Developmental origins of precocial forelimbs in marsupial neonates

Development

Volumn 137, Issue 24, 2010, Pages 4283-4294

  Keyte, Anna L ^a   Smith, Kathleen K ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Gastrulation; Heterochrony; Heterotopy; Limb field

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX4; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL COUNT; CELL MIGRATION; CELL SIZE; CONTROLLED STUDY; EMBRYO; FORELIMB; GASTRULATION; GENE EXPRESSION; HINDLIMB; HOX GENE; LIMB DEVELOPMENT; LIMB MOVEMENT; MARSUPIAL; MOUSE; MUSCLE CELL; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OPOSSUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL NERVE;

ANIMALS; ANIMALS, NEWBORN; FORELIMB; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; MARSUPIALIA;

AMNIOTA; DIDELPHIDAE; EUTHERIA; MAMMALIA; METATHERIA;

EID: 78650215490     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.049445     Document Type: Article

References (74)

1. Agarwal, P., Wylie, J. N., Galceran, J., Arkhitko, O., Li, C., Deng, C., Grosschedl, R. and Bruneau, B. G. (2003). Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 130, 623-633.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Bellairs, R. and Osmund, M. (1998). The Atlas of Chick Development. San Diego: Academic Press.
4. Bininda-Emonds, O. R. P., Jeffery, J. E. and Richardson, M. K. (2003). Is sequence heterochrony an important evolutionary mechanism in mammals? J. Mammal. Evol. 10, 335-361.
5. Bininda-Emonds, O. R. P., Jeffery, J. E., Sanchez-Villagra, M. R., Hanken, J., Colbert, M., Pieau, C., Selwood, L., ten Cate, C., Raynaud, A., Osabutey, C. K. et al. (2007). Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evol. Biol. 7, 182.
6. Blechschmidt, E. (1961). The Stages of Human Development Before Birth: an Introduction to Human Embryology. Philadelphia: W. B. Saunders.
7. Bober, E., Franz, T., Arnold, H. H., Gruss, P. and Tremblay, P. (1994). Pax-3 is required for the development of limb muscles-a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120, 603-612.
8. Boulet, A. M., Moon, A. M., Arenkiel, B. R. and Capecchi, M. R. (2004). The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev. Biol. 273, 361-372.
9. Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Hox genes and the evolution of vertebrate axial morphology. Development 121, 333-346.
10. Capdevila, J. and Belmonte, J. C. I. (2001). Patterning mechanisms controlling vertebrate limb development. Annu. Rev. Cell Dev. Biol. 17, 87-132.
11. Chan, A. O. K., Dong, M., Wang, L. and Chan, W. Y. (2004). Somite as a morphological reference for staging and axial levels of developing structures in mouse embryos. Neuroembryol. Aging 3, 102-110.
12. Charite, J., McFadden, D. G. and Olson, E. N. (2000). The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of the zone of polarizing activity during limb development. Development 127, 2461-2470.
13. Cohn, M. J. and Tickle, C. (1999). Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474-479.
14. Crossley, P. H., Minowada, G., MacArthur, C. A. and Martin, G. R. (1996). Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84, 127-136.
15. de Maximy, A. A., Nakatake, Y., Moncada, S., Itoh, N., Thiery, J. P. and Bellusci, S. (1999). Cloning and expression pattern of a mouse homologue of drosophila sprouty in the mouse embryo. Mech. Dev. 81, 213-216.
16. 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.
17. Fernandez-Teran, M., Piedra, M. E., Simandl, B. K., Fallon, J. F. and Ros, M. A. (1997). Limb initiation and development is normal in the absence of the mesonephros. Dev. Biol. 189, 246-255.
18. Geduspan, J. S. and Solursh, M. (1992). A growth-promoting influence from the mesonephros during limb outgrowth. Dev. Biol. 151, 242-250.
19. Gemmell, R. T., Veitch, C. and Nelson, J. (2002). Birth in marsupials. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131, 621-630.
20. Gibert, Y., Gajewski, A., Meyer, A. and Begemann, G. (2006). Induction and prepatterning of the zebrafish pectoral fin bud requires axial retinoic acid signaling. Development 133, 2649-2659.
21. Gibson-Brown, J. J., Agulnik, S. I., Chapman, D. L., Alexiou, M., Garvey, N., Silver, L. M. and Papaioannou, V. E. (1996). Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech. Dev. 56, 93-101.
22. Gibson-Brown, J. J., Agulnik, S. I., Silver, L. M., Niswander, L. and Papaioannou, V. E. (1998). Involvement of T-box genes Tbx2-Tbx5 in vertebrate limb specification and development. Development 125, 2499-2509.
23. Goulding, M. D., Chalepakis, G., Deutsch, U., Erselius, J. R. and Gruss, P. (1991). Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J. 10, 1135-1147.
24. Harris, W. (1939). The Morphology of the Brachial Plexus. London: Oxford University Press.
25. Hayashi, K. and Ozawa, E. (1995). Myogenic cell migration from somites is induced by tissue contact with medial region of the presumptive limb mesoderm in chick embryos. Development 121, 661-669.
26. Hill, J. P. and Hill, W. C. O. (1955). The growth stages of the pouch young of the native cat (Dasyurus viverrinus) together with observations on the anatomy of the new born young. Trans. Zool. Soc. London. 28, 349-453.
27. Iimura, T. and Pourquie, O. (2006). Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442, 568-571.
28. Kaufman, M. H. (1992). The Atlas of Mouse Development. San Diego: Academic Press.
29. Keyte, A. L. and Smith, K. K. (2009). Opossum (Monodelphis domestica): a marsupial developmental model. In Emerging Model Organisms: a Laboratory Manual, Vol. 1 (ed. D. A. Crotty and A. Gann), pp. 557-576. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
30. Khan, P., Linkhart, B. and Simon, H. G. (2002). Different regulation of T-box genes Tbx4 and Tbx5 during limb development and limb regeneration. Dev. Biol. 250, 383-392.
31. Klima, M. and Bangma, G. C. (1987). Unpublished drawings of marsupial embryos from the Hill collection and some problems of marsupial ontongeny. Zeitschrift für Saugetierkunde 52, 201-211.
32. Komuro, I. and Izumo, S. (1993). Csx: a murine homeobox-containing gene specifically expressed in the developing heart. Proc. Natl. Acad. Sci. USA 90, 8145-8149.
33. Lanctot, C., Lamolet, B. and Drouin, J. (1997). The bicoid-related homeoprotein Ptx1 defines the most anterior domain of the embryo and differentiates posterior from anterior lateral mesoderm. Development 124, 2807-2817.
34. Lints, T. J., Parsons, L. M., Hartley, L., Lyons, I. and Harvey, R. P. (1993). Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119, 419-431.
35. Logan, M. (2003). Finger or toe: the molecular basis of limb identity. Development 130, 6401-6410.
36. Logan, M. and Tabin, C. J. (1999). Role of Pitx1 upstream of Tbx4 in specification of hindlimb identity. Science 283, 1736-1739.
37. Logan, M., Simon, H. G. and Tabin, C. (1998). Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity. Development 125, 2825-2835.
38. Mahmood, R., Bresnick, J., Hornbruch, A., Mahony, C., Morton, N., Colquhoun, K., Martin, P., Lumsden, A., Dickson, C. and Mason, I. (1995). A role for Fgf-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
39. Martin, G. R. (1998). The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12, 1571-1586.
40. Mate, K. E., Robinson, E. S., VandeBerg, J. L. and Pedersen, R. A. (1994). Timetable of in vivo embryonic development in the grey short-tailed opossum (Monodelphis domestica). Mol. Reprod. Dev. 39, 365-374.
41. McCrady, E. (1938). The Embryology of the Opossum. Philadelphia: Wistar Institute of Anatomy and Biology.
42. Mic, F. A., Sirbu, I. O. and Duester, G. (2004). Retinoic acid synthesis controlled by Raldh2 is required early for limb bud initiation and then later as a proximodistal signal during apical ectodermal ridge formation. J. Biol. Chem. 279, 26698-26706.
43. Müller, F. (1967). Zum Vergleich der Ontogenesen von Didelphis virginiana und Mesocricetus auratus. Revue Suisse de Zoologie 74, 607-613.
44. Naiche, L. A. and Papaioannou, V. E. (2003). Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130, 2681-2693.
45. Nakao, T. and Ishizawa, A. (1994). Development of the spinal nerves in the mouse with special reference to innervation of the axial musculature. Anat. Embryol. (Berl.) 189, 115-138.
46. Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P. and Dolle, P. (2002). Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 129, 3563-3574.
47. Ohuchi, H., Nakagawa, T., Yamamoto, A., Araga, A., Ohata, T., Ishimaru, Y., Yoshioka, H., Kuwana, T., Nohno, T., Yamasaki, M. et al. (1997). The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124, 2235-2244.
48. Patten, B. M. (1948). Embryology of the Pig. New York: McGraw-Hill.
49. Rancourt, D. E., Tsuzuki, T. and Capecchi, M. R. (1995). Genetic interaction between hoxb-5 and hoxb-6 is revealed by nonallelic noncomplementation. Genes Dev. 9, 108-122.
50. Saito, D., Yonei-Tamura, S., Takahashi, Y. and Tamura, K. (2006). Level-specific role of paraxial mesoderm in regulation of Tbx5/Tbx4 expression and limb initiation. Dev. Biol. 292, 79-89.
51. Sears, K. E. (2009). Differences in the timing of prechondrogenic limb development in mammals: the marsupial-placental dichotomy resolved. Evolution 68, 2193-2200.
52. Sharpe, P. T., Miller, J. R., Evans, E. P., Burtenshaw, M. D. and Gaunt, S. J. (1988). Isolation and expression of a new mouse homeobox gene. Development 102, 397-407.
53. Smith, K. K. (1994). Development of craniofacial musculature in Monodelphis domestica (Marsupialia, Didelphidae). J. Morphol. 222, 149-173.
54. Smith, K. K. (1997). Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51, 1663-1678.
55. Smith, K. K. (2001). Heterochrony revisited: the evolution of developmental sequences. Biol. J. Linn. Soc. 73, 169-186.
56. Smith, K. K. (2006). Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Dev. Dyn. 235, 1181-1193.
57. Sporle, R. and Schughart, K. (1997). System to identify individual somites and their derivatives in the developing mouse embryo. Dev. Dyn. 210, 216-226.
58. Stephens, T. D. and McNulty, T. R. (1981). Evidence for a metameric pattern in the development of the chick humerus. J. Embryol. Exp. Morphol. 61, 191-205.
59. Strecker, T. R. and Stephens, T. D. (1983). Peripheral-nerves do not play a trophic role in limb skeletal morphogenesis. Teratology 27, 159-167.
60. Szeto, D. P., Ryan, A. K., O'Connell, S. M. and Rosenfeld, M. G. (1996). P-OTX: a PIT-1-interacting homeodomain factor expressed during anterior pituitary gland development. Proc. Natl. Acad. Sci. USA 93, 7706-7710.
61. Takeuchi, J. K., Koshiba-Takeuchi, K., Matsumoto, K., Vogel-Hopker, A., Naitoh-Matsuo, M., Ogura, K., Takahashi, N., Yasuda, K. and Ogura, T. (1999). Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds. Nature 398, 810-814.
62. Takeuchi, J. K., Koshiba-Takeuchi, K., Suzuki, T., Kamimura, M., Ogura, K. and Ogura, T. (2003). Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development 130, 2729-2739.
63. Tamura, K., Yonei-Tamura, S. and Belmonte, J. C. (1999). Differential expression of Tbx4 and Tbx5 in Zebrafish fin buds. Mech. Dev. 87, 181-184.
64. Tanaka, M., Munsterberg, A., Anderson, W. G., Prescott, A. R., Hazon, N. and Tickle, C. (2002). Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 416, 527-531.
65. Theiler, K. (1989). The House Mouse - Atlas of Embryonic Development. New York: Springer.
66. Turney, B. W., Rowan-Hull, A. M. and Brown, J. M. (2003). The innervation of FGF-induced additional limbs in the chick embryo. J. Anat. 202, 83-92.
67. Tyndale-Biscoe, H. (2005). Life of Marsupials. Collingwood: CSIRO Publishing.
68. Vogel, A., Rodriguez, C. and IzpisuaBelmonte, J. C. (1996). Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122, 1737-1750.
69. Wall, N. A., Jones, C. M., Hogan, B. L. and Wright, C. V. (1992). Expression and modification of Hox 2.1 protein in mouse embryos. Mech. Dev. 37, 111-120.
70. Wanek, N., Muneoka, K., Holler-Dinsmore, G., Burton, R. and Bryant, S. V. (1989). A staging system for mouse limb development. J. Exp. Zool. 249, 41-49.
71. Weisbecker, V., Goswami, A., Wroe, S. and Sanchez-Villagra, M. R. (2008). Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62, 2027-2041.
72. Xu, X., Weinstein, M., Li, C., Naski, M., Cohen, R. I., Ornitz, D. M., Leder, P. and Deng, C. (1998). Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125, 753-765.
73. Yamasaki, M., Miyake, A., Tagashira, S. and Itoh, N. (1996). Structure and expression of the rat mRNA encoding a novel member of the fibroblast growth factor family. J. Biol. Chem. 271, 15918-15921.
74. Zhao, X., Sirbu, I. O., Mic, F. A., Molotkova, N., Molotkov, A., Kumar, S. and Duester, G. (2009). Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 19, 1050-1057.