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Structure of the zinc-finger antiviral protein in complex with RNA reveals a mechanism for selective targeting of CG-rich viral sequences
Thursday, 2019/11/28 | 08:12:11

Jennifer L. Meagher, Matthew Takata, Daniel Gonçalves-Carneiro, Sarah C. Keane, Antoine Rebendenne, Heley Ong, Victoria K. Orr, Margaret R. MacDonald, Jeanne A. Stuckey, Paul D. Bieniasz, and Janet L. Smith

PNAS November 26, 2019 116 (48) 24303-24309

Significance

Zinc finger antiviral protein (ZAP) protects cells from infection by diverse RNA viruses through its ability to specifically detect and deplete viral RNAs that have a greater frequency of CG dinucleotides than host messenger RNAs. We solved an X-ray crystal structure of the domain of ZAP that recognizes RNA and found that a crucial component of RNA recognition by ZAP is a pocket on the protein surface that can accommodate a CG dinucleotide but no other dinucleotides. The structure explains in atomic detail how ZAP is able to selectively recognize CG-rich viral RNAs as foreign and thereby provide hosts with a defense against viral infection.

Abstract

Infection of animal cells by numerous viruses is detected and countered by a variety of means, including recognition of nonself nucleic acids. The zinc finger antiviral protein (ZAP) depletes cytoplasmic RNA that is recognized as foreign in mammalian cells by virtue of its elevated CG dinucleotide content compared with endogenous mRNAs. Here, we determined a crystal structure of a protein-RNA complex containing the N-terminal, 4-zinc finger human (h) ZAP RNA-binding domain (RBD) and a CG dinucleotide-containing RNA target. The structure reveals in molecular detail how hZAP is able to bind selectively to CG-rich RNA. Specifically, the 4 zinc fingers create a basic patch on the hZAP RBD surface. The highly basic second zinc finger contains a pocket that selectively accommodates CG dinucleotide bases. Structure guided mutagenesis, cross-linking immunoprecipitation sequencing assays, and RNA affinity assays show that the structurally defined CG-binding pocket is not required for RNA binding per se in human cells. However, the pocket is a crucial determinant of high-affinity, specific binding to CG dinucleotide-containing RNA. Moreover, variations in RNA-binding specificity among a panel of CG-binding pocket mutants quantitatively predict their selective antiviral activity against a CG-enriched HIV-1 strain. Overall, the hZAP RBD RNA structure provides an atomic-level explanation for how ZAP selectively targets foreign, CG-rich RNA.

 

See https://www.pnas.org/content/116/48/24303

Figure 1: hZAP RBD with bound RNA. (A) Schematic of hZAP showing the ZAP-L and ZAP-S isoforms and the positions of the Zn fingers in the RBD. (B) Structure of the hZAP RBD RNA complex. The 4 Zn fingers (ZnF) are colored separately (green, ZnF1; yellow, ZnF2; blue, ZnF3; cyan, ZnF4) in these views from the side (Left) and top (Right) of the hZAP RBD. The RNA CG dinucleotide binds to ZnF2. The UCG trinucleotide and the Zn ligands are shown in stick form with atomic colors (gray, C; red, O; blue, N; orange, P; yellow, S), and the Zn atoms are shown as gray spheres.

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