Late-emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron
Version of Record online: 6 SEP 2013
Copyright © 2013 Wiley Periodicals, Inc.
Volume 242, Issue 11, pages 1223–1235, November 2013
How to Cite
Cebra-Thomas, J. A., Terrell, A., Branyan, K., Shah, S., Rice, R., Gyi, L., Yin, M., Hu, Y., Mangat, G., Simonet, J., Betters, E. and Gilbert, S. F. (2013), Late-emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron. Dev. Dyn., 242: 1223–1235. doi: 10.1002/dvdy.24018
- Issue online: 23 OCT 2013
- Version of Record online: 6 SEP 2013
- Accepted manuscript online: 31 JUL 2013 10:44AM EST
- Manuscript Accepted: 3 JUL 2013
- Manuscript Revised: 13 JUN 2013
- Manuscript Received: 8 JAN 2013
- National Science Foundation. Grant Number: RUI-0748508
- 2005. Chondrogenic potential of mouse calvarial mesenchyme. J Histochem Cytochem 53:653–663. , , , , .
- 2003. Dissimilar regulation of cell differentiation in mesencephalic (cranial) and sacral (trunk) neural crest cells in vitro. Development 130:4567–4579. , , , .
- 2005. Early steps in neural crest specification. Semin Cell Dev Biol 16:642–646. , .
- 2001. Developmental roles of platelet-derived growth factors. Bioessays 23:494–507. , , .
- 2010. Analysis of early human neural crest development. Dev Biol 344:578–592. , , , , .
- 1986. Analysis of the early stages of trunk neural crest cell migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115:44–55. .
- 2007. Sonic hedgehog promotes the development of multipotent neural crest progenitiors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci U S A 104:19879–19884. , , , .
- 2005. How the turtle forms its shell: a paracrine hypothesis of carapace formation. J Exp Zool 304B:558–569. , , , , , , , .
- 2007. Evidence that a late-emerging population of trunk neural crest cells forms the plastron in the turtle Trachemys scripta. Evol Dev 9:268–278. , , , , , .
- 1997. The origin of the bony shell of turtles as a unique evolutionary model in reptiles. Russ J Herpetol 4:155–122. .
- 2005. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8:179–192. , , , , , .
- 2002. HNK-1 sulfotransferase null mice express glucuronyl gycoconjugates and show normal cerebellar granule neuron migration in vivo and in vitro. J Neurochem 82:1239–1251. , , .
- 2004. Dinosaur gastralia: origin, morphology, and function. J Vert Paleontol 24:89–106. .
- 2001. Evidence for the neural crest origin of turtle plastron bones. Genesis 31:111–117. , , , , , , , , .
- 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429. , , .
- 1998. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 128:3445–3459. , , , , .
- 2002. Negative effect of Hox gene expression on the development of the neural crest derived facial skeleton. Development 129:4301–4313. , , , .
- 2002. Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 129:1583–1593. , .
- 2008. MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat Genet 40:290–298. , , , , , , , , , .
- 1989. Migratory pathways of HNK-1 immunoreactive neural crest cells in the rat embryo. Dev Biol 134:112–118. , , .
- 1983. A monoclonal antibody specific for the amino terminal cleavage site of procollagen type I. Eur J Biochem 134:183–189. , , , , , .
- 1983. Neural crest and the origin of vertebrates: a new head. Science 220:268–273. , .
- 1898. Vergleichende Anatomie der Wirbeltiere, vol. 2. Leipzig, Germany: Wilhelm Engelmann. .
- 1996. Skeletal myogenesis: the preferred pathway of chick embryo epiblast cells in vitro. Dev Biol 173:279–291. , , , , , , , , , .
- 2001. Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol Dev 3:47–58. , , , .
- Wyneken J, Gofrey MH, Bels V, editors. Biology of turtles. Boca Raton, FL: CRC Press. p 1–16. , , . 2007. How the turtle gets its shell. In:
- 1997. Neural crest potential for tooth development in a urodele amphibian: developmental and evolutionary significance. Dev Biol 188:34–42. , , .
- 2002. A standardized series of embryonic stages for the emydid turtle Trachemys scripta. Can J Zool 80:1350–1370. .
- 2005. Bones and cartilage: developmental and evolutionary skeletal biology. Burlington, MA: Academic Press.
- 2010. The neural crest and neural crest cells in vertebrate development and evolution. New York: Springer Verlag.
- 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49–92. , .
- 2003. Roles of PDGF in animal development. Development 130:4769–4784. , .
- 1986. Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. Arthritis Rheum 29:400–410. , , , , .
- 1999. Effects of local tissue environment on the differentiation of neural crest cells in turtle, with special reference to understanding the spatial distribution of pigment cells. Pigment Cell Res 12:81–88. .
- 1994. Neural crest development in reptilian embryos, studied with monoclonal antibody, HNK-1. Zool Sci 11:423–431. , .
- 2012. Neural crest cells pattern the surface cephalic ectoderm during FEZ formation. Dev Dyn 241:732–740. , .
- 2006. Expression of chondrogenic potential of mouse trunk neural crest cells by FGF2 treatment. Dev Dyn 235:361–367. , .
- 2013. The embryonic transcriptome of the red-eared slider turtle (Trachemys scripta). PLoS One 8:e66357. , , , , , , , , , , , , , ,
- 2012. Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal. Proc Natl Acad Sci U S A 109:14075–14080. , , .
- 2001. The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128:1467–1479. , , , .
- 2011. Evolutionary developmental perspective for the origin of turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge. Evol Dev 13:1–14. , , .
- 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431:696–699. , , .
- 1998. The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mech Dev 76:185–190. , .
- 1982. The neural crest. Cambridge, UK: Cambridge University Press.
- 2012. The neural crest in vertebrate evolution. Curr Opin Genet Dev 22:1–9. , .
- 1974. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol 41:162–184. , .
- 2011. Sox9 function in craniofacial development and disease. Genesis 49:200–208. , .
- 2008. Ancestral turtle from the late Triassic of southwestern China. Nature 456:497–501. , , , , .
- 1987. The neural crest contribution to tooth development in the mammalian embryo. In: Maderson PFA, editor. Developmental and evolutionary aspects of the neural crest. New York: Wiley. p 261–300.
- 1991. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113:1281–1291. , , .
- 2010. Transitional fossils and the origin of turtles. Biol Lett 6:830–833. , , , , .
- 1998. Neural crest specification regulated by the helix-loop-helix repressor Id2. Science 281:988–991. , .
- 2005. Neural crest origins of the neck and shoulder. Nature 436:347–355. , , , , , , , .
- 2008. Development and tissue origins of the mammalian cranial base. Dev Biol 322:121–132. , , , , .
- 2002. Trunk neural crest has skeletogenic potential. Curr Biol 12:767–771. , .
- 2011. MicroCT for molecular imaging: quantitative visualization of complete 3D distributions of gene products in embryonic limbs. Dev Dyn 240:2301–2308. , .
- 2002. Neural expression of mouse Noelin-1/2 and comparison with other vertebrates. Mech Dev 119:121–125. , .
- 1982. Mesectodermal capabilities of the trunk neural crest of birds. J Embryol Exp Morphol 70:1–18. , .
- 2005. Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 307:720–724. , , .
- 1975. An analysis of the migratory behavior of avian cephalic neural crest cells. Dev Biol 42:106–130. .
- 1991. Vertebrate craniofacial development: the relation between ontogenic processes and morphological outcome. Brain Behav Evol 38:190–225. .
- 1992. Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent, cell layers of the mouse embryo. Development 115:1045–1058. , .
- 1868. A monograph on the structure and development of the shoulder-girdle and sternum in the Vertebrata. London: The Ray Society. .
- 2004. Neural beginnings for the turtle's shell. Science 303:951. .
- 1997. Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol 32:722–746. , .
- 1848. Uber die Entwicklung der Schildkroten. Braunschweig: Friederich Vieweg und Sohn. .
- 2008. Locate, condense, differentiate, grow and confront: developmental mechanisms controlling intramembranous bone and suture formation and function. In: Rice DP, editor. Craniofacial sutures. Development, disease, treatment. Front Oral Biol 12:22–40. ,
- 1985. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90:437–455. , , .
- 1996. Testing the homology by congruence: the pectoral girdle of turtles. Proc R Soc Lond B 263:1395–1398. ,
- 1983. Neural crest cell migration: requirements for exogenous fibronection and high cell density. J Cell Biol 96:462–473. , , , , .
- 1990. Distribution and migration pathways of HNK-1 immunoreactive neural crest cells in teleost fish embryos. Development 110:197–209. , .
- 1992. Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116:297–307. , , .
- 1993. A developmental model for evolution of the vertebrate exoskeleton and teeth: the role of cranial and trunk neural crest. Evol Biol 27:387–448. , .
- 1994. Trunk neural crest origin of caudal fin mesenchyme in the zebrafish Brachydanio rerio. Proc R Soc Lond B 256:137–145. , , , , .
- 2006. In vitro formation of enteric neural network structure in a gut-like organ differentiated from mouse embryonic stem cells. Stem Cells 24:1414–1422. , , , , .
- 2003. Cell autonomous requirement for PDGFRalpha in populations of cranial and cardiac neural crest cells. Development 130:507–518. , .
- 2004. In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 13:6141–6151. , .
- 2009. FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136:1849–1858. , .
- 2005. Foxd3 is required in the trophoblast progenitor cell lineage of the mouse embryo. Dev Biol 285:126–137. , , , , .
- 2003. Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol 47:541–553. , , .
- 1984. Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ 14:223–230. , , , , .
- 2006. Homology of the reptilian coracoid and a reappraisal of the evolution and development of the amniote pectoral apparatus. J Anat 208:263–285. , .
- 2010. Comparative development of the crocodylian interclavicle and avian furcula, with comments on the homology of dermal elements in the pectoral apparatus. J Exp Zool B Mol Dev Evol 314:196–207. , .
- 2009. The integumentary skeleton of tetrapods: origin, evolution, and development. J Anat 214:441–464. , .
- 2011. Dual origins of the prechordal cranium in the chicken embryo. Dev Biol 356:529–540. , , .
- 2008. Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 125:797–808. , , , , .
- 1939. The homology of the shell elements in turtles. J Morphol 65:383–409. .
- 1969. The turtle shell. In: Gans C, Bellairs Ad'A, editors. The biology of the reptilia, Vol. 1. New York: Academic Press. p 311–319. .