Fanzor is a eukaryotic programmable RNA-guided endonuclease

RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR–Cas systems provide adaptive immunity for bacte...

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Published inNature (London) Vol. 620; no. 7974; pp. 660 - 668
Main Authors Saito, Makoto, Xu, Peiyu, Faure, Guilhem, Maguire, Samantha, Kannan, Soumya, Altae-Tran, Han, Vo, Sam, Desimone, AnAn, Macrae, Rhiannon K., Zhang, Feng
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 17.08.2023
Nature Publishing Group
Subjects
42/44
45/91
631/45
631/535
Adaptive immunity
Adaptive systems
Archaea
Archaea - genetics
Archaea - immunology
Bacteria
Bacteria - genetics
Bacteria - immunology
Biological activity
Chytridiomycota - enzymology
Complementarity
Conservation
Conserved Sequence
CRISPR
CRISPR-Associated Protein 9 - metabolism
CRISPR-Associated Proteins - chemistry
CRISPR-Associated Proteins - metabolism
CRISPR-Associated Proteins - ultrastructure
CRISPR-Cas Systems
Cryoelectron Microscopy
Deoxyribonucleic acid
DNA
DNA Transposable Elements - genetics
Electron microscopy
Endonuclease
Endonucleases - chemistry
Endonucleases - metabolism
Endonucleases - ultrastructure
Eukaryota - enzymology
Eukaryotes
Evolution, Molecular
Fungal Proteins - chemistry
Fungal Proteins - metabolism
Fungal Proteins - ultrastructure
Fungi
Gene Editing - methods
Gene sequencing
Genes
Genome editing
Genomes
Humanities and Social Sciences
Humans
multidisciplinary
Nucleic acids
Prokaryotes
Proteins
Ribonucleic acid
RNA
RNA - genetics
RNA - metabolism
RNA modification
RNA, Guide, CRISPR-Cas Systems - genetics
RNA, Guide, CRISPR-Cas Systems - metabolism
RNA-mediated interference
rRNA
Science
Science (multidisciplinary)
Online AccessGet full text

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Abstract RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR–Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage 1 . Although a few eukaryotic RNA-guided systems have been studied, including RNA interference 2 and ribosomal RNA modification 3 , it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported 4 , 5 . The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity 4 , 6 . TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins 4 , 7 , raising the possibility that eukaryotes are also equipped with CRISPR–Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life. Fanzor is shown to be an RNA-guided DNA endonuclease, demonstrating that such endonucleases are found in all domains of life and indicating a potential new tool for genome engineering applications.
AbstractList RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR–Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage 1 . Although a few eukaryotic RNA-guided systems have been studied, including RNA interference 2 and ribosomal RNA modification 3 , it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported 4 , 5 . The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity 4 , 6 . TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins 4 , 7 , raising the possibility that eukaryotes are also equipped with CRISPR–Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life. Fanzor is shown to be an RNA-guided DNA endonuclease, demonstrating that such endonucleases are found in all domains of life and indicating a potential new tool for genome engineering applications.
RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR-Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage1. Although a few eukaryotic RNA-guided systems have been studied, including RNA interference2 and ribosomal RNA modification3, it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported4,5. The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity4,6. TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins4,7, raising the possibility that eukaryotes are also equipped with CRISPR-Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life.RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR-Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage1. Although a few eukaryotic RNA-guided systems have been studied, including RNA interference2 and ribosomal RNA modification3, it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported4,5. The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity4,6. TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins4,7, raising the possibility that eukaryotes are also equipped with CRISPR-Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life.
RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR-Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage. Although a few eukaryotic RNA-guided systems have been studied, including RNA interference and ribosomal RNA modification, it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported. The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity. TnpB may also be the ancestor ofthe eukaryotic transposon-encoded Fanzor (Fz) proteins, raising the possibility that eukaryotes are also equipped with CRISPR-Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life.
RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR-Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage . Although a few eukaryotic RNA-guided systems have been studied, including RNA interference and ribosomal RNA modification , it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported . The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity . TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins , raising the possibility that eukaryotes are also equipped with CRISPR-Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life.
RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in biological processes in both prokaryotes and eukaryotes. For example, the prokaryotic CRISPR–Cas systems provide adaptive immunity for bacteria and archaea against foreign genetic elements. Cas effectors such as Cas9 and Cas12 perform guide-RNA-dependent DNA cleavage 1 . Although a few eukaryotic RNA-guided systems have been studied, including RNA interference 2 and ribosomal RNA modification 3 , it remains unclear whether eukaryotes have RNA-guided endonucleases. Recently, a new class of prokaryotic RNA-guided systems (termed OMEGA) was reported 4,5 . The OMEGA effector TnpB is the putative ancestor of Cas12 and has RNA-guided endonuclease activity 4,6 . TnpB may also be the ancestor of the eukaryotic transposon-encoded Fanzor (Fz) proteins 4,7 , raising the possibility that eukaryotes are also equipped with CRISPR–Cas or OMEGA-like programmable RNA-guided endonucleases. Here we report the biochemical characterization of Fz, showing that it is an RNA-guided DNA endonuclease. We also show that Fz can be reprogrammed for human genome engineering applications. Finally, we resolve the structure of Spizellomyces punctatus Fz at 2.7 Å using cryogenic electron microscopy, showing the conservation of core regions among Fz, TnpB and Cas12, despite diverse cognate RNA structures. Our results show that Fz is a eukaryotic OMEGA system, demonstrating that RNA-guided endonucleases are present in all three domains of life.
Author Maguire, Samantha
Kannan, Soumya
Altae-Tran, Han
Saito, Makoto
Desimone, AnAn
Xu, Peiyu
Faure, Guilhem
Macrae, Rhiannon K.
Vo, Sam
Zhang, Feng
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  surname: Saito
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  orcidid: 0000-0003-3590-4037
  surname: Xu
  fullname: Xu, Peiyu
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  orcidid: 0000-0001-9537-2277
  surname: Faure
  fullname: Faure, Guilhem
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  orcidid: 0000-0002-7332-9662
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  fullname: Kannan, Soumya
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  givenname: Han
  surname: Altae-Tran
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  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  givenname: Sam
  orcidid: 0000-0001-6020-4716
  surname: Vo
  fullname: Vo, Sam
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
– sequence: 9
  givenname: Rhiannon K.
  surname: Macrae
  fullname: Macrae, Rhiannon K.
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
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  givenname: Feng
  orcidid: 0000-0003-0178-7995
  surname: Zhang
  fullname: Zhang, Feng
  email: zhang@broadinstitute.org
  organization: Broad Institute of MIT and Harvard, McGovern Institute for Brain Research at MIT, Department of Brain and Cognitive Science, Massachusetts Institute of Technology, Department of Biological Engineering, Massachusetts Institute of Technology, Howard Hughes Medical Institute
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37380027$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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2023. The Author(s).
Copyright Nature Publishing Group Aug 17, 2023
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Snippet RNA-guided systems, which use complementarity between a guide RNA and target nucleic acid sequences for recognition of genetic elements, have a central role in...
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SubjectTerms 42/44
45/91
631/45
631/535
Adaptive immunity
Adaptive systems
Archaea
Archaea - genetics
Archaea - immunology
Bacteria
Bacteria - genetics
Bacteria - immunology
Biological activity
Chytridiomycota - enzymology
Complementarity
Conservation
Conserved Sequence
CRISPR
CRISPR-Associated Protein 9 - metabolism
CRISPR-Associated Proteins - chemistry
CRISPR-Associated Proteins - metabolism
CRISPR-Associated Proteins - ultrastructure
CRISPR-Cas Systems
Cryoelectron Microscopy
Deoxyribonucleic acid
DNA
DNA Transposable Elements - genetics
Electron microscopy
Endonuclease
Endonucleases - chemistry
Endonucleases - metabolism
Endonucleases - ultrastructure
Eukaryota - enzymology
Eukaryotes
Evolution, Molecular
Fungal Proteins - chemistry
Fungal Proteins - metabolism
Fungal Proteins - ultrastructure
Fungi
Gene Editing - methods
Gene sequencing
Genes
Genome editing
Genomes
Humanities and Social Sciences
Humans
multidisciplinary
Nucleic acids
Prokaryotes
Proteins
Ribonucleic acid
RNA
RNA - genetics
RNA - metabolism
RNA modification
RNA, Guide, CRISPR-Cas Systems - genetics
RNA, Guide, CRISPR-Cas Systems - metabolism
RNA-mediated interference
rRNA
Science
Science (multidisciplinary)
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Title Fanzor is a eukaryotic programmable RNA-guided endonuclease
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