Dlx5 and Dlx6 expression in the anterior neural fold is essential for patterning the dorsal nasal capsule

Development

Volumn 138, Issue 5, 2011, Pages 897-903

  Gitton, Yorick ^a   Benouaiche, Laurence ^a,b   Vincent, Christine ^c   Heude, Eglantine ^a   Soulika, Marina ^a   Bouhali, Kamal ^a   Couly, Gérard ^a,b   Levi, Giovanni ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Dlx5; Dlx6; Nasal capsule; Neural crest; Olfactory placode

Indexed keywords

SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR DLX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR NEURAL FOLD; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; DORSAL NASAL CAPSULE; DOWN REGULATION; ECTODERM; EMBRYO; EMBRYO (ANATOMY); EMBRYO PATTERN FORMATION; ENDODERM; MOUSE; MOUSE EMBRYO; NEURAL CREST; NEURAL TUBE; NEURULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BODY PATTERNING; CHICKENS; ECTODERM; EMBRYO, MAMMALIAN; EMBRYO, NONMAMMALIAN; HOMEODOMAIN PROTEINS; MICE; MORPHOGENESIS; NEURAL CREST; NOSE;

AVES; VERTEBRATA;

EID: 79951520650     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.057505     Document Type: Article

References (56)

1. Abzhanov, A. and Tabin, C. J. (2004). Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev. Biol. 273, 134-148. (Pubitemid 39078372)
2. Abzhanov, A., Cordero, D. R., Sen, J., Tabin, C. J. and Helms, J. A. (2007). Crossregulatory interactions between Fgf8 and Shh in the avian frontonasal prominence. Congenit. Anom. (Kyoto) 47, 136-148.
3. Acampora, D., Merlo, G. R., Paleari, L., Zerega, B., Postiglione, M. P., Mantero, S., Bober, E., Barbieri, O., Simeone, A. and Levi, G. (1999). Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126, 3795-3809. (Pubitemid 29440478)
4. Bailey, A. P., Bhattacharyya, S., Bronner-Fraser, M. and Streit, A. (2006). Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity. Dev. Cell 11, 505-517. (Pubitemid 44467726)
5. Baker, C. V. and Bronner-Fraser, M. (2001). Vertebrate cranial placodes I. Embryonic induction. Dev. Biol. 232, 1-61.
6. Bee, J. and Thorogood, P. (1980). The role of tissue interactions in the skeletogenic differentiation of avian neural crest cells. Dev. Biol. 78, 47-62. (Pubitemid 10013278)
7. Benouaiche, L., Gitton, Y., Vincent, C., Couly, G. and Levi, G. (2008). Sonic hedgehog signalling from foregut endoderm patterns the avian nasal capsule. Development 135, 2221-2225.
8. Beverdam, A., Merlo, G. R., Paleari, L., Mantero, S., Genova, F., Barbieri, O., Janvier, P. and Levi, G. (2002). Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis 34, 221-227. (Pubitemid 35470696)
9. Bhattacharyya, S. and Bronner-Fraser, M. (2004). Hierarchy of regulatory events in sensory placode development. Curr. Opin. Genet. Dev. 14, 520-526. (Pubitemid 39360299)
10. Bhattacharyya, S. and Bronner-Fraser, M. (2008). Competence, specification and commitment to an olfactory placode fate. Development 135, 4165-4177.
11. Bhattacharyya, S., Bailey, A. P., Bronner-Fraser, M. and Streit, A. (2004). Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 271, 403-414. (Pubitemid 38833670)
12. Brugmann, S. A., Tapadia, M. D. and Helms, J. A. (2006). The molecular origins of species-specific facial pattern. Curr. Top. Dev. Biol. 73, 1-42.
13. Brugmann, S. A., Goodnough, L. H., Gregorieff, A., Leucht, P., ten Berge, D., Fuerer, C., Clevers, H., Nusse, R. and Helms, J. A. (2007). Wnt signaling mediates regional specification in the vertebrate face. Development 134, 3283-3295.
14. Couly, G. (1981). Neurocristopathies of the human nasofrontal bud. Ethmoidal syndromes (hypo- and hyper-septoethmoidism). Rev. Stomatol. Chir. Maxillofac. 82, 213-225.
15. Couly, G. and Le Douarin, N. M. (1990). Head morphogenesis in embryonic avian chimeras: evidence for a segmental pattern in the ectoderm corresponding to the neuromeres. Development 108, 543-558.
16. Couly, G., Grapin-Botton, A., Coltey, P., Ruhin, B. and Le Douarin, N. M. (1998). Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125, 3445-3459.
17. Couly, G., Creuzet, S., Bennaceur, S., Vincent, C. and Le Douarin, N. M. (2002). Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129, 1061-1073.
18. Couly, G. F. and Le Douarin, N. M. (1985). Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev. Biol. 110, 422-439.
19. Couly, G. F., Coltey, P. M. and Le Douarin, N. M. (1992). The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114, 1-15.
20. Couly, G. F., Coltey, P. M. and Le Douarin, N. M. (1993). The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117, 409-429.
21. Creuzet, S., Schuler, B., Couly, G. and Le Douarin, N. M. (2004). Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc. Natl. Acad. Sci. USA 101, 4843-4847.
22. Creuzet, S. E., Martinez, S. and Le Douarin, N. M. (2006). The cephalic neural crest exerts a critical effect on forebrain and midbrain development. Proc. Natl. Acad. Sci. USA 103, 14033-14038.
23. De Moerlooze, L., Spencer-Dene, B., Revest, J. M., Hajihosseini, M., Rosewell, I. and Dickson, C. (2000). An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127, 483-492. (Pubitemid 30093396)
24. Depew, M. J., Liu, J. K., Long, J. E., Presley, R., Meneses, J. J., Pedersen, R. A. and Rubenstein, J. L. (1999). Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126, 3831-3846.
25. Depew, M. J., Lufkin, T. and Rubenstein, J. L. (2002). Specification of jaw subdivisions by Dlx genes. Science 298, 381-385.
26. Depew, M. J., Simpson, C. A., Morasso, M. and Rubenstein, J. L. (2005). Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J. Anat. 207, 501-561.
27. Gitton, Y., Heude, E., Vieux-Rochas, M., Benouaiche, L., Fontaine, A., Sato, T., Kurihara, Y., Kurihara, H., Couly, G. and Levi, G. (2010). Evolving maps in craniofacial development. Semin. Cell Dev. Biol. 21, 301-308.
28. Hamburger, V. and Hamilton, H. L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195, 231-272.
29. Kawauchi, S., Shou, J., Santos, R., Hebert, J. M., McConnell, S. K., Mason, I. and Calof, A. L. (2005). Fgf8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 132, 5211-5223.
30. Le Douarin, N. M., Brito, J. M. and Creuzet, S. (2007). Role of the neural crest in face and brain development. Brain Res. Rev. 55, 237-247. (Pubitemid 47538760)
31. Levi, G., Puche, A. C., Mantero, S., Barbieri, O., Trombino, S., Paleari, L., Egeo, A. and Merlo, G. R. (2003). The Dlx5 homeodomain gene is essential for olfactory development and connectivity in the mouse. Mol. Cell. Neurosci. 22, 530-543.
32. Liu, B., Rooker, S. M. and Helms, J. A. (2010). Molecular control of facial morphology. Semin. Cell Dev. Biol. 21, 309-313.
33. Long, J. E., Garel, S., Depew, M. J., Tobet, S. and Rubenstein, J. L. (2003). DLX5 regulates development of peripheral and central components of the olfactory system. J. Neurosci. 23, 568-578.
34. McLarren, K. W., Litsiou, A. and Streit, A. (2003). DLX5 positions the neural crest and preplacode region at the border of the neural plate. Dev. Biol. 259, 34-47. (Pubitemid 36703142)
35. Minoux, M. and Rijli, F. M. (2010). Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137, 2605-2621.
36. O'Malley, J. F. (1923). Evolution of the nasal cavities and sinuses in relation to function. Proc. R. Soc. Med. 16, 83-84.
37. Pera, E. and Kessel, M. (1999). Expression of DLX3 in chick embryos. Mech. Dev. 89, 189-193. (Pubitemid 29528291)
38. Pera, E., Stein, S. and Kessel, M. (1999). Ectodermal patterning in the avian embryo: epidermis versus neural plate. Development 126, 63-73. (Pubitemid 29045900)
39. Price, M., Lemaistre, M., Pischetola, M., Di Lauro, R. and Duboule, D. (1991). A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748-751. (Pubitemid 21896681)
40. Quint, E., Zerucha, T. and Ekker, M. (2000). Differential expression of orthologous Dlx genes in zebrafish and mice: implications for the evolution of the Dlx homeobox gene family. J. Exp. Zool. 288, 235-241.
41. Robledo, R. F., Rajan, L., Li, X. and Lufkin, T. (2002). The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev. 16, 1089-1101. (Pubitemid 34507198)
42. Ruhin, B., Creuzet, S., Vincent, C., Benouaiche, L., Le Douarin, N. M. and Couly, G. (2003). Patterning of the hyoid cartilage depends upon signals arising from the ventral foregut endoderm. Dev. Dyn. 228, 239-246. (Pubitemid 37193636)
43. Sato, T., Kurihara, Y., Asai, R., Kawamura, Y., Tonami, K., Uchijima, Y., Heude, E., Ekker, M., Levi, G. and Kurihara, H. (2008). An endothelin-1 switch specifies maxillomandibular identity. Proc. Natl. Acad. Sci. USA 105, 18806-18811.
44. Simeone, A., Acampora, D., Pannese, M., D'Esposito, M., Stornaiuolo, A., Gulisano, M., Mallamaci, A., Kastury, K., Druck, T., Huebner, K. et al. (1994). Cloning and characterization of two members of the vertebrate Dlx gene family. Proc. Natl. Acad. Sci. USA 91, 2250-2254. (Pubitemid 24092081)
45. Sjodal, M., Edlund, T. and Gunhaga, L. (2007). Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev. Cell 13, 141-149. (Pubitemid 46972033)
46. Solomon, K. S. and Fritz, A. (2002). Concerted action of two dlx paralogs in sensory placode formation. Development 129, 3127-3136. (Pubitemid 34874287)
47. Szabo-Rogers, H. L., Geetha-Loganathan, P., Nimmagadda, S., Fu, K. K. and Richman, J. M. (2008). FGF signals from the nasal pit are necessary for normal facial morphogenesis. Dev. Biol. 318, 289-302.
48. Szabo-Rogers, H. L., Geetha-Loganathan, P., Whiting, C. J., Nimmagadda, S., Fu, K. and Richman, J. M. (2009). Novel skeletogenic patterning roles for the olfactory pit. Development 136, 219-229.
49. 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.
50. Trokovic, N., Trokovic, R., Mai, P. and Partanen, J. (2003). Fgfr1 regulates patterning of the pharyngeal region. Genes Dev. 17, 141-153. (Pubitemid 36062515)
51. Vieux-Rochas, M., Coen, L., Sato, T., Kurihara, Y., Gitton, Y., Barbieri, O., Le Blay, K., Merlo, G., Ekker, M., Kurihara, H. et al. (2007). Molecular dynamics of retinoic acid-induced craniofacial malformations: implications for the origin of gnathostome jaws. PLoS ONE 2, e510.
52. Vieux-Rochas, M., Mantero, S., Heude, E., Barbieri, O., Astigiano, S., Couly, G., Kurihara, H., Levi, G. and Merlo, G. R. (2010). Spatio-temporal dynamics of gene expression of the Edn1-Dlx5/6 pathway during development of the lower jaw. Genesis 48, 262-373.
53. Wang, Y., Spatz, M. K., Kannan, K., Hayk, H., Avivi, A., Gorivodsky, M., Pines, M., Yayon, A., Lonai, P. and Givol, D. (1999). A mouse model for achondroplasia produced by targeting fibroblast growth factor receptor 3. Proc. Natl. Acad. Sci. USA 96, 4455-4460. (Pubitemid 29190357)
54. Wealthall, R. J. and Herring, S. W. (2006). Endochondral ossification of the mouse nasal septum. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288, 1163-1172.
55. Wu, P., Jiang, T. X., Suksaweang, S., Widelitz, R. B. and Chuong, C. M. (2004). Molecular shaping of the beak. Science 305, 1465-1466.
56. Yang, L., Zhang, H., Hu, G., Wang, H., Abate-Shen, C. and Shen, M. M. (1998). An early phase of embryonic Dlx5 expression defines the rostral boundary of the neural plate. J. Neurosci. 18, 8322-8330.