Prokaryotic argonaute proteins: novel genome-editing tools?

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ABSTRACT Argonaute proteins constitute a highly diverse family of nucleic acid-guided proteins. They were first discovered in eukaryotes as key proteins in RNA interference systems, but


homologous prokaryotic Argonaute proteins (pAgos) have also been found in archaea and bacteria. In this Progress article, we focus on long pAgo variants, a class of pAgos that are involved


in nucleic acid-guided host defence against invading nucleic acids, and discuss the potential of pAgos in genome editing. Access through your institution Buy or subscribe This is a preview


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GUIDE AND TARGET STRANDS BY THE _ARCHAEOGLOBUS FULGIDUS_ ARGONAUTE PROTEIN Article Open access 14 April 2023 DNA TARGETING AND INTERFERENCE BY A BACTERIAL ARGONAUTE NUCLEASE Article 30 July


2020 DNA-TARGETING SHORT ARGONAUTES COMPLEX WITH EFFECTOR PROTEINS FOR COLLATERAL NUCLEASE ACTIVITY AND BACTERIAL POPULATION IMMUNITY Article 15 April 2024 ACCESSION CODES ACCESSIONS PROTEIN


DATA BANK * 3F73 * 4Z4C * RCSB Protein Data Bank REFERENCES * Bohmert, K. et al. AGO1 defines a novel locus of _Arabidopsis_ controlling leaf development. _EMBO J._ 17, 170–180 (1998). CAS


  PubMed  PubMed Central  Google Scholar  * Ketting, R. F. The many faces of RNAi. _Dev. Cell_ 20, 148–161 (2011). Article  CAS  PubMed  Google Scholar  * Hammond, S. M., Bernstein, E.,


Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in _Drosophila_ cells. _Nature_ 404, 293–296 (2000). Article  CAS  PubMed  Google Scholar


  * Swarts, D. C. et al. The evolutionary journey of Argonaute proteins. _Nat. Struct. Mol. Biol._ 21, 743–753 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Hutvagner, G.


& Simard, M. J. Argonaute proteins: key players in RNA silencing. _Nat. Rev. Mol. Cell Biol._ 9, 22–32 (2008). Article  CAS  PubMed  Google Scholar  * Hannon, G. J. RNA interference.


_Nature_ 418, 244–251 (2002). Article  CAS  PubMed  Google Scholar  * Song, J. J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of Argonaute and its implications for


RISC slicer activity. _Science_ 305, 1434–1437 (2004). Article  CAS  PubMed  Google Scholar  * Yuan, Y. R. et al. Crystal structure of _A. aeolicus_ Argonaute, a site-specific DNA-guided


endoribonuclease, provides insights into RISC-mediated mRNA cleavage. _Mol. Cell_ 19, 405–419 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Shabalina, S. A. & Koonin,


E. V. Origins and evolution of eukaryotic RNA interference. _Trends Ecol. Evol._ 23, 578–587 (2008). Article  PubMed  PubMed Central  Google Scholar  * Wang, Y. et al. Nucleation,


propagation and cleavage of target RNAs in Ago silencing complexes. _Nature_ 461, 754–761 (2009). Article  CAS  PubMed  PubMed Central  Google Scholar  * Olovnikov, I., Chan, K.,


Sachidanandam, R., Newman, D. & Aravin, A. Bacterial Argonaute samples the transcriptome to identify foreign DNA. _Mol. Cell_ 51, 594–605 (2013). Article  CAS  PubMed  Google Scholar  *


Swarts, D. C. et al. DNA-guided DNA interference by a prokaryotic Argonaute. _Nature_ 507, 258–261 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Swarts, D. C. et al.


Argonaute of the archaeon _Pyrococcus furiosus_ is a DNA-guided nuclease that targets cognate DNA. _Nucleic Acids Res._ 43, 5120–5129 (2015). Article  CAS  PubMed  PubMed Central  Google


Scholar  * Kaya, E. et al. A bacterial Argonaute with noncanonical guide RNA specificity. _Proc. Natl Acad. Sci. USA_ 113, 4057–4062 (2016). Article  CAS  PubMed  Google Scholar  * Zander,


A., Holzmeister, P., Klose, D., Tinnefeld, P. & Grohmann, D. Single-molecule FRET supports the two-state model of Argonaute action. _RNA Biol._ 11, 45–56 (2014). Article  CAS  PubMed 


Google Scholar  * Swarts, D. C., Koehorst, J. J., Westra, E. R., Schaap, P. J. & van der Oost, J. Effects of argonaute on gene expression in _Thermus thermophilus_. _PLoS ONE_ 10,


e0124880 (2015). Article  PubMed  PubMed Central  Google Scholar  * Willkomm, S. et al. Structural and mechanistic insights into the DNA-guided DNA endonuclease activity of an archaeal


Argonaute. _Nat. Microbiol._ 2, 17035 (2017). Article  CAS  PubMed  Google Scholar  * Zander, A. et al. Guide-independent DNA cleavage by archaeal Argonaute from _Methanocaldococcus


jannaschii_. _Nat. Microbiol._ 2, 17034 (2017). Article  CAS  PubMed  Google Scholar  * Swarts, D. C. et al. Autonomous generation and loading of DNA guides by bacterial Argonaute. _Mol.


Cell_ 65, 985–998 (2017). Article  CAS  PubMed  PubMed Central  Google Scholar  * Miyoshi, T., Ito, K., Murakami, R. & Uchiumi, T. Structural basis for the recognition of guide RNA and


target DNA heteroduplex by Argonaute. _Nat. Commun._ 7, 11846 (2016). Article  CAS  PubMed  PubMed Central  Google Scholar  * Wang, Y. et al. Structure of an argonaute silencing complex with


a seed-containing guide DNA and target RNA duplex. _Nature_ 456, 921–926 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * Wang, Y., Sheng, G., Juranek, S., Tuschl, T. &


Patel, D. J. Structure of the guide-strand-containing argonaute silencing complex. _Nature_ 456, 209–213 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * Ma, J. B. et al.


Structural basis for 5′-end-specific recognition of guide RNA by the _A. fulgidus_ Piwi protein. _Nature_ 434, 356–372 (2015). Google Scholar  * Song, J.-J. et al. The crystal structure of


the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. _Nat. Struct. Biol._ 10, 1026–1032 (2003). CAS  PubMed  Google Scholar  * Liu, J. et al. Argonaute2 is the


catalytic engine of mammalian RNAi. _Science_ 305, 1437–1441 (2004). Article  CAS  PubMed  Google Scholar  * Makarova, K. S., Wolf, Y. I., van der Oost, J. & Koonin, E. V. Prokaryotic


homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. _Biol. Direct_ 4, 29 (2009). Article  PubMed  PubMed


Central  Google Scholar  * Kwak, P. B. & Tomari, Y. The N domain of Argonaute drives duplex unwinding during RISC assembly. _Nat. Struct. Mol. Biol._ 19, 145–151 (2012). Article  CAS 


PubMed  Google Scholar  * Sheng, G. et al. Structure-based cleavage mechanism of _Thermus thermophilus_ Argonaute DNA guide strand-mediated DNA target cleavage. _Proc. Natl Acad. Sci. USA_


111, 652–657 (2014). Article  CAS  PubMed  Google Scholar  * Parker, J. S., Roe, S. M. & Barford, D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex.


_Nature_ 434, 663–666 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Burroughs, A. M., Iyer, L. M. & Aravind, L. Two novel PIWI families: roles in inter-genomic


conflicts in bacteria and mediator-dependent modulation of transcription in eukaryotes. _Biol. Direct_ 8, 13 (2013). Article  PubMed  PubMed Central  Google Scholar  * Enghiad, B. &


Zhao, H. Programmable DNA-guided artificial restriction enzymes. _ACS Synth. Biol._ 6, 752–757 (2017). Article  CAS  PubMed  Google Scholar  * Hsu, P. D. et al. DNA targeting specificity of


RNA-guided Cas9 nucleases. _Nat. Biotechnol._ 31, 827–832 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Zetsche, B. et al. Cpf1 is a single RNA-guided endonuclease of a


class 2 CRISPR–Cas system. _Cell_ 163, 759–771 (2015). Article  CAS  PubMed  PubMed Central  Google Scholar  * Sander, J. D. & Joung, J. K. CRISPR–Cas systems for editing, regulating and


targeting genomes. _Nat. Biotechnol._ 32, 347–355 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Gao, F., Shen, X. Z., Jiang, F., Wu, Y. & Han, C. DNA-guided genome


editing using the _Natronobacterium gregoryi_ Argonaute. _Nat. Biotechnol._ 34, 768–772 (2016). Article  CAS  PubMed  Google Scholar  * Cyranoski, D. Replications, ridicule and a recluse:


the controversy over NgAgo gene-editing intensifies. _Nature_ 536, 136–137 (2016). Article  CAS  PubMed  Google Scholar  * Lee, S. H. et al. Failure to detect DNA-guided genome editing using


_Natronobacterium gregoryi_ Argonaute. _Nat. Biotechnol._ 35, 17–18 (2016). Article  PubMed  PubMed Central  Google Scholar  * Javidi-Parsijani, P. et al. No evidence of genome editing


activity from _Natronobacterium gregoryi_ Argonaute (NgAgo) in human cells. _PLoS ONE_ 12, e0177444 (2017). Article  PubMed  PubMed Central  Google Scholar  * Qi, J. et al. NgAgo-based


fabp11a gene knockdown causes eye developmental defects in zebrafish. _Cell Res._ 26, 1349–1352 (2016). Article  CAS  PubMed  PubMed Central  Google Scholar  * Sunghyeok, Y. et al.


DNA-dependent RNA cleavage by the _Natronobacterium gregoryi_ Argonaute. Preprint at _bioRxiv_ http://dx.doi.org/10.1101/101923 (2017). * Qi, L. S. et al. Repurposing CRISPR as an RNA-guided


platform for sequence-specific control of gene expression. _Cell_ 152, 1173–1183 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Smalheiser, N. R. & Gomes, O. L. A.


Mammalian Argonaute-DNA binding? _Biol. Direct_ 10, 27 (2015). Article  Google Scholar  * Blesa, A., César, C. E., Averhoff, B. & Berenguer, J. Noncanonical cell-to-cell DNA transfer in


_Thermus_ spp. is insensitive to argonaute-mediated interference. _J. Bacteriol._ 197, 138–146 (2015). Article  PubMed  Google Scholar  * Averhoff, B. Shuffling genes around in hot


environments: the unique DNA transporter of _Thermus thermophilus_. _FEMS Microbiol. Rev._ 33, 611–626 (2009). Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS Work in the


authors' laboratory was financially supported by a grant from the Netherlands Organization of Scientific Research (NWO-ECHO grant 711013002 and NWO-TOP grant 714015001) to J.v.d.O., and


by a long-term postdoctoral fellowship from the European Molecular Biology Organization (EMBO) to D.C.S. (ALTF 179–2015). AUTHOR INFORMATION Author notes * Jorrit W. Hegge and Daan C.


Swarts: J.W.H and D.C.S contributed equally to this work. AUTHORS AND AFFILIATIONS * Department of Agrotechnology and Food Sciences, Laboratory of Microbiology, Wageningen University,


Stippeneng 4, Wageningen, 6708WE, The Netherlands Jorrit W. Hegge & John van der Oost * Department of Biochemistry, University of Zurich, Winterthurerstrasse 190, Zurich, CH-8057,


Switzerland Daan C. Swarts Authors * Jorrit W. Hegge View author publications You can also search for this author inPubMed Google Scholar * Daan C. Swarts View author publications You can


also search for this author inPubMed Google Scholar * John van der Oost View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR


Correspondence to John van der Oost. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. RELATED LINKS DATABASES RCSB Protein Data Bank 4Z4C 3F73


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ARTICLE CITE THIS ARTICLE Hegge, J., Swarts, D. & van der Oost, J. Prokaryotic Argonaute proteins: novel genome-editing tools?. _Nat Rev Microbiol_ 16, 5–11 (2018).


https://doi.org/10.1038/nrmicro.2017.73 Download citation * Published: 24 July 2017 * Issue Date: January 2018 * DOI: https://doi.org/10.1038/nrmicro.2017.73 SHARE THIS ARTICLE Anyone you


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