Out on a limb: Parallels in vertebrate and invertebrate limb patterning and the origin of appendages

American Zoologist

Volumn 39, Issue 3, 1999, Pages 650-663

  Tabin, Clifford J ^a   Carroll, Sean B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 22644451907     PISSN: 00031569     EISSN: None     Source Type: Journal    
DOI: 10.1093/icb/39.3.650     Document Type: Article

References (67)

1. Aguinaldo, A.-M. A., J. M. Turbeville. L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature. 387:489-493.
2. Abouheif, E. 1997. Developmental genetics and homology: A hierarchical approach. TREE. 12:405408.
3. Abouheif, E., M. Akam, W. J. Dickinson, P. W. H. Holland, A. Meyer, N. H. Patel, R. A. Raff, V. L. Roth, and G. Wray. 1997. Homology and developmental genes. Trends in Genetics 13:432-433.
4. Averof, M. and S. M. Cohen. 1997. Evolutionary origin of insect wings from ancestral gills. Nature 385:627-630.
5. Balavoine, C. R. 1997. The early emergence of platyhelminths is contradicted by the agreement between 18S rRNA and Hox genes data. Acad. Sei. Ser. Ill Sei. Vie. 320:83-94.
6. Basler, K. and G. Struhl. 1994. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208-214.
7. Bitgood, M. J. and A. P. McMahon. 1995. Hedgehog and BMP genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:126-138.
8. Bulfone, A., H. J. Kirn, L. Puelles, M. H. Porteus, J. E Grippo, and J. L. R. Rubenstein. 1993. The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domeains of the forebrain, face and limbs in midgestation mouse embryos. Mech. Dev. 40:129-140.
9. Capdevila, J., M. P. Estrada, E. Sanchez-Herrero, and I. Guerrero. 1994. The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 13:71-82.
10. Carroll, S. B., J. Gates, D. N. Keys, S. W. Paddock, G. E. F. Panganiban, J. Selegue, and J. A. Williams. 1994. Pattern formation and eyespot détermination in butterfly wings. Science 265:109114.
11. Cohen, S. M., G. Bronner, F. Kuttner, G. Jürgens, and H. Jackle. 1989. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338:432-434.
12. Cohen, S. M. and G. Jürgens. 1989. Proximal-distal pattern formation in Drosophila: Cell .autonomous requirement for Distal-less gene activity in limb development. EMBO J. 8:2045-2055.
13. Couso, J. P., E. Knust, and A. Martinez Arias. 1995. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5:1437-1448.
14. De Robertis, E. M. 1997. The ancestry of segmentation. Nature. 387:25-26.
15. Desplan, C. 1997. Eye development: Governed by a dictator or a junta? Cell 91:861-864.
16. Diaz-Benjumea, E J. and S. M. Cohen. 1993. Interaction between dorsal and ventral cells in the imaginai disc directs wing development in Drosophila. Cell 75:741-752.
17. Diaz-Benjumea, E J. and S. M. Cohen. 1995. Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121:4215-4225.
18. Dolle, P., M. Price, and D. Duboule. 1992. Expression of the murine Dls-1 homeobox gene during facial, ocular, and limb development. Differentiation 49: 93-99.
19. Gaunt, S. M. Blum and E. M. De Robertis. 1993. Expression of the mouse goosecoid gene during midembryogenesis may mark mesenchymal cell lineages in the developing head, limbs and body wall. Development 117:769-778.
20. Gerhart, J. and M. Kirschner. 1997. Cells, embryos, and evolution. Blackwell Science. Massachusetts.
21. Gorfinkiel, N., G. Morata, and I. Guerrero. 1997. The homeobox gene Distal-less induces ventral appendage development in Drosophila. Genes Develop. 11:2259-2271.
22. Greco, T. L., S. Takada, M. M. Newhouse, J. A. McMahon, A. P. McMahon, and S. A. Camper. 1996. Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev. 10:313-324.
23. Halder, G., P. Callaerts, and W. J. Gehring. 1995. New perspectives on eye evolution. Curr. Opin. Genet. Dev. 5:602-609.
24. Hardiman, G., S. Albright, J. Tsunoda, T. McClanahan, and F. Lee. 1996. The mouse Wnt-lOB gene isolated from helper T cells is widely expressed and a possible oncogene in BR6 mouse mammary tumorigenesis. Gene 172:199-205.
25. Hirsinger, E., D. Duprez, C. Jouve, P. Malapert, J. Cooke, and O. Pourquie. 1997. Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124:4605-4614.
26. Holley, S. A., P. D. Jackson, Y. Sasai, B. Lu, E. M. De Robertis, F. M. Hoffmann, and E. L. Ferguson. 1995. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376:249-253.
27. Ingham, P. W. and M. J. Fietz. 1995. Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosopliila wing. Curr. Biol. 5:432-440.
28. Irvine, K. D. and E. Wieschaus. 1994. fringe, a Boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79:595-606.
29. Kengaku, M., J. Capdevila, C. Rodriguez-Esteban, J. v De La Pena, R. L. Johnson, J. C. Izpisua Belmonte, and C. J. Tabin. 1998. WNT3a regulates AER formation and utilizes an intracellular signaling pathway distinct from the dorsoventral signal WNT7a during chick limb morphogenesis. Science 280:1274-1277.
30. Kirn, J., K. D. Irvine, and S. B. Caroll. 1995. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosopliila wing. Cell 82:795-802.
31. Kojima, T., T. Michiue, M. Orihara, and K. Saigo. 1994. Induction of a mirror-image duplication of anterior wing structures by localized hedgehog expression in the anterior compartment of Drosopliila melanogaster wing imaginai discs. Gene 148: 211-217.
32. Laufer, E., R. Dann, O. E. Orozco, C. Y. Yeo, J. Pisenti, D. Henrique, U. K. Abbott, J. F. Fallon, and C. Tabin. 1997. Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386:366-373.
33. Laufer, E., C. E. Nelson, R. L. Johnson, B. A. Morgan, and C. Tabin. 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.
34. Lecuit, T, W. J. Brook, M. Ng, M. Calleja, H. Sun, and S. M. Cohen. 1996. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosopliila wing. Nature 381:387-393.
35. Lee, J. J., D. P. von Kessler, S. Parks, and P. A. Beachy. 1992. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71:33-50.
36. Lyons, K. M., R. W. Pelton, and B. L. M. Hogan. 1989. Patterns of expression of murine Vgr-1 and BMP23 suggest that transforming growth factor-b-like genes coordinately regulate aspects of embryonic development. Genes Dev. 3:1657-1668.
37. Lyons, K. M., R. W. Pelton, and B. L. M. Hogan. 1990. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for Bone Morphogenetic Protein-2A. Development 109:833-844.
38. Maley, L. E. and C. R. Marshall. 1998. The coming of age of molecular systematics. Science. 279: 505-506.
39. Masucci, J. D., R. J. Miltenberger, and E M. Hoffmann. 1990. Pattern specific expression of the Drosopliila decapenlaplegic gene in imaginai discs is regulated by 3' cis-regulatory elements. Genes Dev. 4:2011-2023.
40. Mango, V., M. P. Scott, R. L. Johnson, L. V. Goodrich, and C. J. Tabin. 1996. Conservation on hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 122:1225-1233.
41. Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85:357-368. ,!
42. Niswander, L. and G. Martin. 1992. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114: 755-768.
43. Panganiban, G., S. M. Irvine, C. Löwe, H. Roehl, L. S. Corley, B. Sherbon, J. K. Grenier, J. F. Fallon, J. Kimble, M. Walker, G. A. Wray, B. J. Swalla, M. Q. Martindale, and S. B. Carroll. 1997. The origin and evolution of animal appendages. Proc. Natl. Acad. Sei. U.S.A. 94:5162-5166.
44. Panganiban,-G., L. Nagy, and S. B. Carroll. 1994. The development and evolution of insect limb types. Curr. Biol. 4:671-675.
45. Panganiban, G., A. Sebring, L. Nagy, and S. B. Carroll. 1995. The development of crustacean limbs and the evolution of arthropods. Science 270: 1363-1366.
46. Panin, V. M., V. Papayannopoulos, R. Wilson, and K. D. Irvine. 1997. Fringe modulates Notch-ligand interactions. Nature 387:908-912.
47. Posakony, L. G., L. A. Raftery, and W. M. Gelbart. 1990. Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary. Mech. Develop. 33:69-82.
48. Qiu, M., A. Bulfone, S. Martinez, J. J. Meneses, K. Shimamura, R. A. Pedersen, and J. L. R. Rubenstein. 1995. Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev. 9:25232538.
49. Qiu, M., A. Bulfone, I. Ghattas, J. J. Meneses, L. Christensen, P. T. Sharpe, R. Presley, R. A. Pedersen, and J. L. R. Rubenstein. 1997. Role of the Dix homeobox genes in proximal distal patterning of the branchial arches: Mutations of Dix-1, Dix2, and Dix-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev. Biol. 185: 165-184.
50. Riddle, R. D., M. Ensini, C. Nelson, T. Tsuchida, T. M. Jessell, and C. Tabin. 1995. Induction of the LIM homeobox gene Lmxl by WNT7a establishes dorsoventral pattern in the venebrate limb. Cell 83:631-640.
51. Riddle, R. D., R. L. Johnson, E. Laufer, and C. Tabin. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401-1416.
52. Robinson, G. W. and K. A. Mahon. 1994. Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech. Dev. 48:199-215.
53. Rodriguez-Esteban, C., J. W. Schwabe, J. De La Pena, B. Foys, B. Eshelman, and J. C. Belmonte. 1997. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature386:360-366.
54. Roelink, H. and R. Nüsse. 1991. Expression of two members of the Wnt family during mouse development-restricted temporal and spatial patterns in the developing neural tube. Genes Develop. 5: 381-388.
55. Sanicola, M., J. Sekelsky, S. Elson, and W. M. Gelbart. 1995. Drawing a stripe in Drosophila imaginai disks: Negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139: 745-756.
56. Shubin, N., C. Tabin, and S. Carroll. 1997. Fossils, genes, and the evolution of animal limbs. Nature 388:639-648.
57. Speicher, S. A., U. Thomas, U. Hinz, and E. Knust. 1994. The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginai discs: Control of cell proliferation. Development 120: 535-544.
58. Sporle, R. and K. Schughart. 1997. Neural tube morphogenesis. Curr. Opin. Genet. Dev. 7:507-512.
59. Struhl, G. 1982. Genes controlling segmental specification in the Drosophila thorax. Proc. Natl. Acad. Sei. U.S.A. 79:7380-7384.
60. Tabata, T, S. Eaton, and T. B. Kornberg. 1992. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Develop. 6:26352645.
61. Todt, W. L. and J. F. Fallon. 1984. Development of the apical ectodermal ridge in the chick wing bud. J. Embryol. Exp. Morphol. 80:21-41.
62. Van Valen, L. 1982. Homology and causes. J. Morphol. 173:305-312.
63. Vogel, A., C. Rodriguez, W. Warnken, and J. C. Izpisua Belmonte. 1995. Dorsal cell fate specified by chick Lmxl during vertebrate limb development. Nature 378:716-720.
64. Wall, N. A. and B. L. Hogan. 1995. Expression of bone morphogenetic protein-4 (BMP-4), bone morphogenetic protein-7 (BMP-7), fibroblast growth factor-8 (FGF-8) and sonic hedgehog (SHH) during branchial arch development in the chick. Mech. Dev. 53:383-392.
65. Wang, J. and G. M. Shackleford. 1996. Murine WntlOa and WntlOb: Cloning and expression in developing limbs, face and skin of embryos and in adults. Oncogene 13:1537-1544.
66. Yang, Y., G. Drossopoulou, P. T. Chuang, D. Duprez, E. Marti, D. Bumcrot, N. Vargesson, J. Clarke, L. Niswander, A. McMahon, and C. Tickle. 1997. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124:4393.
67. Xiao, S., Y. Zhang, and A. Knoll. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature. 391: 553-558.