Loss and Re-emergence of Legs in Snakes by Modular Evolution of Sonic hedgehog and HOXD Enhancers

Current Biology

Volumn 26, Issue 21, 2016, Pages 2966-2973

  Leal, Francisca ^a,b   Cohn, Martin J ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

anole; digits; embryo; evo devo; genome; limb bud; limblessness; python; skeleton; ZRS

Indexed keywords

REPTILIAN PROTEIN; SONIC HEDGEHOG PROTEIN;

ANATOMY AND HISTOLOGY; ANIMAL; BOIDAE; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; METABOLISM; MOLECULAR EVOLUTION; MORPHOGENESIS;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; BOIDAE; EVOLUTION, MOLECULAR; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; REPTILIAN PROTEINS;

EID: 84994399741     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.09.020     Document Type: Article

References (37)

1. 1 Caldwell, M.W., Lee, M.S.Y., A snake with legs from the marine Cretaceous of the Middle East. Nature 386 (1997), 705–709.
2. 2 Rage, J.C., Escuillié, F., Un nouveau serpent bipède du Cénomanien (Crétacé). Implications phylétiques. C. R. Acad. Sci. Paris Earth Sci. 330 (2000), 513–520.
3. 3 Houssaye, A., Xu, F., Helfen, L., Buffrénil, V.D., Baumbach, T., Tafforeau, P., Three-Dimensional Pelvis and Limb Anatomy of the Cenomanian Hind-Limbed Snake Eupodophis descouensi (Squamata, Ophidia) Revealed by Synchrotron-Radiation Computed Laminography. J. Vertebr. Paleontol. 31 (2011), 2–7.
4. 4 Tchernov, E., Rieppel, O., Zaher, H., Polcyn, M.J., Jacobs, L.L., A fossil snake with limbs. Science 287 (2000), 2010–2012.
5. 5 Apesteguía, S., Zaher, H., A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature 440 (2006), 1037–1040.
6. 6 Pyron, R.A., Burbrink, F.T., Wiens, J.J., A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol., 13, 2013, 93.
7. 7 Head, J.J., Fossil calibration dates for molecular phylogenetic analysis of snakes 1: Serpentes, Alethinophidia, Boidae, Pythonidae. Palaeontol. Electronica 18.1.6FC (2015), 1–17.
8. 8 Zheng, Y., Wiens, J.J., Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 94:Pt B (2016), 537–547.
9. 9 Cohn, M.J., Tickle, C., Developmental basis of limblessness and axial patterning in snakes. Nature 399 (1999), 474–479.
10. 10 Riddle, R.D., Johnson, R.L., Laufer, E., Tabin, C., Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75 (1993), 1401–1416.
11. 11 Zhu, J., Nakamura, E., Nguyen, M.-T., Bao, X., Akiyama, H., Mackem, S., Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev. Cell 14 (2008), 624–632.
12. 12 Sagai, T., Hosoya, M., Mizushina, Y., Tamura, M., Shiroishi, T., Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132 (2005), 797–803.
13. 13 Sagai, T., Masuya, H., Tamura, M., Shimizu, K., Yada, Y., Wakana, S., Gondo, Y., Noda, T., Shiroishi, T., Phylogenetic conservation of a limb-specific, cis-acting regulator of Sonic hedgehog ( Shh). Mamm. Genome 15 (2004), 23–34.
14. 14 Pearse, R.V. 2nd, Vogan, K.J., Tabin, C.J., Ptc1 and Ptc2 transcripts provide distinct readouts of Hedgehog signaling activity during chick embryogenesis. Dev. Biol. 239 (2001), 15–29.
15. 15 Büscher, D., Bosse, B., Heymer, J., Rüther, U., Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mech. Dev. 62 (1997), 175–182.
16. 16 Yang, Y., Niswander, L., Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell 80 (1995), 939–947.
17. 17 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.
18. 18 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 (1993), 579–587.
19. 19 Niswander, L., Jeffrey, S., Martin, G.R., Tickle, C., A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371 (1994), 609–612.
20. 20 Scherz, P.J., Harfe, B.D., McMahon, A.P., Tabin, C.J., The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Science 305 (2004), 396–399.
21. 21 Rowe, D.A., Cairns, J.M., Fallon, J.F., Spatial and temporal patterns of cell death in limb bud mesoderm after apical ectodermal ridge removal. Dev. Biol. 93 (1982), 83–91.
22. 22 Fallon, J.F., López, 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.
23. 23 Galli, A., Robay, D., Osterwalder, M., Bao, X., Bénazet, J.D., Tariq, M., Paro, R., Mackem, S., Zeller, R., Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet., 6, 2010, e1000901.
24. 24 Osterwalder, M., Speziale, D., Shoukry, M., Mohan, R., Ivanek, R., Kohler, M., Beisel, C., Wen, X., Scales, S.J., Christoffels, V.M., et al. HAND2 targets define a network of transcriptional regulators that compartmentalize the early limb bud mesenchyme. Dev. Cell 31 (2014), 345–357.
25. 25 Capellini, T.D., Di Giacomo, G., Salsi, V., Brendolan, A., Ferretti, E., Srivastava, D., Zappavigna, V., Selleri, L., Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 133 (2006), 2263–2273.
26. 26 Lettice, L.A., Heaney, S.J., Purdie, L.A., Li, L., de Beer, P., Oostra, B.A., Goode, D., Elgar, G., Hill, R.E., de Graaff, E., A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12 (2003), 1725–1735.
27. 27 Johnson, E.J., Neely, D.M., Dunn, I.C., Davey, M.G., Direct functional consequences of ZRS enhancer mutation combine with secondary long range SHH signalling effects to cause preaxial polydactyly. Dev. Biol. 392 (2014), 209–220.
28. 28 Charité, J., McFadden, D.G., Olson, E.N., The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of the zone of polarizing activity during limb development. Development 127 (2000), 2461–2470.
29. 29 Litingtung, Y., Dahn, R.D., Li, Y., Fallon, J.F., Chiang, C., Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418 (2002), 979–983.
30. 30 Park, K., Kang, J., Subedi, K.P., Ha, J.H., Park, C., Canine polydactyl mutations with heterogeneous origin in the conserved intronic sequence of LMBR1. Genetics 179 (2008), 2163–2172.
31. 31 Lettice, L.A., Williamson, I., Devenney, P.S., Kilanowski, F., Dorin, J., Hill, R.E., Development of five digits is controlled by a bipartite long-range cis-regulator. Development 141 (2014), 1715–1725.
32. 32 Lettice, L.A., Williamson, I., Wiltshire, J.H., Peluso, S., Devenney, P.S., Hill, A.E., Essafi, A., Hagman, J., Mort, R., Grimes, G., et al. Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 22 (2012), 459–467.
33. 33 Nelson, C.E., Morgan, B.A., Burke, A.C., Laufer, E., DiMambro, E., Murtaugh, L.C., Gonzales, E., Tessarollo, L., Parada, L.F., Tabin, C., Analysis of Hox gene expression in the chick limb bud. Development 122 (1996), 1449–1466.
34. 34 Zakany, J., Duboule, D., The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev. 17 (2007), 359–366.
35. 35 Montavon, T., Soshnikova, N., Mascrez, B., Joye, E., Thevenet, L., Splinter, E., de Laat, W., Spitz, F., Duboule, D., A regulatory archipelago controls Hox genes transcription in digits. Cell 147 (2011), 1132–1145.
36. 36 Leal, F., Cohn, M.J., Development of hemipenes in the ball python snake Python regius. Sex Dev. 9 (2015), 6–20.
37. 37 Lonfat, N., Montavon, T., Darbellay, F., Gitto, S., Duboule, D., Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci. Science 346 (2014), 1004–1006.