The limb field mesoderm determines initial limb bud anteroposterior asymmetry and budding independent of sonic hedgehog or apical ectodermal gene expressions

Development

Volumn 122, Issue 8, 1996, Pages 2319-2330

  Ros, Maria A ^a   López Martínez, Alric ^b   Simandl, B Kay ^b   Rodriguez, Concepción ^c   Belmonte, Juan Carlos Izpisúa ^c   Dahn, Randall ^b   Fallon, John F ^b  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Axial influence; Bone morphogenetic proteins; C Lmx1; Dorsoventral compartments; Engrailed 1; Fibroblast growth factors; Herd genes; Limb initiation; Pattern formation; Sonic hedgehog; Wnt 7a

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CHICKEN; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE INDUCTION; LIMB BUD; LIMB DEVELOPMENT; MESODERM; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL MARKERS; CHICK EMBRYO; ECTODERM; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION; GENES, HOMEOBOX; HEDGEHOG PROTEINS; LIMB BUD; MESODERM; PROTEINS; PROTO-ONCOGENE PROTEINS; TRANS-ACTIVATORS; WNT PROTEINS;

ANIMALIA; ERINACEIDAE; GALLUS GALLUS;

EID: 0029790405     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (97)

1. Bhaumick, B. and Bala, R. M. (1987). Receptors for insulin-like growth factors I and II in developing embryonic mouse limb bud. Biochem. Biophys. Acta. 927, 117-128.
2. Carrington, J. L. and Fallon, J. F. (1984a). The stages of flank ectoderm capable of responding to ridge induction in the chick embryo. J. Embryol. Exp. Morphol. 84, 19-34.
3. Carrington, J. L. and Fallon, J. F. (1984b). Evidence that the ectoderm is the affected layer in the wingless mutant chick embryo. J. Exp. Zool. 232, 297-308.
4. Carrington, J. L. and Fallon, J. F. (1986). Experimental manipulation leading to induction of dorsal ectodermal ridges on normal limb buds results in a phenocopy of the Eudiplopodia chick mutant. Dev. Biol 116, 130-137.
5. Carrington, J. L. and Fallon, J. F. (1988). Initial limb budding is independent of apical ectodermal ridge activity: evidence from a limbless mutant. Development 104, 361-367.
6. Chang, D. T., López, A., Von Kessler, D. P., Chang, C., Simandl, B. K., Zhao, R., Selding, M. F., Fallon, J. F. and Beachy, P. A. (1994). Products. genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120, 3339-3353.
7. Coates, M. I. (1993). Ancestors and homology (the origin of the tetrapod limb). Acta Biotheoretica 41, 411-424.
8. Coates, M. I. (1994). The origin of vertebrate limbs. Development Supplement 169-180.
9. Coelho, C. N. D., Krabbenhoft, K. M., Upholt, W. B., Fallon, J. F. and Kosher, R. A. (1991). Altered expression of the chicken homeo-box containing genes GHox-7 and GHox-8 in the limb buds of limbless mutant chick embryos. Development 113, 1487-1493.
10. Cohn, M. J., Izpisúa-Belmonte, J. C., Abud, H., Heath, J. K. and Tickle, C. (1995). Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80, 739-746.
11. Crossley, H. P. and Martin, G. R. (1995). The mouse Fgf-8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
12. Crossley, H. P., 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.
13. Davis, C. A., Holmyard, D. P., Millen, K. J. and Joyner, A. L. (1991). Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111, 287-298.
14. Dealy, C. N., Roth, A., Ferrari, D., Brown, A. M. C. and Kosher, R. A. (1993). Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech. Dev. 43, 175-186.
15. Dealy, C. N. and Kosher, R. A. (1995). Studies on insulin-like growth factor-I and insulin in chick limb morphogenesis. Dev. Dyn. 202, 67-79.
16. Dealy, C. N. and Kosher, R. A. (1996). IGF-1, insulin and FGFs induce outgrowth of the limb buds of amelic mutant chick embryos. Development 122, 1323-1330.
17. Dono, R. and Zeller, R. (1994). Cell type-specific nuclear translocation of fibroblast growth factor-2 isoforms during chicken kidney and limb morphogenesis. Dev. Biol 163, 316-330.
18. Duboule, D. (1994a). Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development Supplement, 135-142.
19. Duboule, D. (1994b). How to make a limb. Science 266, 575-576.
20. Fallon, J. F., Frederick., J. M., Carrington, J. L., Lanser, M. R. and Simandl, B. K. (1983). Studies on a limbless mutant in the chick embryo. In Limb Development and Regeneration, Part A (eds. J. F. Fallon and A. I. Caplan), pp. 33-43, New York: Alan R. Liss.
21. Fallon, J. F., Lopez, A., Ros, M. A., Savage, M., Olwin, B. and Simandl, B. K. (1994). FGF2: apical ectodermal ridge growth signal for the chick limb development. Science 264, 104-107.
22. Francis, P. H., Richardson, M. K., Brickell, P. M. and Tickle, C. (1994). Bone morphogenetic proteins and a signaling pathway that controls patterning in the developing chick limb. Development 120, 209-218.
23. 3) limb buds: their relationships in the signalling cascade involved in limb patterning. Dev. Dyn. 203, 187-197.
24. Gardner, C. A. and Barald, K. F. (1992). Expression patterns of Engrailed-like proteins in the chick embryo. Dev. Dyn. 193, 370-388.
25. Geduspan, J. S. and MacCabe, J. A. (1987). The ectodermal control of mesodermal patterns of differentiation in the developing chick wing. Dev. Biol. 124, 398-408.
26. Geduspan, J. S. and MacCabe, J. A. (1989). Transfer of dorsoventral information from mesoderm to ectoderm at the onset of limb development. Anat. Rec. 224, 79-87.
27. Geduspan, J. S. and Solursh, M. (1992). A growth-promoting influence from the mesonephros during limb outgrowth. Dev. Biol. 151, 242-250.
28. Geduspan, J. S. and Solursh, M. (1993). Effects on the mesonephros and Insulin-like growth factor I on chondrogenesis of limb explants. Dev. Biol. 156, 500-508.
29. Hamburger, V. (1938). Morphogenetic and axial self-differentiation of transplanted limb primordia of 2-day chick embryos. J. Exp. Zool. 77, 379-399.
30. Hamburger, V. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryos. J. Morphol. 88, 49-92.
31. Hardy, A., Richardson, M. K., Francis-West, P. H., Rodriguez, C., Izpisúa-Belmonte, J. C., Duprez, D. and Wolpert, L. (1995). Gene expression, polarizing activity and skeletal patterning in reaggregated hind limb mesenchyme. Development 121, 4329-4337.
32. Harrison, R. G. (1918). Experiments on the development of the fore limb of amblystoma, a self-differentiating equipotential system. J. Exp. Zool. 25, 13-461.
33. Harrison, R. G. (1921) On relations of symmetry in transplanted limbs. J. Exp. Zool. 32, 1-136.
34. Heikinheimo, M., Lawshe, A., Shackleford, G. M., Wilson, D. B. and MacArthur, C. A. (1994). Fgf-8 expression in the post-gastrulation mouse suggest roles in the development of the face, limbs and central nervous system. Mech. Dev. 48, 129-138.
35. Hornbruch, A. and Wolpert, L. (1991). The spatial and temporal distribution of polarizing activity in the flank of the pre-limb-bud stages in the chick embryo. Development 111, 725-31.
36. Izpisúa-Belmonte, J. C., Tickle, C., Dolle, P., Wolpert, L. and Duboule, D. (1991). Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350, 585-589.
37. Izpisúa-Belmonte, J. C., Brown, J. C., Duboule, D. and Tickle, C. (1992). Expression of Hox-4 genes in the chick wing links pattern formation to the epithelial-mesenchymal interactions that mediate growth. EMBO J. 11, 1451-1457.
38. Kieny, M. (1960). Role inducteur du mesoderme dans la différentiation précoce du bourgeon de membre chez l'embryon de Poulet. J. Embryol. Exp. Morphol. 8, 457-467.
39. Kieny, M. (1968). Variation de la capacité inductrice du mésoderme et de la compétence de l'ectoderme au cours de l'induction primaire du bourgeon de membre chez l'embryon de Poulet. Archs d'Anat. micr. Morphol. Exp. 57, 401-418.
40. Kieny, M. (1969). Sur les relations entre le mésoderme somitque et le mésoderme somatopleural avant et al course de l'induction primoire des membres de l'embryon de Poulet. C. R. Acad. Sci. Paris 268, 3183-3186.
41. Kieny, M. (1971). Les phases d'activité morphogène du mésoderme somatopleural pendent de développement précoce du membre chez l'embryon de Poulet. Ann. Embryol. Morphol. 4, 281-298.
42. Krabbenhoft, K. M. and Fallon, J. F. (1989). The formation of leg or wing specific structures by leg bud cells grafted to the wing bud is influenced by proximity to the apical ridge. Dev. Biol. 131, 373-382.
43. Lanser, M. E. and Fallon, J. F. (1984). Development of the lateral motor column in the limbless mutant chick embryo. J. Neurosci. 4, 2043-2050.
44. Laufer, E., Nelson, C., Johson, R. L. Morgan, B. A. and Tabin, C. (1994). Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
45. Lewis, J. H. and Wolpert, L. (1976). The principle of non-equivalence in development. J. Theor. Biol. 62, 479-90.
46. López-Martínez, A., Chang, D. T., Chiang, C., Porter, J. A., Ros, M. A., Simandl, B. K., Beachy, P. A. and Fallon, J. F. (1995). Limb-patterning activity and restricted posterior localization of the amino terminal product of Sonic hedgehog cleavage. Curr. Biol. 5, 791-796.
47. 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 FGF8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
48. Martin, G. R. (1995). Why thumbs are up. Nature 374, 410-411.
49. MacCabe, J. A., Errick, J. and Saunders, J. W. (1974). Ectodermal control of the dorsoventral axis in the leg bud of the chick embryo. Dev. Biol. 39, 69-82.
50. Meinhardt, H. (1983). A boundary model for pattern formation in vertebrate limbs. J. Embryol. Exp. Morphol. 76, 115-137.
51. Mima, T., Ohuchi, H., Noji, S. and Mikawa, T. (1995). FGF can induce outgrowth of somatic mesoderm both inside and outside of limb-forming regions. Dev. Biol. 167, 617-620.
52. Nieto, M. A., Patel, K. and Wilkinson D. G. (1996). In situ analysis of chick embryos in whole mount and tissue sections. In Methods in Cell Biology (ed. M. Bronner-Fraser), vol. 51, pp. 219-235. New York: Academic Press.
53. Niswander, L. and Martin, G. R. (1992). Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755-768.
54. Niswander, L., Tickle, C., Vogel, A., Booth, I. and Martin, G. R. (1993). FGF4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75, 579-587.
55. Niswander, L., Jeffrey, S., Martin, G. R. and Tickle, C. (1994). Positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609-612.
56. Ohuchi, H., Yoshioka, H., Tanaka, H., Kawakami, Y., Nohno, T. and Noji, S. (1994). Involvement of androgen-induced growth factor (FGF8) gene in mouse embryogenesis and morphogenesis. Biochem. Biophys. Res. Com. 204, 882-888.
57. Ohuchi, H., Nakagawa, T., Yamahuchi, M., Ohata, T., Yoshioka, H., Kuwana, T., Mima, T., Mikawa, T., Nohno, T. and Noji, S. (1995). An additional limb can be induced from the flank of the chick embryo by FGF4. Biochem. Biophys. Res. Com. 209, 809-816.
58. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes in mouse limb. Nature 374, 350-353.
59. Pautou, M. P. and Kieny, M. (1973). Interaction ecto-mesodermique dans l'establishment de la polarité dorso-ventrale du pied de l'embryon de poulet. C.r. hebd Séanc. Acad. Sci., Paris D. 277, 1225-1228.
60. Pinot, M. (1970). Le role du mésoderme somitique dans la morphogenèse précoce des membres de l'embryon de Poulet. J. Embryol. Exp. Morph. 23, 109-151.
61. Prahlad, R. B., Skala, G., Jones, D. B. and Briles, W. S. (1979). Limbless: A new genetic mutant in the chick. J. Exp. Zool. 209, 427-434.
62. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
63. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmx1 by Wnt7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
64. 4 mutant chick limb bud. Dev. Gen. In press.
65. Robert, B., Lyons, G., Simandl, B. K., Kuroiwa, A. and Buckingham, M. (1991). The apical ectodermal ridge regulates Hox-7 and Hox-8 gene expression in developing chick limb buds. Genes and Dev. 5, 2363-2374.
66. Ros, M. A., Lyons, G. E., Mackem, S. and Fallon, J. F. (1994). Recombinant limbs as a model to study homeobox gene regulation during limb development. Dev. Biol. 166, 59-72.
67. Rosenquist, G. C. (1971). The origin and movement of the limb-bud epithelium and mesenchyme in the chick embryo as determined by radioautographic mapping. J. Embryol. Exp. Morphol. 25, 85-96.
68. Rowe, D. A. and Fallon, J. F. (1982). The proximodistal determination of skeletal parts in the developing chick leg. J. Embryol. Exp. Morphol. 68, 1-7.
69. Rubin, L. and Saunders, J. W. Jr. (1972). Ectodermal-mesodermal interactions in the growth of limb buds in the chick embryo: constancy and temporal limits of the ectodermal induction. Dev. Biol. 28, 94-112.
70. Rudnick, D. (1945). Limb-forming potencies of the chick blastoderm: including notes on associated trunk structures. Trans. Conn. Acad. Arts Sci. 36, 353-377.
71. Saunders, J. W., Jr. (1948). The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363-403.
72. Saunders, J. W., Jr. and Gasseling, M. T. (1968). Ectoderm-mesenchymal interaction in the origins of wing symmetry. In Epithelial-Mesenchymal Interactions, (eds. R. Fleischmajer and R. E. Billingham) pp. 78-97. Baltimore: Williams and Wilkins.
73. Saunders, J. W., Jr. and Reuss, C. (1974). Inductive and axial properties of prospective wing-bud mesoderm in the chick embryo. Dev. Biol. 38, 41-50.
74. Saunders, J. W. Jr., Gasseling, M. T. and Errick, J. E. (1976). Inductive activity and enduring cellular constitution of a supernumerary apical ectodermal ridge grafted to the limb bud of the chick embryo. Dev. Biol. 50, 16-25.
75. Savage, M. P., Hart, C. E., Riley, B., Sasse, J., Olwin, B. B. and Fallon, J. F. (1993). Distribution of FGF2 suggests it has a role in chick limb bud growth. Dev. Dyn. 198, 159-170.
76. Savage, M. P. and Fallon, J. F. (1995). FGF2 mRNA and its antisense message are expressed in a developmentally specific manner in the chick limb bud and mesonephros. Dev. Dyn. 202, 343-353.
77. Searls, R. L. and Janners, M. Y. (1971). The initiation of limb bud outgrowth in the embryonic chick. Dev. Biol. 24, 198-213.
78. Shubin, N. H. (1991). Implications of the 'Bauplan' for development and evolution of the tetrapod limb. In Developmental Patterning of the Vertebrate Limb. (eds. J. R. Hinchliffe, J. M. Hurle and D. Summerbell), pp. 411-422. Plenum Press: New York.
79. Shubin, N. H. and Alberch, P. (1986). A morphogenetic approach to the origin and basic organisation of the tetrapod limb. Evolutionary Biol. 20, 318-390.
80. 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.
81. Stephens, T. D., Spall, R., Baker, W. C., Hiatt, S. R., Pugmire, D. E., Shaker, M. R., Willis, H. J. and Winger, K. P. (1991). Axial and paraxial influences on limb morphogenesis. J. Morphol. 208, 367-379.
82. Stephens, T. D., Baker, W. C., Cotterell, J. W., Edwards, D. R., Pugmire, D. S., Roberts, S. G., Shaker, M. R., Willis, H. J. and Winger, K. P. (1993) Evaluation of the chick wing territory as an equipotential self-differentiating system. Dev. Dyn. 197, 157-68.
83. Stocum, D. L. and Fallon, J. F. (1982). Control of pattern formation in urodele limb ontogeny: a review and a hypothesis. J. Embryol. Exp. Morphol. 69, 7-36.
84. Streck, R. D., Wood, T. L., Hsu, M. S. and Pintar, J. E. (1992). Insulin-like growth factor I and II and insulin-like growth factor binding protein-2 RNAs are expressed in adjacent tissues within rat embryonic and fetal limbs. Dev. Biol. 151, 586-96.
85. Summerbell, D., Lewis, J. H. and Wolpert, L. (1973). Positional information in chick limb morphogenesis. Nature 224, 492-496.
86. Summerbell, D. (1974). A quantitative analysis of the effect of excision of the apical ridge from the chick limb bud. J. Embryol. Exp. Morphol. 32, 651-660.
87. Suzuki, H. R., Sakamoto, H., Yoshida, T., Sugimora, T., Terada, M. and Solursh, M. (1992). Localization of Hst1 transcripts to the apical ectodermal ridge in the mouse embryo. Dev. Biol. 150, 219-222.
88. Tickle, C. (1981). The number of polarizing region cells required to specify additional digits in the developing chick wing. Nature 289, 295-298.
89. Tickle, C., Summerbell, D. and Wolpert, L. (1975). Positional signaling and specification of digits in chick limb morphogenesis. Nature 254, 199-202.
90. Todt, W. and Fallon, J. F. (1984). Development of the apical ectodermal ridge in the chick wing bud. J. Embryol. Exp. Morph. 80, 21-41.
91. Vogel, A. and Tickle, C. (1993). FGF4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. Development 119, 199-206.
92. Vogel, A., Rodriguez, C., Warnken, W. and Izpisú Belmonte, J. C. (1995). Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716-720.
93. Vogel, A., Rodriguez, C. and Izpisúa Belmonte, J. C. (1996). Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122, 1737-1750.
94. Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissues sections and whole mounts. Methods Enzymol. 225, 361-373.
95. Yang, Y. and Niswander, L. (1995). Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell 80, 939-947.
96. Zwilling, E. (1955) Ectoderm-mesoderm relationship in the development of the chick embryo limb bud. J. Exp. Zool. 128, 423-442.
97. Zwilling, E. (1968). Morphogenetic phases in development. Dev. Biol. Supplement 2, 184-207.