The evolutionary journey of Argonaute proteins

Swarts, Daan C.; Makarova, Kira S.; Wang, Yanli; Nakanishi, K.; Ketting, René F.; Koonin, Eugene V.; Patel, Dinshaw J.; Oost, John van der

doi:10.1038/nsmb.2879

Cited by 409 publications

(492 citation statements)

References 107 publications

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“…These can serve as substrates for Dicer to generate virus‐derived siRNAs (viRNAs) (Ding & Voinnet, 2007; Kemp & Imler, 2009; Swarts et al , 2014; tenOever, 2016) that are loaded onto RISC and target complementary viral RNA to block virus replication. Indeed, viRNA‐mediated RNAi constitutes the primary antiviral defence strategy of plants and invertebrates (Ding & Voinnet, 2007; Kemp & Imler, 2009; Swarts et al , 2014; tenOever, 2016). Consequently, plant and insect viruses have evolved virulence factors called viral suppressors of RNA silencing (VSRs) that block various steps of the antiviral RNAi mechanism (Haasnoot et al , 2007; Wu et al , 2010).…”

Section: Introductionmentioning

confidence: 99%

Inactivation of the type I interferon pathway reveals long double‐stranded RNA‐mediated RNA interference in mammalian cells

et al. 2016

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RNA interference (RNAi) elicited by long double‐stranded (ds) or base‐paired viral RNA constitutes the major mechanism of antiviral defence in plants and invertebrates. In contrast, it is controversial whether it acts in chordates. Rather, in vertebrates, viral RNAs induce a distinct defence system known as the interferon (IFN) response. Here, we tested the possibility that the IFN response masks or inhibits antiviral RNAi in mammalian cells. Consistent with that notion, we find that sequence‐specific gene silencing can be triggered by long dsRNAs in differentiated mouse cells rendered deficient in components of the IFN pathway. This unveiled response is dependent on the canonical RNAi machinery and is lost upon treatment of IFN‐responsive cells with type I IFN. Notably, transfection with long dsRNA specifically vaccinates IFN‐deficient cells against infection with viruses bearing a homologous sequence. Thus, our data reveal that RNAi constitutes an ancient antiviral strategy conserved from plants to mammals that precedes but has not been superseded by vertebrate evolution of the IFN system.

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Section: Introductionmentioning

confidence: 99%

Inactivation of the type I interferon pathway reveals long double‐stranded RNA‐mediated RNA interference in mammalian cells

et al. 2016

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“…Molecular structures of a eukaryotic Argonaute MID domain and an Archaeoglobus fulgidus Piwi (AfPiwi) enzyme bound to a guide RNA showed the importance of the 5′-terminal base identity, as well as the 5′ phosphate in guide strand binding, to Ago (10,(13)(14)(15)(16)(17). Notably, recognition of the 5′ end of the guide in the MID domain and guide strand preorganization for target interaction are conserved across the entire Argonaute superfamily (1).…”

mentioning

confidence: 99%

“…Members of this protein family are present in all three domains of life (1). In eukaryotes, Argonautes are the key effectors of RNA interference (RNAi) pathways that regulate posttranscriptional gene expression (2)(3)(4).…”

mentioning

confidence: 99%

A bacterial Argonaute with noncanonical guide RNA specificity

Kaya

Doxzen

Knoll

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

127

218

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Eukaryotic Argonaute proteins induce gene silencing by small RNAguided recognition and cleavage of mRNA targets. Although structural similarities between human and prokaryotic Argonautes are consistent with shared mechanistic properties, sequence and structure-based alignments suggested that Argonautes encoded within CRISPR-cas [clustered regularly interspaced short palindromic repeats (CRISPR)-associated] bacterial immunity operons have divergent activities. We show here that the CRISPR-associated Marinitoga piezophila Argonaute (MpAgo) protein cleaves single-stranded target sequences using 5′-hydroxylated guide RNAs rather than the 5′-phosphorylated guides used by all known Argonautes. The 2.0-Å resolution crystal structure of an MpAgo-RNA complex reveals a guide strand binding site comprising residues that block 5′ phosphate interactions. Using structure-based sequence alignment, we were able to identify other putative MpAgo-like proteins, all of which are encoded within CRISPRcas loci. Taken together, our data suggest the evolution of an Argonaute subclass with noncanonical specificity for a 5′-hydroxylated guide.Argonaute | small noncoding RNA | RNA interference A rgonaute (Ago) proteins bind small RNA or DNA guides, which provide base-pairing specificity for recognition and cleavage of complementary nucleic acid targets. Members of this protein family are present in all three domains of life (1). In eukaryotes, Argonautes are the key effectors of RNA interference (RNAi) pathways that regulate posttranscriptional gene expression (2-4). However, the role of Argonaute proteins in bacteria and archaea, which lack RNAi pathways, remains poorly understood (5).Recent studies suggested that DNA-guided bacterial and archaeal Argonaute proteins are directly involved in host defense by cleaving foreign DNA elements, such as DNA viruses and plasmids (6, 7). In addition, a catalytically inactive Argonaute protein in Rhodobacter sphaeroides (RsAgo) was demonstrated to use RNA guides and possibly recruits an associated nuclease for subsequent target cleavage (8). Despite these divergent modes of action, bacterial and archaeal Argonaute proteins adopt a highly conserved bilobed architecture. Herein, an N-terminal and a PIWI-ArgonauteZwille (PAZ) domain constitute one lobe, whereas the other lobe consists of the middle (MID) domain and the catalytic RNase H-like P element-induced wimpy testis (PIWI) domain (9-15). Molecular structures of a eukaryotic Argonaute MID domain and an Archaeoglobus fulgidus Piwi (AfPiwi) enzyme bound to a guide RNA showed the importance of the 5′-terminal base identity, as well as the 5′ phosphate in guide strand binding, to Ago (10,[13][14][15][16][17]. Notably, recognition of the 5′ end of the guide in the MID domain and guide strand preorganization for target interaction are conserved across the entire Argonaute superfamily (1).The nucleic acid-guided binding and cleavage activities of Argonaute proteins are reminiscent of the activities of RNA-guided proteins within CRISPR-Cas systems [cluste...

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“…Prokaryotes possess a system of innate immunity centered around the Argonaute proteins that appears to be the evolutionary antecedent of eukaryotic RNAi (7,11,12) as well as CRISPR-Cas systems of adaptive immunity (13)(14)(15). The CRISPR-Cas systems provide guide RNA-based defense against viruses and other MGE in nearly all archaea and about one third of bacteria (16).…”

mentioning

confidence: 99%

Recruitment of CRISPR-Cas systems by Tn7-like transposons

Peters

Makarova

Shmakov

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

214

246

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A survey of bacterial and archaeal genomes shows that many Tn7-like transposons contain minimal type I-F CRISPR-Cas systems that consist of fused cas8f and cas5f, cas7f, and cas6f genes and a short CRISPR array. Several small groups of Tn7-like transposons encompass similarly truncated type I-B CRISPR-Cas. This minimal gene complement of the transposon-associated CRISPR-Cas systems implies that they are competent for pre-CRISPR RNA (precrRNA) processing yielding mature crRNAs and target binding but not target cleavage that is required for interference. Phylogenetic analysis demonstrates that evolution of the CRISPR-Cas-containing transposons included a single, ancestral capture of a type I-F locus and two independent instances of type I-B loci capture. We show that the transposon-associated CRISPR arrays contain spacers homologous to plasmid and temperate phage sequences and, in some cases, chromosomal sequences adjacent to the transposon. We hypothesize that the transposon-encoded CRISPR-Cas systems generate displacement (R-loops) in the cognate DNA sites, targeting the transposon to these sites and thus facilitating their spread via plasmids and phages. These findings suggest the existence of RNAguided transposition and fit the guns-for-hire concept whereby mobile genetic elements capture host defense systems and repurpose them for different stages in the life cycle of the element.CRISPR-Cas systems | Tn7 transposon | transposition strategy | crRNA guide | target-site selection

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The evolutionary journey of Argonaute proteins

Cited by 409 publications

References 107 publications

Inactivation of the type I interferon pathway reveals long double‐stranded RNA‐mediated RNA interference in mammalian cells

Inactivation of the type I interferon pathway reveals long double‐stranded RNA‐mediated RNA interference in mammalian cells

A bacterial Argonaute with noncanonical guide RNA specificity

Recruitment of CRISPR-Cas systems by Tn7-like transposons

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