|
|
|
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 125, Issue 7 1241-1251, Copyright © 1998 by Company of Biologists
JOURNAL ARTICLES |
HJ Kim, DP Rice, PJ Kettunen and I Thesleff
Institute of Biotechnology, University of Helsinki, Finland.
The development of calvarial bones is tightly co-ordinated with the growth of the brain and needs harmonious interactions between different tissues within the calvarial sutures. Premature fusion of cranial sutures, known as craniosynostosis, presumably involves disturbance of these interactions. Mutations in the homeobox gene Msx2 as well as the FGF receptors cause human craniosynostosis syndromes. Our histological analysis of mouse calvarial development demonstrated morphological differences in the sagittal suture between embryonic and postnatal stages. In vitro culture of mouse calvaria showed that embryonic, but not postnatal, dura mater regulated suture patency. We next analysed by in situ hybridisation the expression of several genes, which are known to act in conserved signalling pathways, in the sagittal suture during embryonic (E15-E18) and postnatal stages (P1-P6). Msx1 and Msx2 were expressed in the sutural mesenchyme and the dura mater. FGFR2(BEK), as well as Bmp2 and Bmp4, were intensely expressed in the osteogenic fronts and Bmp4 also in the mesenchyme of the sagittal suture and in the dura mater. Fgf9 was expressed throughout the calvarial mesenchyme, the dura mater, the developing bones and the overlying skin, but Fgf4 was not detected in these tissues. Interestingly, Shh and Ptc started to be expressed in patched pattern along the osteogenic fronts at the end of embryonic development and, at this time, the expression of Bmp4 and sequentially those of Msx2 and Bmp2 were reduced, and they also acquired patched expression patterns. The expression of Msx2 in the dura mater disappeared after birth. <P> FGF and BMP signalling pathways were further examined in vitro, in E15 mouse calvarial explants. Interestingly, beads soaked in FGF4 accelerated sutural closure when placed on the osteogenic fronts, but had no such effect when placed on the mid-sutural mesenchyme. BMP4 beads caused an increase in tissue volume both when placed on the osteogenic fronts and on the mid-sutural area, but did not effect suture closure. BMP4 induced the expression of both Msx1 and Msx2 genes in sutural tissue, while FGF4 induced only Msx1. We suggest that the local application of FGF on the osteogenic fronts accelerating suture closure in vitro, mimics the pathogenesis of human craniosynostosis syndromes in which mutations in the FGF receptor genes apparently cause constitutive activation of the receptors. Taken together, our data suggest that conserved signalling pathways regulate tissue interactions during suture morphogenesis and intramembranous bone formation of the calvaria and that morphogenesis of mouse sagittal suture is controlled by different molecular mechanisms during the embryonic and postnatal stages. Signals from the dura mater may regulate the maintenance of sutural patency prenatally, whereas signals in the osteogenic fronts dominate after birth.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  M.-C. Ting, N. L. Wu, P. G. Roybal, J. Sun, L. Liu, Y. Yen, and R. E. Maxson Jr EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis Development, March 1, 2009; 136(5): 855 - 864. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. T. Rawlins, C. R. Fernandez, M. E. Cozby, and L. A. Opperman Timing of Egf Treatment Differentially Affects Tgf-{beta}2 Induced Cranial Suture Closure Experimental Biology and Medicine, December 1, 2008; 233(12): 1518 - 1526. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W.-J. Yoon, Y.-D. Cho, K.-H. Cho, K.-M. Woo, J.-H. Baek, J.-Y. Cho, G.-S. Kim, and H.-M. Ryoo The Boston-type Craniosynostosis Mutation MSX2 (P148H) Results in Enhanced Susceptibility of MSX2 to Ubiquitin-dependent Degradation J. Biol. Chem., November 21, 2008; 283(47): 32751 - 32761. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. E. Merrill, B. F. Eames, S. J. Weston, T. Heath, and R. A. Schneider Mesenchyme-dependent BMP signaling directs the timing of mandibular osteogenesis Development, April 1, 2008; 135(7): 1223 - 1234. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D.C. Wescott, M.N. Pinkerton, B.J. Gaffey, K.T. Beggs, T.J. Milne, and M.C. Meikle Osteogenic Gene Expression by Human Periodontal Ligament Cells under Cyclic Tension Journal of Dental Research, December 1, 2007; 86(12): 1212 - 1216. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. P. Eswarakumar, F. Ozcan, E. D. Lew, J. H. Bae, F. Tome, C. J. Booth, D. J. Adams, I. Lax, and J. Schlessinger Attenuation of signaling pathways stimulated by pathologically activated FGF-receptor 2 mutants prevents craniosynostosis PNAS, December 5, 2006; 103(49): 18603 - 18608. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Deckelbaum, A. Majithia, T. Booker, J. E. Henderson, and C. A. Loomis The homeoprotein engrailed 1 has pleiotropic functions in calvarial intramembranous bone formation and remodeling Development, January 1, 2006; 133(1): 63 - 74. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.-H. Lee, Y.-J. Kim, W.-J. Yoon, J.-I. Kim, B.-G. Kim, Y.-S. Hwang, J. M. Wozney, X.-Z. Chi, S.-C. Bae, K.-Y. Choi, et al. Dlx5 Specifically Regulates Runx2 Type II Expression by Binding to Homeodomain-response Elements in the Runx2 Distal Promoter J. Biol. Chem., October 21, 2005; 280(42): 35579 - 35587. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Aberg, R. Rice, D. Rice, I. Thesleff, and J. Waltimo-Siren Chondrogenic Potential of Mouse Calvarial Mesenchyme J. Histochem. Cytochem., May 1, 2005; 53(5): 653 - 663. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Tanimoto, M. Yokozeki, K. Hiura, K. Matsumoto, H. Nakanishi, T. Matsumoto, P. J. Marie, and K. Moriyama A Soluble Form of Fibroblast Growth Factor Receptor 2 (FGFR2) with S252W Mutation Acts as an Efficient Inhibitor for the Enhanced Osteoblastic Differentiation Caused by FGFR2 Activation in Apert Syndrome J. Biol. Chem., October 29, 2004; 279(44): 45926 - 45934. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Mustonen, M. Ilmonen, M. Pummila, A. T. Kangas, J. Laurikkala, R. Jaatinen, J. Pispa, O. Gaide, P. Schneider, I. Thesleff, et al. Ectodysplasin A1 promotes placodal cell fate during early morphogenesis of ectodermal appendages Development, October 15, 2004; 131(20): 4907 - 4919. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Vattikuti and D. A. Towler Osteogenic regulation of vascular calcification: an early perspective Am J Physiol Endocrinol Metab, May 1, 2004; 286(5): E686 - E696. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. K. Hajihosseini, M. D. Lalioti, S. Arthaud, H. R. Burgar, J. M. Brown, S. R. F. Twigg, A. O. M. Wilkie, and J. K. Heath Skeletal development is regulated by fibroblast growth factor receptor 1 signalling dynamics Development, January 15, 2004; 131(2): 325 - 335. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. A. Ibrahimi, F. Zhang, A. V. Eliseenkova, R. J. Linhardt, and M. Mohammadi Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity Hum. Mol. Genet., January 1, 2004; 13(1): 69 - 78. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ishii, A. E. Merrill, Y.-S. Chan, I. Gitelman, D. P. C. Rice, H. M. Sucov, and R. E. Maxson Jr Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault Development, December 15, 2003; 130(24): 6131 - 6142. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Laurikkala, J. Pispa, H.-S. Jung, P. Nieminen, M. Mikkola, X. Wang, U. Saarialho-Kere, J. Galceran, R. Grosschedl, and I. Thesleff Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar Development, March 7, 2003; 129(10): 2541 - 2553. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Yamashiro, M. Tummers, and I. Thesleff Expression of Bone Morphogenetic Proteins and Msx Genes during Root Formation Journal of Dental Research, March 1, 2003; 82(3): 172 - 176. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. K. Yeh, A. V. Eliseenkova, A. N. Plotnikov, D. Green, J. Pinnell, T. Polat, A. Gritli-Linde, R. J. Linhardt, and M. Mohammadi Structural Basis for Activation of Fibroblast Growth Factor Signaling by Sucrose Octasulfate Mol. Cell. Biol., October 15, 2002; 22(20): 7184 - 7192. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. M. Ornitz and P. J. Marie FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease Genes & Dev., June 15, 2002; 16(12): 1446 - 1465. [Full Text] [PDF]
|
|
|
|
|
|
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., April 1, 2002; 16(7): 870 - 879. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. P. Tan, K. Nonaka, G. H. Nuckolls, Y. H. Liu, R. E. Maxson, H. C. Slavkin, and L. Shum YY1 activates Msx2 gene independent of bone morphogenetic protein signaling Nucleic Acids Res., March 1, 2002; 30(5): 1213 - 1223. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Zhao, Q. Chen, F.-C. Hung, and P. A. Overbeek BMP signaling is required for development of the ciliary body Development, January 10, 2002; 129(19): 4435 - 4442. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. K. Hajihosseini, S. Wilson, L. De Moerlooze, and C. Dickson A splicing switch and gain-of-function mutation in FgfR2-IIIc hemizygotes causes Apert/Pfeiffer-syndrome-like phenotypes PNAS, March 27, 2001; 98(7): 3855 - 3860. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. A. Greenwald, B. J. Mehrara, J. A. Spector, S. M. Warren, P. J. Fagenholz, L. P. Smith, P. J. Bouletreau, F. E. Crisera, H. Ueno, and M. T. Longaker In Vivo Modulation of FGF Biological Activity Alters Cranial Suture Fate Am. J. Pathol., February 1, 2001; 158(2): 441 - 452. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y.-X. Zhou, X. Xu, L. Chen, C. Li, S. G. Brodie, and C.-X. Deng A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures Hum. Mol. Genet., August 12, 2000; 9(13): 2001 - 2008. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Mansukhani, P. Bellosta, M. Sahni, and C. Basilico Signaling by Fibroblast Growth Factors (Fgf) and Fibroblast Growth Factor Receptor 2 (Fgfr2)-Activating Mutations Blocks Mineralization and Induces Apoptosis in Osteoblasts J. Cell Biol., June 12, 2000; 149(6): 1297 - 1308. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Rice, T Aberg, Y Chan, Z Tang, P. Kettunen, L Pakarinen, R. Maxson, and I Thesleff Integration of FGF and TWIST in calvarial bone and suture development Development, January 5, 2000; 127(9): 1845 - 1855. [Abstract] [PDF]
|
|
|
|
|
|
A Sukegawa, T Narita, T Kameda, K Saitoh, T Nohno, H Iba, S Yasugi, and K Fukuda The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium Development, January 5, 2000; 127(9): 1971 - 1980. [Abstract] [PDF]
|
|
|
|
|
|
A. Hollnagel, V. Oehlmann, J. Heymer, U. Ruther, and A. Nordheim Id Genes Are Direct Targets of Bone Morphogenetic Protein Induction in Embryonic Stem Cells J. Biol. Chem., July 9, 1999; 274(28): 19838 - 19845. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S Iseki, A. Wilkie, and G. Morriss-Kay Fgfr1 and Fgfr2 have distinct differentiation- and proliferation-related roles in the developing mouse skull vault Development, January 12, 1999; 126(24): 5611 - 5620. [Abstract] [PDF]
|
|
|
|
|
|
E. Hay, J. Lemonnier, O. Fromigue, and P. J. Marie Bone Morphogenetic Protein-2 Promotes Osteoblast Apoptosis through a Smad-independent, Protein Kinase C-dependent Signaling Pathway J. Biol. Chem., July 27, 2001; 276(31): 29028 - 29036. [Abstract] [Full Text] [PDF]
|
|
