Regulation of cranial morphogenesis and cell fate at the neural crest-mesoderm boundary by engrailed 1

Development

Volumn 139, Issue 7, 2012, Pages 1346-1358

  Deckelbaum, Ron A ^a,b   Holmes, Greg ^a,c   Zhao, Zhicheng ^a   Tong, Chunxiang ^a,b   Basilico, Claudio ^a   Loomis, Cynthia A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Craniosynostosis; Morphogenesis; Suture

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 2; PROTEIN; PROTEIN ENGRAILED 1; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALVARIA; CELL FATE; CELL MOTION; EMBRYO; GENE FUNCTION; MESENCHYME; MESENCHYME CELL; MESODERM; MORPHOGENESIS; MOUSE; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SKULL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CROSSES, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MALE; MESODERM; MICE; MORPHOGENESIS; NEURAL CREST; OSTEOGENESIS; SKULL; STEM CELLS; TIME FACTORS;

ERINACEIDAE; MAMMALIA;

EID: 84857926696     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.076729     Document Type: Article

References (56)

1. Ahn, S. and Joyner, A. L. (2004). Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118, 505-516.
2. Araki, I. and Nakamura, H. (1999). Engrailed defines the position of dorsal di-mesencephalic boundary by repressing diencephalic fate. Development 126, 5127-5135.
3. Blair, S. S. and Ralston, A. (1997). Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development 124, 4053-4063.
4. Chai, Y., Jiang, X., Ito, Y., Bringas, P., Han, J., Rowitch, D. H., Soriano, P., McMahon, A. P. and Sucov, H. M. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671-1679.
5. Chen, H. and Johnson, R. L. (2002). Interactions between dorsal-ventral patterning genes lmx1b, engrailed-1 and wnt-7a in the vertebrate limb. Int. J. Dev. Biol. 46, 937-941.
6. Chen, H., Ovchinnikov, D., Pressman, C. L., Aulehla, A., Lun, Y. and Johnson, R. L. (1998). Multiple calvarial defects in lmx1b mutant mice. Dev. Genet. 22, 314-320.
7. Chen, L., Li, D., Li, C., Engel, A. and Deng, C. X. (2003). A Ser252Trp substitution in mouse fibroblast growth factor receptor 2 (Fgfr2) results in craniosynostosis. Bone 33, 169-178.
8. Connerney, J., Andreeva, V., Leshem, Y., Muentener, C., Mercado, M. A. and Spicer, D. B. (2006). Twist1 dimer selection regulates cranial suture patterning and fusion. Dev. Dyn. 235, 1345-1357.
9. Connerney, J., Andreeva, V., Leshem, Y., Mercado, M. A., Dowell, K., Yang, X., Lindner, V., Friesel, R. E. and Spicer, D. B. (2008). Twist1 homodimers enhance FGF responsiveness of the cranial sutures and promote suture closure. Dev. Biol. 318, 323-334.
10. 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.
11. Dahmann, C. and Basler, K. (1999). Compartment boundaries: at the edge of development. Trends Genet. 15, 320-326.
12. Dahmann, C. and Basler, K. (2000). Opposing transcriptional outputs of Hedgehog signaling and engrailed control compartmental cell sorting at the Drosophila A/P boundary. Cell 100, 411-422.
13. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
14. Deckelbaum, R. A., Majithia, A., Booker, T., Henderson, J. E. and Loomis, C. A. (2006). The homeoprotein engrailed 1 has pleiotropic functions in calvarial intramembranous bone formation and remodeling. Development 133, 63-74.
15. 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.
16. El Ghouzzi, V., Le Merrer, M., Perrin-Schmitt, F., Lajeunie, E., Benit, P., Renier, D., Bourgeois, P., Bolcato-Bellemin, A. L., Munnich, A. and Bonaventure, J. (1997). Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat. Genet. 15, 42-46.
17. Evans, D. J. and Noden, D. M. (2006). Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev. Dyn. 235, 1310-1325.
18. Hanafusa, H., Torii, S., Yasunaga, T. and Nishida, E. (2002). Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4, 850-858.
19. Hanks, M. C., Loomis, C. A., Harris, E., Tong, C. X., Anson-Cartwright, L., Auerbach, A. and Joyner, A. (1998). Drosophila engrailed can substitute for mouse Engrailed1 function in mid-hindbrain, but not limb development. Development 125, 4521-4530.
20. Holmes, G., Rothschild, G., Roy, U. B., Deng, C. X., Mansukhani, A. and Basilico, C. (2009). Early onset of craniosynostosis in an Apert mouse model reveals critical features of this pathology. Dev. Biol. 328, 273-284.
21. Hopman, A. H., Ramaekers, F. C. and Speel, E. J. (1998). Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for In situ hybridization using CARD amplification. J. Histochem. Cytochem. 46, 771-777.
22. Hui, C. C., Slusarski, D., Platt, K. A., Holmgren, R. and Joyner, A. L. (1994). Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 162, 402-413.
23. Irvine, K. D. and Rauskolb, C. (2001). Boundaries in development: formation and function. Annu. Rev. Cell Dev. Biol. 17, 189-214.
24. Jabs, E. W., Muller, U., Li, X., Ma, L., Luo, W., Haworth, I. S., Klisak, I., Sparkes, R., Warman, M. L. and Mulliken, J. B. (1993). A mutation in the homeodomain of the human MSX2 gene in a family affected with autosomal dominant craniosynostosis. Cell 75, 443-450.
25. Jenkins, D., Seelow, D., Jehee, F. S., Perlyn, C. A., Alonso, L. G., Bueno, D. F., Donnai, D., Josifova, D., Mathijssen, I. M., Morton, J. E. et al. (2007). RAB23 mutations in Carpenter syndrome imply an unexpected role for hedgehog signaling in cranial-suture development and obesity. Am. J. Hum. Genet. 80, 1162-1170.
26. Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M. and Morriss-Kay, G. M. (2002). Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241, 106-116.
27. Kiecker, C. and Lumsden, A. (2005). Compartments and their boundaries in vertebrate brain development. Nat. Rev. Neurosci. 6, 553-564.
28. Kimmel, R. A., Turnbull, D. H., Blanquet, V., Wurst, W., Loomis, C. A. and Joyner, A. L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 14, 1377-1389.
29. Klopocki, E., Lohan, S., Brancati, F., Koll, R., Brehm, A., Seemann, P., Dathe, K., Stricker, S., Hecht, J., Bosse, K. et al. (2011). Copy-number variations involving the IHH locus are associated with syndactyly and craniosynostosis. Am. J. Hum. Genet. 88, 70-75.
30. Le Douarin, N. M., Ziller, C. and Couly, G. F. (1993). Patterning of neural crest derivatives in the avian embryo: in vivo and in vitro studies. Dev. Biol. 159, 24-49.
31. Le Lievre, C. S. (1978). Participation of neural crest-derived cells in the genesis of the skull in birds. J. Embryol. Exp. Morphol. 47, 17-37.
32. Lenton, K., James, A. W., Manu, A., Brugmann, S. A., Birker, D., Nelson, E. R., Leucht, P., Helms, J. A. and Longaker, M. T. (2011). Indian hedgehog positively regulates calvarial ossification and modulates bone morphogenetic protein signaling. Genesis 49, 784-796.
33. Lenton, K. A., Nacamuli, R. P., Wan, D. C., Helms, J. A. and Longaker, M. T. (2005). Cranial suture biology. Curr. Top. Dev. Biol. 66, 287-328.
34. Li, C., Scott, D. A., Hatch, E., Tian, X. and Mansour, S. L. (2007). Dusp6 (Mkp3) is a negative feedback regulator of FGF-stimulated ERK signaling during mouse development. Development 134, 167-176.
35. Loomis, C. A., Harris, E., Michaud, J., Wurst, W., Hanks, M. and Joyner, A. L. (1996). The mouse Engrailed-1 gene and ventral limb patterning. Nature 382, 360-363.
36. Merrill, A., Bochukova, E., Brugger, S., Ishii, M., Pilz, D., Wall, S., Lyons, K., Wilkie, A. and Maxson, R. J. (2006). Cell mixing at a neural crest-mesoderm boundary and deficient ephrin-Eph signaling in the pathogenesis of craniosynostosis. Hum. Mol. Genet. 15, 1319-1328.
37. Morriss-Kay, G. M. and Wilkie, A. O. (2005). Growth of the normal skull vault and its alteration in craniosynostosis: insights from human genetics and experimental studies. J. Anat. 207, 637-653.
38. Nagata, M., Nuckolls, G. H., Wang, X., Shum, L., Seki, Y., Kawase, T., Takahashi, K., Nonaka, K., Takahashi, I., Noman, A. A. et al. (2010). The primary site of the acrocephalic feature in Apert Syndrome is a dwarf cranial base with accelerated chondrocytic differentiation due to aberrant activation of the FGFR2 signaling. Bone 48, 847-856.
39. Noden, D. M. (1984). Craniofacial development: new views on old problems. Anat. Rec. 208, 1-13.
40. Noden, D. M. and Trainor, P. A. (2005). Relations and interactions between cranial mesoderm and neural crest populations. J. Anat. 207, 575-601.
41. Qiu, Q., Chen, H. and Johnson, R. L. (2009). Lmx1b-expressing cells in the mouse limb bud define a dorsal mesenchymal lineage compartment. Genesis 47, 224-233.
42. Rice, D. P., Aberg, T., Chan, Y., Tang, Z., Kettunen, P. J., Pakarinen, L., Maxson, R. E. and Thesleff, I. (2000). Integration of FGF and TWIST in calvarial bone and suture development. Development 127, 1845-1855.
43. Roybal, P. G., Wu, N. L., Sun, J., Ting, M. C., Schafer, C. A. and Maxson, R. E. (2010). Inactivation of Msx1 and Msx2 in neural crest reveals an unexpected role in suppressing heterotopic bone formation in the head. Dev. Biol. 343, 28-39.
44. Sgaier, S. K., Millet, S., Villanueva, M. P., Berenshteyn, F., Song, C. and Joyner, A. L. (2005). Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45, 27-40.
45. Shen, H., Wilke, T., Ashique, A. M., Narvey, M., Zerucha, T., Savino, E., Williams, T. and Richman, J. M. (1997). Chicken transcription factor AP-2: cloning, expression and its role in outgrowth of facial prominences and limb buds. Dev. Biol. 188, 248-266.
46. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
47. Speel, E. J., Hopman, A. H. and Komminoth, P. (1999). Amplification methods to increase the sensitivity of in situ hybridization: play card(s). J. Histochem. Cytochem. 47, 281-288.
48. Ting, M. C., Wu, N. L., Roybal, P. G., Sun, J., Liu, L., Yen, Y. and Maxson, R. E., Jr (2009). EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development 136, 855-864.
49. Trainor, P. A. and Tam, P. P. (1995). Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 121, 2569-2582.
50. Trainor, P. A., Tan, S. S. and Tam, P. P. (1994). Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development 120, 2397-2408.
51. Wang, Y., Xiao, R., Yang, F., Karim, B. O., Iacovelli, A. J., Cai, J., Lerner, C. P., Richtsmeier, J. T., Leszl, J. M., Hill, C. A. et al. (2005). Abnormalities in cartilage and bone development in the Apert syndrome FGFR2(+/S252W) mouse. Development 132, 3537-3548.
52. Wilkie, A. O. (1997). Craniosynostosis: genes and mechanisms. Hum. Mol. Genet. 6, 1647-1656.
53. Wurst, W., Auerbach, A. B. and Joyner, A. L. (1994). Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065-2075.
54. Yen, H. Y., Ting, M. C. and Maxson, R. E. (2010). Jagged1 functions downstream of Twist1 in the specification of the coronal suture and the formation of a boundary between osteogenic and non-osteogenic cells. Dev. Biol. 347, 258-270.
55. Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y. and Iseki, S. (2008). Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125, 797-808.
56. Zervas, M., Millet, S., Ahn, S. and Joyner, A. L. (2004). Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43, 345-357.