FGF7 and FGF10 directly induce the apical ectodermal ridge in chick embryos

Developmental Biology

Volumn 211, Issue 1, 1999, Pages 133-143

  Yonei Tamura, Sayuri ^a,b   Endo, Tetsuya ^a   Yajima, Hiroshi ^a   Ohuchi, Hideyo ^c   Ide, Hiroyuki ^a   Tamura, Koji ^a,b  

^a TOHOKU UNIVERSITY   (Japan)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Apical ectodermal ridge (AER); FGF10; FGF7; Limb morphogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR; RNA;

ANIMAL TISSUE; ARTICLE; CHICKEN; ECTODERM; EMBRYO; GENE; GENE EXPRESSION; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; LIMB; LIMB BUD; LIMB DEVELOPMENT; MESODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALIA; GALLUS GALLUS; VERTEBRATA;

EID: 0033168590     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9290     Document Type: Article

References (56)

1. Akimenko M.-A., Johnson S. L., Westerfield M., Ekker M. Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development. 121:1995;347-357.
2. Akimenko M.-A., Ekker M. Anterior duplication of the sonic hedgehog expression pattern in the pectoral fin buds of zebrafish treated with retinoic acid. Dev. Biol. 170:1995;243-247.
3. Bodenstein D. Studies on the development of the dorsal fin in amphibians. J. Exp. Zool. 120:1952;213-245.
4. Carrington J. L., Fallon J. F. The stages of flank ectoderm capable of responding to ridge induction in the chick embryo. J. Embryol. Exp. Morphol. 84:1984;19-34.
5. Coates M. I. The origin of vertebrate limbs. Development Suppl. 1994;169-180.
6. Cohn M. J., Izpisua-Belmonte J. C., Abud H., Heath J. K., Tickle C. Fibroblast growth factors induce additional limb development from the flank of chick embryo. Cell. 80:1995;739-746.
7. Crossley P. H., Minowada G., MacArthur C. A., Martin G. R. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell. 84:1996;127-136.
8. Dealy C. N., Kosher R. A. Studies on insulin-like growth factor-I and insulin in chick limb morphogenesis. Dev. Dyn. 202:1995;67-79.
9. Dionne C. A., Crumley G., Bellot F., Kaplow J. M., Searfoss G., Runa M., Burgess H. W., Jaye M., Schlessinger J. Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J. 9:1990;2685-2692.
10. DuShane G. P. An experimental study of the origin of pigment cells in amphibia. J. Exp. Zool. 72:1935;1-31.
11. Eeden F. J. M., Granato M., Schach U., Brand M., Furutani-Seiki M., Haftter P., Hammerschmidt M., Heisenberg C-P., Jiang Y-J., Kane D. A., Kelsh R. N., Mullins M. C., Odenthal J., Warga R. M., Nusslein-Volhard C. Genetic analysis of fin formation in the zebrafish, Danio rerio. Development. 123:1996;255-262.
12. Eisen J. S., Weston J. A. Development of the neural crest in the zebrafish. Dev. Biol. 159:1993;50-59.
13. Emerman J. T., Enami J., Pitelka D. R., Nandi S. Hormonal effects on intracellular and secreted casein in cultures of mouse mammary epithelial cells on floating collagen membranes. Proc. Natl. Acad. Sci. USA. 74:1977;4466-4470.
14. Endo T., Yokoyama H., Tamura K., Ide H. Shh expression in developing and regenerating limb buds of Xenopus laevis. Dev. Dyn. 209:1997;227-232.
15. Fallon J. F., Lopez A., Ros M. A., Savage M. P., Olwin B. B., Simandl B. K. FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science. 264:1994;104-107.
16. Francis P. H., Richardson M. K., Brickell P. M., Tickle C. Bone morphogenetic proteins and a signaling pathway that controls patterning in the developing chick limb. Development. 120:1994;209-218.
17. Furthauer M., Thisse C., Thisse B. A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development. 124:1997;4253-4264.
18. Hall B. K. The evolution of connective and skeletal tissues. Hinchliffe J. R., Hurle J. M., Summerbell D. Developmental Patterning of the Vertebrate Limb. 1991;303-312 Plenum Press, New York.
19. Hamburger V., Hamilton H. A series of normal stages in the development of chick embryo. J. Morphol. 88:1951;49-92.
20. Hara K., Ide H. Msx1 expressing mesoderm is important for the apical ectodermal ridge (AER)-signal transfer in chick limb development. Dev. Growth Differ. 39:1997;705-714.
21. Hinchliffem J. R., Johnson D. R. The Development of the Vertebrate Limb. 1980;Oxford Univ. Press, Oxford.
22. Hou J. Z., Kan M. K., McKeehan K., McBride G., Adams P., McKeehan W. L. Fibroblast growth factor receptors from liver vary in three structural domains. Science. 251:1991;665-668.
23. Igarashi M., Finch P. W., Aaronson S. A. Characterization of recombinant human fibroblast growth factor (FGF)-10 reveals functional similarities with keratinocyte growth factor (FGF-7). J. Biol. Chem. 273:1998;13230-13235.
24. Jarvik E. Basic Structure and Evolution of Vertebrates. 1981;Academic Press, London.
25. Kimmel C. B., Ballard W. W., Kimmel S. R., Ullmann B., Schilling T. F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:1995;253-310.
26. Laufer E., Nelson C. E., Johnson R. L., Morgan B. A., Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell. 79:1994;993-1003.
27. Laufer E., Dahn R., Orozco O. E., Yeo C. Y., Pisenti J., Henrique D., Abbott U. K., Fallon J. F., Tabin C. Expression of radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature. 383:1997;366-373.
28. MacArthur C. A., Lawshe A., Xu J., Santos-Ochampo S., Heikinheimo M., Chellaiah A. T., Ornitz D. M. FGF-8 isoforms activate receptor splice forms that are expressed in mesenchymal regions of mouse development. Development. 121:1995;3603-3613.
29. Mahmood R., Bresnick J., Hornbruch A., Mahony C., Morton N., Colquhoun K., Martin P., Lumsden A., Dickson C., Mason I. A role of FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5:1995;797-806.
30. Mansukhani A., Moscatelli D., Talarico D., Levytska V., Basilico C. A murine fibroblast growth factor (FGF) receptor expressed in CHO cells is activated by basic FGF and Kaposi FGF. Proc. Natl. Acad. Sci. USA. 87:1990;4378-4382.
31. Mason I. J., Fuller-Pace F., Smith R., Dickson C. FGF-7 (keratinocyte growth factor) expression during mouse development suggests the roles in myogenesis, forebrain regionalization and epithelial-mesenchymal interactions. Mech. Dev. 45:1994;15-30.
32. Michaud J. L., Lapointe F., Le Douarinm N. M. The dorsoventral polarity of the presumptive limb is determined by signals produced by the somites and by the lateral somatopleure. Development. 124:1997;1453-1463.
33. Miki T., Fleming T. P., Bottaro D. P., Ruvin J. S., Ron D., Aaronson S. A. Expression cDNA cloning of the KGF receptor by creation of a transforming autocrine loop. Science. 251:1991;72-75.
34. Min H., Danilenko D. M., Scully S. A., Bolon B., Ring B. D., Tarpley J. E., DeRose M., Simonet W. S. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 12:1998;156-161.
35. Niswander L., Tickle C., Vogel A., Booth I., Martin G. R. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 75:1994;579-587.
36. Noji S., Koyama E., Myokai T., Nohno T., Ohuchi H., Nishikawa K., Taniguchi S. Differential expression of three FGF receptor genes, FGFR1, FGFR2, FGFR3, in chick bone formation. Dent. Jpn. 29:1992;36-40.
37. Ohuchi H., Nakagawa T., Yamamoto A., Araga A., Ohata T., Ishimaru Y., Yoshioka H., Kuwana T., Nohno T., Yamasaki M., Itoh N., Noji S. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development. 124:1997;2235-2244.
38. Ornitz D. M., Xu J., Colvin J. S., McEwen D. G., MacArthur C. A., Coulier F., Gao G., Goldfarb M. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271:1997;15292-15297.
39. Orr-Urtreger A., Bedford M. T., Burakova T., Arman E., Zimmer Y., Yayon A., Givol D., Lonai P. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR-2). Dev. Biol. 158:1993;475-486.
40. Post M., Souza P., Liu J., Tseu I., Wang J., Kuliszewski M., Tanswell K. Keratinocyte growth factor and its receptor are involved in regulating early lung branching. Development. 122:1996;3107-3115.
41. Riddle R. D., Ensini M., Nelson C., Tsuchida T., Jessell T. M., Tabin C. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell. 83:1995;631-640.
42. Rubin J. S., Bottaro D. P., Chedid M., Miki T., Ronm D., Cheon H-G., Taylor W. G., Fortney E., Dakata H., Finch P. W., Larochelle W. Keratinocyte growth factor. Cell. Biol. Int. 5:1995;399-411.
43. Saunders J. W. Jr. The proximo-distal sequence of the origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108:1948;363-404.
44. Saunders J. W. Jr., Gasseling M. T., Errick J. E. Inductive activity and enduring cellular constitution of a supernumerary apical ectodermal ridge grafted to the limb bud of the chick embryo. Dev. Biol. 50:1976;16-25.
45. Saunders J. W. Jr., Reuss C. Inductive and axial properties of prospective wing bud mesoderm in the chick embryo. Dev. Biol. 38:1974;41-50.
46. Schulte-Merker S., Ho R. K., Herrmann B. G., Nusslein-Volhard C. The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development. 116:1992;1021-1032.
47. Su M. W., Suzuki H. R., Solursh M., Ramirez F. Progressively restricted expression of a new homeobox-containing gene during Xenopus laevis embryogenesis. Development. 111:1991;1179-1187.
48. Tabin C. J. Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development. 116:1992;289-296.
49. Vogel A., Rodriguez C., Izpisua-Belmonte J. C. Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development. 122:1996;1737-1750.
50. Vogel A., Rodriguez C., Warnken W., Izpisua-Belmonte J. C. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature. 378:1995;716-720.
51. Werner S., Duan D.-S. R., De Vries C., Peters K. P., Johnson D., Williams L. T. Differential splicing in the extracellular region of fibroblast growth factor receptor 1 generates receptor variants with different ligand-binding specificities. Mol. Cell. Biol. 12:1992;82-88.
52. Xu X., Weinstein M., Li C., Naski M., Cohen R. I., Ornitz D. M., Leder P., Deng C. Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development. 125:1998;753-765.
53. Yamasaki M., Miyake A., Tagashira S., Itoh N. Structure and expression of the rat mRNA encoding a novel member of the fibroblast growth factor family. J. Biol. Chem. 271:1996;15918-15921.
54. Yokouchi Y., Ohsugi K., Sasaki H., Kuroiwa A. Chicken homeobox gene Msx-1: Structure, expression in limb buds and effect of retinoic acid. Development. 113:1991;431-444.
55. Yonei S., Tamura K., Ohsugi K., Ide H. MRC-5 cells induce the AER prior to the duplicated pattern formation in chick limb bud. Dev. Biol. 170:1995;542-552.
56. Zwilling E., Hansborough L. A. Interaction between limb bud ectoderm and mesoderm in the chick embryo. III. Experiments with polydactylous limbs. J. Exp. Zool. 132:1956;219-239.