Notochord-dependent expression of Mfh1 and Pax1 cooperates to maintain the proliferation of sclerotome cells during the vertebral column development

Developmental Biology

Volumn 210, Issue 1, 1999, Pages 15-29

  Furumoto, Taka Aki ^a,b   Miura, Naoyuki ^d   Akasaka, Takeshi ^a,b   Mizutani Koseki, Yoko ^a,b   Sudo, Hidefumi ^a,b   Fukuda, Katsuyuki ^b   Maekawa, Mamiko ^b   Yuasa, Shigeki ^b   Fu, Yan ^d   Moriya, Hideshige ^b   Taniguchi, Masaru ^a,c   Imai, Kenji ^e   Dahl, Edger ^e   Balling, Rudi ^e   Pavlova, Maria ^f   Gossler, Achim ^f   Koseki, Haruhiko ^a,b  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b Department of Molecular Embryology ^*  (Japan)

^c CHIBA UNIVERSITY   (Japan)

^d AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f JACKSON LABORATORY   (United States)

Author keywords

Development; Embryo; Mfh1; Mouse; Myelomeningocoele; Notochord; Pax1; Somite; Spina bifida; Vertebral column

Indexed keywords

GENE PRODUCT; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INTERVERTEBRAL DISK; MENINGOMYELOCELE; MESODERM; MITOSIS RATE; MOUSE; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCLEROTOME; SIGNAL TRANSDUCTION; SOMITE; SPINA BIFIDA; SPINE; VERTEBRA BODY;

ANIMALIA; ERINACEIDAE;

EID: 0033152690     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9261     Document Type: Article

References (43)

1. Aoyama, H., and Asamoto, K. (1988). Determination of somite cells: Independence of cell differentiation and morphogenesis. Development 104, 15-28.
2. Chalepakis, G., Fritsch, R., Fickenscher, H., Deutsch, U., Goulding, M., and Gruss, P. (1991). The molecular basis of the undulated/Pax1 mutation. Cell 66, 875-884.
3. Chalepakis, G., Jones, F. S., Edelman, G. M., and Gruss, P. (1994). Pax-3 contains domains for transcription activation and transcription inhibition. Proc. Natl. Acad. Sci. USA 91, 12745-12749.
4. 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.
5. Christ, B., and Ordahl, C. P. (1995). Early stages of chick somite development. Anat. Embryol. 191, 381-396.
6. Dahl, E., Koseki, H., and Balling, R. (1997). Pax genes and organogenesis. BioEssays 19, 755-765.
7. Deutsch, U., Dressler, G. R., and Gruss, P. (1988). Pax1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53, 617-625.
8. Dietrich, S., Schubert, F. R., and Gruss, P. (1993). Altered Pax gene expression in murine notochord mutants: The notochord is required to initiate and maintain ventral identity in the somite. Mech. Dev. 44, 189-207.
9. Dietrich, S., and Gruss, P. (1995). Undurated phenotypes suggest a role of Pax1 for the development of vertebral and extravertebral structures. Dev. Biol. 167, 529-548.
10. Dietrich, S., Schubert, F. R., and Lumsden, A. (1997). Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124, 3895-3908.
11. 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 of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
12. Fan, C. M., and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
13. Goulding, M. D., Chalepakis, G., Deutsch, U., Erselius, J. R., and Gruss, P. (1991). Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J. 10, 1135-1147.
14. Grüneberg, H. (1953). Genetical studies on the skeleton of the mouse. VI. Danforth's shot tail. J. Genet. 51, 317-326.
15. Grüneberg, H. (1954). Genetical studies on the skeleton of the mouse. XII. The development of undulated. J. Genet. 52, 441-455.
16. Hall, B. K., and Miyake, T. (1992). The membranous skeleton: The role of cell condensations in vertebrate skeletogenesis. Anat. Embryol. 186, 107-124.
17. Hamburger, V., and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-91.
18. Helwig, U., Imai, K., Schmahl, W., Thomas, B. E., Varnum, D. S., Nadeau, J. H., and Balling, R. (1995). Interaction between undulated and Patch leads to an extreme form of spina bifida in double-mutant mice. Nat. Genet. 11, 60-63.
19. Hughes, S. H., Greenhouse, J. J., Petropoulous, C. J., and Sutrave, P. (1987). Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61, 3004-3012.
20. Iida, K., Koseki, H., Kakinuma, H., Kato, N., Mizutani-Koseki, Y., Ohuchi, H., Yoshioka, N., Noji, S., Kawamura, K., Kataoka, Y., Ueno, F., Taniguchi, M., Yoshida, N., Sugiyama, T., and Miura, N. (1997). Essential roles of the winged helix transcription factor MFH1 in aortic arch patterning and skeletogenesis. Development 124, 4627-4638.
21. Kaestner, K. H., Bleckman, S. C., Monaghan, A. P., Scholondorff, J., Mincheva, A., Lichter, P., and Schutz, G. (1996). Clustered arrangement of winged helix genes fkh-6 and MFH1: Possible implications for mesoderm development. Development 122, 1751-1758.
22. Kessel, M., and Gruss, P. (1991). Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinotic acid. Cell 67, 89-104.
23. Koseki, H., Wallin, J., Wilting, J., Mizutani, Y., Kispert, A., Ebensperger, C., Herrmann, B. G., Christ, B., and Balling, R. (1993). A role for Pax1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae. Development 119, 649-660.
24. Maatman, R., Zachgo, J., and Gossler, A. (1997). The Danforth's short tail mutation acts cell autonomously in notochord cells and ventral hindgut endoderm. Development 124, 4019-4028.
25. Maulbecker, C. C., and Gruss, P. (1993). The oncogenic potential of Pax genes. EMBO J. 12, 2361-2367.
26. Miura, N., Wanaka, A., Tohyama, M., and Tanaka, K. (1993). MFH1, a new member of the fork head domain family, is expressed in developing mesenchyme. FEBS Lett. 326, 171-176.
27. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H., Joyner, A. L., and Hui, C. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123.
28. Monsoro-Burq, A. H., Duprez, D., Watanabe, Y., Bontoux, M., Vincent, C., Brickell, P., and Le Douarin, N. (1996). The role of bone morphogenetic proteins in vertebral development. Development 122, 3607-3616.
29. Münsterberg, A. E., Kitajewski, J., Bumcrot, D. A., McMahorn, A. P., and Lassar, A. B. (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911-2922.
30. Neubüser, A., Koseki, H., and Balling, R. (1995). Characterization and developmental expression of Pax9, a paired-box-containing gene related to Pax1. Dev. Biol. 170, 701-716.
31. Pourquié, O., Fan, C. M., Coltey, M., Hirsinger, E., Watanabe, Y., Breant, C., Francis-West, P., Brickell, P., Tessier-Lavigne, M., and Le Douarin, N. M. (1996). Lateral and axial signals involved in avian somite patterning: A role for BMP4. Cell 84, 461-471.
32. Roth, K. (1971). Spinal deformities in myelomeningocoele: A radiologic assessment. In "Scoliosis" (Paul R. Harrington, Ed.), pp. 1-29.
33. Sasaki, H., and Hogan, B. L. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
34. Takahashi, Y., Monsoro-Burq, A. H., Bontoux, M., and Le Douarin, N. M. (1992). A role for Quox-8 in the establishment of the dorsoventral pattern during vertebrate development. Proc. Natl. Acad. Sci. USA 89, 10237-10241.
35. Teillet, M., Watanabe, Y., Jeffs, P., Duprez, D., Lapointe, F., and Le Douarin, N. M. (1998). Sonic hedgehog is required for survival of both myogenic and chondrogenic somitic lineages. Development 125, 2019-2030.
36. Timmons, P. M., Wallin, J., Rigby, P. W., and Balling, R. (1994). Expression and function of Pax1 during development of the pectoral girdle. Development 120, 2773-2785.
37. Wallin, J., Wilting, J., Koseki, H., Fritsch, R., Christ, B., and Balling, R. (1994). The role of Pax1 in axial skeleton development. Development 120, 1109-1121.
38. Watanabe, Y., Duprez, D., Monsoro-Burq, 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.
39. Wilkinson, D. G. (1992). "In Situ Hybridization: A Practical Approach." Oxford Univ. Press, Oxford.
40. Wilm, B., Dahl, E., Peters, H., Balling, R., and Imai, K. (1998). Targeted disruption of Pax1 defines its null phenotype and proves haploinsufficiency. Proc. Natl. Acad. Sci. USA 95, 8692-8697.
41. Winner, G. E., Hargett, L., and Hogan, B. L. (1997). The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev. 11, 926-940.
42. Wright, W. E., Sassoon, D. A., and Lin, V. K. (1989). Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56, 607-617.
43. Wu, S. C., Grindley, J., Winnier, G. E., Hargett, L., and Hogan, B. L. (1998). Mouse Mesenchyme forkhead 2 (Mf2): Expression, DNA binding and induction by sonic hedgehog during somitogenesis. Mech. Dev. 70, 3-13.