Loss of FGF-Dependent Mesoderm Identity and Rise of Endogenous Retinoid Signalling Determine Cessation of Body Axis Elongation

PLoS Biology

Volumn 10, Issue 10, 2012, Pages

  Olivera Martinez, Isabel ^a,c   Harada, Hidekiyo ^a,b   Halley, Pamela A ^a   Storey, Kate G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b TOHOKU UNIVERSITY   (Japan)

^c Université René Descartes   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRACHYURY PROTEIN; CELL MARKER; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; RETINOIC ACID; RETINOID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRACHYURY GENE; CELL DEATH; CELL FATE; CELL POPULATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EMBRYO AXIS; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE LOSS; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MARKER GENE; MESODERM; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TAIL; UPREGULATION; WNT SIGNALING PATHWAY;

ANIMALS; BODY PATTERNING; CHICK EMBRYO; FETAL PROTEINS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; NEURONS; RETINOIDS; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

VERTEBRATA;

EID: 84868118715     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001415     Document Type: Article

References (78)

1. Catala M, Teillet MA, Le-Douarin NM, (1995) Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech Dev 51: 51-65.
2. Wilson V, Olivera-Martinez I, Storey KG, (2009) Stem cells, signals and vertebrate body axis extension. Development 136: 1591-1604.
3. Tzouanacou E, Wegener A, Wymeersch FJ, Wilson V, Nicolas JF, (2009) Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17: 365-376.
4. Cambray N, Wilson V, (2007) Two distinct sources for a population of maturing axial progenitors. Development 134: 2829-2840.
5. McGrew MJ, Sherman A, Lillico SG, Ellard FM, Radcliffe PA, et al. (2008) Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135: 2289-2299.
6. Murakami U, Kameyama Y, (1965) Malformations of the mouse fetus caused by hypervitaminosis-A of the mother during pregnancy. Arch Environ Health 10: 732-741.
7. Kessel M, Gruss P, (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67: 89-104.
8. Shum AS, Poon LL, Tang WW, Koide T, Chan BW, et al. (1999) Retinoic acid induces down-regulation of Wnt-3a, apoptosis and diversion of tail bud cells to a neural fate in the mouse embryo. Mech Dev 84: 17-30.
9. Takada S, Stark K, Shea M, Vassileva G, McMahon J, et al. (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes and Development 8: 174-189.
10. Aulehla A, Wehrle C, Brand-Saberi B, Kemler R, Gossler A, et al. (2003) Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 4: 395-406.
11. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, et al. (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65-79.
12. Olivera-Martinez I, Storey KG, (2007) Wnt signals provide a timing mechanism for the FGF-retinoid differentiation switch during vertebrate body axis extension. Development 134: 2125-2135.
13. Wahl MB, Deng C, Lewandoski M, Pourquie O, (2007) FGF signaling acts upstream of the NOTCH and WNT signaling pathways to control segmentation clock oscillations in mouse somitogenesis. Development 134: 4033-4041.
14. Stavridis MP, Collins BJ, Storey KG, (2010) Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation. Development 137: 881-890.
15. Sanders EJ, Khare MK, Ooi VC, Bellairs R, (1986) An experimental and morphological analysis of the tail bud mesenchyme of the chick embryo. Anat Embryol (Berl) 174: 179-185.
16. Gomez C, Ozbudak EM, Wunderlich J, Baumann D, Lewis J, et al. (2008) Control of segment number in vertebrate embryos. Nature 454: 335-339.
17. Tenin G, Wright D, Ferjentsik Z, Bone R, McGrew MJ, et al. (2010) The chick somitogenesis oscillator is arrested before all paraxial mesoderm is segmented into somites. BMC Dev Biol 10: 24.
18. Young T, Rowland JE, van de Ven C, Bialecka M, Novoa A, et al. (2009) Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev Cell 17: 516-526.
19. Savory JG, Bouchard N, Pierre V, Rijli FM, De Repentigny Y, et al. (2009) Cdx2 regulation of posterior development through non-Hox targets. Development 136: 4099-4110.
20. Isaacs HV, Pownall ME, Slack JM, (1998) Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. Embo J 17: 3413-3427.
21. Bel-Vialar S, Itasaki N, Krumlauf R, (2002) Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129: 5103-5115.
22. Naiche LA, Holder N, Lewandoski M, (2011) FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis. Proc Natl Acad Sci U S A 108: 4018-4023.
23. Dobrovolskaia-Zavadskaia N, (1927) Sur la mortification spontanee de la queue chez la souris nouveau-nee et sur l'existence d'un caractere hereditaire "non viable". C R Hebd Soc Biol 97: 114-116.
24. Herrmann BG, Labeit S, Poustka A, King TR, Lehrach H, (1990) Cloning of the T gene required in mesoderm formation in the mouse. Nature 343: 617-622.
25. Martin BL, Kimelman D, (2010) Brachyury establishes the embryonic mesodermal progenitor niche. Genes & Development 24: 2778-2783.
26. Reijntjes S, Blentic A, Gale E, Maden M, (2005) The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol 285: 224-237.
27. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP, (1999) T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13: 3185-3190.
28. Harvey SA, Tumpel S, Dubrulle J, Schier AF, Smith JC, (2010) No tail integrates two modes of mesoderm induction. Development 137: 1127-1135.
29. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, et al. (2001) The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15: 226-240.
30. Ciruna BG, Schwartz L, Harpal K, Yamaguchi TP, Rossant J, (1997) Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development 124: 2829-2841.
31. Sakai Y, Meno C, Fujii H, Nishino J, Shiratori H, et al. (2001) The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev 15: 213-225.
32. Deng C, Bedford M, Li C, Xu X, Yang X, et al. (1997) Fibroblast growth factor receptor-1 (FGFR-1) is essential for normal neural tube and limb development. Dev Biol 185: 42-54.
33. Ribes V, Le Roux I, Rhinn M, Schuhbaur B, Dolle P, (2009) Early mouse caudal development relies on crosstalk between retinoic acid, Shh and Fgf signalling pathways. Development 136: 665-676.
34. Martin BL, Kimelman D, (2012) Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Developmental Cell 22: 223-232.
35. Cunningham TJ, Zhao X, Duester G, (2011) Uncoupling of retinoic acid signaling from tailbud development prior to termination of body axis extension. Genesis.
36. Criley BB, (1969) Analysis of the embryonic sources and mechanisms of development of the posterior levels of chick neural tubes. J Morph 128: 465-502.
37. Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, et al. (1999) Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126: 4465-4475.
38. Miller SA, Briglin A, (1996) Apoptosis removes chick embryo tail gut and remnant of the primitive streak. Developmental Dynamics 206: 212-218.
39. O'Rahilly R, Muller F, (2003) Somites, spinal Ganglia, and centra. Enumeration and interrelationships in staged human embryos, and implications for neural tube defects. Cells, Tissues, Organs 173: 75-92.
40. Takemoto T, Uchikawa M, Yoshida M, Bell DM, Lovell-Badge R, et al. (2011) Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470: 394-398.
41. Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H, (2003) Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 4: 509-519.
42. Takemoto T, Uchikawa M, Kamachi Y, Kondoh H, (2006) Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development 133: 297-306.
43. de The H, Vivanco-Ruiz MM, Tiollais P, Stunnenberg H, Dejean A, (1990) Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343: 177-180.
44. Rossant J, Zirngibl R, Cado D, Shago M, Giguere V, (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev 5: 1333-1344.
45. Bastien J, Rochette-Egly C, (2004) Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328: 1-16.
46. Durand B, Saunders M, Leroy P, Leid M, Chambon P, (1992) All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell 71: 73-85.
47. Kitamoto T, Momoi M, Momoi T, (1989) Expression of cellular retinoic acid binding protein II (chick-CRABP II) in the chick embryo. Biochem Biophys Res Commun 164: 531-536.
48. Maden M, (1994) Distribution of cellular retinoic acid-binding proteins I and II in the chick embryo and their relationship to teratogenesis. Teratology 50: 294-301.
49. Perez-Castro AV, Toth-Rogler LE, Wei LN, Nguyen-Huu MC, (1989) Spatial and temporal pattern of expression of the cellular retinoic acid-binding protein and the cellular retinol-binding protein during mouse embryogenesis. Proc Natl Acad Sci U S A 86: 8813-8817.
50. Ruberte E, Friederich V, Morriss-Kay G, Chambon P, (1992) Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis. Development 115: 973-987.
51. Diez del Corral R, Breitkreuz DN, Storey KG, (2002) Onset of neuronal differentiation is regulated by paraxial mesoderm and requires attenuation of FGF signalling. Development 129: 1681-1691.
52. Kostetskii I, Yuan SY, Kostetskaia E, Linask KK, Blanchet S, et al. (1998) Initial retinoid requirement for early avian development coincides with retinoid receptor coexpression in the precardiac fields and induction of normal cardiovascular development. Dev Dyn 213: 188-198.
53. Niederreither K, Subbarayan V, Dolle P, Chambon P, (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444-448.
54. Bellairs R, (1961) Cell death in chick embryos as studied by electron microscopy. J Anat 95: 54-60.
55. Mills CL, Bellairs R, (1989) Mitosis and cell death in the tail of the chick embryo. Anat Embryol 180: 301-308.
56. Sureka D, Hudgins L, (2010) Fibroblast growth factor receptor 2 and its role in caudal appendage and craniosynostosis. J Craniofac Surg 21: 1346-1349.
57. Gaunt SJ, Drage D, Trubshaw RC, (2008) Increased Cdx protein dose effects upon axial patterning in transgenic lines of mice. Development 135: 2511-2520.
58. Isaacs HV, Pownall ME, Slack JM, (1994) eFGF regulates Xbra expression during Xenopus gastrulation. EMBO J 13: 4469-4481.
59. Arnold SJ, Stappert J, Bauer A, Kispert A, Herrmann BG, et al. (2000) Brachyury is a target gene of the Wnt/beta-catenin signaling pathway. Mech Dev 91: 249-258.
60. Martin BL, Kimelman D, (2008) Regulation of canonical Wnt signaling by Brachyury is essential for posterior mesoderm formation. Developmental Cell 15: 121-133.
61. Hofmann M, Schuster-Gossler K, Watabe-Rudolph M, Aulehla A, Herrmann BG, et al. (2004) WNT signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dll1 expression in the presomitic mesoderm of mouse embryos. Genes Dev 18: 2712-2717.
62. Wardle FC, Papaioannou VE, (2008) Teasing out T-box targets in early mesoderm. Curr Opin Genet Dev 18: 418-425.
63. Abu-Abed S, Dolle P, Metzger D, Wood C, MacLean G, et al. (2003) Developing with lethal RA levels: genetic ablation of Rarg can restore the viability of mice lacking Cyp26a1. Development 130: 1449-1459.
64. Iulianella A, Beckett B, Petkovich M, Lohnes D, (1999) A molecular basis for retinoic acid-induced axial truncation. Dev Biol 205: 33-48.
65. Brondani V, Klimkait T, Egly JM, Hamy F, (2002) Promoter of FGF8 reveals a unique regulation by unliganded RARalpha. J Mol Biol 319: 715-728.
66. Zhao X, Sirbu IO, Mic FA, Molotkova N, Molotkov A, et al. (2009) Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr Biol 19: 1050-1057.
67. Astrom A, Tavakkol A, Pettersson U, Cromie M, Elder JT, et al. (1991) Molecular cloning of two human cellular retinoic acid-binding proteins (CRABP). Retinoic acid-induced expression of CRABP-II but not CRABP-I in adult human skin in vivo and in skin fibroblasts in vitro. The Journal of Biological Chemistry 266: 17662-17666.
68. Giguere V, Lyn S, Yip P, Siu CH, Amin S, (1990) Molecular cloning of cDNA encoding a second cellular retinoic acid-binding protein. Proc Natl Acad Sci U S A 87: 6233-6237.
69. Chen AC, Gudas LJ, (1996) An analysis of retinoic acid-induced gene expression and metabolism in AB1 embryonic stem cells. J Biol Chem 271: 14971-14980.
70. Sonneveld E, van den Brink CE, van der Leede BJ, Maden M, van der Saag PT, (1999) Embryonal carcinoma cell lines stably transfected with mRARbeta2-lacZ: sensitive system for measuring levels of active retinoids. Exp Cell Res 250: 284-297.
71. Schoenwolf GC, (1981) Morphogenetic processes involved in the remodeling of the tail region of the chick embryo. Anat Embryol Berl 162: 183-197.
72. Tickle C, Crawley A, Farrar J, (1989) 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 106: 691-705.
73. Brown JM, Robertson KE, Wedden SE, Tickle C, (1997) Alterations in Msx 1 and Msx 2 expression correlate with inhibition of outgrowth of chick facial primordia induced by retinoic acid. Anat Embryol Berl 195: 203-207.
74. Hamburger H, Hamilton HL, (1951) A series of normal stages in the development of the chick embryo. J Exp Morphol 88: 49-92.
75. Chapman SC, Collignon J, Schoenwolf GC, Lumsden A, (2001) Improved method for chick whole-embryo culture using a filter paper carrier. Dev Dyn 220: 284-289.
76. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, et al. (1997) Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276: 955-960.
77. Davies SP, Reddy H, Caivano M, Cohen P, (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.
78. Brown JM, Storey KG, (2000) A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal cell fates. Curr Biol 10: 869-872.