A feed-forward relay integrates the regulatory activities of Bicoid and Orthodenticle via sequential binding to suboptimal sites
The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In , another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is dis...
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Published in | Genes & development Vol. 32; no. 9-10; pp. 723 - 736 |
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Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Cold Spring Harbor Laboratory Press
01.05.2018
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Abstract | The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In
, another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is distributed as a long-range maternal gradient and activates transcription of a large number of target genes, including
Otd and Bcd bind similar DNA sequences in vitro, but how their transcriptional activities are integrated to pattern anterior regions of the embryo is unknown. Here we define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bcd and Otd. Class 1 enhancers are initially activated by Bcd, and activation is transferred to Otd via a feed-forward relay (FFR) that involves sequential binding of the two proteins to the same DNA motif. Class 2 enhancers are activated by Bcd and maintained by an Otd-independent mechanism. Class 3 enhancers are never bound by Bcd, but Otd binds and activates them in a second wave of zygotic transcription. The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. Our results define specific patterning roles for Bcd and Otd and provide mechanisms for coordinating the precise timing of gene expression patterns during embryonic development. |
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AbstractList | The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In
, another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is distributed as a long-range maternal gradient and activates transcription of a large number of target genes, including
Otd and Bcd bind similar DNA sequences in vitro, but how their transcriptional activities are integrated to pattern anterior regions of the embryo is unknown. Here we define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bcd and Otd. Class 1 enhancers are initially activated by Bcd, and activation is transferred to Otd via a feed-forward relay (FFR) that involves sequential binding of the two proteins to the same DNA motif. Class 2 enhancers are activated by Bcd and maintained by an Otd-independent mechanism. Class 3 enhancers are never bound by Bcd, but Otd binds and activates them in a second wave of zygotic transcription. The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. Our results define specific patterning roles for Bcd and Otd and provide mechanisms for coordinating the precise timing of gene expression patterns during embryonic development. The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In Drosophila melanogaster, another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is distributed as a long-range maternal gradient and activates transcription of a large number of target genes, including otd Otd and Bcd bind similar DNA sequences in vitro, but how their transcriptional activities are integrated to pattern anterior regions of the embryo is unknown. Here we define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bcd and Otd. Class 1 enhancers are initially activated by Bcd, and activation is transferred to Otd via a feed-forward relay (FFR) that involves sequential binding of the two proteins to the same DNA motif. Class 2 enhancers are activated by Bcd and maintained by an Otd-independent mechanism. Class 3 enhancers are never bound by Bcd, but Otd binds and activates them in a second wave of zygotic transcription. The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. Our results define specific patterning roles for Bcd and Otd and provide mechanisms for coordinating the precise timing of gene expression patterns during embryonic development. Datta et al. define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bicoid (Bcd) and Orthodenticle (Otd). The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In Drosophila melanogaster , another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is distributed as a long-range maternal gradient and activates transcription of a large number of target genes, including otd . Otd and Bcd bind similar DNA sequences in vitro, but how their transcriptional activities are integrated to pattern anterior regions of the embryo is unknown. Here we define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bcd and Otd. Class 1 enhancers are initially activated by Bcd, and activation is transferred to Otd via a feed-forward relay (FFR) that involves sequential binding of the two proteins to the same DNA motif. Class 2 enhancers are activated by Bcd and maintained by an Otd-independent mechanism. Class 3 enhancers are never bound by Bcd, but Otd binds and activates them in a second wave of zygotic transcription. The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. Our results define specific patterning roles for Bcd and Otd and provide mechanisms for coordinating the precise timing of gene expression patterns during embryonic development. The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in most metazoans. In Drosophila melanogaster , another K50HD protein, Bicoid (Bcd), has evolved to replace Otd's ancestral function in embryo patterning. Bcd is distributed as a long-range maternal gradient and activates transcription of a large number of target genes, including otd . Otd and Bcd bind similar DNA sequences in vitro, but how their transcriptional activities are integrated to pattern anterior regions of the embryo is unknown. Here we define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bcd and Otd. Class 1 enhancers are initially activated by Bcd, and activation is transferred to Otd via a feed-forward relay (FFR) that involves sequential binding of the two proteins to the same DNA motif. Class 2 enhancers are activated by Bcd and maintained by an Otd-independent mechanism. Class 3 enhancers are never bound by Bcd, but Otd binds and activates them in a second wave of zygotic transcription. The specific activities of enhancers in each class are mediated by DNA motif variants preferentially bound by Bcd or Otd and the presence or absence of sites for cofactors that interact with these proteins. Our results define specific patterning roles for Bcd and Otd and provide mechanisms for coordinating the precise timing of gene expression patterns during embryonic development. |
Author | Ling, Jia Xu, Zhe Struffi, Paolo Yucel, Gozde Shokri, Leila Ren, Xiaotong Bishop, Timothy Johnston, Jr, Robert J Baker, Isabel Kurland, Jesse Levina, Rimma Small, Stephen Datta, Rhea R Bulyk, Martha L Moore, Jackie |
AuthorAffiliation | 3 Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA 2 Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA 1 Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA 4 Department of Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA |
AuthorAffiliation_xml | – name: 4 Department of Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA – name: 2 Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA – name: 3 Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA – name: 1 Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA |
Author_xml | – sequence: 1 givenname: Rhea R orcidid: 0000-0002-2382-8930 surname: Datta fullname: Datta, Rhea R organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 2 givenname: Jia surname: Ling fullname: Ling, Jia organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 3 givenname: Jesse surname: Kurland fullname: Kurland, Jesse organization: Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA – sequence: 4 givenname: Xiaotong surname: Ren fullname: Ren, Xiaotong organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 5 givenname: Zhe surname: Xu fullname: Xu, Zhe organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 6 givenname: Gozde surname: Yucel fullname: Yucel, Gozde organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 7 givenname: Jackie surname: Moore fullname: Moore, Jackie organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 8 givenname: Leila surname: Shokri fullname: Shokri, Leila organization: Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA – sequence: 9 givenname: Isabel surname: Baker fullname: Baker, Isabel organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 10 givenname: Timothy surname: Bishop fullname: Bishop, Timothy organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 11 givenname: Paolo surname: Struffi fullname: Struffi, Paolo organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 12 givenname: Rimma surname: Levina fullname: Levina, Rimma organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA – sequence: 13 givenname: Martha L surname: Bulyk fullname: Bulyk, Martha L organization: Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA – sequence: 14 givenname: Robert J surname: Johnston, Jr fullname: Johnston, Jr, Robert J organization: Department of Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA – sequence: 15 givenname: Stephen surname: Small fullname: Small, Stephen organization: Center for Developmental Genetics, Department of Biology, New York University, New York, New York 10003, USA |
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Keywords | Bicoid transcription factor binding embryo suboptimal binding enhancer Orthodenticle |
Language | English |
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Snippet | The K50 (lysine at amino acid position 50) homeodomain (HD) protein Orthodenticle (Otd) is critical for anterior patterning and brain and eye development in... Datta et al. define three major classes of enhancers that are differentially sensitive to binding and transcriptional activation by Bicoid (Bcd) and... |
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SubjectTerms | Amino Acid Motifs Animals Body Patterning - genetics Drosophila melanogaster - embryology Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Embryonic Development - drug effects Embryonic Development - genetics Enhancer Elements, Genetic - genetics Gene Expression Regulation, Developmental Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Protein Binding Research Paper Trans-Activators - genetics Trans-Activators - metabolism |
Title | A feed-forward relay integrates the regulatory activities of Bicoid and Orthodenticle via sequential binding to suboptimal sites |
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