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Universal promoter scanning by Pol II during transcription initiation in Saccharomyces cerevisiae

C. Qiu, H. Jin, I. Vvedenskaya, JA. Llenas, T. Zhao, I. Malik, AM. Visbisky, SL. Schwartz, P. Cui, P. Čabart, KH. Han, WKM. Lai, RP. Metz, CD. Johnson, SH. Sze, BF. Pugh, BE. Nickels, CD. Kaplan

. 2020 ; 21 (1) : 132. [pub] 20200602

Jazyk angličtina Země Velká Británie

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/bmc21020466

Grantová podpora
R01 GM088343 NIGMS NIH HHS - United States
R35 GM118059 NIGMS NIH HHS - United States
R01 GM120450 NIGMS NIH HHS - United States
R01 GM097260 NIGMS NIH HHS - United States

BACKGROUND: The majority of eukaryotic promoters utilize multiple transcription start sites (TSSs). How multiple TSSs are specified at individual promoters across eukaryotes is not understood for most species. In Saccharomyces cerevisiae, a pre-initiation complex (PIC) comprised of Pol II and conserved general transcription factors (GTFs) assembles and opens DNA upstream of TSSs. Evidence from model promoters indicates that the PIC scans from upstream to downstream to identify TSSs. Prior results suggest that TSS distributions at promoters where scanning occurs shift in a polar fashion upon alteration in Pol II catalytic activity or GTF function. RESULTS: To determine the extent of promoter scanning across promoter classes in S. cerevisiae, we perturb Pol II catalytic activity and GTF function and analyze their effects on TSS usage genome-wide. We find that alterations to Pol II, TFIIB, or TFIIF function widely alter the initiation landscape consistent with promoter scanning operating at all yeast promoters, regardless of promoter class. Promoter architecture, however, can determine the extent of promoter sensitivity to altered Pol II activity in ways that are predicted by a scanning model. CONCLUSIONS: Our observations coupled with previous data validate key predictions of the scanning model for Pol II initiation in yeast, which we term the shooting gallery. In this model, Pol II catalytic activity and the rate and processivity of Pol II scanning together with promoter sequence determine the distribution of TSSs and their usage.

Citace poskytuje Crossref.org

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$a Qiu, Chenxi $u Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA $u Present Address: Department of Medicine, Division of Translational Therapeutics, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, 02215, USA
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$a BACKGROUND: The majority of eukaryotic promoters utilize multiple transcription start sites (TSSs). How multiple TSSs are specified at individual promoters across eukaryotes is not understood for most species. In Saccharomyces cerevisiae, a pre-initiation complex (PIC) comprised of Pol II and conserved general transcription factors (GTFs) assembles and opens DNA upstream of TSSs. Evidence from model promoters indicates that the PIC scans from upstream to downstream to identify TSSs. Prior results suggest that TSS distributions at promoters where scanning occurs shift in a polar fashion upon alteration in Pol II catalytic activity or GTF function. RESULTS: To determine the extent of promoter scanning across promoter classes in S. cerevisiae, we perturb Pol II catalytic activity and GTF function and analyze their effects on TSS usage genome-wide. We find that alterations to Pol II, TFIIB, or TFIIF function widely alter the initiation landscape consistent with promoter scanning operating at all yeast promoters, regardless of promoter class. Promoter architecture, however, can determine the extent of promoter sensitivity to altered Pol II activity in ways that are predicted by a scanning model. CONCLUSIONS: Our observations coupled with previous data validate key predictions of the scanning model for Pol II initiation in yeast, which we term the shooting gallery. In this model, Pol II catalytic activity and the rate and processivity of Pol II scanning together with promoter sequence determine the distribution of TSSs and their usage.
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$a Jin, Huiyan $u Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA
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$a Llenas, Jordi Abante $u Department of Electrical and Computer Engineering, Texas A&M University, College Station, TX, 77843-3128, USA $u Present Address: Whitaker Biomedical Engineering Institute, Johns Hopkins University, Baltimore, MD, 21218, USA
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$a Zhao, Tingting $u Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA
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$a Malik, Indranil $u Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA $u Present Address: Department of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA
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$a Visbisky, Alex M $u Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA
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$a Schwartz, Scott L $u Genomics and Bioinformatics Service, Texas A&M AgriLife, College Station, TX, 77845, USA
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$a Čabart, Pavel $u Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA $u Present Address: First Faculty of Medicine, Charles University, BIOCEV, 252 42, Vestec, Czech Republic
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$a Han, Kang Hoo $u Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, 16802, USA
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$a Metz, Richard P $u Genomics and Bioinformatics Service, Texas A&M AgriLife, College Station, TX, 77845, USA
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$a Sze, Sing-Hoi $u Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA $u Department of Computer Science and Engineering, Texas A&M University, College Station, TX, 77843-3127, USA
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$a Pugh, B Franklin $u Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, 16802, USA $u Present Address: Department of Molecular Biology and Genetics, 458 Biotechnology, Cornell University, New York, 14853, USA
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$a Nickels, Bryce E $u Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA $u Department of Genetics, Rutgers University, Piscataway, NJ, 08854, USA
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$a Kaplan, Craig D $u Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA. craig.kaplan@pitt.edu
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