SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements

Oliver Nayler; Wolf Strätling; Jean Pierre Bourquin; Igor Stagljar; Lothar Lindemann; Heinrich Jasper; Annette M. Hartmann; Frank O. Fackelmayer; Axel Ullrich; Stefan Stamm

doi:10.1093/nar/26.15.3542

SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements

Oliver Nayler
, Wolf Strätling
, Jean Pierre Bourquin
, Igor Stagljar
, Lothar Lindemann
, Heinrich Jasper
, Annette M. Hartmann
, Frank O. Fackelmayer
, Axel Ullrich
, Stefan Stamm

Research output: Contribution to journal › Article › peer-review

161 Scopus citations

Abstract

Interphase chromatin is arranged into topologically separated domains comprising gene expression and replication units through genomic sequence elements so-called MAR or SAR regions (for matrix- or scaffold-associating regions). S/MAR regions are located near the boundaries of actively transcribed genes and were shown to influence their activity. We show that scaffold attachment factor B (SAF-B), which specifically binds to S/MAR regions, interacts with RNA polymerase II (RNA pol II) and a subset of serine-/arginine-rich RNA processing factors (SR proteins). SAF-B localized to the nucleus in a speckled pattern that coincided with the distribution of the SR protein SC35. Furthermore, we show that overexpressed SAF-B induced an increase of the 10S splice product using an E1A reporter gene and repressed the activity of an S/MAR flanked CAT reporter gene construct in vivo. This indicates an association of SAF-B with SR proteins and components of the transcription machinery. Our results describe the coupling of a chromatin organizing S/MAR element with transcription and pre-mRNA processing components and we propose that SAF-B serves as a molecular base to assemble a 'transcriptosome complex' in the vicinity of actively transcribed genes.

Original language	English
Pages (from-to)	3542-3549
Number of pages	8
Journal	Nucleic Acids Research
Volume	26
Issue number	15
DOIs	https://doi.org/10.1093/nar/26.15.3542
State	Published - Aug 1 1998

Bibliographical note

Funding Information:
We thank C.Cap for help with sequencing, O.Georgiev for his contribution to the isolation of CTD interacting clones, J.Cáceres for the E1A construct and I.Sures and M.Stein-Gerlach for reading the manuscript. We also thank J.Chalcroft and Yuh-Shin Chang for technical assistance, and Walter Schaffner for support and helpful discussions. This work was supported by the Swiss National Science Foundation, the Kanton Zürich, the Max-Planck-Society, the Human Frontier Science Program RG-562/96 to S.S. and SUGEN.

Funding

We thank C.Cap for help with sequencing, O.Georgiev for his contribution to the isolation of CTD interacting clones, J.Cáceres for the E1A construct and I.Sures and M.Stein-Gerlach for reading the manuscript. We also thank J.Chalcroft and Yuh-Shin Chang for technical assistance, and Walter Schaffner for support and helpful discussions. This work was supported by the Swiss National Science Foundation, the Kanton Zürich, the Max-Planck-Society, the Human Frontier Science Program RG-562/96 to S.S. and SUGEN.

Funders	Funder number
Krebsregister Kanton Zürich
International Human Frontier Science Program Organization	RG-562/96
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

ASJC Scopus subject areas

Genetics

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10.1093/nar/26.15.3542

Cite this

@article{d87218f1b6884532910fb2515311d67a,

title = "SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements",

abstract = "Interphase chromatin is arranged into topologically separated domains comprising gene expression and replication units through genomic sequence elements so-called MAR or SAR regions (for matrix- or scaffold-associating regions). S/MAR regions are located near the boundaries of actively transcribed genes and were shown to influence their activity. We show that scaffold attachment factor B (SAF-B), which specifically binds to S/MAR regions, interacts with RNA polymerase II (RNA pol II) and a subset of serine-/arginine-rich RNA processing factors (SR proteins). SAF-B localized to the nucleus in a speckled pattern that coincided with the distribution of the SR protein SC35. Furthermore, we show that overexpressed SAF-B induced an increase of the 10S splice product using an E1A reporter gene and repressed the activity of an S/MAR flanked CAT reporter gene construct in vivo. This indicates an association of SAF-B with SR proteins and components of the transcription machinery. Our results describe the coupling of a chromatin organizing S/MAR element with transcription and pre-mRNA processing components and we propose that SAF-B serves as a molecular base to assemble a 'transcriptosome complex' in the vicinity of actively transcribed genes.",

author = "Oliver Nayler and Wolf Str{\"a}tling and Bourquin, \{Jean Pierre\} and Igor Stagljar and Lothar Lindemann and Heinrich Jasper and Hartmann, \{Annette M.\} and Fackelmayer, \{Frank O.\} and Axel Ullrich and Stefan Stamm",

note = "Funding Information: We thank C.Cap for help with sequencing, O.Georgiev for his contribution to the isolation of CTD interacting clones, J.C{\'a}ceres for the E1A construct and I.Sures and M.Stein-Gerlach for reading the manuscript. We also thank J.Chalcroft and Yuh-Shin Chang for technical assistance, and Walter Schaffner for support and helpful discussions. This work was supported by the Swiss National Science Foundation, the Kanton Z{\"u}rich, the Max-Planck-Society, the Human Frontier Science Program RG-562/96 to S.S. and SUGEN.",

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doi = "10.1093/nar/26.15.3542",

language = "English",

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AU - Nayler, Oliver

AU - Strätling, Wolf

AU - Bourquin, Jean Pierre

AU - Stagljar, Igor

AU - Lindemann, Lothar

AU - Jasper, Heinrich

AU - Hartmann, Annette M.

AU - Fackelmayer, Frank O.

AU - Ullrich, Axel

AU - Stamm, Stefan

N1 - Funding Information: We thank C.Cap for help with sequencing, O.Georgiev for his contribution to the isolation of CTD interacting clones, J.Cáceres for the E1A construct and I.Sures and M.Stein-Gerlach for reading the manuscript. We also thank J.Chalcroft and Yuh-Shin Chang for technical assistance, and Walter Schaffner for support and helpful discussions. This work was supported by the Swiss National Science Foundation, the Kanton Zürich, the Max-Planck-Society, the Human Frontier Science Program RG-562/96 to S.S. and SUGEN.

PY - 1998/8/1

Y1 - 1998/8/1

N2 - Interphase chromatin is arranged into topologically separated domains comprising gene expression and replication units through genomic sequence elements so-called MAR or SAR regions (for matrix- or scaffold-associating regions). S/MAR regions are located near the boundaries of actively transcribed genes and were shown to influence their activity. We show that scaffold attachment factor B (SAF-B), which specifically binds to S/MAR regions, interacts with RNA polymerase II (RNA pol II) and a subset of serine-/arginine-rich RNA processing factors (SR proteins). SAF-B localized to the nucleus in a speckled pattern that coincided with the distribution of the SR protein SC35. Furthermore, we show that overexpressed SAF-B induced an increase of the 10S splice product using an E1A reporter gene and repressed the activity of an S/MAR flanked CAT reporter gene construct in vivo. This indicates an association of SAF-B with SR proteins and components of the transcription machinery. Our results describe the coupling of a chromatin organizing S/MAR element with transcription and pre-mRNA processing components and we propose that SAF-B serves as a molecular base to assemble a 'transcriptosome complex' in the vicinity of actively transcribed genes.

AB - Interphase chromatin is arranged into topologically separated domains comprising gene expression and replication units through genomic sequence elements so-called MAR or SAR regions (for matrix- or scaffold-associating regions). S/MAR regions are located near the boundaries of actively transcribed genes and were shown to influence their activity. We show that scaffold attachment factor B (SAF-B), which specifically binds to S/MAR regions, interacts with RNA polymerase II (RNA pol II) and a subset of serine-/arginine-rich RNA processing factors (SR proteins). SAF-B localized to the nucleus in a speckled pattern that coincided with the distribution of the SR protein SC35. Furthermore, we show that overexpressed SAF-B induced an increase of the 10S splice product using an E1A reporter gene and repressed the activity of an S/MAR flanked CAT reporter gene construct in vivo. This indicates an association of SAF-B with SR proteins and components of the transcription machinery. Our results describe the coupling of a chromatin organizing S/MAR element with transcription and pre-mRNA processing components and we propose that SAF-B serves as a molecular base to assemble a 'transcriptosome complex' in the vicinity of actively transcribed genes.

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SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

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