Global shape mimicry of tRNA within a viral internal ribosome entry site mediates translational reading frame selection

Au, Hilda H.; Cornilescu, Gabriel; Mouzakis, Kathryn D.; Ren, Qian; Burke, Jordan E.; Lee, Seonghoon; Butcher, Samuel E.; Jan, Eric

doi:10.1073/pnas.1512088112

Title: Global shape mimicry of tRNA within a viral internal ribosome entry site mediates translational reading frame selection

Journal Article · Mon Nov 09 00:00:00 EST 2015 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1512088112· OSTI ID:1236267

Au, Hilda H. ^[1]; Cornilescu, Gabriel ^[2]; Mouzakis, Kathryn D. ^[2]; Ren, Qian ^[1]; Burke, Jordan E. ^[2]; Lee, Seonghoon ^[1]; Butcher, Samuel E. ^[2]; Jan, Eric ^[1]

Univ. of British Columbia, Vancouver, BC (Canada)
Univ. of Wisconsin, Madison, WI (United States)

The dicistrovirus intergenic region internal ribosome entry site (IRES) adopts a triple-pseudoknotted RNA structure and occupies the core ribosomal E, P, and A sites to directly recruit the ribosome and initiate translation at a non-AUG codon. A subset of dicistrovirus IRESs directs translation in the 0 and +1 frames to produce the viral structural proteins and a +1 overlapping open reading frame called ORFx, respectively. Here we show that specific mutations of two unpaired adenosines located at the core of the three-helical junction of the honey bee dicistrovirusIsraeli acute paralysis virus(IAPV) IRES PKI domain can uncouple 0 and +1 frame translation, suggesting that the structure adopts distinct conformations that contribute to 0 or +1 frame translation. Using a reconstituted translation system, we show that ribosomes assembled on mutant IRESs that direct exclusive 0 or +1 frame translation lack reading frame fidelity. Finally, a nuclear magnetic resonance/small-angle X-ray scattering hybrid approach reveals that the PKI domain of the IAPV IRES adopts an RNA structure that resembles a complete tRNA. Here, the tRNA shape-mimicry enables the viral IRES to gain access to the ribosome tRNA-binding sites and form intermolecular contacts with the ribosome that are necessary for initiating IRES translation in a specific reading frame.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Canadian Institutes of Health Research; Natural Science and Engineering Resources Council Discovery; National Institutes of Health (NIH); USDOE

Grant/Contract Number:: MOP-81244; RGPIN 341459-12; DMB-8415048; OIA-9977486; S10RR027000; BIR-9214394; GM072447; P41GM103399; S10RR02781; S10RR08438; S10RR023438; S10RR025062; S10RR029220

OSTI ID:: 1236267

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 47; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 20 works

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59 BASIC BIOLOGICAL SCIENCES
translation
virus
RNA
ribosome
internal ribosome entry site

Title: Global shape mimicry of tRNA within a viral internal ribosome entry site mediates translational reading frame selection

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