The structural basis of recognition and removal of cellular mRNA 7-methyl G ?caps? by a viral capsid protein: a unique viral response to host defense

Tang, Jinghua; Naitow, Hisashi; Gardner, Nora A.; Kolesar, Anna; Tang, Liang; Wickner, Reed B.; Johnson, John E.

doi:10.1002/jmr.724

Cited by 33 publications

(43 citation statements)

References 50 publications

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“…In the trench, Tyr150, Asp152, Tyr452, and Tyr538 are located close to the bound m 7 GDP, suggesting their involvement in cap recognition (23). Mutagenesis studies indicate that these residues are crucial for decapping activity.…”

Section: Discussionmentioning

confidence: 97%

“…Crystallographic studies of the L-A virion have identified a trench on the outer surface of Gag that includes His154 (22,23). L-A transcripts are made inside the virion and presumably released to the cytoplasm through one of the pores located at the icosahedral 5-fold symmetric axes (22).…”

Section: Discussionmentioning

confidence: 99%

“…Upon ligand binding (m 7 GDP) the rim moves inwardly and forms a closed conformation (23). Guanylyltransferase also contains a trench that can adopt either open or closed conformations during the mRNA capping reaction (25,26).…”

Section: Discussionmentioning

confidence: 99%

“…Mutagenesis studies indicate that these residues are crucial for decapping activity. Tyr452 and Tyr538 sandwich m 7 GDP by a potential stacking (23). Cap-binding proteins normally use two aromatic rings of Tyr, Phe, or Trp in cap recognition to sandwich the m 7 G moiety (31,32).…”

Section: Discussionmentioning

confidence: 99%

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Cap-snatching mechanism in yeast L-A double-stranded RNA virus

Fujimura

Esteban

2011

Proc. Natl. Acad. Sci. U.S.A.

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The 5′ cap structure (m 7 GpppX-) is an essential feature of eukaryotic mRNA required for mRNA stability and efficient translation. Influenza virus furnishes its mRNA with this structure by a capsnatching mechanism, in which the viral polymerase cleaves host mRNA endonucleolytically 10-13 nucleotides from the 5′ end and utilizes the capped fragment as a primer to synthesize viral transcripts. Here we report a unique cap-snatching mechanism by which the yeast double-stranded RNA totivirus L-A furnishes its transcript with a cap structure derived from mRNA. Unlike influenza virus, L-A transfers only m 7 Gp from the cap donor to the 5′ end of the viral transcript, thus preserving the 5′ α-and β-phosphates of the transcript in the triphosphate linkage of the final product. This in vitro capping reaction requires His154 of the coat protein Gag, a residue essential for decapping of host mRNA and known to form m 7 Gp-His adduct. Furthermore, the synthesis of capped viral transcripts in vivo and their expression were greatly compromised by the Arg154 mutation, indicating the involvement of Gag in the cap-snatching reaction. The overall reaction and the structure around the catalytic site in Gag resemble those of guanylyltransferase, a key enzyme of cellular mRNA capping, suggesting convergent evolution. Given that Pol of L-A is confined inside the virion and unable to access host mRNA in the cytoplasm, the structural protein Gag rather than Pol catalyzing this unique cap-snatching reaction exemplifies the versatility as well as the adaptability of eukaryotic RNA viruses.transcription | Saccharomyces cerevisiae | killer toxin E ukaryotic mRNA is capped at the 5′ end by a 7-methyl GMP moiety via an inverted 5′-5′ triphosphate linkage (m 7 GpppX) (1, 2). The cap structure is required for mRNA stability and efficient translation. Capping of the RNA 5′ end is accomplished in cells and for most viruses in three sequential catalytic reactions (3, 4): removal of the 5′ γ-phosphate by RNA triphosphatase, addition of GMP from GTP by guanylyltransferase, and methylation of the added GMP by methyltransferase. Influenza virus, how-

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Cap-snatching mechanism in yeast L-A double-stranded RNA virus

Fujimura

Esteban

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…These different roles are directly reflected in the distinct features of the particle surfaces. PcV and L-A CP outer surfaces are highly corrugated, and Gag has a decapping activity (66). It is plausible that PcV CP, in addition to its structural role, might also have enzymatic activity, like L-A Gag.…”

Section: Discussionmentioning

confidence: 99%

The T=1 Capsid Protein of Penicillium chrysogenum Virus Is Formed by a Repeated Helix-Rich Core Indicative of Gene Duplication

Luque

González

Garriga

et al. 2010

J Virol

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Penicillium chrysogenum virus (PcV), a member of the Chrysoviridae family, is a double-stranded RNA (dsRNA) fungal virus with a multipartite genome, with each RNA molecule encapsidated in a separate particle. Chrysoviruses lack an extracellular route and are transmitted during sporogenesis and cell fusion. The PcV capsid, based on a T‫1؍‬ lattice containing 60 subunits of the 982-amino-acid capsid protein, remains structurally undisturbed throughout the viral cycle, participates in genome metabolism, and isolates the virus genome from host defense mechanisms. Using three-dimensional cryoelectron microscopy, we determined the structure of the PcV virion at 8.0 Å resolution. The capsid protein has a high content of rod-like densities characteristic of ␣-helices, forming a repeated ␣-helical core indicative of gene duplication. Whereas the PcV capsid protein has two motifs with the same fold, most dsRNA virus capsid subunits consist of dimers of a single protein with similar folds. The spatial arrangement of the ␣-helical core resembles that found in the capsid protein of the L-A virus, a fungal totivirus with an undivided genome, suggesting a conserved basic fold. The encapsidated genome is organized in concentric shells; whereas the inner dsRNA shells are well defined, the outermost layer is dense due to numerous interactions with the inner capsid surface, specifically, six interacting areas per monomer. The outermost genome layer is arranged in an icosahedral cage, sufficiently well ordered to allow for modeling of an A-form dsRNA. The genome ordering might constitute a framework for dsRNA transcription at the capsid interior and/or have a structural role for capsid stability.Viruses with double-stranded RNA (dsRNA) genomes are found in a broad range of organisms, ranging from bacteria to simple (fungi and protozoa) and complex (animals and plants) eukaryotes.

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The frenemies within: viruses, retrotransposons and plasmids that naturally infectSaccharomycesyeasts

Rowley

2017

Yeast

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Viruses are a major focus of current research efforts because of their detrimental impact on humanity and their ubiquity within the environment. Bacteriophages have long been used to study host-virus interactions within microbes, but it is often forgotten that the single-celled eukaryote Saccharomyces cerevisiae and related species are infected with double-stranded RNA viruses, single-stranded RNA viruses, LTR-retrotransposons and double-stranded DNA plasmids. These intracellular nucleic acid elements have some similarities to higher eukaryotic viruses, i.e. yeast retrotransposons have an analogous lifecycle to retroviruses, the particle structure of yeast totiviruses resembles the capsid of reoviruses and segregation of yeast plasmids is analogous to segregation strategies used by viral episomes. The powerful experimental tools available to study the genetics, cell biology and evolution of S. cerevisiae are well suited to further our understanding of how cellular processes are hijacked by eukaryotic viruses, retrotransposons and plasmids. This article has been written to briefly introduce viruses, retrotransposons and plasmids that infect Saccharomyces yeasts, emphasize some important cellular proteins and machineries with which they interact, and suggest the evolutionary consequences of these interactions. Copyright © 2017 John Wiley & Sons, Ltd.

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The structural basis of recognition and removal of cellular mRNA 7-methyl G ?caps? by a viral capsid protein: a unique viral response to host defense

Cited by 33 publications

References 50 publications

Cap-snatching mechanism in yeast L-A double-stranded RNA virus

Cap-snatching mechanism in yeast L-A double-stranded RNA virus

The T=1 Capsid Protein of Penicillium chrysogenum Virus Is Formed by a Repeated Helix-Rich Core Indicative of Gene Duplication

The frenemies within: viruses, retrotransposons and plasmids that naturally infectSaccharomycesyeasts

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