and N.L. Thompson Role of transforming growth factor-beta in the development of the mouse embryo J. Cell Biol. 105 1987 2861 2876
29. T. Iwata, L. Chen, C. Li, D.A. Ovchinnikov, R.R. Behringer, C.A. Francomano, and C.X. Deng A neonatal lethal mutation in FGFR3 uncouples proliferation and differentiation of growth plate chondrocytes in embryos Hum. Mol. Genet. 9 2000 1603 1613
30. T. Iwata, C.L. Li, C.X. Deng, and C.A. Francomano Highly activated Fgfr3 with the K644M mutation causes prolonged survival in severe dwarf mice Hum. Mol. Genet. 10 2001 1255 1264
31. Y. Kato, M. Iwamoto, T. Koike, F. Suzuki, and Y. Takano Terminal differentiation and calcification in rabbit chondrocyte cultures grown in centrifuge tubes: regulation by transforming growth factor beta and serum factors Proc. Natl Acad. Sci. USA 85 1988 9552 9556
32. K. Kono, T. Ueba, J.A. Takahashi, N. Murai, N. Hashimoto, A. Myoumoto, N. Itoh, and M. Fukumoto In vitro growth suppression of human glioma cells by a 16-mer oligopeptide: a potential new treatment modality for malignant glioma J. Neurooncol. 63 2003 163 171
33. M. Kveiborg, A. Flyvbjerg, E.F. Eriksen, and M. Kassem Transforming growth factor-beta1 stimulates the production of insulin-like growth factor-I and insulin-like growth factor-binding protein-3 in human bone marrow stromal osteoblast progenitors J. Endocrinol. 169 2001 549 561
34. C.M. Leonard, H.M. Fuld, D.A. Frenz, S.A. Downie, J. Massague, and S.A. Newman Role of transforming growth factorβ in chondrogenic pattern formation in the embryonic limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenenous TGF-β and evidence for endogenous TGF-β-like activity Dev. Biol. 145 1991 99 109
35. C. Li, L. Chen, T. Iwata, M. Kitagawa, X.Y. Fu, and C.X. Deng A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and ink4 cell cycle inhibitors Hum. Mol. Genet. 8 1999 35 44
36. S. Liekens, D. Leali, J. Neyts, R. Esnouf, M. Rusnati, and P. Dell'Era Modulation of fibroblast growth factor-2 receptor binding, signaling, and mitogenic activity by heparin-mimicking polysulfonated compounds Mol. Pharmacol. 56 1999 204 213
37. J.P. Liu, J. Baker, A.S. Perkins, E.J. Robertson, and A. Efstratiadis Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r) Cell 75 1993 59 72
38. Z. Liu, J. Xu, J.S. Colvin, and D.M. Ornitz Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18 Genes Dev. 16 2002 859 869
39. F. Long, and T.F. Linsenmayer Regulation of growth region cartilage proliferation and differentiation by perichondrium Development 125 1998 1067 1073
40. F. Long, X.M. Zhang, S. Karp, Y. Yang, and A.P. McMahon Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation Development 128 2001 5099 5108
41. E.E. Mancilla, F. de Luca, J.A. Uyeda, F.S. Czerwiec, and J. Baron Effects of fibroblast growth factor-2 on longitudinal bone growth Endocrinology 139 1998 2900 2904
42. J. Massague TGF-β signal transduction Annu. Rev. Biochem. 67 1998 753 791
43. F.A. Millan, F. Denhez, P. Kondaiah, and R. Akhurst Embryonic gene expression patterns of TGF beta 1, beta 2, and beta 3 suggest different developmental functions in vivo Development 111 1991 131 143
44. H.L. Moses, and R. Serra Regulation of Differentiation by TGF-β Curr. Opin. Genet. Dev. 6 1996 581 586
45. S. Murakami, G. Balmes, S. McKinney, Z. Zhang, D. Givol, and B. de Crombrugghe Constitutive activation of MEK1 in chondrocytes causes Stat1-independent achondroplasia-like dwarfism and rescues the Fgfr3-deficient mouse phenotype Genes Dev. 18 2004 290 305
46. M.C. Naski, and D.M. Ornitz FGF signaling in skeletal development Front Biosci. 3 1998 D781 D794
47. M. Naski, J. Colvin, J. Coffin, and D. Ornitz Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3 Development 125 1998 4977 4988
48. N. Ohbayashi, M. Shibayama, Y. Kurotaki, M. Imanishi, T. Fujimori, N. Itoh, and S. Takada FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis Genes Dev. 16 2002 870 879
49. A. Orr-Urtreger, D. Givol, A. Yayon, Y. Yarden, and P. Lonai Developmental expression of two murine fibroblast growth factor receptors, flg and bek Development 113 1991 1419 1434
50. R.W. Pelton, M.E. Dickinson, H.L. Moses, and B.L.M. Hogan In situ hybridization analysis of TGF-β3 RNA expression during mouse development: comparative studies with TGF-β1 and β2 Development 110 1990 600 620
51. R.W. Pelton, B. Saxena, M. Jones, H.L. Moses, and L.I. Gold Immunohistochemical localization of TGF-β1, TGF-β2, and TGF-β3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development J. Cell Biol. 115 1991 1091 1105
52. K.G. Peters, S. Werner, G. Chen, and L.T. Williams FGF Two receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse Development 114 1992 233 243
53. K. Peters, D. Ornitz, S. Werner, and L. Williams Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis Dev. Biol. 155 1993 423 430
54. A.B. Roberts, and M.B. Sporn The transforming growth factor-βs M.B. Sporn A.B. Roberts Peptide Growth Factors and their Receptors 1990 Springer Heidelberg 419 472
55. M. Sandberg, T. Vurio, H. Hirrovan, K. Alitalo, and E. Vuorio Enhanced expression of TGF-beta and c-fos mRNAs in the growth plates of developing human long bones Development 102 1988 461 470
56. C. Schmid Insulin-like growth factors Cell Biol. Int. 19 1995 445 457
57. R. Serra, and C. Chang TGF-beta signaling in human skeletal and patterning disorders Birth Defects Res. (Part C) 69 2003 333 351
58. R. Serra, A. Karapalis, and P. Sohn PTHrP-dependent and -independent effects of TGF-β on endochondral bone formation J. Cell Biol. 145 1999 783 794
59. C. Thesingh, and E. Burger The role of mesenchyme in embryonic long bones as early deposition site for osteoclast progenitor cells Dev. Biol. 95 2 1983 429 438
60. T. Tschan, K. Bohme, E.M. Conscience, G. Zenke, K.H. Winterhalter, and P. Bruckner Autocrine or paracrine TGF-β modulates the phenotype of chick embryo sternal chondrocytes in serum-free agarose culture J. Biol. Chem. 5 1993 5156 5161
61. T. Tsukazaki, T. Usa, T. Matsumoto, H. Enomoto, A. Ohtsuru, and H. Namba Effect of transforming growth factor-beta on the insulin-like growth factor-I autocrine/paracrine axis in cultured rat articular chondrocytes Exp. Cell Res. 215 1994 9 16
62. M. Van Kleffens, C. Groffen, R.R. Rosato, S.M. Van den Eijnde, J.W. Van Neck, and D.J. Lindenbergh-Kortleve mRNA expression patterns of the IGF system during mouse limb bud development, determined by whole mount in situ hybridization Mol. Cell Endocrinol. 138 1998 151 161
63. E. Wang, J. Wang, E. Chin, J. Zhou, and C.A. Bondy Cellular patterns of insulin-like growth factor system gene expression in murine chondrogenesis and osteogenesis Endocrinology 136 1995 2741 2751
64. T.A. Wilke, S. Gubbels, J. Schwartz, and J.M. Richman Expression of fibroblast growth factor receptors (FGFR1, FGFR2, FGFR3) in the developing head and face Dev. Dyn. 210 1997 41 52
65. J. Xu, Z. Liu, and D.M. Ornitz Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures Development 127 2000 1833 1843