Development of the carapacial ridge: Implications for the evolution of genetic networks in turtle shell development

Evolution and Development

Volumn 10, Issue 1, 2008, Pages 29-36

  Moustakas, Jacqueline E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PAIRED BOX TRANSCRIPTION FACTOR; PAX1 TRANSCRIPTION FACTOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

BIOLOGICAL DEVELOPMENT; BONE; EVOLUTION; GENETICS; MORPHOLOGY; PALEONTOLOGY; SHELL; TURTLE;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BONE DEVELOPMENT; CYTOLOGY; EMBRYO DEVELOPMENT; EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; METABOLISM; PRENATAL DEVELOPMENT; SOMITE; TURTLE;

ANIMALS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EVOLUTION; EXTREMITIES; GENE EXPRESSION PROFILING; HEDGEHOG PROTEINS; OSTEOGENESIS; PAIRED BOX TRANSCRIPTION FACTORS; SOMITES; TURTLES;

ALLIGATOR; ARMADILLO; CROCODYLIDAE (ALL CROCODILES); DASYPODIDAE; TESTUDINES; VERTEBRATA;

EID: 37749010301     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2007.00210.x     Document Type: Article

References (68)

1. Bardot, B., Lecoin, L., Huillard, E., Calothy, G. Marx, M. 2001. Expression of the drm/gremlin gene during chicken embryonic development. Mech. Dev. 101 : 263 265.
2. Burke, A. C. 1989. Development of the turtle carapace: implications for the evolution of a novel bauplan. J. Morphol. 199 : 363 378.
3. Burke, A. C. 1991. The development and evolution of the turtle body plan: inferring intrinsic aspects of the evolutionary process from experimental embryology. Am. Zool. 31 : 616 627.
4. Capdevila, J., Tsukui, T., Esteban, C. R., Zappavigna, V. Izpisua-Belmonte, J. C. 1999. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell 4 : 839 849.
5. Carroll, R. L. 1988. Vertebrate Paleontology and Evolution. W.H. Freeman & Company, New York.
6. Cebra-Thomas, J., et al. 2005. How the turtle forms its shell: a paracrine hypothesis of carapace formation. J. Exp. Zool. B (Mol. Dev. Evol.) 304 : 558 569.
7. Cebra-Thomas, J. A., Betters, E., Yin, M., Plafkin, C., McDow, K. Gilbert, S. F. 2007. Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evol. Dev. 9 : 267 277.
8. Chiang, C., et al. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 : 407 413.
9. Christ, B., Huang, R. Scaal, M. 2004. Formation and differentiation of the avian sclerotome. Anat. Embryol. 208 : 333 350.
10. Couly, G. F., Coltey, P. M. Le Douarin, N. 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117 : 409 429.
11. Deutsch, U., Dressler, G. R. Gruss, P. 1988. Pax 1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53 : 617 625.
12. Echelard, Y., et al. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75 : 1417 1430.
13. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 : 783 791.
14. Francis, P. H., Richardson, M. K., Brickell, P. M. Tickle, C. 1994. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120 : 209 218.
15. Fuchtbauer, E.-M. 1995. Expression of M-Twist during postimplantation development of the mouse. Dev. Dyn. 204 : 316 322.
16. Gaffney, E. S., Hutchison, J. H., Jenkins, F. A. Meeker, L. J. 1987. Modern turtle origins: the oldest known cryptodire. Science 237 : 289 291.
17. Goulding, M., Lumsden, A. Paquette, A. 1994. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120 : 957 971.
18. Gross, J. B. Hanken, J. 2005. Cranial neural crest contributes to the bony skull vault in adult Xenopus laevis: insights from cell labeling studies. J. Exp. Zool. B (Mol. Dev. Evol.) 304 : 169 176.
19. Hebrok, M., Fuchtbauer, A. Huchtbauer, E.-M. 1997. Repression of muscle-specific gene activation by the murine Twist protein. Exp. Cell Res. 232 : 295 303.
20. Hsu, D. R., Economides, A. N., Wang, X., Eimon, P. M. Harland, R. M. 1998. The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1 : 673 683.
21. Huang, L.-F., Fukai, N., Selby, P. B., Olsen, B. R. Mundlos, S. 1997. Mouse clavicular development: analysis of wild-type and cleidocranial dysplasia mutant mice. Dev. Dyn. 210 : 33 40.
22. Huang, R., Zhi, Q., Patel, K., Wilting, J. Christ, B. 2000. Dual origin and segmental organisation of the avian scapula. Development 127 : 3789 3794.
23. Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M. Morriss-Kay, G. M. 2002. Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241 : 106 116.
24. Johnson, R. L., Laufer, E., Riddle, R. D. Tabin, C. 1994. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79 : 1165 1173.
25. Khokha, M. K., Hsu, D., Brunet, L. J., Dionne, M. S. Harland, R. M. 2003. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat. Genet. 34 : 303 307.
26. Krauss, S., Concordet, J.-P. Ingham, P. W. 1993. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75 : 1431 1444.
27. Kuraku, S., Usuda, R. Kuratani, S. 2005. Comprehensive survey of carapacial ridge specific genes in turtle implies co-option of some regulatory genes in carapace evolution. Evol. Dev. 7 : 3 17.
28. Lallemand, Y., Nicola, M.-A., Ramos, C., Bach, A., Cloment, C. S. Robert, B. 2005. Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development 132 : 3003 3014.
29. Lee, M. S. Y. 1997. Pareiasaur phylogeny and the origin of turtles. Zool. J. Linn. Soc. 120 : 197 280.
30. Lescher, B., Haenig, B. Kispert, A. 1998. sFRP-2 is a target of the Wnt-4 signaling pathway in the developing metanephric kidney. Dev. Dyn. 213 : 440 451.
31. Li, L., Cserjesi, P. Olson, E. N. 1995. Dermo-1: a novel Twist-related bHLH protein expressed in the developing dermis. Dev. Biol. 172 : 280 292.
32. Lillie, R. D. 1965. Histopathologic Technic and Practical Histochemistry. McGraw-Hill, New York.
33. Loredo, G. A., et al. 2001. Development of an evolutionarily novel structure: fibroblast growth factor expression in the carapacial ridge of turtle embryos. J. Exp. Zool. 291 : 274 281.
34. Martin, G. R. 1998. The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12 : 1571 1586.
35. Merino, R., Rodriguez-Leon, J., Macias, D., Ganan, Y., Economides, A. N. Hurle, J. M. 1999. The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126 : 5515 5522.
36. Nagashima, H., Kuraku, S., Uchida, K., Ohya, Y. K., Narita, Y. Kuratani, S. 2007. On the carapacial ridge in turtle embryos: its developmental origin, function and the chelonian body plan. Development 134 : 2219 2226.
37. Olivera-Martinez, I., Missier, S., Fraboulet, S., Thelu, J. Dhouailly, D. 2002. Differential regulation of the chick dorsal thoracic dermal progenitors from the medial dermomyotome. Development 129 : 4763 4772.
38. Pearce, J. J. H., Penny, G. Rossant, J. 1999. A mouse Cerberus/Dan-related gene family. Dev. Biol. 209 : 98 110.
39. Peters, H., Doll, U. Niessing, J. 1995. Differential expression of the chicken Pax-1 and Pax-9 gene: in situ hybridization and immunohistochemical analysis. Dev. Dyn. 203 : 1 16.
40. Pizette, S., Abate-Shen, C. Niswander, L. 2001. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 128 : 4463 4474.
41. Pizette, S. Niswander, L. 1999. BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126 : 883 894.
42. Presnell, J. K. Schreibman, M. P. 1997. Humason's Animal Tissue Techniques. The Johns Hopkins University Press, Baltimore.
43. Rambaut, A 1996. Se-Al, Sequence Alignment Editor. Version 1.0 alpha 1. University of Oxford, Oxford, U.K.
44. Riddle, R. D., Johnson, R. L., Laufer, E. Tabin, C. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75 : 1401 1416.
45. Rieppel, O. Reisz, R. R. 1999. The origin and early evolution of turtles. Annu. Rev. Ecol. Syst. 30 : 1 22.
46. Rodrigo, I., Hill, R. E., Balling, R., Munsterberg, A. Imai, K. 2003. Pax1 and Pax9 activate Bapx1 to induce chondrogenic differentiation in the sclerotome. Development 130 : 473 482.
47. Roelink, H., et al. 1994. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76 : 761 775.
48. Romer, A. S. 1956. Osteology of the Reptiles. University of Chicago Press, Chicago.
49. Ros, M. A., Lyons, G., Kosher, R. A., Upholt, W. B., Coelho, C. N. D. Fallon, J. F. 1992. Apical ridge dependent and independent mesodermal domains of GHox-7 and GHox-8 expression in chick limb buds. Development 116 : 811 818.
50. Ruckes, H. 1929. The morphological relationships between the girdles, ribs and carapace. Ann. NY. Acad. Sci. 31 : 81 120.
51. Ruiz i Altaba, A., Jessell, T. M. Roelink, H. 1995. Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos. Mol. Cell. Neurosci. 6 : 106 121.
52. Saitou, N. Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 : 406 425.
53. Scaal, M. Christ, B. 2004. Formation and differentiation of the avian dermomyotome. Anat. Embryol. 208 : 411 424.
54. Selever, J., Liu, W., Lu, M.-F., Behringer, R. R. Martin, J. F. 2004. Bmp4 in limb bud mesoderm regulates digit pattern by controlling AER development. Dev. Biol. 276 : 268 279.
55. Sive, H. L., Grainger, R. M. Harland, R. M. 2000. Early Development of Xenopus laevis: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
56. Smith, M. M. Hall, B. K. 1990. Developmental and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65 : 277 374.
57. Smith, M. M. Hall, B. K. 1993. A developmental model for evolution of the vertebrate exoskeleton and teeth: role of cranial and trunk neural crest. Evol. Biol. 27 : 387 448.
58. Smith, M. M., Hickman, A., Amanze, D., Lumsden, A. Thorogood, P. 1994. Trunk neural crest origin of caudal fin mesenchyme in the zebrafish Brachydanio rerio. Proc. R. Soc. Lond. B 256 : 137 145.
59. Sun, J., et al. 2006. BMP4 activation and secretion are negatively regulated by an intracellular Gremlin-BMP4 interaction. J. Biol. Chem. 281 : 29349 29356.
60. *and Other Methods). Version 4.0 Beta 10. Sinauer Associates, Sunderland, MA.
61. Tajbakhsh, S., Rocancourt, D., Cossu, G. Buckingham, M. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89 : 127 138.
62. Tavares, A. T., Izpisua-Belmonte, J. C. Rodriguez-Leon, J. 2001. Developmental expression of chick Twist and its regulation during limb patterning. Int. J. Dev. Biol. 45 : 707 713.
63. Vincent, C., Bontoux, M., Le Douarin, N. M., Pieau, C. Monsoro-Burq, A.-H. 2003. Msx genes are expressed in the carapacial ridge of turtle shell: a study of the European pond turtle, Emys orbicularis. Dev. Genes Evol. 213 : 464 469.
64. Williams, B. A. Ordahl, C. P. 1994. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120 : 785 796.
65. Wright, E., et al. 1995. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat. Genet. 9 : 15 20.
66. Yntema, C. L. 1968. A series of stages in the embryonic development of Chelydra serpentina. J. Morphol. 125 : 219 252.
67. Yntema, C. L. 1970. Extirpation experiments on the embryonic rudiments of the carapace of Chelydra serpentina. J. Morphol. 132 : 235 244.
68. Zuniga, A., Haramis, A.-P. G., McMahon, A. P. Zeller, R. 1999. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limbs. Nature 401 : 598 602.