Bapx1 regulates patterning in the middle ear: Altered regulatory role in the transition from the proximal jaw during vertebrate evolution

Development

Volumn 131, Issue 6, 2004, Pages 1235-1245

  Tucker, Abigail S ^a   Watson, Robert P ^b   Lettice, Laura A ^b   Yamada, Gen ^c   Hill, Robert E ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Bapx1; Evolution; Gonium; Goosecoid; Middle ear; Mouse; Tympanic ring

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 5; GROWTH DIFFERENTIATION FACTOR 6; GROWTH FACTOR; HOMEODOMAIN PROTEIN; PROTEIN GSC; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BAPX1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUDITORY OSSICLE; BRANCHIAL ARCH; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; EARDRUM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE STRUCTURE; GENETIC REGULATION; INCUS; MALLEUS; MANDIBLE; MIDDLE EAR; MOLECULAR EVOLUTION; MOUSE; MOUSE MUTANT; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATOR GENE; SEQUENCE HOMOLOGY;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CHICK EMBRYO; EAR, MIDDLE; EVOLUTION; HOMEODOMAIN PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JAW; MALLEUS; MICE; NUCLEAR PROTEINS; PROTEIN-TYROSINE-PHOSPHATASE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA; GNATHOSTOMATA (VERTEBRATE); GONIUM; MALLEUS; MAMMALIA; MURINAE; VERTEBRATA;

EID: 1842454975     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01017     Document Type: Article

References (48)

1. Akazawa, H., Komuro, I., Sugitani, Y., Yazaki, Y., Nagai, R. and Nodal, T. (2000). Targeted disruption of the homeobox transcription factor Bapx1 results in lethal skeletal dysplasia with asplenia and gastroduodenal malformation. Genes Cells 5, 499-513.
2. Allin, E. F. (1975). Evolution of the mammalian middle ear. J. Morphol. 147, 403-437.
3. Allin, E. F. and Hopson, J. A. (1992). Evolution of the auditory system in Synapsida ('mammal-like reptiles' and primitive mammals) as seen in the fossil record. In The Evolutionary Biology of Hearing (ed. D. B. Webster, R. R. Fay, A. N. Popper), pp. 587-614. New York: Springer-Verlag.
4. De Beer, G. (1937). The Development of the Vertebrate Skull. Chicago. IL: University of Chicago Press.
5. Depew, M. J., Tucker, A. S. and Sharpe, P. T. (2002). Mouse development - Patterning, Morphogenesis and Organogenesis. In Craniofacial Development (ed. J. Rossant and P. Tam), Chapter 19. London, Academic Press.
6. Ducy, P., Zhang, R., Geoffroy, V., Ridall, A. L. and Karsenty, G. (1997). Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89, 747-754.
7. Fleischer, G. (1978). Evolutionary principles of the mammalian middle ear. Adv. Anat. Embry. Cell Biol. 55, 1-70.
8. Gaunt, S. J., Blum, M., de Robertis, E. M. (1993). Expression of the mouse goosecoid gene during mid-embryogenesis may mark mesenchymal cell lineages in the developing head, limbs and body wall. Development 117, 769-778
9. Gaupp, E. (1911). Beiträge zur Kenntnis des Unterkiefers der Wirbeltiere I; der Proc. Anterior (Folii) des Hammers der Säuger und das Gonial der Nichtsäuger. Anat. Anz. 39, 97-135.
10. Goodrich, E. S. (1986). Studies on the Structure and Development of Vertebrates. Chicago, IL. University of Chicago Press.
11. Grandien, K. and Sommer, R. J. (2001). Functional comparison of the nematode Hox gene lin-39 in C. elegans and P. pacificus reveals evolutionary conservation of protein function despite divergence of primary sequences. Genes Dev. 15, 2161-2172.
12. Grenier, J. K. and Carroll, S. B. (2000). Functional evolution of the Ultrabithorax protein. Proc. Natl. Acad Sci. USA 97, 704-709.
13. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
14. Henson, O. W. (1974). Comparative anatomy of the middle ear. In Handbook of Sensory Physiology, Vol. V/1 (ed. W. D. Keidel and W. D. Neff), pp. 81-85. Berlin, Heidelberg, New York: Springer-Verlag.
15. Herbrand, H., Pabst, O., Hill, R. and Arnold, H. H. (2002). Transcription factors Nkx3.1 and Nkx3.2 (Bapx1) play an overlapping role in sclerotomal development of the mouse. Mech. Dev. 117, 217-224.
16. Huangff, M. and Saunders, J. C. (1983). Auditory development in the mouse: Structural maturation of the middle ear. J. Morphol. 176, 249-259.
17. Kalatzis, V., Sahly, I., El-Amraoui, A. and Petit, C. (1998). Eya1 expression in the developing ear and kidney: Towards the understanding of the pathogenesis of Branchio-Oto-Renal syndrome. Dev. Dyn. 213, 486-499.
18. Kessel, M. and Gruss, P. (1991). Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67, 89-104.
19. Kim, Y. and Nirenberg, M. (1989). Drosophila NK-homeobox genes. Proc. Natl. Acad Sci. USA 86, 7716-7720.
20. Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R. T., Gao, Y. H., Inada, M. et al. (1997). Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764.
21. Kuratani, S., Satakata, I, Blum, M., Komatsu, Y., Haraguchi, R., Nakamura, S., Suzuki, K., Kosai, K., Maas, R. and Yamada, G. (1999). Middle ear defects associated with the double knockout mutation of murine goosecoid and Msx1 genes. Cell. Mol. Biol. 45, 589-599.
22. Lettice, L. A., Purdie, L. A., Carlson, G. J., Kilanowski, F., Dorin, J. and Hill, R. E. (1999). The mouse bagpipe gene controls development of axial skeleton, skull, and spleen. Proc. Natl. Acad. Sci. USA 96, 9695-9700.
23. Mallo, M. (1997). Retinoic acid disturbs mouse middle ear development in a stage-dependent fashion. Dev. Biol. 184, 175-186.
24. Mallo, M. (2001). Formation of the middle ear: Recent progress on the developmental and molecular mechanisms. Dev. Biol. 231, 410-419.
25. Mallo, M. and Gridley, T. (1996). Development of the mammalian ear: Coordinate regulation of formation of the tympanic ring and the external acoustic meatus. Development 122, 173-179.
26. Martin, J. F., Bradley, A. and Olson, E. N. (1995). The paired-like homeo box gene Mhox is required for early events of skeletogenesis in multiple lineages. Genes Dev. 9, 1237-1249.
27. Miller, C. T., Yelon, D., Stainier, D. Y. R. and Kimmel, C. B. (2003). Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130, 1353-1365 Newman, C. S., Grow, M. W., Cleaver, O., Chia, F. and Krieg, P. (1997). Xbap, a vertebrate gene related to bagpipe, is expressed in developing craniofacial structures and in anterior gut muscle. Dev. Biol. 181, 223-233.
28. Reichert, C. (1837). Über die Visceralbogen der Wirbeltiere im allgemeinen und deren Metamophose bei den Vögelm und Säugetieren. Arch. Anat. Physiol. 120-222.
29. Rivera-Pérez, J. A., Mallo, M., Gendron-Maguire, M., Gridley, T. and Behringer, R. R. (1995). goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development 121, 3005-3012
30. Romanoff, A. L. (1960). The Avian Embryo: Structural and Functional Development. New York: Macmillan.
31. Rosowski, J. J. (1992). Hearing in transitional mammals. In The Evolutionary Biology of Hearing (ed. D. B. Webster, R. R. Fay and A. N. Popper), pp. 615-631. New York: Springer-Verlag.
32. Satokata, I. and Maas, R. (1994). Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356.
33. Schilling, T. and Kimmel, C. (1997). Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 120, 483-494.
34. Settle, S. H., Jr, Rountree, R. B., Sinha, A., Thacker, A., Higgins, K. and David, M. and Kingsley, D. M. (2003). Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev. Biol. 254, 116-130.
35. Sharpe, J., Ahlgren, U., Perry, P., Hill, B., Ross, A., Hecksher-Sorensen, J., Baldock, R. and Davidson, D. (2002). Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296, 541-545.
36. Storm, E. E., Huynh, T. V., Copeland, N. G., Jenkins, N. A., Kingsley, D. M. and Lee, S.-J. (1994). Limb alterations in brachypodism mice due to mutations in a new member of the Tgf-beta superfamily. Nature 368, 639-643.
37. Storm, E. E. and Kingsley, D. M. (1999). Gdf5 coordinates bone and joint formation during digit development. Dev. Biol. 209, 11-27.
38. Tanaka, M., Lyons, G. E. and Izumo, S. (1999). Expression of the Nkx3.1 homeobox gene during pre and postnatal development. Mech. Dev. 85, 179-182.
39. Tribioli, C. and Lufkin, T. (1997). Molecular cloning, chromosomal mapping and developmental expression of Bapx1, a novel human homeobox-containing gene homologous to Drosophila bagpipe. Gene 203, 225-233.
40. Tribioli, C. and Lufkin, T. (1999). The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126, 5699-5711.
41. Tribioli, C., Frasch, M. and Lufkin, T. (1997). Bapx1: An evolutionary conserved homologue of the Drosophila bagpipe homeobox gene is expressed in splanchnic mesoderm and the embryonic skeleton. Mech. Dev. 65, 145-162.
42. Trumpp, A., Depew, M. J., Rubenstein, J. L. R., Bishop, M. J. and Martin, G. R. (1999). Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 13, 3136-3148.
43. Tucker, A. S., Al Khamis, A., Ferguson, C. A., Bach, I., Rosenfeld, M. G. and Sharpe, P. T. (1999). Conserved regulation of mesenchymal gene expression by Fgf-8 in face and limb development. Development 126, 221-228.
44. Voit, M. (1924). Uber das Goniale am Unterkiefer der Vogel. Z. Morphol. Anthrop. 24, 75-82.
45. Wilkinson, D. (1992). Whole mount in situ hybridization of vertebrate embryos. In In Situ Hybridization: A Practical Approach (ed. D. Wilkinson), pp. 75-83. Oxford: IRL Press at Oxford University Press.
46. Wilson, J. and Tucker, A. S. (2004). Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev. Biol. (in press).
47. Xu, P-X., Adams, J., Peters, H., Brown, M. C., Heaney, S. and Maas, R. (1999). Eya-1 deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nature 23, 113-117.
48. Yamada G., Mansouril, A., Torres, M., Stuart, E. T., Blum, M., Schultz, M., de Robertis, E. M. and Gruss, P. (1995). Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death. Development 121, 2917-2922.