Timed interactions between the Hox expressing non-organiser mesoderm and the Spemann organiser generate positional information during vertebrate gastrulation

Developmental Biology

Volumn 268, Issue 1, 2004, Pages 207-219

  Wacker, Stephan A ^a   Jansen, Hans J ^a   McNulty, Claire L ^a   Houtzager, Erwin ^a   Durston, Antony J ^a  

^a HUBRECHT INSTITUTE   (Netherlands)

Author keywords

Gastrulation; Hox gene; Spemann organiser

Indexed keywords

ANTERIOR POSTERIOR AXIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GASTRULATION; GENE ACTIVATION; GENE EXPRESSION; HOX GENE; MESODERM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VERTEBRATE; XENOPUS;

VERTEBRATA; XENOPUS LAEVIS;

EID: 1642278656     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.12.022     Document Type: Article

References (87)

1. Agathon A., Thisse C., Thisse B. The molecular nature of the zebrafish tail organizer. Nature. 424:2003;448-452.
2. Alexandre D., Clarke J.D., Oxtoby E., Yan Y.L., Jowett T., Holder N. Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype. Development. 122:1996;735-746.
3. Bang A.G., Papalopulu N., Kintner C., Goulding M.D. Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development. 124:1997;2075-2085.
4. Bang A.G., Papalopulu N., Goulding M.D., Kintner C. Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm. Dev. Biol. 212:1999;366-380.
5. Barnett M.W., Old R.W., Jones E.A. Neural induction and patterning by fibroblast growth factor, notochord and somite tissue in Xenopus. Dev. Growth Differ. 40:1998;47-57.
6. Beddington R.S., Robertson E.J. Anterior patterning in mouse. Trends Genet. 14:1998;277-284.
7. Bradley L.C., Snape A., Bhatt S., Wilkinson D.G. The structure and expression of the Xenopus Krox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest. Mech. Dev. 40:1993;73-84.
8. Busse U., Seguin C. Molecular analysis of the Wnt-1 proto-oncogene in Ambystoma mexicanum (axolotl) embryos. Differentiation. 53:1993;7-15.
9. Chen Y., Hollemann T., Pieler T., Grunz H. Planar signalling is not sufficient to generate a specific anterior/posterior neural pattern in pseudoexogastrula explants from Xenopus and Triturus. Mech. Dev. 90:2000;53-63.
10. Condie B.G., Harland R.M. Posterior expression of a homeobox gene in early Xenopus embryos. Development. 101:1987;93-105.
11. Conlon F.L., Smith J.C. Interference with brachyury function inhibits convergent extension, causes apoptosis, and reveals separate requirements in the FGF and activin signalling pathways. Dev. Biol. 213:1999;85-100.
12. Cooke J., Smith J.C. Gastrulation and larval pattern in Xenopus after blastocoelic injection of a Xenopus-derived inducing factor: experiments testing models for the normal organization of mesoderm. Dev. Biol. 131:1989;383-400.
13. Cox W.G., Hemmati-Brivanlou A. Caudalization of neural fate by tissue recombination and bFGF. Development. 121:1995;4349-5821.
14. Darnell D.K., Stark M.R., Schoenwolf G.C. Timing and cell interactions underlying neural induction in the chick embryo. Development. 126:1999;2505-2514.
15. De Robertis E.M., Sasai Y. A common plan for dorsoventral patterning in Bilateria. Nature. 380:1996;37-40.
16. Deschamps J., Wijgerde M. Two phases in the establishment of HOX expression domains. Dev. Biol. 156:1993;473-480.
17. Deschamps J., van den Akker E., Forlani S., De Graaff W., Oosterveen T., Roelen B., Roelfsema J. Initiation, establishment and maintenance of Hox gene expression patterns in the mouse. Int. J. Dev. Biol. 43:1999;635-650.
18. Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl. 1994;135-142.
19. Duboule D., Dolle P. The structural and functional organization of the murine Hox gene family resembles that of Drosophila homeotic genes. EMBO J. 8:1989;1497-1505.
20. Duboule D., Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10:1994;358-364.
21. Durston A.J., Timmermans J.P., Hage W.J., Hendriks H.F., de Vries N.J., Heideveld M., Nieuwkoop P.D. Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature. 340:1989;140-146.
22. Erter C.E., Wilm T.P., Basler N., Wright C.V., Solnica-Krezel L. Wnt8 is required in lateral mesendodermal precursors for neural posteriorization in vivo. Development. 128:2001;3571-3583.
23. Fujii H., Nagai T., Shirasawa H., Doi J., Yasui K., Nishimatsu S., Takeda H., Sakai M. Anteroposterior patterning in Xenopus embryos: egg fragment assay system reveals a synergy of dorsalizing and posteriorizing embryonic domains. Dev. Biol. 252:2002;15-30.
24. Gaunt S.J. Evolutionary shifts of vertebrate structures and Hox expression up and down the axial series of segments: a consideration of possible mechanisms. Int. J. Dev. Biol. 44:2000;109-117.
25. Gaunt S.J., Strachan L. Forward spreading in the establishment of a vertebrate Hox expression boundary: the expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev. Dyn. 199:1994;229-240.
26. Gaunt S.J., Strachan L. Temporal colinearity in expression of anterior Hox genes in developing chick embryos. Dev. Dyn. 207:1996;270-280.
27. Gaunt S.J., Dean W., Sang H., Burton R.D. Evidence that Hoxa expression domains are evolutionarily transposed in spinal ganglia, and are established by forward spreading in paraxial mesoderm. Mech. Dev. 82:1999;109-118.
28. Godsave S.F., Koster C.H., Getahun A., Mathu M., Hooiveld M., van der Wees J., Hendriks J., Durston A.J. Graded retinoid responses in the developing hindbrain. Dev. Dyn. 213:1998;39-49.
29. Gould A., Itasaki N., Krumlauf R. Initiation of rhombomeric Hoxb-4 expression requires induction by somites and a retinoid pathway. Neuron. 21:1998;39-51.
30. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell. 57:1989;367-378.
31. Grapin-Botton A., Bonnin M.A., Le Douarin N.M. Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group. Development. 124:1997;849-859.
32. Green J.B., Cook T.L., Smith J.C., Grainger R.M. Anteroposterior neural tissue specification by activin-induced mesoderm. Proc. Natl. Acad. Sci. U. S. A. 94:1997;8596-8601.
33. Griffin K., Patient R., Holder N. Analysis of FGF function in normal and no tail zebrafish embryos reveals separate mechanisms for formation of the trunk and the tail. Development. 121:1995;2983-2994.
34. Grinblat Y., Gamse J., Patel M., Sive H. Determination of the zebrafish forebrain: induction and patterning. Development. 125:1998;4403-4416.
35. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36:1991;685-695.
36. Harland R. Neural induction. Curr. Opin. Genet. Dev. 10:2000;357-362.
37. Harland R.M., Gerhart J. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13:1997;611-667.
38. Hedgepeth C.M., Conrad L.J., Zhang J., Huang H.C., Lee V.M., Klein P.S. Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev. Biol. 185:1997;82-91.
39. Hemmati-Brivanlou A., de la Torre J., Holt C., Harland R.M. Cephalic expression and molecular characterization of Xenopus En-2. Development. 111:1991;715-724.
40. Hoppler S., Moon R.T. BMP-2/-4 and Wnt-8 cooperatively pattern the Xenopus mesoderm. Mech. Dev. 71:1998;119-129.
41. Itasaki N., Sharpe J., Morrison A., Krumlauf R. Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron. 16:1996;487-500.
42. Izpisua-Belmonte J.C., Falkenstein H., Dolle P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 10:1991;2279-2289.
43. Kao K.R., Elinson R.P. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127:1988;64-77.
44. Keller R.E., Danilchik M. Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. Development. 103:1988;193-209.
45. Keller R.E., Danilchik M., Gimlich R., Shih J. Convergent extension by cell intercalation during gastrulation of Xenopus laevis. Molecular Determinants of Animal Form. 1985;Alan R. Liss, New York.
46. Kengaku M., Okamoto H. bFGF as a possible morphogen for the anteroposterior axis of the central nervous system in Xenopus. Development. 121:1995;3022-3121.
47. Kiecker C., Niehrs C. A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development. 128:2001;4189-4201.
48. Kolm P.J., Apekin V., Sive H. Xenopus hindbrain patterning requires retinoid signaling. Dev. Biol. 192:1997;1-16.
49. Kühl M., Geis K., Sheldahl L.C., Pukrop T., Moon R.T., Wedlich D. Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. Mech. Dev. 106:2001;61-76.
50. Lamb T.M., Harland R.M. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development. 121:1995;3627-3636.
51. Larabell C.A., Torres M., Rowning B.A., Yost C., Miller J.R., Wu M., Kimelman D., Moon R.T. Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway. J. Cell Biol. 136:1997;1123-1136.
52. Lemaire P., Kodjabachian L. The vertebrate organizer: structure and molecules. Trends Genet. 12:1996;525-531.
53. Leroy P., De Robertis E.M. Effects of lithium chloride and retinoic acid on the expression of genes from the Xenopus laevis Hox 2 complex. Dev. Dyn. 194:1992;21-32.
54. Mangold O. Über die Induktionsfähigkeit der verschiedenen Bezirke der Neurula von Urodelen. Naturwissenschaften. 21:1933;761-766.
55. McGrew L.L., Hoppler S., Moon R.T. Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech. Dev. 69:1997;105-114.
56. Muhr J., Jessell T.M., Edlund T. Assignment of early caudal identity to neural plate cells by a signal from caudal paraxial mesoderm. Neuron. 19:1997;487-502.
57. Muhr J., Graziano E., Wilson S., Jessell T.M., Edlund T. Convergent inductive signals specify midbrain, hindbrain, and spinal cord identity in gastrula stage chick embryos. Neuron. 23:1999;689-702.
58. Niehrs C. Head in the WNT: the molecular nature of Spemann's head organizer. Trends Genet. 15:1999;314-319.
59. Nieuwkoop P.D. Activation and organisation of the central nervous system in amphibians, III. Synthesis of a new working hypothesis. J. Exp. Zool. 120:1952;83-108.
60. Nieuwkoop P., Albers B. The role of competence in the cranio-caudal segregation of the central nervous system. Dev. Growth Differ. 32:1990;23-31.
61. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin). 1956;North-Holland, Amsterdam.
62. Nieuwkoop P.D., Koster K. Vertical versus planar induction in amphibian early development. Dev. Growth Differ. 37:1995;653-668.
63. Pownall M.E., Tucker A.S., Slack J.M., Isaacs H.V. eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development. 122:1996;3881-3892.
64. Poznanski A., Keller R. The role of planar and early vertical signaling in patterning the expression of Hoxb-1 in Xenopus. Dev. Biol. 184:1997;351-366.
65. Richter K., Good P.J., Dawid I.B. A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. New Biol. 2:1990;556-565.
66. Ruiz I Altaba A., Jessell T.M. Retinoic acid modifies the pattern of cell differentiation in the central nervous system of neurula stage Xenopus embryos. Development. 112:1991;945-958.
67. Saha M.S., Grainger R.M. A labile period in the determination of the anterior-posterior axis during early neural development in Xenopus. Neuron. 8:1992;1003-1014.
68. Scharf S.R., Gerhart J.C. Axis determination in eggs of Xenopus laevis: a critical period before first cleavage, identified by the common effects of cold, pressure and ultraviolet irradiation. Dev. Biol. 99:1983;75-87.
69. Schohl A., Fagotto F. Beta-catenin, MAPK and Smad signaling during early Xenopus development. Development. 129:2002;37-52.
70. Sharpe C.R. Retinoic acid can mimic endogenous signals involved in transformation of the Xenopus nervous system. Neuron. 7:1991;239-247.
71. Sive H.L., Cheng P.F. Retinoic acid perturbs the expression of Xhox.lab genes and alters mesodermal determination in Xenopus laevis. Genes Dev. 5:1991;1321-1332.
72. Slack J.M., Forman D. An interaction between dorsal and ventral regions of the marginal zone in early amphibian embryos. J. Embryol. Exp. Morphol. 56:1980;283-299.
73. Smith J.C., Price B.M., Green J.B., Weigel D., Herrmann B.G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell. 67:1991;79-87.
74. Smith W.C., Knecht A.K., Wu M., Harland R.M. Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature. 361:1993;547-549.
75. Spemann H. Über den Anteil von Implantat und Wirtskeim an der Orientierung und Beschaffenheit der induzierten Embryonalanlage. W. Roux's Arch. Entwicklungsmech. Org. 123:1931;390-517.
76. Storey K.G., Crossley J.M., De Robertis E.M., Norris W.E., Stern C.D. Neural induction and regionalisation in the chick embryo. Development. 114:1992;729-741.
77. Streit A., Berliner A.J., Papanayotou C., Sirulnik A., Stern C.D. Initiation of neural induction by FGF signalling before gastrulation. Nature. 406:2000;74-78.
78. Takada S., Stark K.L., Shea M.J., Vassileva G., McMahon J.A., McMahon A.P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8:1994;174-189.
79. Wacker S., Grimm K., Joos T., Winklbauer R. Development and control of tissue separation at gastrulation in Xenopus. Dev. Biol. 224:2000;428-439.
80. Wacker S.A., McNulty C.L., Durston A.J. The initiation of Hox gene expression in Xenopus laevis is controlled by Brachyury and BMP-4. Dev. Biol. 266:2004;123-137.
81. Weinstein D.C., Hemmati-Brivanlou A. Neural induction. Annu. Rev. Cell Dev. Biol. 15:1999;411-433.
82. Wilson S.I., Edlund T. Neural induction: toward a unifying mechanism. Nat. Neurosci. 4 Suppl. 2001;1161-1168.
83. Wilson P.A., Keller R.E. Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. Development. 112:1991;289-300.
84. Winklbauer R. Mesodermal cell migration during Xenopus gastrulation. Dev. Biol. 142:1990;155-168.
85. Woo K., Fraser S.E. Specification of the zebrafish nervous system by nonaxial signals. Science. 277:1997;254-257.
86. Woo K., Fraser S.E. Specification of the hindbrain fate in the zebrafish. Dev. Biol. 197:1998;283-296.
87. Zoltewicz J.S., Gerhart J.C. The Spemann organizer of Xenopus is patterned along its anteroposterior axis at the earliest gastrula stage. Dev. Biol. 192:1997;482-491.