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TitleOligomerization-mediated activation of a short prokaryotic Argonaute.
Journal, issue, pagesNature, Vol. 621, Issue 7977, Page 154-161, Year 2023
Publish dateJul 26, 2023
AuthorsZhangfei Shen / Xiao-Yuan Yang / Shiyu Xia / Wei Huang / Derek J Taylor / Kotaro Nakanishi / Tian-Min Fu /
PubMed AbstractAlthough eukaryotic and long prokaryotic Argonaute proteins (pAgos) cleave nucleic acids, some short pAgos lack nuclease activity and hydrolyse NAD(P) to induce bacterial cell death. Here we present ...Although eukaryotic and long prokaryotic Argonaute proteins (pAgos) cleave nucleic acids, some short pAgos lack nuclease activity and hydrolyse NAD(P) to induce bacterial cell death. Here we present a hierarchical activation pathway for SPARTA, a short pAgo consisting of an Argonaute (Ago) protein and TIR-APAZ, an associated protein. SPARTA progresses through distinct oligomeric forms, including a monomeric apo state, a monomeric RNA-DNA-bound state, two dimeric RNA-DNA-bound states and a tetrameric RNA-DNA-bound active state. These snapshots together identify oligomerization as a mechanistic principle of SPARTA activation. The RNA-DNA-binding channel of apo inactive SPARTA is occupied by an auto-inhibitory motif in TIR-APAZ. After the binding of RNA-DNA, SPARTA transitions from a monomer to a symmetric dimer and then an asymmetric dimer, in which two TIR domains interact through charge and shape complementarity. Next, two dimers assemble into a tetramer with a central TIR cluster responsible for hydrolysing NAD(P). In addition, we observe unique features of interactions between SPARTA and RNA-DNA, including competition between the DNA 3' end and the auto-inhibitory motif, interactions between the RNA G2 nucleotide and Ago, and splaying of the RNA-DNA duplex by two loops exclusive to short pAgos. Together, our findings provide a mechanistic basis for the activation of short pAgos, a large section of the Ago superfamily.
External linksNature / PubMed:37494956 / PubMed Central
MethodsEM (single particle)
Resolution2.48 - 3.52 Å
Structure data

EMDB-29033, PDB-8fex:
Inactivate state of Maribacter polysiphoniae Argonuate (short pAgo system)
Method: EM (single particle) / Resolution: 3.07 Å

EMDB-29043, PDB-8ffi:
Structure of tetramerized MapSPARTA upon guide RNA-mediated target DNA binding
Method: EM (single particle) / Resolution: 2.7 Å

EMDB-29219: Raw map for structure of tetramerized short MapSPARTA (short prokaryotic Agronuate) system upon guide RNA-mediated target ssDNA binding
Method: EM (single particle) / Resolution: 2.79 Å

EMDB-29222: Focused refined map of TIR domain for MapSPARTA
Method: EM (single particle) / Resolution: 2.48 Å

EMDB-29223: Focused map for corner area4 of MapSPARTA
Method: EM (single particle) / Resolution: 2.71 Å

EMDB-29224: Local refined map of corner area 3 for the MapSPARTA
Method: EM (single particle) / Resolution: 2.74 Å

EMDB-29225: Focused refinement of corner area2 for MapSPARTA
Method: EM (single particle) / Resolution: 2.64 Å

EMDB-29226: Focused refinement for corner area1 of MapSPARTA
Method: EM (single particle) / Resolution: 2.74 Å

EMDB-40672, PDB-8sp0:
Symmetric dimer of MapSPARTA bound with gRNA/tDNA hybrid
Method: EM (single particle) / Resolution: 3.33 Å

EMDB-40673, PDB-8sp3:
Asymmetric dimer of MapSPARTA bound with gRNA/tDNA hybrid
Method: EM (single particle) / Resolution: 3.52 Å

EMDB-40679: Incomplete map of Maribacter polysiphoniae Argonaute (MapSPARTA) bound with guide RNA and target DNA duplex.
Method: EM (single particle) / Resolution: 3.04 Å

EMDB-40680, PDB-8spo:
Tetramerized activation of MapSPARTA bound with NAD+
Method: EM (single particle) / Resolution: 2.98 Å

EMDB-40713, PDB-8squ:
Monomeric MapSPARTA bound with guide RNA and target DNA hybrid
Method: EM (single particle) / Resolution: 3.28 Å

Chemicals

ChemComp-MG:
Unknown entry

ChemComp-NAD:
NICOTINAMIDE-ADENINE-DINUCLEOTIDE / NAD*YM

Source
  • maribacter polysiphoniae (bacteria)
  • synthetic construct (others)
KeywordsIMMUNE SYSTEM / Argonuate / TIR domain / Oligomerization / NAD+ / pAgo / SPARTA / Argonuare / NAD / Argonaute / TIR / bacterial Immume system / Short prokaryotic argonaute / NADase activity / Bacterial immune system / MapSPARTA / Short pAgo / Prokaryotic Argonaute / gRNA mediated DNA binding / Microbiology / microbic immune system

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