The apical ectodermal ridge is a timer for generating distal limb progenitors

Development

Volumn 135, Issue 8, 2008, Pages 1395-1405

  Lu, Pengfei ^a   Yu, Ying ^a   Perdue, Yasmine ^a   Werb, Zena ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Autopod progenitors; Cell proliferation; FGF signaling; Limb patterning; Mouse; Wnt signaling

Indexed keywords

BETA CATENIN; BIOLOGICAL MARKER; FIBROBLAST GROWTH FACTOR RECEPTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA13; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ECTODERM; EMBRYO; GENE FUNCTION; LIMB BUD; LIMB DEVELOPMENT; MESENCHYME CELL; MOLECULAR DYNAMICS; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BETA CATENIN; BODY PATTERNING; CELL PROLIFERATION; DNA-BINDING PROTEINS; ECTODERM; EMBRYONIC STEM CELLS; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTATION; PREGNANCY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; WNT PROTEINS;

MUS; VERTEBRATA;

EID: 44449091452     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.018945     Document Type: Article

References (55)

1. Ahn, K., Mishina, Y., Hanks, M. C., Behringer, R. R. and Crenshaw, E. B., 3rd (2001). BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128, 4449-4461.
2. Altabef, M., Clarke, J. D. and Tickle, C. (1997). Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124, 4547-4556.
3. Arman, E., Haffner-Krausz, R., Chen, Y., Heath, J. K. and Lonai, P. (1998). Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl. Acad. Sci. USA 95, 5082-5087.
4. Arman, E., Haffner-Krausz, R., Gorivodsky, M. and Lonai, P. (1999). Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc. Natl. Acad. Sci. USA 96, 11895-11899.
5. Barrow, J. R., Thomas, K. R., Boussadia-Zahui, O., Moore, R., Kemler, R., Capecchi, M. R. and McMahon, A. P. (2003). Ectodermal Wnt3/ beta-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev. 17, 394-409.
6. Capdevila, J. and Izpisua Belmonte, J. C. (2001). Patterning mechanisms controlling vertebrate limb development. Annu. Rev. Cell Dev. Biol. 17, 87-132.
7. Coumoul, X., Shukla, V., Li, C., Wang, R. H. and Deng, C. X. (2005). Conditional knockdown of Fgfr2 in mice using Cre-LoxP induced RNA interference. Nucleic Acids Res. 33, e102.
8. 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.
9. De Moerlooze, L., Spencer-Dene, B., Revest, J., Hajihosseini, M., Rosewell, I. and Dickson, C. (2000). An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127, 483-492.
10. Dudley, A. T., Ros, M. A. and Tabin, C. J. (2002). A re-examination of proximodistal patterning during vertebrate limb development. Nature 418, 539-544.
11. Fromental-Ramain, C., Warot, X., Messadecq, N., LeMeur, M., Dolle, P. and Chambon, P. (1996). Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011.
12. Galceran, J., Farinas, I., Depew, M. J., Clevers, H. and Grosschedl, R. (1999). Wnt3a-/-like phenotype and limb deficiency in Lef1(-/ -)Tcf1(-/-) mice. Genes Dev. 13, 709-717.
13. Gorivodsky, M. and Lonai, P. (2003). Novel roles of Fgfr2 in AER differentiation and positioning of the dorsoventral limb interface. Development 130, 5471-5479.
14. Guo, Q., Loomis, C. and Joyner, A. L. (2003). Fate map of mouse ventral limb ectoderm and the apical ectodermal ridge. Dev. Biol. 264, 166-178.
15. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
16. Hashimoto, K., Yokouchi, X, Yamamoto, M. and Kuroiwa, A. (1999). Distinct signaling molecules control Hoxa-11 and Hoxa-13 expression in the muscle precursor and mesenchyme of the chick limb bud. Development 126, 2771-2783.
17. Itoh, N. and Ornitz, D. M. (2004). Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569.
18. Janners, M. Y. and Searls, R. L. (1971). Effect of removal of the apical ectodermal ridge on the rate of cell division in the subridge mesenchyme of the embryonic chick wing. Dev. Biol. 24, 465-476.
19. Kawakami, Y., Capdevila, J., Buscher, D., Itoh, T., Rodriguez Esteban, C. and Izpisua Belmonte, J. C. (2001). WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104, 891-900.
20. Kawakami, Y., Rodriguez-Leon, J., Koth, C. M., Buscher, D., Itoh, T., Raya, A., Ng, J. K., Esteban, C. R., Takahashi, S., Henrique, D. et al. (2003). MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat. Cell Biol. 5, 513-519.
21. Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., De La Pena, J., Johnson, R. L., Belmonte, J. C. and Tabin, C. J. (1998). Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280, 1274-1277.
22. Kimmel, R. A., Turnbull, D. H., Blanquet, V., Wurst, W., Loomis, C. A. and Joyner, A. L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 14, 1377-1389.
23. Lewancloski, M., Sun, X. and Martin, G. R. (2000). Fgf8 signalling from the AER is essential for normal limb development. Nat Genet. 26, 460-463.
24. Li, C., Xu, X., Nelson, D. K., Williams, T., Kuehn, M. R. and Deng, C. X. (2005). FGFR1 function at the earliest stages of mouse limb development plays an dispensable role in subsequent autopod morphogenesis. Development 132, 4755-4764.
25. Loomis, C., Kimmel, R., Tong, C., Michaud, J. and Joyner, A. (1998). Analysis of the genetic pathway leading to formation of ectopic apical ectodermal ridges in mouse Engrailed-1 mutant limbs. Development 125, 1137-1148.
26. Lu, P., Minowada, G. and Martin, G. R. (2006). Increasing Fgf4 expression in the mouse limb bud causes polysyndactyly and rescues the skeletal defects that result from loss of Fgf8 function. Development 133, 33-42.
27. Maretto, S., Cordenonsi, M., Dupont S., Braghetta, R, Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/betacatenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
28. Mariani, F. V. and Martin, G. R. (2003). Deciphering skeletal patterning: clues from the limb. Nature 423, 319-325.
29. Martin, G. R. (1998). The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12, 1571-1586.
30. Mercader, N., Leonardo, E., Piedra, M. E., Martinez, A. C., Ros, M. A. and Torres, M. (2000). Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127, 3961-3970.
31. Min, H., Danilenko, D. M., Scully, S. A., Bolon, B., Ring, B. D., Tarpley, J. E., DeRose, M. and Simonet, W. S. (1998). Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 12, 3156-3161.
32. Moon, A. M. and Capecchi, M. R. (2000). Fgf8 is required for outgrowth and patterning of the limbs. Nat. Genet. 26, 455-459.
33. Nelson, C. E., Morgan, B. A., Burke, A. C., Laufer, E., DiMambro, E., Murtaugh, L. C., Gonzales, E., Tessarollo, L., Parada, L. F. and Tabin Tabin, C. (1996). Analysis of Hox gene expression in the chick limb bud. Development 122, 1449-1466.
34. Niswander, L. (2003). Pattern formation: old models out on a limb. Nat. Rev. Genet. 4, 133-143.
35. Niswander, L., Tickle, C., Vogel, A., Booth, I. and Martin, G. R. (1993). FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75, 579-587.
36. 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.
37. Pizette, S. and Niswander, L. (1999). BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126, 883-894.
38. Revest, J. M., Spencer-Dene, B., Kerr, K., De Moerlooze, L., Rosewell, I. and Dickson, C. (2001). Fibroblast growth factor receptor 2-111b acts upstream of Shh and Fgf4 and is required for limb bud maintenance but not for the induction of Fgf8, Fgf10, Msx1, or Bmp4. Dev Biol. 231, 47-62.
39. Sato, K., Koizumi, Y., Takahashi, M., Kuroiwa, A. and Tamura, K. (2007). Specification of cell fate along the proximal-distal axis in the developing chick limb bud. Development 134, 1397-1406.
40. Saunders, J. W., Jr (1948). The proximo-distal sequence of the origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363-403.
41. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N. et al. (1999). Fgf10 is essential for limb and lung formation. Nat Genet. 21, 138-141.
42. Sherman, L., Wainwright, D., Ponta, H. and Herrlich, P. (1998). A splice variant of CD44 expressed in the apical ectodermal ridge presents fibroblast growth factors to limb mesenchyme and is required for limb outgrowth. Genes Dev. 12, 1058-1071.
43. Summerbell, D. (1974). A quantitative analysis of the effect of excision of the AER from the chick limb bud. J. Embryol. Exp. Morphol. 32, 651-660.
44. Summerbell, D., Lewis, J. H. and Wolpert, L. (1973). Positional information in chick limb morphogenesis. Nature 244, 492-496.
45. Sun, X., Lewandoski, M., Meyers, E. N., Liu, Y. H., Maxson, R. E., Jr and Martin, G. R. (2000). Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat. Genet. 25, 83-86.
46. Sun, X., Mariani, F. V. and Martin, G. R. (2002). Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418, 501-508.
47. Tabin, C. and Wolpert, L. (2007). Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev. 21, 1433-1442.
48. Tarchini, B. and Duboule, D. (2006). Control of Hoxcl genes' collinearity during early limb development. Dev. Cell 10, 93-103.
49. Vargesson, N., Clarke, J. D., Vincent, K., Coles, C., Wolpert, L. and Tickle, C. (1997). Cell fate in the chick limb bud and relationship to gene expression. Development 124, 1909-1918.
50. Vargesson, N., Kostakopoulou, K., Drossopoulou, G., Papageorgiou, S. and Tickle, C. (2001). Characterisation of hoxa gene expression in the chick limb bud in response to FGF. Dev. Dyn. 220, 87-90.
51. Verheyden, J. M., Lewandoski, M., Deng, C., Harfe, B. D. and Sun, X. (2005). Conditional inactivation of Fgfr1 in mouse defines its role in limb bud establishment, outgrowth and digit patterning. Development 132, 4235-4245.
52. Wolpert, L., Tickle, C. and Sampford, M. (1979). The effect of cell killing by x-irradiation on pattern formation in the chick limb. J. Embryol. Exp. Morphol. 50, 175-193.
53. Xu, X., Weinstein, M., Li, C., Naski, M., Cohen, R., Ornitz, D., 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.
54. Yu, K. and Ornitz, D. M. (2008). FGF signaling regulates mesenchymal differentiation and skeletal patterning along the limb bud proximodistal axis. Development 135, 483-491.
55. Yu, K., Xu, J., Liu, Z., Sosic, D., Shao, J., Olson, E. N., Towler, D. A. and Ornitz, D. M. (2003). Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074.