Genetic basis of hindlimb loss in a naturally occurring vertebrate model

Biology Open

Volumn 5, Issue 3, 2016, Pages 359-366

  Don, Emily K ^a,b   De Jong Curtain, Tanya A ^c   Doggett, Karen ^c   Hall, Thomas E ^d   Heng, Benjamin ^a   Badrock, Andrew P ^a   Winnick, Claire ^a   Nicholson, Garth A ^a   Guillemin, Gilles J ^a   Currie, Peter D ^e   Hesselson, Daniel ^f,g   Heath, Joan K ^c   Cole, Nicholas J ^a,b  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Development; Hindlimb; Pelvic fin; TALENs; Tbx4

Indexed keywords

T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TRANSCRIPTION FACTOR TBX4; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CLONING; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EVOLUTION; GENE; GENE EXPRESSION; GENE MUTATION; HINDLIMB; HISTOLOGY; HUMAN; HUMAN CELL; LIMB DEVELOPMENT; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PELVIC FIN; PROTEIN LOCALIZATION; ZEBRA FISH;

EID: 84978476526     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.016295     Document Type: Article

References (58)

1. Ahn, D.-G., Kourakis, M. J., Rohde, L. A., Silver, L. M. and Ho, R. K. (2002). T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417, 754-758.
2. Alvarado, D. M., Aferol, H., Mccall, K., Huang, J. B., Techy, M., Buchan, J., Cady, J., Gonzales, P. R., Dobbs, M. B. and Gurnett, C. A. (2010). Familial isolated clubfoot is associated with recurrent chromosome 17q23.1q23.2 microduplications containing TBX4. Am. J. Hum. Genet. 87, 154-160.
3. Ballif, B. C., Theisen, A., Rosenfeld, J. A., Traylor, R. N., Gastier-Foster, J., Thrush, D. L., Astbury, C., Bartholomew, D., McBride, K. L., Pyatt, R. E. et al. (2010). Identification of a recurrent microdeletion at 17q23.1q23.2 flanked by segmental duplications associated with heart defects and limb abnormalities. Am. J. Hum. Genet. 86, 454-461.
4. Barrow, J. R., Thomas, K. R., Boussadia-Zahui, O., Moore, R., Kemler, R., Capecchi, M. R. and Mcmahon, A. P. (2003). Ectodermal Wnt3/β-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev. 17, 394-409.
5. Basson, C. T., Huang, T., Lin, R. C., Bachinsky, D. R., Weremowicz, S., Vaglio, A., Bruzzone, R., Quadrelli, R., Lerone, M., Romeo, G. et al. (1999). Different TBX5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc. Natl. Acad. Sci. USA 96, 2919-2924.
6. Bongers, E. M. H. F., Van Bokhoven, H., Van Thienen, M.-N., Kooyman, M. A. P., Van Beersum, S. E. C., Boetes, C., Knoers, N. V. A. M. and Hamel, B. C. J. (2001). The small patella syndrome: description of five cases from three families and examination of possible allelism with familial patella aplasia-hypoplasia and nail-patella syndrome. J. Med. Genet. 38, 209-214.
7. Bongers, E. M. H. F., Van Bokhoven, H., Knoers, N. V. A. M., Hamel, B. C. J. and Woods, C. G. (2002). Evidence for genetic heterogeneity in familial isolated patella aplasia-hypoplasia. Am. J. Med. Genet. 108, 78-79.
8. Bongers, E. M. H. F., Duijf, P. H. G., Van Beersum, S. E. M., Schoots, J., Van Kampen, A., Burckhardt, A., Hamel, B. C. J., Lošan, F., Hoefsloot, L. H., Yntema, H. G. et al. (2004). Mutations in the Human TBX4 Gene Cause Small Patella Syndrome. Am. J. Hum. Genet. 74, 1239-1248.
9. Boulet, A. M., Moon, A. M., Arenkiel, B. R. and Capecchi, M. R. (2004). The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev. Biol. 273, 361-372.
10. Camarata, T., Bimber, B., Kulisz, A., Chew, T.-L., Yeung, J. and Simon, H.-G. (2006). LMP4 regulates Tbx5 protein subcellular localization and activity. J. Cell Biol. 174, 339-348.
11. Carroll, R. (ed.) (1988). Vertebrate Paleontology. San Francisco: Freeman.
12. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J. and Voytas, D. F. (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, 7879.
13. Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G., Jr., Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J., Schmutz, J. et al. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305.
14. Coates, M. I. (1994). The origin of vertebrate limbs. Dev. Suppl, 169-180.
15. Cole, N. J., Tanaka, M., Prescott, A. and Tickle, C. (2003). Expression of limb initiation genes and clues to the morphological diversification of threespine stickleback. Curr. Biol. 13, R951-R952.
16. Collavoli, A., Hatcher, C. J., He, J., Okin, D., Deo, R. and Basson, C. T. (2003). TBX5 nuclear localization is mediated by dual cooperative intramolecular signals. J. Mol. Cell. Cardiol. 35, 1191-1195.
17. 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.
18. Don, E. K., Hall, T. E., Currie, P. D. and Cole, N. J. (2011). Morphology of pelvic fin loss in a zebrafish strain (Danio rerio). J. Morphol. 272, 583-589.
19. Don, E. K., Currie, P. D. and Cole, N. J. (2013). The evolutionary history of the development of the pelvic fin/hindlimb. J. Anat. 222, 114-133.
20. Fan, C., Liu, M. and Wang, Q. (2003). Functional analysis of TBX5 missense mutations associated with Holt-Oram syndrome. J. Biol. Chem. 278, 8780-8785.
21. 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.
22. Garrity, D. M., Childs, S. and Fishman, M. C. (2002). The heartstrings mutation in zebrafish causes heart/fin Tbx5 deficiency syndrome. Development 129, 4635-4645.
23. Gupta, T., Marlow, F. L., Ferriola, D., Mackiewicz, K., Dapprich, J., Monos, D. and Mullins, M. C. (2010). Microtubule actin crosslinking factor 1 regulates the Balbiani body and animal-vegetal polarity of the zebrafish oocyte. PLoS Genet. 6, e1001073.
24. Kawakami, Y., Esteban, C. R., Matsui, T., Rodíguez-León, J., Kato, S. and Belmonte, J. C. I. (2004). Sp8 and Sp9, two closely related buttonhead-like transcription factors, regulate Fgf8 expression and limb outgrowth in vertebrate embryos. Development 131, 4763-4774.
25. Komisarczuk, A. Z., Kawakami, K. and Becker, T. S. (2009). Cis-regulation and chromosomal rearrangement of the fgf8 locus after the teleost/tetrapod split. Dev. Biol. 336, 301-312.
26. Lewandoski, M., Sun, X. and Martin, G. R. (2000). Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26, 460-463.
27. Li, H. and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
28. Li, Q. Y., Newbury-Ecob, R. A., Terrett, J. A., Wilson, D. I., Curtis, A. R. J., Yi, C. H., Gebuhr, T., Bullen, P. J., Robson, S. C., Strachan, T. et al. (1997). Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet. 15, 21-29.
29. Li, R., Li, Y., Fang, X., Yang, H., Wang, J., Kristiansen, K. and Wang, J. (2009a). SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124-1132.
30. Li, R., Yu, C., Li, Y., Lam, T.-W., Yiu, S.-M., Kristiansen, K. and Wang, J. (2009b). SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967.
31. Lu, W., Bacino, C. A., Richards, B. S., Alvarez, C., Vandermeer, J. E., Vella, M., Ahituv, N., Sikka, N., Dietz, F. R., Blanton, S. H. et al. (2012). Studies of TBX4 and chromosome 17q23.1q23.2: an uncommon cause of nonsyndromic clubfoot. Am. J. Med. Genet. A 158A, 1620-1627.
32. Mangino, M., Sanchez, O., Torrente, I., De Luca, A., Capon, F., Novelli, G. and Dallapiccola, B. (1999). Localization of a gene for familial Patella Aplasia-Hypoplasia (PTLAH) to chromosome 17q21-22. Am. J. Hum. Genet. 65, 441-447.
33. Mckenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S. , Daly, M. et al. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.
34. Mercader, N. (2007). Early steps of paired fin development in zebrafish compared with tetrapod limb development. Dev. Growth Differ. 49, 421-437.
35. 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.
36. Minguillon, C., Del Buono, J. and Logan, M. P. (2005). Tbx5 and Tbx4 Are not sufficient to determine limb-specific morphologies but have common roles in initiating limb outgrowth. Dev. Cell 8, 75-84.
37. Minguillon, C., Gibson-Brown, J. J. and Logan, M. P. (2009). Tbx4/5 gene duplication and the origin of vertebrate paired appendages. Proc. Natl. Acad. Sci. USA 106, 21726-21730.
38. Moon, A. M. and Capecchi, M. R. (2000). Fgf8 is required for outgrowth and patterning of the limbs. Nat. Genet. 26, 455-459.
39. Nagayoshi, S., Hayashi, E., Abe, G., Osato, N., Asakawa, K., Urasaki, A., Horikawa, K., Ikeo, K., Takeda, H. and Kawakami, K. (2008). Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like. Development 135, 159-169.
40. Naiche, L. A. and Papaioannou, V. E. (2003). Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130, 2681-2693.
41. Naiche, L. A. and Papaioannou, V. E. (2007). Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134, 93-103.
42. Narita, T., Sasaoka, S., Udagawa, K., Ohyama, T., Wada, N., Nishimatsu, S.-I., Takada, S. and Nohno, T. (2005). Wnt10a is involved in AER formation during chick limb development. Dev. Dyn. 233, 282-287.
43. Ng, J. K., Kawakami, Y., Büscher, D., Raya, Á., Itoh, T., Koth, C. M., Esteban, C. R., Rodríguez-León, J., Garrity, D. M., Fishman, M. C. et al. (2002). The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 129, 5161-5170.
44. Norton, W. H. J., Ledin, J., Grandel, H. and Neumann, C. J. (2005). HSPG synthesis by zebrafish Ext2 and Extl3 is required for Fgf10 signalling during limb development. Development 132, 4963-4973.
45. Ouimette, J.-F., Jolin, M. L., L'honoré, A., Gifuni, A. and Drouin, J. (2010). Divergent transcriptional activities determine limb identity. Nat. Commun. 1, 35
46. Papaioannou, V. E. (2001). T-box genes in development: from hydra to humans. Int. Rev. Cytol. 207, 1-70.
47. Rallis, C., Bruneau, B. G., Del Buono, J., Seidman, C. E., Seidman, J. G., Nissim, S., Tabin, C. J. and Logan, M. P. O. (2003). Tbx5 is required for forelimb bud formation and continued outgrowth. Development 130, 2741-2751.
48. Rodriguez-Esteban, C., Tsukui, T., Yonei, S., Magallon, J., Tamura, K. and Belmonte, J. C. I. (1999). The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398, 814-818.
49. Ruvinsky, I., Oates, A. C., Silver, L. M. and Ho, R. K. (2000). The evolution of paired appendages in vertebrates: T-box genes in the zebrafish. Dev. Genes Evol. 210, 82-91.
50. 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.
51. Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D. and Kingsley, D. M. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717-723.
52. Takeuchi, J. K., Koshiba-Takeuchi, K., Suzuki, T., Kamimura, M., Ogura, K. and Ogura, T. (2003). Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development 130, 2729-2739.
53. Tamura, K., Yonei-Tamura, S. and Belmonte, J. C. I. (1999). Differential expression of Tbx4 and Tbx5 in Zebrafish Fin buds. Mech. Dev. 87, 181-184.
54. Tanaka, M., Hale, L. A., Amores, A., Yan, Y.-L., Cresko, W. A., Suzuki, T. and Postlethwait, J. H. (2005). Developmental genetic basis for the evolution of pelvic fin loss in the pufferfish Takifugu rubripes. Dev. Biol. 281, 227-239.
55. Wang, K., Shi, D., Zhu, P., Dai, J., Zhu, L., Zhu, H., Lv, Y., Zhao, B. and Jiang, Q. (2010). Association of a single nucleotide polymorphism in Tbx4 with developmental dysplasia of the hip: a case-control study. Osteoarthritis Cartilage 18, 1592-1595.
56. Westerfield, M. (2000). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene: Univ. of Oregon Press.
57. Zaragoza, M. V., Lewis, L. E., Sun, G., Wang, E., Li, L., Said-Salman, I., Feucht, L. and Huang, T. (2004). Identification of the TBX5 transactivating domain and the nuclear localization signal. Gene 330, 9-18.
58. Zhou, Y. and Zon, L. I. (2011). The zon laboratory guide to positional cloning in zebrafish. Methods Cell Biol. 104, 287-309.