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Article ; Online: Three-step mechanism of promoter escape by RNA polymerase II.

Zhan, Yumeng / Grabbe, Frauke / Oberbeckmann, Elisa / Dienemann, Christian / Cramer, Patrick

2024 Volume 84, Issue 9, Page(s) 1699–1710.e6

Abstract: The transition from transcription initiation to elongation is highly regulated in human cells but remains incompletely understood at the structural level. In particular, it is unclear how interactions between RNA polymerase II (RNA Pol II) and initiation ...

Abstract	The transition from transcription initiation to elongation is highly regulated in human cells but remains incompletely understood at the structural level. In particular, it is unclear how interactions between RNA polymerase II (RNA Pol II) and initiation factors are broken to enable promoter escape. Here, we reconstitute RNA Pol II promoter escape in vitro and determine high-resolution structures of initially transcribing complexes containing 8-, 10-, and 12-nt ordered RNAs and two elongation complexes containing 14-nt RNAs. We suggest that promoter escape occurs in three major steps. First, the growing RNA displaces the B-reader element of the initiation factor TFIIB without evicting TFIIB. Second, the rewinding of the transcription bubble coincides with the eviction of TFIIA, TFIIB, and TBP. Third, the binding of DSIF and NELF facilitates TFIIE and TFIIH dissociation, establishing the paused elongation complex. This three-step model for promoter escape fills a gap in our understanding of the initiation-elongation transition of RNA Pol II transcription.
MeSH term(s)	RNA Polymerase II/metabolism ; RNA Polymerase II/genetics ; Promoter Regions, Genetic ; Humans ; Transcription Factor TFIIB/metabolism ; Transcription Factor TFIIB/genetics ; TATA-Box Binding Protein/metabolism ; TATA-Box Binding Protein/genetics ; Transcription Factors/metabolism ; Transcription Factors/genetics ; Transcription Initiation, Genetic ; Transcription Factor TFIIH/metabolism ; Transcription Factor TFIIH/genetics ; Transcription Factor TFIIH/chemistry ; Nuclear Proteins/metabolism ; Nuclear Proteins/genetics ; Protein Binding ; Transcription Factor TFIIA/metabolism ; Transcription Factor TFIIA/genetics ; Transcription, Genetic ; Transcription Elongation, Genetic ; RNA/metabolism ; RNA/genetics ; Transcription Factors, TFII/metabolism ; Transcription Factors, TFII/genetics ; Phosphoproteins
Chemical Substances	RNA Polymerase II (EC 2.7.7.-) ; Transcription Factor TFIIB ; TATA-Box Binding Protein ; Transcription Factors ; Transcription Factor TFIIH (148710-81-0) ; transcription factor TFIIE ; Nuclear Proteins ; down-regulator of transcription 1 ; NSMF protein, human ; Transcription Factor TFIIA ; TBP protein, human ; RNA (63231-63-0) ; Transcription Factors, TFII ; Phosphoproteins
Language	English
Publishing date	2024-04-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2024.03.016
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Article ; Online: Structural basis of transcription reduction by a promoter-proximal +1 nucleosome

Abril-Garrido, Julio / Dienemann, Christian / Grabbe, Frauke / Velychko, Taras / Lidschreiber, Michael / Wang, Haibo / Cramer, Patrick

Molecular Cell. 20232023 June 05, May 05, v. 83, no. 11 p.1798-1809.e7

2023

Abstract: At active human genes, the +1 nucleosome is located downstream of the RNA polymerase II (RNA Pol II) pre-initiation complex (PIC). However, at inactive genes, the +1 nucleosome is found further upstream, at a promoter-proximal location. Here, we ... ...

Abstract	At active human genes, the +1 nucleosome is located downstream of the RNA polymerase II (RNA Pol II) pre-initiation complex (PIC). However, at inactive genes, the +1 nucleosome is found further upstream, at a promoter-proximal location. Here, we establish a model system to show that a promoter-proximal +1 nucleosome can reduce RNA synthesis in vivo and in vitro, and we analyze its structural basis. We find that the PIC assembles normally when the edge of the +1 nucleosome is located 18 base pairs (bp) downstream of the transcription start site (TSS). However, when the nucleosome edge is located further upstream, only 10 bp downstream of the TSS, the PIC adopts an inhibited state. The transcription factor IIH (TFIIH) shows a closed conformation and its subunit XPB contacts DNA with only one of its two ATPase lobes, inconsistent with DNA opening. These results provide a mechanism for nucleosome-dependent regulation of transcription initiation.
Keywords	DNA ; DNA-directed RNA polymerase ; RNA ; adenosinetriphosphatase ; humans ; nucleosomes ; transcription factors ; transcription initiation ; transcription initiation site ; RNA polymerase II ; pre-initiation complex ; +1 nucleosome ; promoter-proximal +1 nucleosome ; gene regulation ; transcription reduction
Language	English
Dates of publication	2023-0505
Size	p. 1798-1809.e7.
Publishing place	Elsevier Inc.
Document type	Article ; Online
Note	Use and reproduction
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2023.04.011
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Article ; Online: Structure of RNA polymerase II pre-initiation complex at 2.9 Å defines initial DNA opening.

Schilbach, Sandra / Aibara, Shintaro / Dienemann, Christian / Grabbe, Frauke / Cramer, Patrick

Cell

2021 Volume 184, Issue 15, Page(s) 4064–4072.e28

Abstract: Transcription initiation requires assembly of the RNA polymerase II (Pol II) pre-initiation complex (PIC) and opening of promoter DNA. Here, we present the long-sought high-resolution structure of the yeast PIC and define the mechanism of initial DNA ... ...

Abstract	Transcription initiation requires assembly of the RNA polymerase II (Pol II) pre-initiation complex (PIC) and opening of promoter DNA. Here, we present the long-sought high-resolution structure of the yeast PIC and define the mechanism of initial DNA opening. We trap the PIC in an intermediate state that contains half a turn of open DNA located 30-35 base pairs downstream of the TATA box. The initially opened DNA region is flanked and stabilized by the polymerase "clamp head loop" and the TFIIF "charged region" that both contribute to promoter-initiated transcription. TFIIE facilitates initiation by buttressing the clamp head loop and by regulating the TFIIH translocase. The initial DNA bubble is then extended in the upstream direction, leading to the open promoter complex and enabling start-site scanning and RNA synthesis. This unique mechanism of DNA opening may permit more intricate regulation than in the Pol I and Pol III systems.
MeSH term(s)	Amino Acid Sequence ; Cryoelectron Microscopy ; DNA/chemistry ; DNA/ultrastructure ; Models, Biological ; Models, Molecular ; Nucleic Acid Conformation ; Promoter Regions, Genetic ; RNA Polymerase II/chemistry ; RNA Polymerase II/metabolism ; RNA Polymerase II/ultrastructure ; Saccharomyces cerevisiae/metabolism ; Sequence Deletion ; Transcription Factor TFIIH ; Transcription Factors, TFII/metabolism ; Transcription Initiation, Genetic
Chemical Substances	Transcription Factors, TFII ; transcription factor TFIIE ; Transcription Factor TFIIH (148710-81-0) ; DNA (9007-49-2) ; RNA Polymerase II (EC 2.7.7.-)
Language	English
Publishing date	2021-06-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2021.05.012
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Article ; Online: Structural basis of transcription reduction by a promoter-proximal +1 nucleosome.

Abril-Garrido, Julio / Dienemann, Christian / Grabbe, Frauke / Velychko, Taras / Lidschreiber, Michael / Wang, Haibo / Cramer, Patrick

Molecular cell

2023 Volume 83, Issue 11, Page(s) 1798–1809.e7

Abstract	At active human genes, the +1 nucleosome is located downstream of the RNA polymerase II (RNA Pol II) pre-initiation complex (PIC). However, at inactive genes, the +1 nucleosome is found further upstream, at a promoter-proximal location. Here, we establish a model system to show that a promoter-proximal +1 nucleosome can reduce RNA synthesis in vivo and in vitro, and we analyze its structural basis. We find that the PIC assembles normally when the edge of the +1 nucleosome is located 18 base pairs (bp) downstream of the transcription start site (TSS). However, when the nucleosome edge is located further upstream, only 10 bp downstream of the TSS, the PIC adopts an inhibited state. The transcription factor IIH (TFIIH) shows a closed conformation and its subunit XPB contacts DNA with only one of its two ATPase lobes, inconsistent with DNA opening. These results provide a mechanism for nucleosome-dependent regulation of transcription initiation.
MeSH term(s)	Humans ; Nucleosomes/genetics ; RNA Polymerase II/metabolism ; Promoter Regions, Genetic ; Transcription Factor TFIIH/metabolism ; DNA/genetics ; DNA/chemistry ; Transcription, Genetic ; Transcription Initiation Site
Chemical Substances	Nucleosomes ; RNA Polymerase II (EC 2.7.7.-) ; Transcription Factor TFIIH (148710-81-0) ; DNA (9007-49-2)
Language	English
Publishing date	2023-05-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2023.04.011
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Article: Structure of RNA polymerase II pre-initiation complex at 2.9 Å defines initial DNA opening

Schilbach, Sandra / Aibara, Shintaro / Dienemann, Christian / Grabbe, Frauke / Cramer, Patrick

Cell. 2021 July 22, v. 184, no. 15

2021

Abstract	Transcription initiation requires assembly of the RNA polymerase II (Pol II) pre-initiation complex (PIC) and opening of promoter DNA. Here, we present the long-sought high-resolution structure of the yeast PIC and define the mechanism of initial DNA opening. We trap the PIC in an intermediate state that contains half a turn of open DNA located 30–35 base pairs downstream of the TATA box. The initially opened DNA region is flanked and stabilized by the polymerase “clamp head loop” and the TFIIF “charged region” that both contribute to promoter-initiated transcription. TFIIE facilitates initiation by buttressing the clamp head loop and by regulating the TFIIH translocase. The initial DNA bubble is then extended in the upstream direction, leading to the open promoter complex and enabling start-site scanning and RNA synthesis. This unique mechanism of DNA opening may permit more intricate regulation than in the Pol I and Pol III systems.
Keywords	DNA ; DNA-directed RNA polymerase ; RNA ; TATA box ; head ; transcription initiation ; yeasts
Language	English
Dates of publication	2021-0722
Size	p. 4064-4072.e28.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2021.05.012
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Article ; Online: A digital atlas of ion channel expression patterns in the two-week-old rat brain.

Shcherbatyy, Volodymyr / Carson, James / Yaylaoglu, Murat / Jäckle, Katharina / Grabbe, Frauke / Brockmeyer, Maren / Yavuz, Halenur / Eichele, Gregor

Neuroinformatics

2014 Volume 13, Issue 1, Page(s) 111–125

Abstract: The approximately 350 ion channels encoded by the mammalian genome are a main pillar of the nervous system. We have determined the expression pattern of 320 channels in the two-week-old (P14) rat brain by means of non-radioactive robotic in situ ... ...

Abstract	The approximately 350 ion channels encoded by the mammalian genome are a main pillar of the nervous system. We have determined the expression pattern of 320 channels in the two-week-old (P14) rat brain by means of non-radioactive robotic in situ hybridization. Optimized methods were developed and implemented to generate stringently coronal brain sections. The use of standardized methods permits a direct comparison of expression patterns across the entire ion channel expression pattern data set and facilitates recognizing ion channel co-expression. All expression data are made publically available at the Genepaint.org database. Inwardly rectifying potassium channels (Kir, encoded by the Kcnj genes) regulate a broad spectrum of physiological processes. Kcnj channel expression patterns generated in the present study were fitted with a deformable subdivision mesh atlas produced for the P14 rat brain. This co-registration, when combined with numerical quantification of expression strengths, allowed for semi-quantitative automated annotation of expression patterns as well as comparisons among and between Kcnj subfamilies. The expression patterns of Kcnj channel were also cross validated against previously published expression patterns of Kcnj channel genes.
MeSH term(s)	Animals ; Atlases as Topic ; Brain/anatomy & histology ; Brain/metabolism ; Datasets as Topic ; In Situ Hybridization ; Potassium Channels, Inwardly Rectifying ; Rats
Chemical Substances	Potassium Channels, Inwardly Rectifying
Language	English
Publishing date	2014-10-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2111941-7
ISSN	1559-0089 ; 1539-2791
ISSN (online)	1559-0089
ISSN	1539-2791
DOI	10.1007/s12021-014-9247-0
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Article ; Online: A high-resolution anatomical atlas of the transcriptome in the mouse embryo.

Diez-Roux, Graciana / Banfi, Sandro / Sultan, Marc / Geffers, Lars / Anand, Santosh / Rozado, David / Magen, Alon / Canidio, Elena / Pagani, Massimiliano / Peluso, Ivana / Lin-Marq, Nathalie / Koch, Muriel / Bilio, Marchesa / Cantiello, Immacolata / Verde, Roberta / De Masi, Cristian / Bianchi, Salvatore A / Cicchini, Juliette / Perroud, Elodie /

Mehmeti, Shprese / Dagand, Emilie / Schrinner, Sabine / Nürnberger, Asja / Schmidt, Katja / Metz, Katja / Zwingmann, Christina / Brieske, Norbert / Springer, Cindy / Hernandez, Ana Martinez / Herzog, Sarah / Grabbe, Frauke / Sieverding, Cornelia / Fischer, Barbara / Schrader, Kathrin / Brockmeyer, Maren / Dettmer, Sarah / Helbig, Christin / Alunni, Violaine / Battaini, Marie-Annick / Mura, Carole / Henrichsen, Charlotte N / Garcia-Lopez, Raquel / Echevarria, Diego / Puelles, Eduardo / Garcia-Calero, Elena / Kruse, Stefan / Uhr, Markus / Kauck, Christine / Feng, Guangjie / Milyaev, Nestor / Ong, Chuang Kee / Kumar, Lalit / Lam, MeiSze / Semple, Colin A / Gyenesei, Attila / Mundlos, Stefan / Radelof, Uwe / Lehrach, Hans / Sarmientos, Paolo / Reymond, Alexandre / Davidson, Duncan R / Dollé, Pascal / Antonarakis, Stylianos E / Yaspo, Marie-Laure / Martinez, Salvador / Baldock, Richard A / Eichele, Gregor / Ballabio, Andrea

PLoS biology

2011 Volume 9, Issue 1, Page(s) e1000582

Abstract: Ascertaining when and where genes are expressed is of crucial importance to understanding or predicting the physiological role of genes and proteins and how they interact to form the complex networks that underlie organ development and function. It is, ... ...

Abstract	Ascertaining when and where genes are expressed is of crucial importance to understanding or predicting the physiological role of genes and proteins and how they interact to form the complex networks that underlie organ development and function. It is, therefore, crucial to determine on a genome-wide level, the spatio-temporal gene expression profiles at cellular resolution. This information is provided by colorimetric RNA in situ hybridization that can elucidate expression of genes in their native context and does so at cellular resolution. We generated what is to our knowledge the first genome-wide transcriptome atlas by RNA in situ hybridization of an entire mammalian organism, the developing mouse at embryonic day 14.5. This digital transcriptome atlas, the Eurexpress atlas (http://www.eurexpress.org), consists of a searchable database of annotated images that can be interactively viewed. We generated anatomy-based expression profiles for over 18,000 coding genes and over 400 microRNAs. We identified 1,002 tissue-specific genes that are a source of novel tissue-specific markers for 37 different anatomical structures. The quality and the resolution of the data revealed novel molecular domains for several developing structures, such as the telencephalon, a novel organization for the hypothalamus, and insight on the Wnt network involved in renal epithelial differentiation during kidney development. The digital transcriptome atlas is a powerful resource to determine co-expression of genes, to identify cell populations and lineages, and to identify functional associations between genes relevant to development and disease.
MeSH term(s)	Animals ; Atlases as Topic ; Databases, Genetic ; Embryo, Mammalian ; Gene Expression Profiling ; Internet ; Mice/anatomy & histology ; Mice/embryology ; Mice/genetics ; Mice, Inbred C57BL ; Organ Specificity
Language	English
Publishing date	2011-01-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.1000582
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