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Inhibition of translation by IFIT family members is determined by their ability to interact selectively with the 5′-terminal regions of cap0-, cap1- and 5’ppp- mRNAs

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Kumar, Parimal, Sweeney, Trevor R., Skabkin, Maxim A., Skabkina, Olga V., Hellen, Christopher U. T., Pestova, Tatyana V.·2014·Nucleic Acids Research
DOI 10.1093/nar/gkt1321PMC PMC3950709
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Abstract

Ribosomal recruitment of cellular mRNAs depends on binding of eIF4F to the mRNA’s 5′-terminal ‘cap’. The minimal ‘cap0’ consists of N7-methylguanosine linked to the first nucleotide via a 5′-5′ triphosphate (ppp) bridge. Cap0 is further modified by 2′-O-methylation of the next two riboses, yielding ‘cap1’ (m7GpppNmN) and ‘cap2’ (m7GpppNmNm). However, some viral RNAs lack 2′-O-methylation, whereas others contain only ppp- at their 5′-end. Interferon-induced proteins with tetratricopeptide repeats (IFITs) are highly expressed effectors of innate immunity that inhibit viral replication by incompletely understood mechanisms. Here, we investigated the ability of IFIT family members to interact with cap1-, cap0- and 5′ppp- mRNAs and inhibit their translation. IFIT1 and IFIT1B showed very high affinity to cap-proximal regions of cap0-mRNAs (K1/2,app ∼9 to 23 nM). The 2′-O-methylation abrogated IFIT1/mRNA interaction, whereas IFIT1B retained the ability to bind cap1-mRNA, albeit with reduced affinity (K1/2,app ∼450 nM). The 5′-terminal regions of 5′ppp-mRNAs were recognized by IFIT5 (K1/2,app ∼400 nM). The activity of individual IFITs in inhibiting initiation on a specific mRNA was determined by their ability to interact with its 5′-terminal region: IFIT1 and IFIT1B efficiently outcompeted eIF4F and abrogated initiation on cap0-mRNAs, whereas inhibition on cap1- and 5′ppp- mRNAs by IFIT1B and IFIT5 was weaker and required higher protein concentrations.

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Authors
Kumar, P., Sweeney, T. R., Skabkin, M. A., Skabkina, O. V., Hellen, C. U. T., & Pestova, T. V.
Affiliations
SUNY Downstate Health Sciences University (US)
Corresponding author
  • Hellen, Christopher U. T.
  • Pestova, Tatyana V.
ORCID
Venue
Nucleic Acids Research
Publisher
Oxford University Press (OUP)
Published
2013-12-25
Volume
42
Issue
5
Pages
3228-3245
ISSN
  • 0305-1048 (ISSN-L)
  • 1362-4962
DOI
10.1093/nar/gkt1321
PMC
PMC3950709
OpenAlex
W2058492139
Cited by
210
References
1
Citations by year
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FWCI
4.66
Type
journal article
Language
en
Open access
Licence
Locations
  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by-nc)
  • Apollo
Funders
  • National Institutes of Health
  • National Institute of General Medical Sciences (GM59660, R01GM059660)
  • National Institute of Allergy and Infectious Diseases (AI51340, R56AI051340)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
Keywords
IFIT1, IFIT5, mRNA cap, 2'-O-methylation, eIF4F, translation initiation inhibition, ribosome recruitment, innate immunity, antiviral innate immunity, mRNA-protein interactions
MeSH terms
Binding, Competitive, Carrier Proteins, Neoplasm Proteins, Peptide Chain Initiation, Translational, Proteins, Recombinant Proteins, Ribosomes, RNA Caps, RNA, Transfer, RNA-Binding Proteins, Eukaryotic Initiation Factor-4E, Eukaryotic Initiation Factor-4F, Intracellular Signaling Peptides and Proteins, Adaptor Proteins, Signal Transducing, Apoptosis Regulatory Proteins

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