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  1. Article ; Online: Widespread regulatory specificities between transcriptional co-repressors and enhancers in

    Jacobs, Jelle / Pagani, Michaela / Wenzl, Christoph / Stark, Alexander

    Science (New York, N.Y.)

    2023  Volume 381, Issue 6654, Page(s) 198–204

    Abstract: Gene expression is controlled by the precise activation and repression of transcription. Repression is mediated by specialized transcription factors (TFs) that recruit co-repressors (CoRs) to silence transcription, even in the presence of activating cues. ...

    Abstract Gene expression is controlled by the precise activation and repression of transcription. Repression is mediated by specialized transcription factors (TFs) that recruit co-repressors (CoRs) to silence transcription, even in the presence of activating cues. However, whether CoRs can dominantly silence all enhancers or display distinct specificities is unclear. In this work, we report that most enhancers in
    MeSH term(s) Animals ; Chromatin/metabolism ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism ; Drosophila Proteins/chemistry ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Enhancer Elements, Genetic ; Gene Expression Regulation, Developmental ; Repressor Proteins/chemistry ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Amino Acid Motifs
    Chemical Substances Chromatin ; Drosophila Proteins ; Repressor Proteins
    Language English
    Publishing date 2023-07-13
    Publishing country United States
    Document type Journal Article
    ZDB-ID 128410-1
    ISSN 1095-9203 ; 0036-8075
    ISSN (online) 1095-9203
    ISSN 0036-8075
    DOI 10.1126/science.adf6149
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  2. Article ; Online: DeepSTARR predicts enhancer activity from DNA sequence and enables the de novo design of synthetic enhancers.

    de Almeida, Bernardo P / Reiter, Franziska / Pagani, Michaela / Stark, Alexander

    Nature genetics

    2022  Volume 54, Issue 5, Page(s) 613–624

    Abstract: Enhancer sequences control gene expression and comprise binding sites (motifs) for different transcription factors (TFs). Despite extensive genetic and computational studies, the relationship between DNA sequence and regulatory activity is poorly ... ...

    Abstract Enhancer sequences control gene expression and comprise binding sites (motifs) for different transcription factors (TFs). Despite extensive genetic and computational studies, the relationship between DNA sequence and regulatory activity is poorly understood, and de novo enhancer design has been challenging. Here, we built a deep-learning model, DeepSTARR, to quantitatively predict the activities of thousands of developmental and housekeeping enhancers directly from DNA sequence in Drosophila melanogaster S2 cells. The model learned relevant TF motifs and higher-order syntax rules, including functionally nonequivalent instances of the same TF motif that are determined by motif-flanking sequence and intermotif distances. We validated these rules experimentally and demonstrated that they can be generalized to humans by testing more than 40,000 wildtype and mutant Drosophila and human enhancers. Finally, we designed and functionally validated synthetic enhancers with desired activities de novo.
    MeSH term(s) Animals ; Base Sequence ; Binding Sites/genetics ; Drosophila/genetics ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism ; Enhancer Elements, Genetic/genetics ; Gene Expression Regulation, Developmental ; Transcription Factors/genetics ; Transcription Factors/metabolism
    Chemical Substances Transcription Factors
    Language English
    Publishing date 2022-05-12
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 1108734-1
    ISSN 1546-1718 ; 1061-4036
    ISSN (online) 1546-1718
    ISSN 1061-4036
    DOI 10.1038/s41588-022-01048-5
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  3. Article ; Online: Targeted design of synthetic enhancers for selected tissues in the Drosophila embryo.

    de Almeida, Bernardo P / Schaub, Christoph / Pagani, Michaela / Secchia, Stefano / Furlong, Eileen E M / Stark, Alexander

    Nature

    2023  Volume 626, Issue 7997, Page(s) 207–211

    Abstract: Enhancers control gene expression and have crucial roles in development and ... ...

    Abstract Enhancers control gene expression and have crucial roles in development and homeostasis
    MeSH term(s) Animals ; Chromatin/genetics ; Chromatin/metabolism ; Datasets as Topic ; Deep Learning ; Drosophila melanogaster/embryology ; Drosophila melanogaster/genetics ; Embryo, Nonmammalian/embryology ; Embryo, Nonmammalian/metabolism ; Enhancer Elements, Genetic/genetics ; Neural Networks, Computer ; Organ Specificity/genetics ; Reproducibility of Results ; Single-Cell Analysis ; Transposases/metabolism ; Synthetic Biology/methods
    Chemical Substances Chromatin ; Transposases (EC 2.7.7.-)
    Language English
    Publishing date 2023-12-12
    Publishing country England
    Document type Journal Article
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-023-06905-9
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  4. Article ; Online: STARR-seq and UMI-STARR-seq: Assessing Enhancer Activities for Genome-Wide-, High-, and Low-Complexity Candidate Libraries.

    Neumayr, Christoph / Pagani, Michaela / Stark, Alexander / Arnold, Cosmas D

    Current protocols in molecular biology

    2019  Volume 128, Issue 1, Page(s) e105

    Abstract: The identification of transcriptional enhancers and the quantitative assessment of enhancer activities is essential to understanding how regulatory information for gene expression is encoded in animal and human genomes. Further, it is key to ... ...

    Abstract The identification of transcriptional enhancers and the quantitative assessment of enhancer activities is essential to understanding how regulatory information for gene expression is encoded in animal and human genomes. Further, it is key to understanding how sequence variants affect enhancer function. STARR-seq enables the direct and quantitative assessment of enhancer activity for millions of candidate sequences of arbitrary length and origin in parallel, allowing the screening of entire genomes and the establishment of genome-wide enhancer activity maps. In STARR-seq, the candidate sequences are cloned downstream of the core promoter into a reporter gene's transcription unit (i.e., the 3' UTR). Candidates that function as active enhancers lead to the transcription of reporter mRNAs that harbor the candidates' sequences. This direct coupling of enhancer sequence and enhancer activity in cis enables the straightforward and efficient cloning of complex candidate libraries and the assessment of enhancer activities of millions of candidates in parallel by quantifying the reporter mRNAs by deep sequencing. This article describes how to create focused and genome-wide human STARR-seq libraries and how to perform STARR-seq screens in mammalian cells, and also describes a novel STARR-seq variant (UMI-STARR-seq) that allows the accurate counting of reporter mRNAs for STARR-seq libraries of low complexity. © 2019 The Authors. Basic Protocol 1: STARR-seq plasmid library cloning Basic Protocol 2: Mammalian STARR-seq screening protocol Alternate Protocol: UMI-STARR-seq screening protocol-unique molecular identifier integration Support Protocol: Transfection of human cells using the MaxCyte STX scalable transfection system.
    MeSH term(s) Animals ; Cloning, Molecular ; Enhancer Elements, Genetic ; Genetic Techniques ; Genomic Library ; HeLa Cells ; Humans ; Plasmids ; Transfection
    Language English
    Publishing date 2019-09-05
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ISSN 1934-3647
    ISSN (online) 1934-3647
    DOI 10.1002/cpmb.105
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  5. Article ; Online: An unbiased AAV-STARR-seq screen revealing the enhancer activity map of genomic regions in the mouse brain in vivo.

    Chan, Ya-Chien / Kienle, Eike / Oti, Martin / Di Liddo, Antonella / Mendez-Lago, Maria / Aschauer, Dominik F / Peter, Manuel / Pagani, Michaela / Arnold, Cosmas / Vonderheit, Andreas / Schön, Christian / Kreuz, Sebastian / Stark, Alexander / Rumpel, Simon

    Scientific reports

    2023  Volume 13, Issue 1, Page(s) 6745

    Abstract: Enhancers are important cis-regulatory elements controlling cell-type specific expression patterns of genes. Furthermore, combinations of enhancers and minimal promoters are utilized to construct small, artificial promoters for gene delivery vectors. ... ...

    Abstract Enhancers are important cis-regulatory elements controlling cell-type specific expression patterns of genes. Furthermore, combinations of enhancers and minimal promoters are utilized to construct small, artificial promoters for gene delivery vectors. Large-scale functional screening methodology to construct genomic maps of enhancer activities has been successfully established in cultured cell lines, however, not yet applied to terminally differentiated cells and tissues in a living animal. Here, we transposed the Self-Transcribing Active Regulatory Region Sequencing (STARR-seq) technique to the mouse brain using adeno-associated-viruses (AAV) for the delivery of a highly complex screening library tiling entire genomic regions and covering in total 3 Mb of the mouse genome. We identified 483 sequences with enhancer activity, including sequences that were not predicted by DNA accessibility or histone marks. Characterizing the expression patterns of fluorescent reporters controlled by nine candidate sequences, we observed differential expression patterns also in sparse cell types. Together, our study provides an entry point for the unbiased study of enhancer activities in organisms during health and disease.
    MeSH term(s) Animals ; Mice ; Enhancer Elements, Genetic ; Genomics/methods ; Chromosome Mapping/methods ; Promoter Regions, Genetic ; Brain
    Language English
    Publishing date 2023-04-25
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 2615211-3
    ISSN 2045-2322 ; 2045-2322
    ISSN (online) 2045-2322
    ISSN 2045-2322
    DOI 10.1038/s41598-023-33448-w
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  6. Article ; Online: Transcriptional cofactors display specificity for distinct types of core promoters.

    Haberle, Vanja / Arnold, Cosmas D / Pagani, Michaela / Rath, Martina / Schernhuber, Katharina / Stark, Alexander

    Nature

    2019  Volume 570, Issue 7759, Page(s) 122–126

    Abstract: Transcriptional cofactors (COFs) communicate regulatory cues from enhancers to promoters and are central effectors of transcription activation and gene ... ...

    Abstract Transcriptional cofactors (COFs) communicate regulatory cues from enhancers to promoters and are central effectors of transcription activation and gene expression
    MeSH term(s) Animals ; Cell Line ; Chromatin/genetics ; CpG Islands/genetics ; Drosophila melanogaster/cytology ; Drosophila melanogaster/genetics ; Enhancer Elements, Genetic/genetics ; Histones/metabolism ; Humans ; Promoter Regions, Genetic/genetics ; Substrate Specificity ; TATA Box/genetics ; Transcription Factors/metabolism ; Transcription Initiation Site ; Transcription, Genetic ; Transcriptional Activation
    Chemical Substances Chromatin ; Histones ; Transcription Factors ; histone H3 trimethyl Lys4
    Language English
    Publishing date 2019-05-15
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-019-1210-7
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  7. Article ; Online: Genome-Wide Ultrabithorax Binding Analysis Reveals Highly Targeted Genomic Loci at Developmental Regulators and a Potential Connection to Polycomb-Mediated Regulation.

    Shlyueva, Daria / Meireles-Filho, Antonio C A / Pagani, Michaela / Stark, Alexander

    PloS one

    2016  Volume 11, Issue 8, Page(s) e0161997

    Abstract: Hox homeodomain transcription factors are key regulators of animal development. They specify the identity of segments along the anterior-posterior body axis in metazoans by controlling the expression of diverse downstream targets, including transcription ...

    Abstract Hox homeodomain transcription factors are key regulators of animal development. They specify the identity of segments along the anterior-posterior body axis in metazoans by controlling the expression of diverse downstream targets, including transcription factors and signaling pathway components. The Drosophila melanogaster Hox factor Ultrabithorax (Ubx) directs the development of thoracic and abdominal segments and appendages, and loss of Ubx function can lead for example to the transformation of third thoracic segment appendages (e.g. halters) into second thoracic segment appendages (e.g. wings), resulting in a characteristic four-wing phenotype. Here we present a Drosophila melanogaster strain with a V5-epitope tagged Ubx allele, which we employed to obtain a high quality genome-wide map of Ubx binding sites using ChIP-seq. We confirm the sensitivity of the V5 ChIP-seq by recovering 7/8 of well-studied Ubx-dependent cis-regulatory regions. Moreover, we show that Ubx binding is predictive of enhancer activity as suggested by comparison with a genome-scale resource of in vivo tested enhancer candidates. We observed densely clustered Ubx binding sites at 12 extended genomic loci that included ANTP-C, BX-C, Polycomb complex genes, and other regulators and the clustered binding sites were frequently active enhancers. Furthermore, Ubx binding was detected at known Polycomb response elements (PREs) and was associated with significant enrichments of Pc and Pho ChIP signals in contrast to binding sites of other developmental TFs. Together, our results show that Ubx targets developmental regulators via strongly clustered binding sites and allow us to hypothesize that regulation by Ubx might involve Polycomb group proteins to maintain specific regulatory states in cooperative or mutually exclusive fashion, an attractive model that combines two groups of proteins with prominent gene regulatory roles during animal development.
    MeSH term(s) Animals ; Binding Sites ; Chromatin Immunoprecipitation ; Drosophila Proteins/metabolism ; Drosophila melanogaster/embryology ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism ; Enhancer Elements, Genetic ; Gene Expression Regulation, Developmental ; Genome ; High-Throughput Nucleotide Sequencing ; Homeodomain Proteins/metabolism ; Polycomb-Group Proteins/genetics ; Sequence Analysis, DNA ; Transcription Factors/metabolism
    Chemical Substances Drosophila Proteins ; Homeodomain Proteins ; Polycomb-Group Proteins ; Transcription Factors ; Ubx protein, Drosophila
    Language English
    Publishing date 2016-08-30
    Publishing country United States
    Document type Journal Article
    ISSN 1932-6203
    ISSN (online) 1932-6203
    DOI 10.1371/journal.pone.0161997
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  8. Article ; Online: Differential cofactor dependencies define distinct types of human enhancers.

    Neumayr, Christoph / Haberle, Vanja / Serebreni, Leonid / Karner, Katharina / Hendy, Oliver / Boija, Ann / Henninger, Jonathan E / Li, Charles H / Stejskal, Karel / Lin, Gen / Bergauer, Katharina / Pagani, Michaela / Rath, Martina / Mechtler, Karl / Arnold, Cosmas D / Stark, Alexander

    Nature

    2022  Volume 606, Issue 7913, Page(s) 406–413

    Abstract: All multicellular organisms rely on differential gene transcription regulated by genomic enhancers, which function through cofactors that are recruited by transcription ... ...

    Abstract All multicellular organisms rely on differential gene transcription regulated by genomic enhancers, which function through cofactors that are recruited by transcription factors
    MeSH term(s) Cell Cycle Proteins/metabolism ; Chromatin/genetics ; Enhancer Elements, Genetic/genetics ; Humans ; Nuclear Proteins/metabolism ; Transcription Factors/metabolism ; Tumor Suppressor Protein p53/metabolism
    Chemical Substances BRD4 protein, human ; Cell Cycle Proteins ; Chromatin ; Nuclear Proteins ; Transcription Factors ; Tumor Suppressor Protein p53
    Language English
    Publishing date 2022-06-01
    Publishing country England
    Document type Journal Article
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-022-04779-x
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  9. Article ; Online: A high-throughput method to identify trans-activation domains within transcription factor sequences.

    Arnold, Cosmas D / Nemčko, Filip / Woodfin, Ashley R / Wienerroither, Sebastian / Vlasova, Anna / Schleiffer, Alexander / Pagani, Michaela / Rath, Martina / Stark, Alexander

    The EMBO journal

    2018  Volume 37, Issue 16

    Abstract: Even though transcription factors (TFs) are central players of gene regulation and have been extensively studied, their ... ...

    Abstract Even though transcription factors (TFs) are central players of gene regulation and have been extensively studied, their regulatory
    MeSH term(s) Animals ; Cell Line ; Drosophila Proteins/biosynthesis ; Drosophila Proteins/genetics ; Drosophila melanogaster ; Protein Domains ; Trans-Activators/biosynthesis ; Trans-Activators/genetics ; Transcription, Genetic
    Chemical Substances Drosophila Proteins ; Trans-Activators
    Language English
    Publishing date 2018-07-13
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 586044-1
    ISSN 1460-2075 ; 0261-4189
    ISSN (online) 1460-2075
    ISSN 0261-4189
    DOI 10.15252/embj.201798896
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  10. Article ; Online: Genome-wide assessment of sequence-intrinsic enhancer responsiveness at single-base-pair resolution.

    Arnold, Cosmas D / Zabidi, Muhammad A / Pagani, Michaela / Rath, Martina / Schernhuber, Katharina / Kazmar, Tomáš / Stark, Alexander

    Nature biotechnology

    2016  Volume 35, Issue 2, Page(s) 136–144

    Abstract: Gene expression is controlled by enhancers that activate transcription from the core promoters of their target genes. Although a key function of core promoters is to convert enhancer activities into gene transcription, whether and how strongly they ... ...

    Abstract Gene expression is controlled by enhancers that activate transcription from the core promoters of their target genes. Although a key function of core promoters is to convert enhancer activities into gene transcription, whether and how strongly they activate transcription in response to enhancers has not been systematically assessed on a genome-wide level. Here we describe self-transcribing active core promoter sequencing (STAP-seq), a method to determine the responsiveness of genomic sequences to enhancers, and apply it to the Drosophila melanogaster genome. We cloned candidate fragments at the position of the core promoter (also called minimal promoter) in reporter plasmids with or without a strong enhancer, transfected the resulting library into cells, and quantified the transcripts that initiated from each candidate for each setup by deep sequencing. In the presence of a single strong enhancer, the enhancer responsiveness of different sequences differs by several orders of magnitude, and different levels of responsiveness are associated with genes of different functions. We also identify sequence features that predict enhancer responsiveness and discuss how different core promoters are employed for the regulation of gene expression.
    MeSH term(s) Algorithms ; Animals ; Base Pairing/genetics ; Chromosome Mapping/methods ; Drosophila melanogaster ; Enhancer Elements, Genetic/genetics ; Gene Expression Regulation/genetics ; Promoter Regions, Genetic/genetics ; Sequence Analysis, DNA/methods ; Software ; Transcription Initiation, Genetic
    Language English
    Publishing date 2016-12-26
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 1311932-1
    ISSN 1546-1696 ; 1087-0156
    ISSN (online) 1546-1696
    ISSN 1087-0156
    DOI 10.1038/nbt.3739
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