Transient downregulation of Bmp signalling induces extra limbs in vertebrates

Development (Cambridge)

Volumn 139, Issue 14, 2012, Pages 2557-2565

  Christen, Bea ^a   Rodrigues, Alexandre Miguel Cavaco ^a   Monasterio, Monserrat Barragán ^a   Roig, Carme Fabregat ^a   Belmonte, Juan Carlos Izpisua ^a,b  

^a CENTER OF REGENERATIVE MEDICINE IN BARCELONA   (Spain)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Appendage development; Bmp signalling; Vertebrate; Xenopus; Zebrafish

Indexed keywords

ALK4 RECEPTOR; ALK5 RECEPTOR; ALK7 RECEPTOR; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN INHIBITOR; NOGGIN; PROTEIN INHIBITOR; RECEPTOR; RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT2 PROTEIN; WNT2BA PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FIN (ORGAN); GASTRULATION; GENE OVEREXPRESSION; LIMB BUD; LIMB DEFORMITY; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TADPOLE; XENOPUS; ZEBRA FISH;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; EXTREMITIES; IN SITU HYBRIDIZATION; PYRAZOLES; PYRIMIDINES; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; SIGNAL TRANSDUCTION; XENOPUS LAEVIS; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 84863105886     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.078774     Document Type: Article

References (59)

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. Albalat, R., Baquero, M. and Minguillon, C. (2010). Identification and characterisation of the developmental expression pattern of tbx5b, a novel tbx5 gene in zebrafish. Gene Expr. Patterns 10, 24-30.
3. Beck, C. W., Christen, B. and Slack, J. M. W. (2003). Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev. Cell 5, 429-439.
4. Beck, C. W., Christen, B., Barker, D. and Slack, J. M. W. (2006). Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech. Dev. 123, 674-688.
5. Begemann, G., Schilling, T. F., Rauch, G. J., Geisler, R. and Ingham, P. W. (2001). The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128, 3081-3094.
6. Boniface, E. J., Lu, J., Victoroff, T., Zhu, M. and Chen, W. (2009). FlEx-based transgenic reporter lines for visualization of Cre and Flp activity in live zebrafish. Genesis 47, 484-491.
7. Carlson, M. R., Komine, Y., Bryant, S. V. and Gardiner, D. M. (2001). Expression of Hoxb13 and Hoxc10 in developing and regenerating Axolotl limbs and tails. Dev. Biol. 229, 396-406.
8. Christen, B. and Slack, J. M. (1997). FGF-8 is associated with anteroposterior patterning and limb regeneration in Xenopus. Dev. Biol. 192, 455-466.
9. Christen, B. and Slack, J. M. W. (1998). All limbs are not the same. Nature 395, 230-231.
10. Christensen, R. N., Weinstein, M. and Tassava, R. A. (2002). Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev. Dyn. 223, 193-203.
11. De Robertis, E. M. (2009). Spemann's organizer and the self-regulation of embryonic fields. Mech. Dev. 126, 925-941.
12. De Robertis, E. M. and Kuroda, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308.
13. Duboc, V. and Logan, M. P. (2011). Regulation of limb bud initiation and limb-type morphology. Dev. Dyn. 240, 1017-1027.
14. Fischer, S., Draper, B. W. and Neumann, C. J. (2003). The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 130, 3515-3524.
15. Furthauer, M., Van Celst, J., Thisse, C. and Thisse, B. (2004). Fgf signalling controls the dorsoventral patterning of the zebrafish embryo. Development 131, 2853-2864.
16. Galis, F., Wagner, G. P. and Jockusch, E. L. (2003). Why is limb regeneration possible in amphibians but not in reptiles, birds, and mammals? Evol. Dev. 5, 208-220.
17. 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.
18. Gilardelli, C. N., Pozzoli, O., Sordino, P., Matassi, G. and Cotelli, F. (2004). Functional and hierarchical interactions among zebrafish vox/vent homeobox genes. Dev. Dyn. 230, 494-508.
19. Grandel, H. and Brand, M. (2011). Zebrafish limb development is triggered by a retinoic acid signal during gastrulation. Dev. Dyn. 240, 1116-1126.
20. Grandel, H., Lun, K., Rauch, G. J., Rhinn, M., Piotrowski, T., Houart, C., Sordino, P., Kuchler, A. M., Schulte-Merker, S., Geisler, R. et al. (2002). Retinoic acid signalling in the zebrafish embryo is necessary during presegmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129, 2851-2865.
21. Groppe, J., Greenwald, J., Wiater, E., Rodriguez-Leon, J., Economides, A. N., Kwiatkowski, W., Affolter, M., Vale, W. W., Belmonte, J. C. and Choe, S. (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420, 636-642.
22. Isaac, A., Cohn, M. J., Ashby, P., Ataliotis, P., Spicer, D. B., Cooke, J. and Tickle, C. (2000). FGF and genes encoding transcription factors in early limb specification. Mech. Dev. 93, 41-48.
23. Ito, T., Ando, H., Suzuki, T., Ogura, T., Hotta, K., Imamura, Y., Yamaguchi, Y. and Handa, H. (2010). Identification of a primary target of thalidomide teratogenicity. Science 327, 1345-1350.
24. Katoh, M. and Katoh, M. (2009). Transcriptional regulation of WNT2B based on the balance of Hedgehog, Notch, BMP and WNT signals. Int. J. Oncol. 34, 1411-1415.
25. 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.
26. Kawakami, Y., Esteban, C. R., Matsui, T., Rodriguez-Leon, J., Kato, S. and Izpisua Belmonte, J. C. (2004). Sp8 and Sp9, two closely related buttonhead-like transcription factors, regulate Fgf8 expression and limb outgrowth in vertebrate embryos. Development 131, 4763-4774.
27. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
28. 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.
29. Koshiba, K., Kuroiwa, A., Yamamoto, H., Tamura, K. and Ide, H. (1998). Expression of Msx genes in regenerating and developing limbs of axolotl. J. Exp. Zool. 282, 703-714.
30. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C. B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
31. Liu, W., Selever, J., Murali, D., Sun, X., Brugger, S. M., Ma, L., Schwartz, R. J., Maxson, R., Furuta, Y. and Martin, J. F. (2005). Threshold-specific requirements for Bmp4 in mandibular development. Dev. Biol. 283, 282-293.
32. Maatouk, D. M., Choi, K. S., Bouldin, C. M. and Harfe, B. D. (2009). In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth. Dev. Biol. 327, 516-523.
33. Matsuda, T. and Crepko, C. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA 104, 1027-1032.
34. McPherron, A. C., Huynh, T. V. and Lee, S. J. (2009). Redundancy of myostatin and growth/differentiation factor 11 function. BMC Dev. Biol. 9, 24.
35. Mercader, N. (2007). Early steps of paired fin development in zebrafish compared with tetrapod limb development. Dev. Growth Differ. 49, 421-437.
36. Mercader, N., Fischer, S. and Neumann, C. J. (2006). Prdm1 acts downstream of a sequential RA, Wnt and Fgf signaling cascade during zebrafish forelimb induction. Development 133, 2805-2815.
37. 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.
38. Murali, D., Yoshikawa, S., Corrigan, R. R., Plas, D. J., Crair, M. C., Oliver, G., Lyons, K. M., Mishina, Y. and Furuta, Y. (2005). Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132, 913-923.
39. Neave, B., Holder, N. and Patient, R. (1997). A graded response to BMP-4 spatially coordinates patterning of the mesoderm and ectoderm in the zebrafish. Mech. Dev. 62, 183-195.
40. Neto, A., Mercader, N. and Gomez-Skarmeta, J. L. (2012). The Osr1 and Osr2 genes act in the pronephric anlage downstream of retinoic acid signaling and upstream of Wnt2b to maintain pectoral fin development. Development 139, 301-311.
41. Niederreither, K., Ward, S. J., Dolle, P. and Chambon, P. (1996). Morphological and molecular characterization of retinoic acid-induced limb duplications in mice. Dev. Biol. 176, 185-198.
42. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21, 444-448.
43. 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.
44. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam, The Netherands: North-Holland.
45. 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.
46. Ovchinnikov, D. A., Selever, J., Wang, Y., Chen, Y. T., Mishina, Y., Martin, J. F. and Behringer, R. R. (2006). BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev. Biol. 295, 103-115.
47. Pizette, S., Abate-Shen, C. and Niswander, L. (2001). BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 128, 4463-4474.
48. Pownall, M. E., Tucker, A. S., Slack, J. M. and Isaacs, H. V. (1996). An eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 122, 3881-3892.
49. Pyati, U. J., Webb, A. E. and Kimelman, D. (2005). Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132, 2333-2343.
50. Robert, B. (2007). Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev. Growth Differ. 49, 455-68.
51. Rutledge, J. C., Shourbaji, A. G., Hughes, L. A., Polifka, J. E., Cruz, Y. P., Bishop, J. B. and Generoso, W. M. (1994). Limb and lower-body duplications induced by retinoic acid in mice. Proc. Natl. Acad. Sci. USA 91, 5436-5440.
52. Satoh, A., Sakamaki, K., Ide, H. and Tamura, K. (2005). Characteristics of initiation and early events for muscle development in the Xenopus limb bud. Dev. Dyn. 234, 846-857.
53. 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.
54. Shih, J. and Fraser, S. E. (1996). Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage. Development 122, 1313-1322.
55. Sleep, E., Boue, S., Jopling, C., Raya, M., Raya, A. and Izpisua Belmonte, J. C. (2010). Transcriptomics approach to investigate zebrafish heart regeneration. J. Cardiovasc. Med. 11, 369-380.
56. Vandersea, M. W., Fleming, P., McCarthy, R. A. and Smith, D. G. (1998). Fin duplications and deletions induced by disruption of retinoic acid signaling. Dev. Genes Evol. 208, 61-68.
57. Wagner, D. S. and Mullins, M. C. (2002). Modulation of BMP activity in dorsal-ventral pattern formation by the chordin and ogon antagonists. Dev. Biol. 245, 109-123.
58. Westerfield, M. (1995). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
59. Whitman, M. and Raftery, L. (2005). TGFβ signaling at the summit. Development 132, 4205-4210.