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Dynamic monomer-dimer transition regulates DNA-guided RNA cleavage by MbpAgo.

Xiaolong Zhao1, Wen Yang1, Linfeng An1

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Mucilaginibacter paludis Argonaute (MbpAgo) uses guide DNA to cleave target RNA. Structural studies reveal a dynamic monomer-dimer transition regulates MbpAgo activity, enabling programmable RNA targeting.

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Area of Science:

  • Biochemistry
  • Structural Biology
  • Molecular Biology

Background:

  • Prokaryotic Argonaute proteins (pAgos) are versatile nucleic acid-guided endonucleases.
  • Mucilaginibacter paludis Argonaute (MbpAgo) uniquely utilizes guide DNA (gDNA) for target RNA (tgRNA) cleavage, but its structural basis was unknown.

Purpose of the Study:

  • To elucidate the structural mechanisms underlying MbpAgo's unique DNA-guided RNA cleavage activity.
  • To investigate the role of protein structure in MbpAgo's regulation and function.

Main Methods:

  • Cryo-electron microscopy (cryo-EM) was used to determine MbpAgo structures in apo, binary (bound to gDNA), and ternary (bound to gDNA and tgRNA) states.
  • High-resolution structures (up to 2.55 Å) were obtained to analyze conformational changes and interactions.

Main Results:

  • The apo MbpAgo structure shows a conserved scaffold with unique domain insertions stabilizing its catalytic state.
  • gDNA binding induces MbpAgo dimerization, stabilized by protein-protein interfaces and auxiliary nucleic acid interactions, crucial for double-stranded DNA (dsDNA) guides.
  • tgRNA binding destabilizes the dimer, reverting MbpAgo to an active monomer capable of cleaving structured viral RNAs (e.g., SARS-CoV-2 5'UTR, HIV-1 CES).

Conclusions:

  • MbpAgo activity is regulated by a dynamic monomer-dimer transition.
  • This transition is an adaptation for processing dsDNA-derived guides and enables programmable RNA targeting.
  • The study provides a structural framework for understanding and engineering MbpAgo for RNA manipulation.