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Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway

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  • Ashton Trey Belew

    (University of Maryland, College Park)

  • Arturas Meskauskas

    (University of Maryland, College Park
    Vilnius University)

  • Sharmishtha Musalgaonkar

    (University of Maryland, College Park)

  • Vivek M. Advani

    (University of Maryland, College Park)

  • Sergey O. Sulima

    (University of Maryland, College Park
    Present address: VIB Center for the Biology of Disease, KU Leuven, Campus Gasthuisberg, Herestraat 49, bus 602, 3000 Leuven, Belgium.)

  • Wojciech K. Kasprzak

    (Basic Science Program, Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Bruce A. Shapiro

    (Basic Research Laboratory, National Cancer Institute)

  • Jonathan D. Dinman

    (University of Maryland, College Park)

Abstract

Programmed −1 ribosomal frameshift (−1 PRF) signals redirect translating ribosomes to slip back one base on messenger RNAs. Although well characterized in viruses, how these elements may regulate cellular gene expression is not understood. Here we describe a −1 PRF signal in the human mRNA encoding CCR5, the HIV-1 co-receptor. CCR5 mRNA-mediated −1 PRF is directed by an mRNA pseudoknot, and is stimulated by at least two microRNAs. Mapping the mRNA–miRNA interaction suggests that formation of a triplex RNA structure stimulates −1 PRF. A −1 PRF event on the CCR5 mRNA directs translating ribosomes to a premature termination codon, destabilizing it through the nonsense-mediated mRNA decay pathway. At least one additional mRNA decay pathway is also involved. Functional −1 PRF signals that seem to be regulated by miRNAs are also demonstrated in mRNAs encoding six other cytokine receptors, suggesting a novel mode through which immune responses may be fine-tuned in mammalian cells.

Suggested Citation

  • Ashton Trey Belew & Arturas Meskauskas & Sharmishtha Musalgaonkar & Vivek M. Advani & Sergey O. Sulima & Wojciech K. Kasprzak & Bruce A. Shapiro & Jonathan D. Dinman, 2014. "Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway," Nature, Nature, vol. 512(7514), pages 265-269, August.
    • Handle: RePEc:nat:nature:v:512:y:2014:i:7514:d:10.1038_nature13429
    DOI: 10.1038/nature13429
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    Cited by:

    1. Matthias M. Zimmer & Anuja Kibe & Ulfert Rand & Lukas Pekarek & Liqing Ye & Stefan Buck & Redmond P. Smyth & Luka Cicin-Sain & Neva Caliskan, 2021. "The short isoform of the host antiviral protein ZAP acts as an inhibitor of SARS-CoV-2 programmed ribosomal frameshifting," Nature Communications, Nature, vol. 12(1), pages 1-15, December.

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