RA Acts in a Coherent Feed-Forward Mechanism with Tbx5 to Control Limb Bud Induction and Initiation

Cell Reports

Volumn 12, Issue 5, 2015, Pages 879-891

  Nishimoto, Satoko ^a   Wilde, Susan M ^a   Wood, Sophie ^b   Logan, Malcolm P O ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR 10; PROTEIN LEF; RETINOIC ACID; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX4; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; AVIAN PROTEIN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5;

ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; ECTODERM; EMBRYO; FGF10 GENE; FORELIMB; GENE EXPRESSION REGULATION; HINDLIMB; LIMB BUD; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CHICKEN; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENETICS; METABOLISM; ORGANOGENESIS;

ANIMALS; AVIAN PROTEINS; CHICK EMBRYO; CHICKENS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIMB BUDS; ORGANOGENESIS; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRETINOIN;

EID: 84938556850     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.068     Document Type: Article

References (62)

1. Agarwal P., Wylie J.N., Galceran J., Arkhitko O., Li C., Deng C., Grosschedl R., Bruneau B.G. Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 2003, 130:623-633.
2. Barak H., Preger-Ben Noon E., Reshef R. Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation. Dev. Dyn. 2012, 241:1637-1649.
3. Bastien J., Rochette-Egly C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004, 328:1-16.
4. Begemann G., Schilling T.F., Rauch G.J., Geisler R., Ingham P.W. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 2001, 128:3081-3094.
5. Boulet A.M., Moon A.M., Arenkiel B.R., Capecchi M.R. The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev. Biol. 2004, 273:361-372.
6. Cohn M.J., Izpisúa-Belmonte J.C., Abud H., Heath J.K., Tickle C. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 1995, 80:739-746.
7. Cohn M.J., Patel K., Krumlauf R., Wilkinson D.G., Clarke J.D., Tickle C. Hox9 genes and vertebrate limb specification. Nature 1997, 387:97-101.
8. Crossley P.H., Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 1995, 121:439-451.
9. Cunningham T.J., Zhao X., Sandell L.L., Evans S.M., Trainor P.A., Duester G. Antagonism between retinoic acid and fibroblast growth factor signaling during limb development. Cell Rep. 2013, 3:1503-1511.
10. Duboc V., Logan M.P. Regulation of limb bud initiation and limb-type morphology. Dev. Dyn. 2011, 240:1017-1027.
11. Eichele G., Tickle C., Alberts B.M. Microcontrolled release of biologically active compounds in chick embryos: beads of 200-microns diameter for the local release of retinoids. Anal. Biochem. 1984, 142:542-555.
12. Forman B.M., Casanova J., Raaka B.M., Ghysdael J., Samuels H.H. Half-site spacing and orientation determines whether thyroid hormone and retinoic acid receptors and related factors bind to DNA response elements as monomers, homodimers, or heterodimers. Mol. Endocrinol. 1992, 6:429-442.
13. Galceran J., Fariñas I., Depew M.J., Clevers H., Grosschedl R. Wnt3a-/--like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 1999, 13:709-717.
14. Gibert Y., Gajewski A., Meyer A., Begemann G. Induction and prepatterning of the zebrafish pectoral fin bud requires axial retinoic acid signaling. Development 2006, 133:2649-2659.
15. Grandel H., Brand M. Zebrafish limb development is triggered by a retinoic acid signal during gastrulation. Dev. Dyn. 2011, 240:1116-1126.
16. Grandel H., Lun K., Rauch G.J., Rhinn M., Piotrowski T., Houart C., Sordino P., Küchler A.M., Schulte-Merker S., Geisler R., et al. Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 2002, 129:2851-2865.
17. Gros J., Tabin C.J. Vertebrate limb bud formation is initiated by localized epithelial-to-mesenchymal transition. Science 2014, 343:1253-1256.
18. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 1951, 88:49-92.
19. Hasson P., Del Buono J., Logan M.P. Tbx5 is dispensable for forelimb outgrowth. Development 2007, 134:85-92.
20. Hill T.P., Taketo M.M., Birchmeier W., Hartmann C. Multiple roles of mesenchymal beta-catenin during murine limb patterning. Development 2006, 133:1219-1229.
21. Huelsken J., Vogel R., Erdmann B., Cotsarelis G., Birchmeier W. beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 2001, 105:533-545.
22. Kaufman M.H. The Atlas of Mouse Development 2001, Academic Press, Cambridge, UK. Second Edition.
23. Kawakami Y., Capdevila J., Büscher D., Itoh T., Rodríguez Esteban C., Izpisúa Belmonte J.C. WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 2001, 104:891-900.
24. Kawakami Y., Marti M., Kawakami H., Itou J., Quach T., Johnson A., Sahara S., O'Leary D.D., Nakagawa Y., Lewandoski M., et al. Islet1-mediated activation of the β-catenin pathway is necessary for hindlimb initiation in mice. Development 2011, 138:4465-4473.
25. Kengaku M., Capdevila J., Rodriguez-Esteban C., De La Peña J., Johnson R.L., Izpisúa Belmonte J.C., Tabin C.J. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 1998, 280:1274-1277.
26. Kieny M. [On the relations between somatic and somatopleural mesoderm before and during primary induction of chick embryo limbs]. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 1969, 268:3183-3186.
27. Lee J., Tickle C. Retinoic acid and pattern formation in the developing chick wing: SEM and quantitative studies of early effects on the apical ectodermal ridge and bud outgrowth. J. Embryol. Exp. Morphol. 1985, 90:139-169.
28. Logan M., Simon H.G., Tabin C. Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity. Development 1998, 125:2825-2835.
29. McLeod M.J. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 1980, 22:299-301.
30. Mic F.A., Haselbeck R.J., Cuenca A.E., Duester G. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 2002, 129:2271-2282.
31. Mic F.A., Sirbu I.O., Duester G. Retinoic acid synthesis controlled by Raldh2 is required early for limb bud initiation and then later as a proximodistal signal during apical ectodermal ridge formation. J. Biol. Chem. 2004, 279:26698-26706.
32. 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. 1998, 12:3156-3161.
33. Minguillon C., Nishimoto S., Wood S., Vendrell E., Gibson-Brown J.J., Logan M.P. Hox genes regulate the onset of Tbx5 expression in the forelimb. Development 2012, 139:3180-3188.
34. Monkley S.J., Delaney S.J., Pennisi D.J., Christiansen J.H., Wainwright B.J. Targeted disruption of the Wnt2 gene results in placentation defects. Development 1996, 122:3343-3353.
35. Murillo-Ferrol N.L. [Causal study of the earliest differentiation of the morphological rudiments of the extremities. Experimental analysis on bird embryos]. Acta Anat. (Basel) 1965, 62:80-103.
36. Naiche L.A., Papaioannou V.E. Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 2003, 130:2681-2693.
37. Narkis G., Tzchori I., Cohen T., Holtz A., Wier E., Westphal H. Isl1 and Ldb co-regulators of transcription are essential early determinants of mouse limb development. Dev. Dyn. 2012, 241:787-791.
38. Ng J.K., Kawakami Y., Büscher D., Raya A., Itoh T., Koth C.M., Rodríguez Esteban C., Rodríguez-León J., Garrity D.M., Fishman M.C., Izpisúa Belmonte J.C. The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 2002, 129:5161-5170.
39. Niederreither K., McCaffery P., Dräger U.C., Chambon P., Dollé P. Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev. 1997, 62:67-78.
40. Niederreither K., Subbarayan V., Dollé P., Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 1999, 21:444-448.
41. Niederreither K., Vermot J., Schuhbaur B., Chambon P., Dollé P. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 2002, 129:3563-3574.
42. Nishimoto S., Minguillon C., Wood S., Logan M.P. A combination of activation and repression by a colinear Hox code controls forelimb-restricted expression of Tbx5 and reveals Hox protein specificity. PLoS Genet. 2014, 10:e1004245.
43. Ohuchi H., Nakagawa T., Yamamoto A., Araga A., Ohata T., Ishimaru Y., Yoshioka H., Kuwana T., Nohno T., Yamasaki M., et al. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 1997, 124:2235-2244.
44. Pinot M. [The role of the somitic mesoderm in the early morphogenesis of the limbs in the fowl embryo]. J. Embryol. Exp. Morphol. 1970, 23:109-151.
45. Rallis C., Bruneau B.G., Del Buono J., Seidman C.E., Seidman J.G., Nissim S., Tabin C.J., Logan M.P. Tbx5 is required for forelimb bud formation and continued outgrowth. Development 2003, 130:2741-2751.
46. Riddle R.D., Johnson R.L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993, 75:1401-1416.
47. Roselló-Díez A., Arques C.G., Delgado I., Giovinazzo G., Torres M. Diffusible signals and epigenetic timing cooperate in late proximo-distal limb patterning. Development 2014, 141:1534-1543.
48. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Sato T., Yagishita N., Matsui D., Koga Y., Itoh N., Kato S. Fgf10 is essential for limb and lung formation. Nat. Genet. 1999, 21:138-141.
49. Shtutman M., Zhurinsky J., Simcha I., Albanese C., D'Amico M., Pestell R., Ben-Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 1999, 96:5522-5527.
50. Stephens T.D., McNulty T.R. Evidence for a metameric pattern in the development of the chick humerus. J. Embryol. Exp. Morphol. 1981, 61:191-205.
51. Stratford T., Horton C., Maden M. Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr. Biol. 1996, 6:1124-1133.
52. Strecker T.R., Stephens T.D. Peripheral nerves do not play a trophic role in limb skeletal morphogenesis. Teratology 1983, 27:159-167.
53. Sweeney R.M., Watterson R.L. Rib development in chick embryos analyzed by means of tantalum foil blocks. Am. J. Anat. 1969, 126:127-149.
54. Swindell E.C., Thaller C., Sockanathan S., Petkovich M., Jessell T.M., Eichele G. Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev. Biol. 1999, 216:282-296.
55. Takeuchi J.K., Koshiba-Takeuchi K., Suzuki T., Kamimura M., Ogura K., Ogura T. Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development 2003, 130:2729-2739.
56. Tee W.W., Shen S.S., Oksuz O., Narendra V., Reinberg D. Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell 2014, 156:678-690.
57. Tickle C., Crawley A., Farrar J. Retinoic acid application to chick wing buds leads to a dose-dependent reorganization of the apical ectodermal ridge that is mediated by the mesenchyme. Development 1989, 106:691-705.
58. Umesono K., Murakami K.K., Thompson C.C., Evans R.M. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 1991, 65:1255-1266.
59. Valasek P., Theis S., Krejci E., Grim M., Maina F., Shwartz Y., Otto A., Huang R., Patel K. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. J. Anat. 2010, 216:482-488.
60. Vogel A., Rodriguez C., Izpisúa-Belmonte J.C. Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 1996, 122:1737-1750.
61. 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 1998, 125:753-765.
62. Zhao X., Sirbu I.O., Mic F.A., Molotkova N., Molotkov A., Kumar S., Duester G. Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 2009, 19:1050-1057.