Enhanced Bacterial Immunity and Mammalian Genome Editing via RNA-Polymerase-Mediated Dislodging of Cas9 from Double-Strand DNA Breaks
The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome editing and an essential component of adaptive immune systems in bacteria. After generating a double-stranded break (DSB), Cas9 remains stably...
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Published in | Molecular cell Vol. 71; no. 1; pp. 42 - 55.e8 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
05.07.2018
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Abstract | The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome editing and an essential component of adaptive immune systems in bacteria. After generating a double-stranded break (DSB), Cas9 remains stably bound to DNA. Here, we show persistent Cas9 binding blocks access to the DSB by repair enzymes, reducing genome editing efficiency. Cas9 can be dislodged by translocating RNA polymerases, but only if the polymerase approaches from one direction toward the Cas9-DSB complex. By exploiting these RNA-polymerase/Cas9 interactions, Cas9 can be conditionally converted into a multi-turnover nuclease, mediating increased mutagenesis frequencies in mammalian cells and enhancing bacterial immunity to bacteriophages. These consequences of a stable Cas9-DSB complex provide insights into the evolution of protospacer adjacent motif (PAM) sequences and a simple method of improving selection of highly active sgRNAs for genome editing.
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•Persistent Cas9 binding blocks DNA repair proteins from accessing Cas9-generated breaks•RNA polymerase can dislodge Cas9 from DNA breaks in a highly strand-biased manner•Dislodging Cas9 with RNA polymerase generates multi-turnover nuclease activity•Targeting of Cas9 to phage genome is strand biased toward multi-turnover activities
Clarke et al. show that persistent Cas9 binding to double-strand DNA breaks (DSBs) blocks DNA break repair. The Cas9-DSB complex can be disrupted by translocating RNA polymerases in a strand-biased manner, increasing genome editing frequencies and enhancing bacterial immunity to phages through multi-turnover Cas9 cleavage of phage genomes. |
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AbstractList | The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome editing and an essential component of adaptive immune systems in bacteria. After generating a double-stranded break (DSB), Cas9 remains stably bound to DNA. Here, we show persistent Cas9 binding blocks access to the DSB by repair enzymes, reducing genome editing efficiency. Cas9 can be dislodged by translocating RNA polymerases, but only if the polymerase approaches from one direction toward the Cas9-DSB complex. By exploiting these RNA-polymerase/Cas9 interactions, Cas9 can be conditionally converted into a multi-turnover nuclease, mediating increased mutagenesis frequencies in mammalian cells and enhancing bacterial immunity to bacteriophages. These consequences of a stable Cas9-DSB complex provide insights into the evolution of protospacer adjacent motif (PAM) sequences and a simple method of improving selection of highly active sgRNAs for genome editing.
[Display omitted]
•Persistent Cas9 binding blocks DNA repair proteins from accessing Cas9-generated breaks•RNA polymerase can dislodge Cas9 from DNA breaks in a highly strand-biased manner•Dislodging Cas9 with RNA polymerase generates multi-turnover nuclease activity•Targeting of Cas9 to phage genome is strand biased toward multi-turnover activities
Clarke et al. show that persistent Cas9 binding to double-strand DNA breaks (DSBs) blocks DNA break repair. The Cas9-DSB complex can be disrupted by translocating RNA polymerases in a strand-biased manner, increasing genome editing frequencies and enhancing bacterial immunity to phages through multi-turnover Cas9 cleavage of phage genomes. The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome editing and an essential component of adaptive immune systems in bacteria. After generating a double-stranded break (DSB), Cas9 remains stably bound to DNA. Here, we show persistent Cas9 binding blocks access to the DSB by repair enzymes, reducing genome editing efficiency. Cas9 can be dislodged by translocating RNA polymerases, but only if the polymerase approaches from one direction toward the Cas9-DSB complex. By exploiting these RNA-polymerase/Cas9 interactions, Cas9 can be conditionally converted into a multi-turnover nuclease, mediating increased mutagenesis frequencies in mammalian cells and enhancing bacterial immunity to bacteriophages. These consequences of a stable Cas9-DSB complex provide insights into the evolution of protospacer adjacent motif (PAM) sequences and a simple method of improving selection of highly active sgRNAs for genome editing. The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome editing and an essential component of adaptive immune systems in bacteria. After generating a double strand break n(DSB), Cas9 remains stably bound to the DNA. Here we show persistent Cas9 binding blocks access to the DSB by repair enzymes, reducing genome editing efficiency. Cas9 can be dislodged by translocating RNA polymerases, but only if the polymerase approaches from one direction towards the Cas9-DSB complex. By exploiting these RNA polymerase-Cas9 interactions, Cas9 can be conditionally converted into a multi-turnover nuclease, mediating increased mutagenesis frequencies in mammalian cells and enhancing bacterial immunity to bacteriophages. These consequences of a stable Cas9-DSB complex provide insights into the evolution of PAM sequences and a simple method of improving selection of highly active sgRNA for genome editing. Clarke et al show that persistent DNA binding of Cas9 precludes repair of DNA breaks. Translocating RNA polymerases can dislodge Cas9 from DNA, but only in a highly strand-biased manner. This effect is suggested to mediate strand-biased increases in genome editing efficiency in mammalian cells and CRISPR immunity bacteria. |
Author | Heler, Robert Yeo, Nan Cher Merrill, Bradley J. Clarke, Ryan Hanakahi, Leslyn Regan, Maureen Church, George M. Chavez, Alejandro Marraffini, Luciano A. MacDougall, Matthew S. |
AuthorAffiliation | 2 Laboratory of Bacteriology, The Rockefeller University, New York, NY 10065 3 Department of Genetics, Harvard Medical School, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115 5 Department of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, University of Illinois at Chicago, Rockford Health Science Campus, Rockford, IL 61107 1 Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607 4 Genome Editing Core, University of Illinois at Chicago, Chicago, IL 60607 |
AuthorAffiliation_xml | – name: 1 Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607 – name: 2 Laboratory of Bacteriology, The Rockefeller University, New York, NY 10065 – name: 4 Genome Editing Core, University of Illinois at Chicago, Chicago, IL 60607 – name: 5 Department of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, University of Illinois at Chicago, Rockford Health Science Campus, Rockford, IL 61107 – name: 3 Department of Genetics, Harvard Medical School, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115 |
Author_xml | – sequence: 1 givenname: Ryan surname: Clarke fullname: Clarke, Ryan organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA – sequence: 2 givenname: Robert surname: Heler fullname: Heler, Robert organization: Laboratory of Bacteriology, The Rockefeller University, New York, NY 10065, USA – sequence: 3 givenname: Matthew S. surname: MacDougall fullname: MacDougall, Matthew S. organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA – sequence: 4 givenname: Nan Cher surname: Yeo fullname: Yeo, Nan Cher organization: Department of Genetics, Harvard Medical School, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA – sequence: 5 givenname: Alejandro surname: Chavez fullname: Chavez, Alejandro organization: Department of Genetics, Harvard Medical School, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA – sequence: 6 givenname: Maureen surname: Regan fullname: Regan, Maureen organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA – sequence: 7 givenname: Leslyn surname: Hanakahi fullname: Hanakahi, Leslyn organization: Department of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, University of Illinois at Chicago, Rockford Health Science Campus, Rockford, IL 61107, USA – sequence: 8 givenname: George M. surname: Church fullname: Church, George M. organization: Department of Genetics, Harvard Medical School, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA – sequence: 9 givenname: Luciano A. surname: Marraffini fullname: Marraffini, Luciano A. organization: Laboratory of Bacteriology, The Rockefeller University, New York, NY 10065, USA – sequence: 10 givenname: Bradley J. surname: Merrill fullname: Merrill, Bradley J. email: merrillb@uic.edu organization: Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL 60607, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29979968$$D View this record in MEDLINE/PubMed |
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Keywords | CRISPR genome editing strand bias phage biology transcription Cas9 RNA polymerase DNA repair |
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Snippet | The ability to target the Cas9 nuclease to DNA sequences via Watson-Crick base pairing with a single guide RNA (sgRNA) has provided a dynamic tool for genome... |
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SubjectTerms | Animals Bacteria - genetics Bacteria - metabolism Bacteria - virology Bacteriophages - genetics Bacteriophages - metabolism Cas9 Cell Line CRISPR CRISPR-Associated Protein 9 - genetics CRISPR-Associated Protein 9 - metabolism DNA Breaks, Double-Stranded DNA Repair Gene Editing genome editing Mice Mouse Embryonic Stem Cells - metabolism phage biology RNA polymerase strand bias transcription |
Title | Enhanced Bacterial Immunity and Mammalian Genome Editing via RNA-Polymerase-Mediated Dislodging of Cas9 from Double-Strand DNA Breaks |
URI | https://dx.doi.org/10.1016/j.molcel.2018.06.005 https://www.ncbi.nlm.nih.gov/pubmed/29979968 https://search.proquest.com/docview/2066482751 https://pubmed.ncbi.nlm.nih.gov/PMC6063522 |
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