The dynamic interplay of host and viral enzymes in type III CRISPR-mediated cyclic nucleotide signalling

Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic oligoadenylate (cOA) upon detecting foreign RNA, activating ancillary nucleases that can be toxic to cells, necessitating mechanisms to remove cOA in s...

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Published ineLife Vol. 9
Main Authors Athukoralage, Januka S, Graham, Shirley, Rouillon, Christophe, Grüschow, Sabine, Czekster, Clarissa M, White, Malcolm F
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 27.04.2020
eLife Sciences Publications, Ltd
Subjects
Antiviral agents
Biochemistry and Chemical Biology
Chromatography
CRISPR
CRISPR-Cas Systems
cyclic oligoadenylate
Enzymes
Escherichia coli - enzymology
Escherichia coli - genetics
Host Microbial Interactions
Immune system
Nuclease
Nucleotides, Cyclic - metabolism
Research Advance
Ribonuclease
Ribonucleic acid
ring nuclease
RNA
Second messengers
Signal Transduction
Sulfolobus solfataricus
Sulfolobus solfataricus - genetics
Sulfolobus solfataricus - metabolism
Viruses
Viruses - enzymology
Viruses - genetics
CRISPR
chemical biology
biochemistry
Sulfolobus solfataricus
cyclic oligoadenylate
E. coli
ring nuclease
ribonuclease
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Abstract Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic oligoadenylate (cOA) upon detecting foreign RNA, activating ancillary nucleases that can be toxic to cells, necessitating mechanisms to remove cOA in systems that operate via immunity rather than abortive infection. Previously, we demonstrated that the type III-D CRISPR complex generates cyclic tetra-adenylate (cA ), activating the ribonuclease Csx1, and showed that subsequent RNA cleavage and dissociation acts as an 'off-switch' for the cyclase activity. Subsequently, we identified the cellular ring nuclease Crn1, which slowly degrades cA to reset the system (Rouillon et al., 2018), and demonstrated that viruses can subvert type III CRISPR immunity by means of a potent anti-CRISPR ring nuclease variant AcrIII-1. Here, we present a comprehensive analysis of the dynamic interplay between these enzymes, governing cyclic nucleotide levels and infection outcomes in virus-host conflict.
AbstractList Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic oligoadenylate (cOA) upon detecting foreign RNA, activating ancillary nucleases that can be toxic to cells, necessitating mechanisms to remove cOA in systems that operate via immunity rather than abortive infection. Previously, we demonstrated that the Sulfolobus solfataricus type III-D CRISPR complex generates cyclic tetra-adenylate (cA4), activating the ribonuclease Csx1, and showed that subsequent RNA cleavage and dissociation acts as an ‘off-switch’ for the cyclase activity. Subsequently, we identified the cellular ring nuclease Crn1, which slowly degrades cA4 to reset the system (Rouillon et al., 2018), and demonstrated that viruses can subvert type III CRISPR immunity by means of a potent anti-CRISPR ring nuclease variant AcrIII-1. Here, we present a comprehensive analysis of the dynamic interplay between these enzymes, governing cyclic nucleotide levels and infection outcomes in virus-host conflict.
Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic oligoadenylate (cOA) upon detecting foreign RNA, activating ancillary nucleases that can be toxic to cells, necessitating mechanisms to remove cOA in systems that operate via immunity rather than abortive infection. Previously, we demonstrated that the type III-D CRISPR complex generates cyclic tetra-adenylate (cA ), activating the ribonuclease Csx1, and showed that subsequent RNA cleavage and dissociation acts as an 'off-switch' for the cyclase activity. Subsequently, we identified the cellular ring nuclease Crn1, which slowly degrades cA to reset the system (Rouillon et al., 2018), and demonstrated that viruses can subvert type III CRISPR immunity by means of a potent anti-CRISPR ring nuclease variant AcrIII-1. Here, we present a comprehensive analysis of the dynamic interplay between these enzymes, governing cyclic nucleotide levels and infection outcomes in virus-host conflict.
Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic oligoadenylate (cOA) upon detecting foreign RNA, activating ancillary nucleases that can be toxic to cells, necessitating mechanisms to remove cOA in systems that operate via immunity rather than abortive infection. Previously, we demonstrated that the Sulfolobus solfataricus type III-D CRISPR complex generates cyclic tetra-adenylate (cA 4 ), activating the ribonuclease Csx1, and showed that subsequent RNA cleavage and dissociation acts as an ‘off-switch’ for the cyclase activity. Subsequently, we identified the cellular ring nuclease Crn1, which slowly degrades cA 4 to reset the system (Rouillon et al., 2018), and demonstrated that viruses can subvert type III CRISPR immunity by means of a potent anti-CRISPR ring nuclease variant AcrIII-1. Here, we present a comprehensive analysis of the dynamic interplay between these enzymes, governing cyclic nucleotide levels and infection outcomes in virus-host conflict.
Author White, Malcolm F
Rouillon, Christophe
Grüschow, Sabine
Czekster, Clarissa M
Athukoralage, Januka S
Graham, Shirley
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  givenname: Christophe
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  fullname: Grüschow, Sabine
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  surname: White
  fullname: White, Malcolm F
  organization: Biomedical Sciences Research Complex, School of Biology, University of St Andrews, St Andrews, United Kingdom
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32338598$$D View this record in MEDLINE/PubMed
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Keywords CRISPR
chemical biology
biochemistry
Sulfolobus solfataricus
cyclic oligoadenylate
E. coli
ring nuclease
ribonuclease
Language English
License 2020, Athukoralage et al.
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Snippet Cyclic nucleotide second messengers are increasingly implicated in prokaryotic anti-viral defence systems. Type III CRISPR systems synthesise cyclic...
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SubjectTerms Antiviral agents
Biochemistry and Chemical Biology
Chromatography
CRISPR
CRISPR-Cas Systems
cyclic oligoadenylate
Enzymes
Escherichia coli - enzymology
Escherichia coli - genetics
Host Microbial Interactions
Immune system
Nuclease
Nucleotides, Cyclic - metabolism
Research Advance
Ribonuclease
Ribonucleic acid
ring nuclease
RNA
Second messengers
Signal Transduction
Sulfolobus solfataricus
Sulfolobus solfataricus - genetics
Sulfolobus solfataricus - metabolism
Viruses
Viruses - enzymology
Viruses - genetics
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Title The dynamic interplay of host and viral enzymes in type III CRISPR-mediated cyclic nucleotide signalling
URI https://www.ncbi.nlm.nih.gov/pubmed/32338598
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Volume 9
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