Position of the kissing-loop interaction associated with PTE-type 3′CITEs can affect enhancement of cap-independent translation

Chattopadhyay, Maitreyi; Kuhlmann, Micki M.; kumar, K. Mahesh; Simon, Anne

doi:10.1016/j.virol.2014.03.027

Cited by 13 publications

(34 citation statements)

References 33 publications

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“…The 3′ location of translation elements would also enable tombusvirid and luteovirid gRNA and any 3′ co-terminal sgRNA to share the same 3′CITE-dependent translation mechanism. For that reason, the few reports that include translation of sgRNAs mainly emphasize the presence and location of any 5′/3′ interacting sequences (Chattopadhyay et al , 2014; Fabian and White, 2004; Shen et al , 2006) and not possible differences between translation requirements of gRNA and sgRNA templates.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, the distance from the base of sgH1 to AUG 26 (45 nt) is similar to the distance from the base of 5H2 (the gRNA hairpin that interacts with the kl-TSS) to the p33 initiation codon (36 nt). Location of hairpins involved in long-distance interactions in the coding region of gRNA and sgRNA can also be found for some carmoviruses (Chattopadhyay et al , 2014; Chattopadhyay et al , 2011; Simon and Miller, 2013), which differs from tombusviruses, luteoviruses and necroviruses where the interacting sequence is in their longer 5′UTRs (Simon and Miller, 2013). The location of the interacting hairpin either upstream or downstream of the initiation codon may not be consequential as ribosomes are apparently recruited to the 5′ end followed by scanning to the appropriate initiation codon (Guo et al , 2001; Rakotondrafara et al , 2006; Sarawaneeyaruk et al , 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Recruited translation elements are usually delivered to the 5′ end of the gRNA via a long-distance RNA:RNA interaction between the terminal loop of a hairpin associated with the 3′CITE and accessible sequences in the 5′UTR or nearby coding region (Chattopadhyay et al , 2011; Fabian and White, 2004, 2006; Gao et al , 2012; Nicholson and White, 2008; Nicholson et al , 2010; Simon and Miller, 2013; Wu et al , 2009). 3′CITEs are also assumed to enhance translation of any 3′ co-terminal sgRNAs, and complementary sequences allowing for long-distance interactions between sgRNA 5′ regions and 3′CITE hairpins have been predicted and in a few cases validated (Chattopadhyay et al , 2014). However, sgRNA sequences suggested as potential pairing partners for the BTE of Tobacco necrosis virus D are not required for efficient translation of viral proteins in vitro (Chkuaseli et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

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Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

Gao

Simon

2017

Virology

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The genomic RNA (gRNA) of Pea enation mosaic virus 2 (PEMV2) is the template for p33 and −1 frameshift product p94. The PEMV2 subgenomic RNA (sgRNA) encodes two overlapping ORFs, p26 and p27, which are required for movement and stability of the gRNA. Efficient translation of p33 requires two of three 3′ proximal cap-independent translation enhancers (3′CITEs): the kl-TSS, which binds ribosomes and engages in a long-distance interaction with the 5’end; and the adjacent eIF4E-binding PTE. Unlike the gRNA, all three 3′CITEs were required for efficient translation of the sgRNA, which included the ribosome-binding 3′TSS. A hairpin in the 5′ proximal coding region of p26/p27 supported translation by the 3′CITEs by engaging in a long-distance RNA:RNA interaction with the kl-TSS. These results strongly suggest that the 5′ ends of PEMV2 gRNA and sgRNA connect with the 3′UTR through similar long-distance interactions while having different requirements for 3′CITEs.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

Gao

Simon

2017

Virology

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“…These pentamers may create a long-distance base-pairing interaction between the 3’ and 5’ UTRs (discussed later). The overall structure obtained from the SHAPE probing assays indicates that the MTE has a similar structure to those of Panicum mosaic virus-like 3’ CITES (PTEs) [38, 52], but differing by the presence of three hypermodified bases rather than a single hypermodified G in the purine-rich bulge in the presence of Mg 2+ [53].…”

Section: Resultsmentioning

confidence: 99%

“…Most plant viral 3’ CITEs that have been studied interact with the 5’ end of the viral genomic RNA and subgenomic mRNA via long-distance base pairing of the 3’ CITE to the 5’ UTR, presumably to deliver initiation factors to the 5’ end where they recruit the ribosomal 40S subunit to the RNA [35, 52, 60–62]. Thus, we sought to determine if the same interaction occurs in MCMV RNA.…”

Section: Resultsmentioning

confidence: 99%

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

Carino

Scheets

Miller

2020

Preprint

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Maize chlorotic mottle virus (MCMV) combines with a potyvirus in maize lethal necrosis disease (MLND), an emerging disease worldwide that often causes catastrophic yield loss. To inform resistance strategies, we characterized the translation initiation mechanism of MCMV. We report that, like other tombusvirids, MCMV RNA contains a cap-independent translation element (CITE) in its 3’ untranslated region (UTR). The MCMV 3’ CITE (MTE) was mapped to nucleotides 4164-4333 in the genomic RNA. SHAPE probing revealed that the MTE is a variant of the panicum mosaic virus-like 3’ CITE (PTE). Like the PTE, electrophoretic mobility shift assays (EMSAs) indicated that eukaryotic translation initiation factor 4E (eIF4E) binds the MTE despite the absence of a m7GpppN cap structure, which is normally required for eIF4E to bind RNA. The MTE interaction with eIF4E suggests eIF4E may be a soft target for engineered resistance to MCMV. Using a luciferase reporter system, mutagenesis to disrupt and restore base pairing revealed that the MTE interacts with the 5’ UTRs of both genomic RNA and the 3’-coterminal subgenomic RNA1 via long-distance kissing stem-loop base pairing to facilitate translation in wheat germ extract and in protoplasts. However, the MTE is a relatively weak stimulator of translation and has a weak, if any, pseudoknot, which is present in the most active PTEs. Most mutations designed to form a pseudoknot decreased translation activity. Mutations in the viral genome that reduced or restored translation prevented and restored virus replication, respectively, in maize protoplasts and in plants. We propose that MCMV, and some other positive strand RNA viruses, favors a weak translation element to allow highly efficient viral RNA synthesis.Author SummaryIn recent years, maize lethal necrosis disease has caused massive crop losses in East Africa and Ecuador. It has also emerged in East Asia. Maize chlorotic mottle virus (MCMV) infection is required for this disease. While some tolerant maize lines have been identified, there are no known resistance genes that confer full immunity to MCMV. In order to design better resistance strategies against MCMV, we focused on how the MCMV genome is translated, the first step of gene expression required for infection by all positive strand RNA viruses. We identified a structure (cap-independent translation element) in the 3’ untranslated region of the viral RNA genome that allows the virus to usurp a host translation initiation factor in a way that differs from host mRNA interactions with the translational machinery. This difference may guide engineering of – or breeding for – resistance to MCMV. Moreover, this work adds to the diversity of known eukaryotic translation initiation mechanisms, as it provides more information on mRNA structural features that permit noncanonical interaction with a translation factor. Finally, owing to the conflict between ribosomes translating and viral replicase copying viral RNA, we propose that MCMV has evolved a relatively weak translation element in order to permit highly efficient RNA synthesis, and that this replication-translation trade-off may apply to other positive strand RNA viruses.

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3′UTRs of carmoviruses

Simon

2015

Virus Research

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Carmovirus is a genus of small, single-stranded, positive-strand RNA viruses in the Tombusviridae. One member of the carmoviruses, Turnip crinkle virus (TCV), has been used extensively as a model for examining the structure and function of RNA elements in 3'UTR as well as in other regions of the virus. Using a variety of genetic, biochemical and computational methods, a structure for the TCV 3'UTR has emerged where secondary structures and tertiary interactions combine to adopt higher order 3-D structures including an internal, ribosome-binding tRNA-shaped configuration that functions as a 3' cap-independent translation enhancer (3'CITE). The TCV 3'CITE also serves as a scaffold for non-canonical interactions throughout the 3'UTR and extending into the upstream open reading frame, interactions that are significantly disrupted upon binding by the RNA-dependent RNA polymerase. Long-distance interactions that connect elements in the 3'UTR with both the 5' end and the internal ribosome recoding site suggest that 3'UTR of carmoviruses are intimately involved in multiple functions in the virus life cycle. Although carmoviruses share very similar genome organizations, lengths of 5' and 3'UTRs, and structural features at the 3' end, the similarity rapidly breaks down the further removed from the 3' terminus revealing different 3'CITEs and unique virus-specific structural features. This review summarizes 20 years of work dissecting the structure and function of the 3'UTR of TCV and other carmoviruses. The astonishing structural complexity of the 3'UTRs of these simple carmoviruses provides lessons that are likely applicable to many other plant and animal RNA viruses.

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Position of the kissing-loop interaction associated with PTE-type 3′CITEs can affect enhancement of cap-independent translation

Cited by 13 publications

References 33 publications

Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

Differential use of 3’CITEs by the subgenomic RNA of Pea enation mosaic virus 2

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

3′UTRs of carmoviruses

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