Skip to main content
NCBI home page
Journal of Anatomy logoLink to Journal of Anatomy
. 2001 Jul-Aug;199(Pt 1-2):143–151. doi: 10.1046/j.1469-7580.2001.19910143.x

Derivation of the mammalian skull vault

GILLIAN M MORRISS-KAY 1,✉
PMCID: PMC1594961  PMID: 11523816

Abstract

This review describes the evolutionary history of the mammalian skull vault as a basis for understanding its complex structure. Current information on the developmental tissue origins of the skull vault bones (mesoderm and neural crest) is assessed for mammals and other tetrapods. This information is discussed in the context of evolutionary changes in the proportions of the skull vault bones at the sarcopterygian-tetrapod transition. The dual tissue origin of the skull vault is considered in relation to the molecular mechanisms underlying osteogenic cell proliferation and differentiation in the sutural growth centres and in the proportionate contributions of different sutures to skull growth.

Keywords: Dermal bone, vertebrate evolution, neural crest, cranial mesoderm

Full Text

The Full Text of this article is available as a PDF (323.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Chai Y., Jiang X., Ito Y., Bringas P., Jr, Han J., Rowitch D. H., Soriano P., McMahon A. P., Sucov H. M. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development. 2000 Apr;127(8):1671–1679. doi: 10.1242/dev.127.8.1671. [DOI] [PubMed] [Google Scholar]
  2. Chibon P. Marquage nucléaire par la thymidine tritiée DES D'ERIV'ES DE LA CR?ETE NEURALE CHEZ L'amphibien Urodèle Pleurodeles waltlii Michah. J Embryol Exp Morphol. 1967 Dec;18(3):343–358. [PubMed] [Google Scholar]
  3. Couly G. F., Coltey P. M., Le Douarin N. M. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development. 1993 Feb;117(2):409–429. doi: 10.1242/dev.117.2.409. [DOI] [PubMed] [Google Scholar]
  4. Dodig M., Tadic T., Kronenberg M. S., Dacic S., Liu Y. H., Maxson R., Rowe D. W., Lichtler A. C. Ectopic Msx2 overexpression inhibits and Msx2 antisense stimulates calvarial osteoblast differentiation. Dev Biol. 1999 May 15;209(2):298–307. doi: 10.1006/dbio.1999.9258. [DOI] [PubMed] [Google Scholar]
  5. Gans C., Northcutt R. G. Neural crest and the origin of vertebrates: a new head. Science. 1983 Apr 15;220(4594):268–273. doi: 10.1126/science.220.4594.268. [DOI] [PubMed] [Google Scholar]
  6. Greenwald J. A., Mehrara B. J., Spector J. A., Warren S. M., Crisera F. E., Fagenholz P. J., Bouletreau P. J., Longaker M. T. Regional differentiation of cranial suture-associated dura mater in vivo and in vitro: implications for suture fusion and patency. J Bone Miner Res. 2000 Dec;15(12):2413–2430. doi: 10.1359/jbmr.2000.15.12.2413. [DOI] [PubMed] [Google Scholar]
  7. Holland L. Z., Holland N. D. Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate? J Anat. 2001 Jul-Aug;199(Pt 1-2):85–98. doi: 10.1046/j.1469-7580.2001.19910085.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Howard T. D., Paznekas W. A., Green E. D., Chiang L. C., Ma N., Ortiz de Luna R. I., Garcia Delgado C., Gonzalez-Ramos M., Kline A. D., Jabs E. W. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet. 1997 Jan;15(1):36–41. doi: 10.1038/ng0197-36. [DOI] [PubMed] [Google Scholar]
  9. Hunt P., Gulisano M., Cook M., Sham M. H., Faiella A., Wilkinson D., Boncinelli E., Krumlauf R. A distinct Hox code for the branchial region of the vertebrate head. Nature. 1991 Oct 31;353(6347):861–864. doi: 10.1038/353861a0. [DOI] [PubMed] [Google Scholar]
  10. Iseki S., Wilkie A. O., Heath J. K., Ishimaru T., Eto K., Morriss-Kay G. M. Fgfr2 and osteopontin domains in the developing skull vault are mutually exclusive and can be altered by locally applied FGF2. Development. 1997 Sep;124(17):3375–3384. doi: 10.1242/dev.124.17.3375. [DOI] [PubMed] [Google Scholar]
  11. Iseki S., Wilkie A. O., Morriss-Kay G. M. Fgfr1 and Fgfr2 have distinct differentiation- and proliferation-related roles in the developing mouse skull vault. Development. 1999 Dec;126(24):5611–5620. doi: 10.1242/dev.126.24.5611. [DOI] [PubMed] [Google Scholar]
  12. Jabs E. W., Müller U., Li X., Ma L., Luo W., Haworth I. S., Klisak I., Sparkes R., Warman M. L., Mulliken J. B. A mutation in the homeodomain of the human MSX2 gene in a family affected with autosomal dominant craniosynostosis. Cell. 1993 Nov 5;75(3):443–450. doi: 10.1016/0092-8674(93)90379-5. [DOI] [PubMed] [Google Scholar]
  13. Jiang X., Rowitch D. H., Soriano P., McMahon A. P., Sucov H. M. Fate of the mammalian cardiac neural crest. Development. 2000 Apr;127(8):1607–1616. doi: 10.1242/dev.127.8.1607. [DOI] [PubMed] [Google Scholar]
  14. Johnson D., Iseki S., Wilkie A. O., Morriss-Kay G. M. Expression patterns of Twist and Fgfr1, -2 and -3 in the developing mouse coronal suture suggest a key role for twist in suture initiation and biogenesis. Mech Dev. 2000 Mar 1;91(1-2):341–345. doi: 10.1016/s0925-4773(99)00278-6. [DOI] [PubMed] [Google Scholar]
  15. Kim H. J., Rice D. P., Kettunen P. J., Thesleff I. FGF-, BMP- and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development. Development. 1998 Apr;125(7):1241–1251. doi: 10.1242/dev.125.7.1241. [DOI] [PubMed] [Google Scholar]
  16. Kimmel C. B., Miller C. T., Keynes R. J. Neural crest patterning and the evolution of the jaw. J Anat. 2001 Jul-Aug;199(Pt 1-2):105–120. doi: 10.1046/j.1469-7580.2001.19910105.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R. T., Gao Y. H., Inada M. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997 May 30;89(5):755–764. doi: 10.1016/s0092-8674(00)80258-5. [DOI] [PubMed] [Google Scholar]
  18. Köntges G., Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996 Oct;122(10):3229–3242. doi: 10.1242/dev.122.10.3229. [DOI] [PubMed] [Google Scholar]
  19. Le Douarin N. A biological cell labeling technique and its use in expermental embryology. Dev Biol. 1973 Jan;30(1):217–222. doi: 10.1016/0012-1606(73)90061-4. [DOI] [PubMed] [Google Scholar]
  20. Mavrogiannis L. A., Antonopoulou I., Baxová A., Kutílek S., Kim C. A., Sugayama S. M., Salamanca A., Wall S. A., Morriss-Kay G. M., Wilkie A. O. Haploinsufficiency of the human homeobox gene ALX4 causes skull ossification defects. Nat Genet. 2001 Jan;27(1):17–18. doi: 10.1038/83703. [DOI] [PubMed] [Google Scholar]
  21. Meinhardt H. Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol. 1983 Apr;96(2):375–385. doi: 10.1016/0012-1606(83)90175-6. [DOI] [PubMed] [Google Scholar]
  22. Morriss-Kay G. M. Growth and development of pattern in the cranial neural epithelium of rat embryos during neurulation. J Embryol Exp Morphol. 1981 Oct;65 (Suppl):225–241. [PubMed] [Google Scholar]
  23. Muenke M., Gripp K. W., McDonald-McGinn D. M., Gaudenz K., Whitaker L. A., Bartlett S. P., Markowitz R. I., Robin N. H., Nwokoro N., Mulvihill J. J. A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome. Am J Hum Genet. 1997 Mar;60(3):555–564. [PMC free article] [PubMed] [Google Scholar]
  24. Noden D. M. Interactions and fates of avian craniofacial mesenchyme. Development. 1988;103 (Suppl):121–140. doi: 10.1242/dev.103.Supplement.121. [DOI] [PubMed] [Google Scholar]
  25. Opperman L. A., Sweeney T. M., Redmon J., Persing J. A., Ogle R. C. Tissue interactions with underlying dura mater inhibit osseous obliteration of developing cranial sutures. Dev Dyn. 1993 Dec;198(4):312–322. doi: 10.1002/aja.1001980408. [DOI] [PubMed] [Google Scholar]
  26. Ornitz D. M. Regulation of chondrocyte growth and differentiation by fibroblast growth factor receptor 3. Novartis Found Symp. 2001;232:63-76; discussion 76-80, 272-82. doi: 10.1002/0470846658.ch6. [DOI] [PubMed] [Google Scholar]
  27. Osumi-Yamashita N., Ninomiya Y., Doi H., Eto K. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev Biol. 1994 Aug;164(2):409–419. doi: 10.1006/dbio.1994.1211. [DOI] [PubMed] [Google Scholar]
  28. Rice D. P., Aberg T., Chan Y., Tang Z., Kettunen P. J., Pakarinen L., Maxson R. E., Thesleff I. Integration of FGF and TWIST in calvarial bone and suture development. Development. 2000 May;127(9):1845–1855. doi: 10.1242/dev.127.9.1845. [DOI] [PubMed] [Google Scholar]
  29. Rousseau F., Bonaventure J., Legeai-Mallet L., Pelet A., Rozet J. M., Maroteaux P., Le Merrer M., Munnich A. Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature. 1994 Sep 15;371(6494):252–254. doi: 10.1038/371252a0. [DOI] [PubMed] [Google Scholar]
  30. Sansom I. J., Smith M. P., Armstrong H. A., Smith M. M. Presence of the earliest vertebrate hard tissue in conodonts. Science. 1992 May 29;256(5061):1308–1311. doi: 10.1126/science.1598573. [DOI] [PubMed] [Google Scholar]
  31. Serbedzija G. N., Bronner-Fraser M., Fraser S. E. Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development. 1992 Oct;116(2):297–307. doi: 10.1242/dev.116.2.297. [DOI] [PubMed] [Google Scholar]
  32. Shiang R., Thompson L. M., Zhu Y. Z., Church D. M., Fielder T. J., Bocian M., Winokur S. T., Wasmuth J. J. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell. 1994 Jul 29;78(2):335–342. doi: 10.1016/0092-8674(94)90302-6. [DOI] [PubMed] [Google Scholar]
  33. Tan S. S., Morriss-Kay G. M. Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimaeras. J Embryol Exp Morphol. 1986 Nov;98:21–58. [PubMed] [Google Scholar]
  34. Tan S. S., Morriss-Kay G. The development and distribution of the cranial neural crest in the rat embryo. Cell Tissue Res. 1985;240(2):403–416. doi: 10.1007/BF00222353. [DOI] [PubMed] [Google Scholar]
  35. Wilkie A. O. Craniosynostosis: genes and mechanisms. Hum Mol Genet. 1997;6(10):1647–1656. doi: 10.1093/hmg/6.10.1647. [DOI] [PubMed] [Google Scholar]
  36. Wilkie A. O., Tang Z., Elanko N., Walsh S., Twigg S. R., Hurst J. A., Wall S. A., Chrzanowska K. H., Maxson R. E., Jr Functional haploinsufficiency of the human homeobox gene MSX2 causes defects in skull ossification. Nat Genet. 2000 Apr;24(4):387–390. doi: 10.1038/74224. [DOI] [PubMed] [Google Scholar]
  37. Zhou Y. X., Xu X., Chen L., Li C., Brodie S. G., Deng C. X. A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum Mol Genet. 2000 Aug 12;9(13):2001–2008. doi: 10.1093/hmg/9.13.2001. [DOI] [PubMed] [Google Scholar]
  38. el Ghouzzi V., Le Merrer M., Perrin-Schmitt F., Lajeunie E., Benit P., Renier D., Bourgeois P., Bolcato-Bellemin A. L., Munnich A., Bonaventure J. Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat Genet. 1997 Jan;15(1):42–46. doi: 10.1038/ng0197-42. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES