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Development, Vol 122, Issue 10 3035-3044, Copyright © 1996 by Company of Biologists
JOURNAL ARTICLES |
Y Chen, M Bei, I Woo, I Satokata and R Maas
Howard Hughes Medical Institute, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Members of the Msx homeobox family are thought to play important roles in inductive tissue interactions during vertebrate organogenesis, but their precise developmental function has been unclear. Mice deficient for Msx1 exhibit defects in craniofacial development and a failure of tooth morphogenesis, with an arrest in molar tooth development at the E13.5 bud stage. Because of its potential for experimental manipulation, the murine molar tooth germ provides a powerful system for studying the role of Msx genes in inductive signaling during organogenesis. To further analyze the role of Msx1 in regulating epithelial-mesenchymal interactions during tooth morphogenesis, we have examined the expression of several potential Msx1 downstream genes in Msx1 mutant tooth germs and we have performed functional experiments designed to order these genes into a pathway. Our results show that expression of Bone Morphogenetic Protein 4 (BMP4), the HMG box gene Lef1 and the heparan sulfate proteoglycan syndecan-1 is specifically reduced in Msx1 mutant dental mesenchyme, while expression of the extracellular matrix protein tenascin is unaffected. BMP4 soaked beads can induce Bmp4 and Lef1 expression in explanted wild-type dental mesenchymes, but only Lef1 expression in Msx1 mutant dental mesenchyme. We thus conclude that epithelial BMP4 induces its own expression in dental mesenchyme in a manner that requires Msx1. In turn, we show that addition of BMP4 to Msx1 deficient tooth germs bypasses the requirement for Msx1 and rescues epithelial development from the bud stage to the E14.5 cap stage. Lastly, we show that FGFs induce syndecan-1 expression in dental mesenchyme in a manner that also requires Msx-1. These results integrate Msx1 into a regulatory hierarchy in early tooth morphogenesis and demonstrate that Msx1 is not only expressed in dental mesenchyme in response to epithelial signals, but also in turn regulates the reciprocal expression of inductive signals in the mesenchyme which then act back upon the dental epithelium. We propose that Msx genes function repetitively during vertebrate organogenesis to permit inductive signaling to occur back and forth between tissue layers.
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|
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|
|
|
|
|
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|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
A. Tucker, G Yamada, M Grigoriou, V Pachnis, and P. Sharpe Fgf-8 determines rostral-caudal polarity in the first branchial arch Development, January 1, 1999; 126(1): 51 - 61. [Abstract] [PDF]
|
|
|
|
|
|
A. Tucker, A Al Khamis, C. Ferguson, I Bach, M. Rosenfeld, and P. Sharpe Conserved regulation of mesenchymal gene expression by Fgf-8 in face and limb development Development, January 1, 1999; 126(2): 221 - 228. [Abstract] [PDF]
|
|
|
|
 |
|
 G. Hu, H. Vastardis, A. J. Bendall, Z. Wang, M. Logan, H. Zhang, C. Nelson, S. Stein, N. Greenfield, C. E. Seidman, et al. Haploinsufficiency of MSX1: a Mechanism for Selective Tooth Agenesis Mol. Cell. Biol., October 1, 1998; 18(10): 6044 - 6051. [Abstract] [Full Text]
|
|
|
|
|
|
C. A. Ferguson, A. S. Tucker, L. Christensen, A. L. Lau, M. M. Matzuk, and P. T. Sharpe Activin is an essential early mesenchymal signal in tooth development that is required for patterning of the murine dentition Genes & Dev., August 15, 1998; 12(16): 2636 - 2649. [Abstract] [Full Text]
|
|
|
|
 |
|
 M. V. Dhodapkar, E. Abe, A. Theus, M. Lacy, J. K. Langford, B. Barlogie, and R. D. Sanderson Syndecan-1 Is a Multifunctional Regulator of Myeloma Pathobiology: Control of Tumor Cell Survival, Growth, and Bone Cell Differentiation Blood, April 15, 1998; 91(8): 2679 - 2688. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z Hardcastle, R Mo, C. Hui, and P. Sharpe The Shh signalling pathway in tooth development: defects in Gli2 and Gli3 mutants Development, January 8, 1998; 125(15): 2803 - 2811. [Abstract] [PDF]
|
|
|
|
|
|
H. Kim, D. Rice, P. Kettunen, and I Thesleff FGF-, BMP- and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development Development, January 4, 1998; 125(7): 1241 - 1251. [Abstract] [PDF]
|
|
|
|
|
|
K.M. Weiss, D.W. Stock, and Z. Zhao Dynamic Interactions and the Evolutionary Genetics of Dental Patterning Critical Reviews in Oral Biology & Medicine, January 1, 1998; 9(4): 369 - 398. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J Jernvall, T Aberg, P Kettunen, S Keranen, and I Thesleff The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot Development, January 1, 1998; 125(2): 161 - 169. [Abstract] [PDF]
|
|
|
|
|
|
B. Thomas, A. Tucker, M Qui, C. Ferguson, Z Hardcastle, J. Rubenstein, and P. Sharpe Role of Dlx-1 and Dlx-2 genes in patterning of the murine dentition Development, January 12, 1997; 124(23): 4811 - 4818. [Abstract] [PDF]
|
|
|
|
|
|
R Maeda, A Kobayashi, R Sekine, J. Lin, H Kung, and M Maeno Xmsx-1 modifies mesodermal tissue pattern along dorsoventral axis in Xenopus laevis embryo Development, January 7, 1997; 124(13): 2553 - 2560. [Abstract] [PDF]
|
|
|
|
|
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R. Maas and M. Bei The Genetic Control of Early Tooth Development Critical Reviews in Oral Biology & Medicine, January 1, 1997; 8(1): 4 - 39. [Abstract] [Full Text] [PDF]
|
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|
 |
|
 I. Thesleff and J. Jernvall The Enamel Knot: A Putative Signaling Center Regulating Tooth Development Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 257 - 267. [Abstract] [PDF]
|
|
|
|
 |
|
 C. Blin-Wakkach, F. Lezot, S. Ghoul-Mazgar, D. Hotton, S. Monteiro, C. Teillaud, L. Pibouin, S. Orestes-Cardoso, P. Papagerakis, M. Macdougall, et al. Endogenous Msx1 antisense transcript: In vivo and in vitro evidences, structure, and potential involvement in skeleton development in mammals PNAS, June 19, 2001; 98(13): 7336 - 7341. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Chen, Y. Zhang, T.-X. Jiang, A. J. Barlow, T. R. St. Amand, Y. Hu, S. Heaney, P. Francis-West, C.-M. Chuong, and R. Maas Conservation of early odontogenic signaling pathways in Aves PNAS, August 29, 2000; 97(18): 10044 - 10049. [Abstract] [Full Text] [PDF]
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