Three different noggin genes antagonize the activity of bone morphogenetic proteins in the zebrafish embryo.
The dorsoventral polarity of the vertebrate embryo is established through interactions between ventrally expressed bone morphogenetic proteins and their organizer-borne antagonists Noggin, Chordin, and Follistatin. While the opposing interactions between Short Gastrulation/Chordin and Decapentaplegic/BMP4 have been evolutionarily conserved in arthropods and vertebrates, there has been up to now no functional evidence of an implication of Noggin in the early patterning of organisms other than Xenopus. We have studied the contribution of Noggin to the embryonic development of the zebrafish. While single-copy noggin genes have been characterized in several vertebrate species, we report that the zebrafish genome harbors three noggin homologues. Overexpression experiments show that Noggin1, Noggin2, and Noggin3 can antagonize ventralizing BMPs. While all three factors have similar biological activities, their embryonic expression is different. The combined expression of the three genes recapitulates the different aspects of the expression of the single-copy noggin genes of other organisms. This suggests that the three zebrafish noggin genes and the single noggin genes of other vertebrates have evolved from a common ancestor and that subsequent differential loss of tissue-specific elements in the promoters of the different zebrafish genes accounts for their more restricted spatiotemporal expression. Finally we show that noggin1 is expressed in the fish organizer and able to dorsalize the embryo, suggesting its implication in the dorsoventral patterning of the zebrafish.
Fürthauer
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Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS, INSERM, ULP, 1 rue Laurent Fries, Illkirch Cedex, 67404, France.
Thisse
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Thisse
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D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D001755:Blastocyst / Q000502:physiology*; D019521:Body Patterning; D055415:Bone Morphogenetic Protein 4; D019485:Bone Morphogenetic Proteins / Q000235:genetics*; D002352:Carrier Proteins; D017931:DNA Primers; D004625:Embryo, Nonmammalian / Q000502:physiology*; D019143:Evolution, Molecular; D005775:Gastrula / Q000502:physiology*; D018507:Gene Expression Regulation, Developmental; D008969:Molecular Sequence Data; D009420:Nervous System / Q000196:embryology; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D011506:Proteins / Q000235:genetics*; D016415:Sequence Alignment; D017386:Sequence Homology, Amino Acid; D029867:Xenopus Proteins; D015027:Zebrafish / Q000196:embryology*; D029961:Zebrafish Proteins; D000099176:Noggin Protein
D055415:Bone Morphogenetic Protein 4; D019485:Bone Morphogenetic Proteins; D002352:Carrier Proteins; D017931:DNA Primers; D011506:Proteins; D029867:Xenopus Proteins; D029961:Zebrafish Proteins; D000099176:Noggin Protein; C525812:bmp4 protein, Xenopus; C525813:bmp4 protein, zebrafish