Crossref journal-article
The Company of Biologists
Development (237)
Abstract

ABSTRACT This study first shows a striking parallel between the expression patterns of the Bmp4, Msx1 and Msx2 genes in the lateral ridges of the neural plate before neural tube closure and later on, in the dorsal neural tube and superficial midline ectoderm. We have previously shown that the spinous process of the vertebra is formed from Msx1- and 2-expressing mesenchyme and that the dorsal neural tube can induce the differentiation of subcutaneous cartilage from the somitic mesenchyme. We show here that mouse BMP4- or human BMP2-producing cells grafted dorsally to the neural tube at E2 or E3 increase considerably the amount of Msx-expressing mesenchymal cells which are normally recruited from the somite to form the spinous process of the vertebra. Later on, the dorsal part of the vertebra is enlarged, resulting in vertebral fusion and, in some cases (e.g. grafts made at E3), in the formation of a ‘giant’ spinous process-like structure dorsally. In strong contrast, BMP-producing cells grafted laterally to the neural tube at E2 exerted a negative effect on the expression of Pax1 and Pax3 genes in the somitic mesenchyme, which then turned on Msx genes. Moreover, scle-rotomal cell growth and differentiation into cartilage were then inhibited. Dorsalization of the neural tube, manifested by expression of Msx and Pax3 genes in the basal plate contacting the BMP-producing cells, was also observed. In conclusion, this study demonstrates that differentiation of the ventrolateral and dorsal parts of the vertebral cartilage is controlled by different molecular mechanisms. The former develops under the influence of signals arising from the floor plate-notochord complex. These signals inhibit the development of dorsal subcutaneous cartilage forming the spinous process, which requires the influence of BMP4 to differentiate.

Bibliography

Monsoro-Burq, A.-H., Duprez, D., Watanabe, Y., Bontoux, M., Vincent, C., Brickell, P., & Douarin, N. L. (1996). The role of bone morphogenetic proteins in vertebral development. Development, 122(11), 3607–3616.

Authors 7
  1. Anne-Hélène Monsoro-Burq (first)
  2. Delphine Duprez (additional)
  3. Yuji Watanabe (additional)
  4. Martine Bontoux (additional)
  5. Christine Vincent (additional)
  6. Paul Brickell (additional)
  7. Nicole Le Douarin (additional)
References 53 Referenced 136
  1. 10.1007/BF00188215 / Anat. Embryol. (Berl.) / The ventralizing effect of the notochord on somite differentiation in chick embryos by Brand-Saberi (1993)
  2. {'key': '2025021323542090300_DEVELOP_122_11_3607C2', 'first-page': '2354', 'article-title': 'Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of 3 murine homeodomain proteins', 'volume': '13', 'author': 'Catron', 'year': '1993', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of 3 murine homeodomain proteins by Catron (1993)
  3. 10.1242/dev.113.4.1487 / Development / Altered expression of the chicken homeobox- containing genes GHox-7 and GHox-8 in the limb buds of limbless mutant chick embryos by Coelho (1991)
  4. 10.1016/0925-4773(91)90051-7 / Mech. Dev / Expression of the chicken homeobox-containing gene GHox-8 during embryonic chick limb development by Coelho (1991)
  5. 10.1242/dev.117.2.409 / Development / The triple origin of skull in higher vertebrates – a study in quail-chick chimeras by Couly (1993)
  6. 10.1038/352429a0 / Nature / Position- dependent expression of two related homeobox genes in developing vertebrate limbs by Davidson (1991)
  7. 10.1242/dev.122.6.1821 / Development / Activation of Fgf-4 and HoxD gene expression by BMP-2 expressing cells in the developing chick limb by Duprez (1996)
  8. 10.1016/0925-4773(96)00540-0 / Mech. Dev. (in press) / Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb by Duprez (1996)
  9. 10.1007/BF00534682 / Anat. Embryol / Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos by Ebensperger (1995)
  10. 10.1038/365644a0 / Nature / The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development by Estevez (1993)
  11. 10.1016/0092-8674(94)90009-4 / Cell / Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog by Fan (1994)
  12. 10.1016/0092-8674(95)90398-4 / Cell / Long-range sclerotome induction by Sonic hedgehog: Direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway by Fan (1995)
  13. 10.1002/aja.1002010207 / Dev. Dyn / Expression patterns of the bone morphogenetic protein genes Bmp-4 and Bmp-2 in the developing chick face suggest a role in outgrowth of the primordia by Francis-West (1994)
  14. 10.1242/dev.120.1.209 / Development / Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb by Francis (1994)
  15. 10.1242/dev.120.4.957 / Development / Regulation of Pax-3 expression in the dermomyotome and its role in muscle development by Goulding (1994)
  16. 10.1038/372684a0 / Nature / The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest by Graham (1994)
  17. 10.1002/jmor.1050880104 / J. Morphol / A series of normal stages in the development of the chick embryo by Hamburger (1951)
  18. 10.1038/375787a0 / Nature / Expression of a Delta homologue in prospective neurons in the chick by Henrique (1995)
  19. 10.1073/pnas.91.26.12887 / Proc. Natl. Acad. Sci. USA / Transcriptional control of the tissue-specific, developmentally regulated osteocalcin gene requires a binding motif for the Msx family of homeodomain proteins by Hoffmann (1994)
  20. 10.1128/jvi.61.10.3004-3012.1987 / J. Virol / Adaptor plasmids simplify the insertion of foreign DNA into helper- independent retroviral vectors by Hughes (1987)
  21. 10.1016/0092-8674(94)90008-6 / Cell / Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites by Johnson (1994)
  22. 10.1242/dev.117.2.461 / Development / Epithelial-mesenchymal interactions are required for msx 1 and msx 2 gene expression in the developing murine molar tooth by Jowett (1993)
  23. 10.1128/MCB.14.9.5961 / Mol. Cell. Biol / Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells by Koenig (1994)
  24. 10.1016/0092-8674(95)90276-7 / Cell / Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm by Liem (1995)
  25. 10.1128/MCB.15.7.3479 / Mol. Cell. Biol / Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs by Liu (1995)
  26. 10.1242/dev.111.2.269 / Development / The homeobox gene Hox 7. 1 has specific regional and temporal expression patterns during early murine cranio facial embryogenesis, especially tooth development in vivo and in vitro by MacKenzie (1991)
  27. 10.1242/dev.113.2.601 / Development / Hox-7 expression during murine craniofacial development by MacKenzie (1991)
  28. 10.1006/bbrc.1995.1043 / Biochem. Biophys. Res. Commun / Genomic organization and chromosomal location of the mouse type I BMP-2/4 receptor by Mishina (1995)
  29. 10.1073/pnas.91.22.10435 / Proc. Natl. Acad. Sci. USA / Heterogeneity in the development of the vertebra by Monsoro-Burq (1994)
  30. 10.1016/0925-4773(95)00426-2 / Mech. Dev / The developmental relationships of the neural tube and the notochord: short and long term effects of the notochord on the dorsal spinal cord by Monsoro-Burq (1995)
  31. 10.1111/1523-1747.ep12606960 / J. Invest. Dermatol / Homeobox genes Msx-1 and Msx-2 are associated with induction and growth of skin appendages by Noveen (1995)
  32. 10.1242/dev.114.2.339 / Development / Two myogenic lineages within the developing somite by Ordahl (1992)
  33. 10.1038/325081a0 / Nature / A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family by Padgett (1987)
  34. 10.1016/0925-4773(93)90035-V / Mech. Dev / Ectopic expression of genes during chicken limb pattern formation using replication defective retroviral vectors by Pompa de la (1993)
  35. 10.1073/pnas.89.12.5261 / Proc. Natl. Acad. Sci. USA / BEN, a surface glycoprotein of the immunoglobulin superfamily, is expressed in a variety of developing systems by Pourquié (1992)
  36. 10.1073/pnas.90.11.5242 / Proc. Natl. Acad. Sci. USA / Control of dorsoventral patterning of somitic derivatives by notochord and floor plate by Pourquié (1993)
  37. 10.1073/pnas.92.8.3219 / Proc. Natl. Acad. Sci. USA / Control of somite patterning by signals from the lateral plate by Pourquié (1995)
  38. 10.1016/S0092-8674(00)81291-X / Cell / Lateral and axial signals involved in avian somite patterning: a role for BMP4 by Pourquié (1996)
  39. 10.1101/gad.5.12b.2363 / Genes Dev / The apical ectodermal ridge regulates Hox-7 and Hox-8 gene expression in developing chick limb buds by Robert (1991)
  40. 10.1242/dev.115.3.657 / Development / The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation by Rong (1992)
  41. 10.1242/dev.116.3.811 / Development / Apical ridge dependent and independent mesodermal domains of GHox-7 and GHox-8 expression in chick limb buds by Ros (1992)
  42. 10.1073/pnas.92.17.7632 / Proc. Natl. Acad. Sci. USA / Cloning and characterization of a human type II receptor for bone morphogenetic proteins by Rosenzweig (1995)
  43. 10.1073/pnas.91.1.118 / Proc. Natl. Acad. Sci. USA / DNA affinity cleaving analysis of homeodomain-DNA interaction: identification of homeodomain consensus sites in genomic DNA by Shang (1994)
  44. 10.1016/0012-1606(91)90345-4 / Dev. Biol / Repeating developmental expression of G-Hox 7, a novel homeobox- containing gene in the chicken by Suzuki (1991)
  45. 10.1073/pnas.87.19.7482 / Proc. Natl. Acad. Sci. USA / cDNA cloning of a quail homeobox gene and its expression in neural crest-derived mesenchyme and lateral plate mesoderm by Takahashi (1990)
  46. 10.1002/j.1460-2075.1991.tb07777.x / EMBO J / Epithelio- mesenchymal interactions are critical for Quox-7 expression and membrane bone differentiation in the neural crest-derived mandibular mesenchyme by Takahashi (1991)
  47. 10.1073/pnas.89.21.10237 / Proc. Natl. Acad. Sci. USA / A role for Quox-8 in the establishment of the dorsoventral attern during vertebrate development by Takahashi (1992)
  48. 10.1016/S0092-8674(05)80083-2 / Cell / Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development by Vainio (1993)
  49. 10.1016/0925-4773(96)00534-5 / Mech. Dev / A role for BMP-4 in the development of subcutaneous cartilage by Watanabe (1996)
  50. 10.1242/dev.120.4.785 / Development / Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification by Williams (1994)
  51. 10.1126/science.3201241 / Science / Novel regulators of bone formation: molecular clones and activities by Wozney (1988)
  52. 10.1006/bbrc.1994.2898 / Biochem. Biophys. Res. Commun / A mammalian serine/threonine kinase receptor specifically binds BMP-2 and BMP-4 by Yamaji (1994)
  53. 10.1242/dev.113.2.431 / Development / Chicken homeobox gene Msx-1: structure, expression in limbs buds and effect of retinoic acid by Yokouchi (1991)
Dates
Type When
Created 4 years, 4 months ago (April 23, 2021, 2:59 p.m.)
Deposited 6 months, 2 weeks ago (Feb. 13, 2025, 6:54 p.m.)
Indexed 2 months, 1 week ago (June 25, 2025, 10:52 a.m.)
Issued 28 years, 10 months ago (Nov. 1, 1996)
Published 28 years, 10 months ago (Nov. 1, 1996)
Published Online 28 years, 10 months ago (Nov. 1, 1996)
Published Print 28 years, 10 months ago (Nov. 1, 1996)
Funders 0

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@article{Monsoro_Burq_1996, title={The role of bone morphogenetic proteins in vertebral development}, volume={122}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.122.11.3607}, DOI={10.1242/dev.122.11.3607}, number={11}, journal={Development}, publisher={The Company of Biologists}, author={Monsoro-Burq, Anne-Hélène and Duprez, Delphine and Watanabe, Yuji and Bontoux, Martine and Vincent, Christine and Brickell, Paul and Douarin, Nicole Le}, year={1996}, month=nov, pages={3607–3616} }