Recognition of phylogenetically diverse pathogens through enzymatically amplified recruitment of RNF213

Innate immunity senses microbial ligands known as pathogen-associated molecular patterns (PAMPs). Except for nucleic acids, PAMPs are exceedingly taxa-specific, thus enabling pattern recognition receptors to detect cognate pathogens while ignoring others. How the E3 ubiquitin ligase RNF213 can respond to phylogenetically distant pathogens, including Gram-negative Salmonella, Gram-positive Listeria, and eukaryotic Toxoplasma, remains unknown. Here we report that the evolutionary history of RNF213 is indicative of repeated adaptation to diverse pathogen target structures, especially in and around its newly identified CBM20 carbohydrate-binding domain, which we have resolved by cryo-EM. We find that RNF213 forms coats on phylogenetically distant pathogens. ATP hydrolysis by RNF213's dynein-like domain is essential for coat formation on all three pathogens studied as is RZ finger-mediated E3 ligase activity for bacteria. Coat formation is not diffusion-limited but instead relies on rate-limiting initiation events and subsequent cooperative incorporation of further RNF213 molecules. We conclude that RNF213 responds to evolutionarily distant pathogens through enzymatically amplified cooperative recruitment.

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Publication Details

Journal
EMBO Reports
Published
2024-10-07
DOI
https://doi.org/10.1038/s44319-024-00280-w
Citations
11
Primary Topic
Cytomegalovirus and herpesvirus research
Type
article
Field-Weighted Citation Impact
4.25

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article

Recognition of phylogenetically diverse pathogens through enzymatically amplified recruitment of RNF213

Vimisha Dharamdasani, Felix Randow, Keith B. Boyle, Ana Crespillo-Casado et al.
11 citations
EMBO Reports
Cytomegalovirus and herpesvirus research
4.25
article

Recognition of phylogenetically diverse pathogens through enzymatically amplified recruitment of RNF213

Vimisha Dharamdasani, Felix Randow, Keith B. Boyle, Ana Crespillo-Casado, Elsje G. Otten, Harmit Singh Malik, Pierre‐Mehdi Hammoudi, Prathyush Pothukuchi, Janet M. Young, Matthew C. J. Yip, Jérôme Boulanger, Mayuri Gogoi, Katerina Naydenova, Ceara M. Harper
article en
11 citations

Abstract

Innate immunity senses microbial ligands known as pathogen-associated molecular patterns (PAMPs). Except for nucleic acids, PAMPs are exceedingly taxa-specific, thus enabling pattern recognition receptors to detect cognate pathogens while ignoring others. How the E3 ubiquitin ligase RNF213 can respond to phylogenetically distant pathogens, including Gram-negative Salmonella, Gram-positive Listeria, and eukaryotic Toxoplasma, remains unknown. Here we report that the evolutionary history of RNF213 is indicative of repeated adaptation to diverse pathogen target structures, especially in and around its newly identified CBM20 carbohydrate-binding domain, which we have resolved by cryo-EM. We find that RNF213 forms coats on phylogenetically distant pathogens. ATP hydrolysis by RNF213's dynein-like domain is essential for coat formation on all three pathogens studied as is RZ finger-mediated E3 ligase activity for bacteria. Coat formation is not diffusion-limited but instead relies on rate-limiting initiation events and subsequent cooperative incorporation of further RNF213 molecules. We conclude that RNF213 responds to evolutionarily distant pathogens through enzymatically amplified cooperative recruitment.

EMBO ReportsVol. 25(11)
Howard Hughes Medical Institute (US), MRC Laboratory of Molecular Biology (GB), University of Cambridge (GB), Fred Hutch Cancer Center (US), Addenbrooke's Hospital (GB)
Howard Hughes Medical Institute, Wellcome Trust, Diamond Light Source, UK Research and Innovation, National Institutes of Health
Openalex Percentile: Top 5%
Cytomegalovirus and herpesvirus research
4.25
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