A new function of BMP4: Dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ

Development

Volumn 127, Issue 7, 2000, Pages 1431-1443

  Zhang, Yanding ^a   Zhang, Zunyi ^a,c   Zhao, Xiang ^a   Yu, Xueyan ^a,b   Hu, Yueping ^a   Geronimo, Benedicto ^c   Fromm, Sigurd H ^c   Chen, YiPing ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Bmp; Limb; Mouse; Msx1 mutant; Shh; Tooth development

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; SONIC HEDGEHOG PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EPITHELIUM; LIMB BUD; MESENCHYME; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; TOOTH DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; DNA PRIMERS; EPITHELIUM; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; IN SITU HYBRIDIZATION; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MSX1 TRANSCRIPTION FACTOR; ORGAN CULTURE TECHNIQUES; PROTEINS; SIGNAL TRANSDUCTION; TOOTH GERM; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; ERINACEIDAE; MURINAE; MUS MUSCULUS; VERTEBRATA;

EID: 0034010334     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (82)

1. Arkell R. and Beddington, R. S. P. (1997). BMP-7 influences pattern and growth of the developing hindbrain of mouse embryo. Development 124, 1-12.
2. Barlow, A. J. and Francis-West, P. H. (1997). Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia. Development 124, 391-398.
3. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
4. Bei, M. and Maas, R. (1998). FGFs and BMP4 induce both Msxl-independent and Msxl-dependent signaling pathways in early tooth development. Development 125, 4325-4333.
5. Bellusci, S., Furuta, Y., Rush, M. G., Henderson, R., Winnier, G. and Hogan, B. L. M. (1997). Involvement of sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124, 53-63.
6. Bitgood, M. J. and McMahon, A. P. (1995). Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138.
7. Capdevila, J. and Guerrero, I. (1994). Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alternations in Drosophila wings. EMBO J. 13, 4459-4468.
8. Chen, Y. P. and Maas, R. (1998). Signaling loops in the reciprocal epithelial-mesenchymal interactions of mammalian tooth development. In Molecular Basic of Ephithelial Appendage Morphogenesis (ed. C.-M. Chuong), pp. 265-282. R.G. Landes, Austin, TX.
9. Chen, Y. P and Zhao, X. (1998). Shaping limbs by apoptosis. J. Exp. Zool. 282, 691-702.
10. Chen, Y. P., Bei, M., Woo, I., Satokata, I. and Maas, R. (1996). Msxl controls reciprocal inductive signaling in mammalian tooth morphogenesis. Development 122, 3035-3044.
11. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
12. Dassule, H. R. and McMahon, A. P. (1998). Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev. Biol. 202, 215-227.
13. Dewulf, N., Verschueren, K., Lonnoy, O., Morén, A., Grimsby, S., Spiegle, K. V., Miyazono, K., Huylebroeck, D. and ten Dijik, P. (1995). Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136, 2652-2663.
14. Dunn, N. R., Winner, G. K., Hargett, L. K., Schrick, J. J., Fogo, A. B. and Hogan, B. L. M. (1997). Haploinsufficient pgenotypes in Bmp4 heterozygous null mice and modification by mutations in Gli3 and Alex4. Dev. Biol. 188, 235-247.
15. Duprez, D. M., Kostakopoulou, K., Francis-West, P. H. and Tickle, C. (1996). Activation of Fgf-4 and HoxD gene expression by Bmp-2 expressing cells in the developing limb. Development 122, 1821-1828.
16. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog a member of a family putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
17. Ericson, J., Morton, S., Kawakami, A., Roelink, H. and Jessell, T. M. (1996). Two critical periods of sonic hedgehog signaling required for specification of motor neuron identity. Cell 87, 661-673.
18. Ferguson, C. A., Tucker, A. S., Christensen, L., Lau, A. L., Matzuk, M. M. and Sharpe, P. T. (1998). Activin is an essential early mesenchymal signal in tooth development that is required for patterning of the murine dentition. Genes Dev. 12, 2636-2649.
19. Francis, P. H., Richardson, M. K., Brickell, P. M., and Tickle, C. (1994). Bone morphogenetic proteins and a signaling pathway that controls patterning in the developing chick limb. Development 120, 209-218.
20. Gañan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M. A. and Hurle, J. M. (1996). Role of TGFβs 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.
21. Graham, A., Francis-West, P. H., Brickell, P. and Lumsden, A. (1994). The signaling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684-686.
22. Hammerschmidt, M., Brook, A. and McMahon, A. P (1997). The world according to hedgehog. Trends Genet. 13, 14-21.
23. Hardcastle, Z., Mo, R., Hui, C.-C. and Sharpe, P. T. (1998). The Shh signaling pathway in tooth development: defects in Gli2 and Gli3 mutants. Development 125, 2803-2811.
24. Heikinheimo, M., Lawshe, A., Shackleford, G. M., Wilson, D. B. and Mac-Arthur, C. A. (1994). Fgf-8 expression in the post-gastrulation mouse suggests roles in the development of the face, limbs and central nervous system. Mech. Dev. 48, 129-138.
25. Hogan, B. L. M., Beddington, R., Constantini, F. and Lacy, E. (1994). Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor. New York: Cold Spring Harbor Publications.
26. Hoodless, P. A., Haerry, T., Abodollah, S., Stapleton, M., O'Connor, M. B., Attisano, L. and Wrana, J. L. (1996). MADRl, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
27. Ingham, P. W. and Fietz, M. J. (1995). Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing. Curr. Biol. 5, 432-440.
28. Iseki, S., Araga, A., Ohuchi, H., Nohon, T., Yoshipka, H., Hayashi, F. and Noji, S. (1996). Sonic hedgehog is expressed in epithelial cells during development of whisker, hair and tooth. Biochem. Biophys. Res. Commun. 218, 688-693.
29. Jernvall, J., Åbert, T., Kettunen, P., Keränen, S. and Thesleff, I. (1998). The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development 125, 161-169.
30. Johnson, R. L. and Tabin, C. J. (1997). Molecular models for vertebrate limb development. Cell 90, 979-990.
31. Kawakami, Y., Ishikawa, T., Shimabara, M., Tanda, N., Enomoto-Iwamoto, M., Iwamoto, M., Kuwana, T., Ueki, A., Noji, S. and Nohno, T. (1996). BMP signaling during bone pattern determination in the developing limb. Development 122, 3557-3566.
32. Kettunen, P. and Thesleff, I. (1998). Expression and function of FGFs-4, -8 and -9 suggest redundancy and repetitive use as epithelial signals during tooth morphogenesis. Dev. Dyn. 211, 256-268.
33. Koenig, B. B., Cook, J. S., Wolsing, D. H., Ting, J., Tiesman, J. P., Correa, P. E., Olson, C. A., Pecquet, A.,L., Ventura, F., Grant, R. A., Chen, G. X., Wrana, J. L., Massagué, J. and Rosenbaum, J. S. (1994). Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell Biol. 14, 5961-5974.
34. Koyama, E., Yamaai, T., Iseki, S., Ohuchi, H., Nohno, T., Yoshioka, H., Hayashi, Y., Leatherman, J. L., Golden, E. B., Noji, S. and Pacific, M. (1996). Polarizing activity. Sonic hedgehog, and tooth development in embryonic and postnatal mouse. Dev. Dyn. 206, 59-72.
35. Kratochwil, K., Dull, M., Farinas, I., Galceran, J. and Grosschedl, R. (1996). Lefl expression is activated by BMP-4 and regulates inductive sittue interactions in tooth and hair development. Genes Dev. 10, 1382-1394.
36. Kretzschmar, M., Liu, F., Hata, A., Doody, J. and Massagué, J. (1997). The TGFβ family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995.
37. Kuzuoka, M., Takahashi, T., Guron, C. and Raghow, R. (1994). Murine homeobox-containing gene, Msx-1: Analysis of genomic organisation, promoter structure, and potential autoregulatory cis-acting elements. Genomics 21, 85-91.
38. Lamb T. M., Knecht, A. K., Smith, W. C., Stachel, S. E., Economides, A. N., Stahl, N., Yancopolous, G. D. and Harland, R. M. (1993). Neural induction by the secreted polypeptide noggin. Science 262, 713-718.
39. Laufer, E., Nelson, C. E., Johnson, R. L., Morgan, B. A. and Tabin, C. (1994). Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
40. Levin, M., Johnson, R. L., Stern, C. D., Kuehn, M. and Tabin, C. (1995). A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82, 803-814.
41. Liem, K. F., Tremml, G., Roelink, H. and Jessell, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979.
42. Liu, F., Ventura, F., Doody, J. and Massagué, J. (1995). Human type II receptor for bone morphogenetic proteins (BMPs): extension of the two-kinase receptor model for the BMPs. Mol. Cell Biol. 15, 3479-3486.
43. Lumsden, A. G. (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103 (Suppl.), 155-169.
44. Mackenzie, A., Leeming, G. L., Jowett, A. K., Ferguson, M. W. J. and Sharpe, P. T. (1991a). The homeobox gene Hox7.1 has specific regional and temporal expression patterns during early murine craniofacial embryogenesis, especially tooth development in vivo and in vitro. Development 111, 269-285.
45. Mackenzie, A., Ferguson, M. W. J. and Sharpe, P. T. (1991b) Hox-7 expression during murine craniofacial development. Development 113, 601-611.
46. Mansour, S. L., Goddard, J. M. and Capecchi, M. R. (1993). Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in tail and inner ear. Development 117, 13-29.
47. Massagué, J. (1996). TGFβ signaling: Receptors, transducers, and Mad protein. Cell 85, 947-950.
48. Mina, M. and Kollar, E. J. (1987). The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Archs. oral Biol. 32, 123-127.
49. Mucchielli, M.-L., Mitsiadis, T. A., Raffo, S., Brunet, J.-F., Proust, J.-P., and Goridis, C. (1997). Mouse Otlx2/RIEG expression in the odontogenic epithelium precedes tooth initiation and requires mesenchyme-derived signals for its maintenance. Dev. Biol. 189, 275-284.
50. Neubüser, A., Peters, H., Balling, R. and Martin, G. R. (1997). Antagonistic interactions between FGF and BMP signaling pathways: A mechanism for positioning the sites of tooth formation. Cell 90, 247-255.
51. Niswander, L. and Martin, G. R. (1993). FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361, 68-71.
52. Niswander, L., Jeffrey, S., Martin, G. R. and Tickle, C. (1994). A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609-612.
53. Nohno, T., Ishikawa, T., Saito, T., Hosokawa, K., Noji, S., Wolsing, D. H. and Rosenbaum, J. S. (1995). Identification of a human type 11 receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogentic protein type I receptors. J. Biol. Chem. 270, 22522-22526.
54. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
55. Pizette, S. and Niswander, L. (1999). BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126, 883-894.
56. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
57. Roberts, D. J., Johnson, R. L., Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalisation of the chick hindgut. Development 121, 3163-3174.
58. Roelink, H., Augsburger, A, Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. and Dodd, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
59. Rosenzweig, B. L., Imamura, T., Okadome, T., Cox, G. N., Yamashita, H., ten Dijke, P., Heldin, C. H. and Miyazono, K. (1995). Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 92, 7632-7636.
60. Satokata, I. and Maas, R. (1994). Msx-1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nature Genet. 6, 348-356.
61. Schughart, K., Bieberich, C. J., Eid, R. and Ruddle, F. H. (1991). A regulatory region from the mouse Hox-2.2 promoter directs gene expression into developing limbs. Development 112, 807-811.
62. Smith, W. C. and Harland, R. M. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
63. St Amand, T. R., Zhang, Y., Semina, E. V., Zhao, X., Hu, Y., Nguyen, L., Murray, J. C. and Chen, Y. P. (2000). Antagonistic signals between BMP4 and FGF8 define the expression of Pitx1 and Pitx2 in mouse tooth forming anlage. Dev. Biol., in press.
64. Takahashi, T., Guron, C., Shetty, S., Matsui, H. and Raghow, R. (1997). A minimal murine Msx-1 gene promoter: organization of its as-regulatory motifs and their role in transcriptional activation in cells in culture and in transgenic mice. J. Biol. Chem. 272, 22667-22678.
65. ten Dijke, P., Yamashita, H., Sampath, T. K., Reddi, A. H., Estevez, M., Riddle, D. L., Ichijo, H., Heldin, C. H. and Miyazono, K. (1994). Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 269, 16985-16988.
66. Thesleff, I., Vaahtokari, I., and Partanen, A.-M. (1995). Regulation of organogenesis: Common molecular mechanisms regulating the development of teeth and other organs. Int. J. Dev. Biol. 39, 35-50.
67. Thesleff, I. and Sahlberg, C. (1996). Growth factors as inductive signals regulating tooth morphogenesis. Sem. Cell Dev. Biol. 7, 185-193.
68. Thesleff, I. and Sharpe, P. T. (1997). Signaling networks regulating dental development. Mech. Dev. 67, 111-123.
69. Tucker, A. S., Matthews, K. L. and Sharpe, P. T. (1998a). Transformation of tooth type induced by inhibition of BMP signaling. Science 282, 1136-1138.
70. Tucker, A. S., Al Khamis, A. and Sharpe, P. T. (1998b). Interactions between Bmp-4 and Msx-1 act to restrict gene expression to odontogenic mesenchyme. Dev. Dyn. 212, 533-539.
71. Tucker. A. S., Yamada, G., Grigoriou, M., Pachnis, V. and Sharpe, P. T. (1999). Fgf-8 determines rostral-caudal polarity in the first branchial arch. Development 126, 51-61.
72. Vaahtokari, A., Åberg, T., Jernvall, J., Keranen, S. and Thesleff, I. (1996). The enamel knot as a signaling center in the developing mouse tooth. Mech. Dev. 54, 39-43.
73. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I. (1993). Identitication of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
74. Watanabe, Y., Duprez, D., Monsoro-Burg, A.-H., Vincent, C. and Le Douarin, N. M. (1998). Two domains in vertebral development: antagonistic regulation by SHH and BMP4 proteins. Development 125, 2631-2639.
75. Wieser, R., Wrana, J. L. and Massagué, J. (1995). GS domain mutations that constitutively activate TβR-1. the downstream signaling component in the TGFβ receptor complex. EMBO J. 14, 2199-2208.
76. Wozney, J. M., Rosen, V., Celeste, A. J., Mitsock, L. M., Whitters, M. J., Kriz, R. W., Hewick, R. M. and Wang, E. A. (1988). Novel regulators of bone formation: Molecular clones and activities. Science 242, 1528-1534.
77. Yang, Y. and Niswander, L. (1995). Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anterior-posterior patterning. Cell 80, 939-947.
78. Zakany, J., Tuggle, C. K., Patel, M. D. and Nguyen-Huu, M. (1988). Spatial regulation of homeobox gene fusions in the embryonic central nervous system. Neuron 1, 679-691.
79. Zhang, Y., Zhao, X., Hu, Y., St. Amand, T., Zhang, M., Ramanurthy, R., Qiu, M. S. and Chen, Y. P. (1999). Msx1 is required for the induction of Patched by Sonic hedgehog in the mammalian tooth germ. Dev. Dyn. 215, 45-53.
80. Zhang, Z. Y., Yu, X., Zhang, Y., Geronimo, B., Løvlie, A., Fromm, S. H. and Chen, Y. P. (2000). Targeted misexpression of constitutively active BMP receptor-IB causes bifurcation and duplication and posterior transformation of digit in mouse limb. Dev. Biol. in press.
81. Zimmerman, L. B., De Jesus-Escobar, J. M. and Harland, R. M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.
82. Zou, H., Wieser, R., Massagué, J. and Niswander, L. (1997). Distinct roles of typo I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191-2203.