Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene

Abstract Background In Drosophila, architectural proteins are frequently found in promoters, including those of genes with extremely high expression levels, such as ribosomal protein genes (RPGs). The involvement of several of these proteins in gene regulation in Drosophila has been shown, but the e...

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Main Authors: Igor Osadchiy, Anastasia Umnova, Galina V. Pokholkova, Anton Golovnin, Vladimir A. Gvozdev, Igor F. Zhimulev, Pavel Georgiev, Oksana Maksimenko
Format: Article
Language:English
Published: BMC 2025-04-01
Series:Epigenetics & Chromatin
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Online Access:https://doi.org/10.1186/s13072-025-00584-8
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author Igor Osadchiy
Anastasia Umnova
Galina V. Pokholkova
Anton Golovnin
Vladimir A. Gvozdev
Igor F. Zhimulev
Pavel Georgiev
Oksana Maksimenko
author_facet Igor Osadchiy
Anastasia Umnova
Galina V. Pokholkova
Anton Golovnin
Vladimir A. Gvozdev
Igor F. Zhimulev
Pavel Georgiev
Oksana Maksimenko
author_sort Igor Osadchiy
collection DOAJ
description Abstract Background In Drosophila, architectural proteins are frequently found in promoters, including those of genes with extremely high expression levels, such as ribosomal protein genes (RPGs). The involvement of several of these proteins in gene regulation in Drosophila has been shown, but the exact mechanisms of their possible cooperative action have not been fully elucidated. Results In this study we dissected the contribution of the architectural proteins Opbp and M1BP, which are co-localized at several RPG promoters near the transcription start site, to promoter functioning. We found that Opbp has two domains that directly interact with CP190, Putzig (Pzg), and Chromator (Chro) proteins, the cofactors which are required for the activation of housekeeping (hk) gene promoters. These domains have redundant functions in vivo and can tether the cofactors forming open chromatin regions when are artificially recruited to the “closed” chromatin. Additionally, we observed interactions between M1BP and the same cofactors. In the transgene assay, the transcription driven by the 192-bp part of Rpl27A RPG promoter is fully dependent on the presence of at least one Opbp or M1BP binding site and it is sufficient for the very high activity of this promoter integrated into the hk gene cluster and moderate expression outside the cluster, while presence of both sites even more facilitates transcription. Conclusions This study demonstrates that different architectural proteins can work independently and in cooperation and fulfill partially redundant functions in the activation of RPG promoters.
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spelling doaj-art-1fe7ea0c7eaa4fe984456092d4cd74442025-08-20T02:28:11ZengBMCEpigenetics & Chromatin1756-89352025-04-0118111610.1186/s13072-025-00584-8Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein geneIgor Osadchiy0Anastasia Umnova1Galina V. Pokholkova2Anton Golovnin3Vladimir A. Gvozdev4Igor F. Zhimulev5Pavel Georgiev6Oksana Maksimenko7Center for Precision Genome Editing and Genetic Technologies for Biomedicine, Institute of Gene Biology, Russian Academy of SciencesDepartment of the Control of Genetic Processes, Institute of Gene Biology, Russian Academy of SciencesLaboratory of Molecular Cytogenetics, Institute of Molecular and Cellular Biology SB RASDepartment of Drosophila Molecular Genetics, Institute of Gene Biology, Russian Academy of SciencesNRC “Kurchatov Institute”-Institute of Molecular GeneticsLaboratory of Molecular Cytogenetics, Institute of Molecular and Cellular Biology SB RASDepartment of the Control of Genetic Processes, Institute of Gene Biology, Russian Academy of SciencesCenter for Precision Genome Editing and Genetic Technologies for Biomedicine, Institute of Gene Biology, Russian Academy of SciencesAbstract Background In Drosophila, architectural proteins are frequently found in promoters, including those of genes with extremely high expression levels, such as ribosomal protein genes (RPGs). The involvement of several of these proteins in gene regulation in Drosophila has been shown, but the exact mechanisms of their possible cooperative action have not been fully elucidated. Results In this study we dissected the contribution of the architectural proteins Opbp and M1BP, which are co-localized at several RPG promoters near the transcription start site, to promoter functioning. We found that Opbp has two domains that directly interact with CP190, Putzig (Pzg), and Chromator (Chro) proteins, the cofactors which are required for the activation of housekeeping (hk) gene promoters. These domains have redundant functions in vivo and can tether the cofactors forming open chromatin regions when are artificially recruited to the “closed” chromatin. Additionally, we observed interactions between M1BP and the same cofactors. In the transgene assay, the transcription driven by the 192-bp part of Rpl27A RPG promoter is fully dependent on the presence of at least one Opbp or M1BP binding site and it is sufficient for the very high activity of this promoter integrated into the hk gene cluster and moderate expression outside the cluster, while presence of both sites even more facilitates transcription. Conclusions This study demonstrates that different architectural proteins can work independently and in cooperation and fulfill partially redundant functions in the activation of RPG promoters.https://doi.org/10.1186/s13072-025-00584-8Architectural С2Н2 proteinsZinc-finger proteinsPutzigChromatorCP190Housekeeping genes
spellingShingle Igor Osadchiy
Anastasia Umnova
Galina V. Pokholkova
Anton Golovnin
Vladimir A. Gvozdev
Igor F. Zhimulev
Pavel Georgiev
Oksana Maksimenko
Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
Epigenetics & Chromatin
Architectural С2Н2 proteins
Zinc-finger proteins
Putzig
Chromator
CP190
Housekeeping genes
title Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
title_full Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
title_fullStr Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
title_full_unstemmed Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
title_short Drosophila architectural proteins M1BP and Opbp cooperatively form the active promoter of a ribosomal protein gene
title_sort drosophila architectural proteins m1bp and opbp cooperatively form the active promoter of a ribosomal protein gene
topic Architectural С2Н2 proteins
Zinc-finger proteins
Putzig
Chromator
CP190
Housekeeping genes
url https://doi.org/10.1186/s13072-025-00584-8
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