Krox20 hindbrain regulation incorporates multiple modes of cooperation between cis-acting elements

Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis-acting elements are poorly documented, notably in vertebrates. The mouse gen...

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Published inPLoS genetics Vol. 13; no. 7; p. e1006903
Main Authors Thierion, Elodie, Le Men, Johan, Collombet, Samuel, Hernandez, Céline, Coulpier, Fanny, Torbey, Patrick, Thomas-Chollier, Morgane, Noordermeer, Daan, Charnay, Patrick, Gilardi-Hebenstreit, Pascale
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 27.07.2017
Public Library of Science (PLoS)
Subjects
Animals
Biochemistry, Molecular Biology
Bioinformatics
Biology and Life Sciences
Body Patterning - genetics
Chromatin
Chromatin - genetics
Cooperation
Development Biology
Early Growth Response Protein 1 - biosynthesis
Early Growth Response Protein 1 - genetics
Enhancer Elements, Genetic
Enhancers
Feedback
Funding
Gene expression
Gene Expression Regulation, Developmental
Genetic aspects
Genetic regulation
Genomes
Hindbrain
Kinases
Krox-20 protein
Life Sciences
Medical research
Mice, Knockout
Mutation
Observations
Positive feedback
Proteins
Regulatory Elements, Transcriptional - genetics
Rhombencephalon
Rhombencephalon - growth & development
Rhombencephalon - metabolism
Rodents
Sequence Homology, Nucleic Acid
Software
Supervision
Vertebrates
France
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Abstract Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis-acting elements are poorly documented, notably in vertebrates. The mouse gene Krox20 encodes a transcription factor required for the specification of two segments (rhombomeres) of the developing hindbrain. In rhombomere 3, Krox20 is subject to direct positive feedback governed by an autoregulatory enhancer, element A. In contrast, a second enhancer, element C, distant by 70 kb, is active from the initiation of transcription independent of the presence of the KROX20 protein. Here, using both enhancer knock-outs and investigations of chromatin organisation, we show that element C possesses a dual activity: besides its classical enhancer function, it is also permanently required in cis to potentiate the autoregulatory activity of element A, by increasing its chromatin accessibility. This work uncovers a novel, asymmetrical, long-range mode of cooperation between cis-acting elements that might be essential to avoid promiscuous activation of positive autoregulatory elements.
AbstractList Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis-acting elements are poorly documented, notably in vertebrates. The mouse gene Krox20 encodes a transcription factor required for the specification of two segments (rhombomeres) of the developing hindbrain. In rhombomere 3, Krox20 is subject to direct positive feedback governed by an autoregulatory enhancer, element A. In contrast, a second enhancer, element C, distant by 70 kb, is active from the initiation of transcription independent of the presence of the KROX20 protein. Here, using both enhancer knock-outs and investigations of chromatin organisation, we show that element C possesses a dual activity: besides its classical enhancer function, it is also permanently required in cis to potentiate the autoregulatory activity of element A, by increasing its chromatin accessibility. This work uncovers a novel, asymmetrical, long-range mode of cooperation between cis-acting elements that might be essential to avoid promiscuous activation of positive autoregulatory elements.
Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis-acting elements are poorly documented, notably in vertebrates. The mouse gene Krox20 encodes a transcription factor required for the specification of two segments (rhombomeres) of the developing hindbrain. In rhombomere 3, Krox20 is subject to direct positive feedback governed by an autoregulatory enhancer, element A. In contrast, a second enhancer, element C, distant by 70 kb, is active from the initiation of transcription independent of the presence of the KROX20 protein. Here, using both enhancer knock-outs and investigations of chromatin organisation, we show that element C possesses a dual activity: besides its classical enhancer function, it is also permanently required in cis to potentiate the autoregulatory activity of element A, by increasing its chromatin accessibility. This work uncovers a novel, asymmetrical, long-range mode of cooperation between cis-acting elements that might be essential to avoid promiscuous activation of positive autoregulatory elements.Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis-acting elements are poorly documented, notably in vertebrates. The mouse gene Krox20 encodes a transcription factor required for the specification of two segments (rhombomeres) of the developing hindbrain. In rhombomere 3, Krox20 is subject to direct positive feedback governed by an autoregulatory enhancer, element A. In contrast, a second enhancer, element C, distant by 70 kb, is active from the initiation of transcription independent of the presence of the KROX20 protein. Here, using both enhancer knock-outs and investigations of chromatin organisation, we show that element C possesses a dual activity: besides its classical enhancer function, it is also permanently required in cis to potentiate the autoregulatory activity of element A, by increasing its chromatin accessibility. This work uncovers a novel, asymmetrical, long-range mode of cooperation between cis-acting elements that might be essential to avoid promiscuous activation of positive autoregulatory elements.
Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal expression. However, the mechanisms underlying cooperation between cis -acting elements are poorly documented, notably in vertebrates. The mouse gene Krox20 encodes a transcription factor required for the specification of two segments (rhombomeres) of the developing hindbrain. In rhombomere 3, Krox20 is subject to direct positive feedback governed by an autoregulatory enhancer, element A. In contrast, a second enhancer, element C, distant by 70 kb, is active from the initiation of transcription independent of the presence of the KROX20 protein. Here, using both enhancer knock-outs and investigations of chromatin organisation, we show that element C possesses a dual activity: besides its classical enhancer function, it is also permanently required in cis to potentiate the autoregulatory activity of element A, by increasing its chromatin accessibility. This work uncovers a novel, asymmetrical, long-range mode of cooperation between cis -acting elements that might be essential to avoid promiscuous activation of positive autoregulatory elements. The formation of multicellular organisms from the egg to the adult stage is largely under genetic control. The activation of specific genes is governed by regulatory DNA sequences present nearby on the chromosome. Most of these sequences promote activation and are called enhancers. In this paper, we study two enhancers governing the expression of a gene involved in the formation of the posterior brain in vertebrates. One of these enhancers is involved in a positive feedback loop: it is itself activated by the protein product of the gene that it regulates. The other enhancer was thought to be only involved in the initial accumulation of the protein, necessary for the subsequent activation of the feedback loop. Here we show that the second enhancer directly cooperates with the autoregulatory enhancer to increase its accessibility and its activity. Our work uncovers a novel, long-range mode of cooperation between enhancers that restricts the domain of action of autoregulatory enhancers within embryos and might be essential to avoid their inappropriate activation.
Audience Academic
Author Hernandez, Céline
Collombet, Samuel
Charnay, Patrick
Coulpier, Fanny
Torbey, Patrick
Thierion, Elodie
Le Men, Johan
Thomas-Chollier, Morgane
Gilardi-Hebenstreit, Pascale
Noordermeer, Daan
AuthorAffiliation 1 Ecole normale supérieure, PSL Research University, CNRS, Inserm, Institut de Biologie de l’Ecole normale supérieure (IBENS), Paris, France
3 Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, France
Centro Andaluz de Biología del Desarrollo, SPAIN
2 Sorbonne Universités, UPMC Univ Paris 06, IFD, Paris, France
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -acting elements. PLoS Genet 13(7): e1006903. https://doi.org/10.1371/journal.pgen.1006903
Distributed under a Creative Commons Attribution 4.0 International License
2017 Thierion et al 2017 Thierion et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -acting elements. PLoS Genet 13(7): e1006903. https://doi.org/10.1371/journal.pgen.1006903
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -acting elements. PLoS Genet 13(7): e1006903. https://doi.org/10.1371/journal.pgen.1006903
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: 2017 Thierion et al 2017 Thierion et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -acting elements. PLoS Genet 13(7): e1006903. https://doi.org/10.1371/journal.pgen.1006903
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Public Library of Science (PLoS)
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– name: Public Library of Science (PLoS)
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Snippet Developmental genes can harbour multiple transcriptional enhancers that act simultaneously or in succession to achieve robust and precise spatiotemporal...
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StartPage e1006903
SubjectTerms Animals
Biochemistry, Molecular Biology
Bioinformatics
Biology and Life Sciences
Body Patterning - genetics
Chromatin
Chromatin - genetics
Cooperation
Development Biology
Early Growth Response Protein 1 - biosynthesis
Early Growth Response Protein 1 - genetics
Enhancer Elements, Genetic
Enhancers
Feedback
Funding
Gene expression
Gene Expression Regulation, Developmental
Genetic aspects
Genetic regulation
Genomes
Hindbrain
Kinases
Krox-20 protein
Life Sciences
Medical research
Mice, Knockout
Mutation
Observations
Positive feedback
Proteins
Regulatory Elements, Transcriptional - genetics
Rhombencephalon
Rhombencephalon - growth & development
Rhombencephalon - metabolism
Rodents
Sequence Homology, Nucleic Acid
Software
Supervision
Vertebrates
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Title Krox20 hindbrain regulation incorporates multiple modes of cooperation between cis-acting elements
URI https://www.ncbi.nlm.nih.gov/pubmed/28749941
https://www.proquest.com/docview/1929400851
https://www.proquest.com/docview/1924604655
https://inserm.hal.science/inserm-02158641
https://pubmed.ncbi.nlm.nih.gov/PMC5549768
https://doaj.org/article/d3a4bbc3b0594c56bff0e9b49f7f0575
http://dx.doi.org/10.1371/journal.pgen.1006903
Volume 13
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