Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid

This study analyzes the function of the homeobox gene goosecoid in Xenopus development. First, we find that goosecoid mRNA distribution closely mimics the expected localization of organizer tissue in normal embryos as well as in those treated with LiCl and UV light. Second, goosecoid mRNA accumulation is induced by activin, even in the absence of protein synthesis. It is not affected by bFGF and is repressed by retinoic acid. Lastly, microinjection of goosecoid mRNA into the ventral side of Xenopus embryos, where goosecoid is normally absent, leads to the formation of an additional complete body axis, including head structures and abundant notochordal tissue. The results suggest that the goosecoid homeodomain protein plays a central role in executing Spemann's organizer phenomenon.

[1]  W. Busa,et al.  Lithium-induced teratogenesis in frog embryos prevented by a polyphosphoinositide cycle intermediate or a diacylglycerol analog. , 1989, Developmental biology.

[2]  A. Simeone,et al.  Sequential activation of human HOX2 homeobox genes by retinoic acid in embryonal carcinoma cells. , 1990 .

[3]  J. Cooke,et al.  Mesoderm-inducing factors and Spemann's organiser phenomenon in amphibian development. , 1989, Development.

[4]  H. Spemann.  Embryonic development and induction , 1938 .

[5]  C. Niehrs,et al.  Ectopic expression of a homeobox gene changes cell fate in Xenopus embryos in a position‐specific manner. , 1991, The EMBO journal.

[6]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage , 1982, Cell.

[7]  C. Phillips,et al.  Signals from the dorsal blastopore lip region during gastrulation bias the ectoderm toward a nonepidermal pathway of differentiation in Xenopus laevis. , 1989, Developmental biology.

[8]  C. Kintner,et al.  Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals. , 1989, Development.

[9]  E. D. De Robertis,et al.  Differential activation of Xenopus homeo box genes by mesoderm-inducing growth factors and retinoic acid. , 1990, Genes & development.

[10]  R. Keller,et al.  Vital dye mapping of the gastrula and neurula of Xenopus laevis: I. Prospective areas and morphogenetic movements of the superficial layer , 1976 .

[11]  P. Nieuwkoop.  The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. , 1973, Advances in morphogenesis.

[12]  S. L. Klein.  The first cleavage furrow demarcates the dorsal-ventral axis in Xenopus embryos. , 1987, Developmental biology.

[13]  J. Vaughan,et al.  Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures , 1990, Cell.

[14]  J. Gerhart,et al.  Early cellular interactions promote embryonic axis formation in Xenopus laevis. , 1984, Developmental biology.

[15]  J. Cooke.  Properties of the primary organization field in the embryo of Xenopus laevis. V. Regulation after removal of the head organizer, in normal early gastrulae and in those already possessing a second implanted organizer. , 1973, Journal of embryology and experimental morphology.

[16]  D. Melton,et al.  Pattern formation during animal development. , 1991, Science.

[17]  E. D. De Robertis,et al.  Homeobox genes and the vertebrate body plan. , 1990, Scientific American.

[18]  C. Nüsslein-Volhard,et al.  Determination of the embryonic axes of Drosophila. , 1991, Development (Cambridge, England). Supplement.

[19]  H. Hendriks,et al.  Retinoic acid causes an anteroposterior transformation in the developing central nervous system , 1989, Nature.

[20]  D. Melton,et al.  Interaction between peptide growth factors and homoeobox genes in the establishment of antero-posterior polarity in frog embryos , 1989, Nature.

[21]  A. Simeone,et al.  Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells , 1990, Nature.

[22]  T. Jessell,et al.  Retinoic acid modifies mesodermal patterning in early Xenopus embryos. , 1991, Genes & development.

[23]  P. Gruss,et al.  Murine developmental control genes. , 1990, Science.

[24]  H. Weintraub,et al.  Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. , 1990, Genes & development.

[25]  J. Cooke.  Properties of the primary organization field in the embryo of Xenopus laevis. II. Positional information for axial organization in embryos with two head organizers. , 1972, Journal of embryology and experimental morphology.

[26]  L. Wolpert.  Positional information revisited. , 1989, Development.

[27]  E. D. De Robertis,et al.  Differential utilization of the same reading frame in a Xenopus homeobox gene encodes two related proteins sharing the same DNA‐binding specificity. , 1988, The EMBO journal.

[28]  J. Gerhart,et al.  Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. , 1989, Development.

[29]  P. Cheng,et al.  Retinoic acid perturbs the expression of Xhox.lab genes and alters mesodermal determination in Xenopus laevis. , 1991, Genes & development.

[30]  R. Harland,et al.  Localization of specific mRNAs in Xenopus embryos by whole-mount in situ hybridization. , 1990, Development.

[31]  J. Slack,et al.  The role of fibroblast growth factor in early Xenopus development. , 1989, Development.

[32]  R. R. Bensley,et al.  Embryonic Development and Induction , 1938, The Yale Journal of Biology and Medicine.

[33]  J. Slack.  From Egg to Embryo , 1983 .

[34]  J. Smith,et al.  Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate , 1990, Nature.

[35]  J. Gerhart,et al.  The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the late blastula. , 1990, Development.

[36]  Ken W. Y. Cho,et al.  Overexpression of a homeodomain protein confers axis-forming activity to uncommitted xenopus embryonic cells , 1991, Cell.

[37]  R. Keller,et al.  Vital Dye Mapping of the Gastrula and Neurula of Xenopus Laevis , 1975 .

[38]  J. Faber,et al.  Normal Table of Xenopus Laevis (Daudin) , 1958 .

[39]  K. Kao,et al.  The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. , 1988, Developmental biology.

[40]  K. Kao,et al.  The Location of Dorsal Information in Frog Early Development , 1989, Development, growth & differentiation.

[41]  C. Nüsslein-Volhard,et al.  The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner , 1988, Cell.

[42]  F. Rosa.  Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos , 1989, Cell.

[43]  E. D. De Robertis,et al.  Duplicated homeobox genes in Xenopus. , 1989, Developmental biology.

[44]  D. Melton,et al.  Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. , 1984, Nucleic acids research.

[45]  J C Smith,et al.  The organization of mesodermal pattern in Xenopus laevis: experiments using a Xenopus mesoderm-inducing factor. , 1987, Development.

[46]  W. Gehring,et al.  Homeo boxes in the study of development. , 1987, Science.

[47]  E. D. De Robertis,et al.  Gradient fields and homeobox genes. , 1991, Development.

[48]  J A Dent,et al.  A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. , 1989, Development.

[49]  J C Smith,et al.  Cell lineage labels and region-specific markers in the analysis of inductive interactions. , 1985, Journal of embryology and experimental morphology.

[50]  J. Cooke,et al.  Inducing factors and the control of mesodermal pattern in Xenopus laevis. , 1989, Development.

[51]  M. Kirschner,et al.  Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in xenopus embryos , 1991, Cell.

[52]  R. Gimlich.  Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. , 1986, Developmental biology.

[53]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: II. control of the onset of transcription , 1982, Cell.

[54]  Y. Kobayakawa,et al.  A cytoplasmic determinant for dorsal axis formation in an early embryo of Xenopus laevis. , 1990, Development.

[55]  B. Blumberg,et al.  Organizer-specific homeobox genes in Xenopus laevis embryos. , 1991, Science.