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A metazoan/plant-like capping enzyme and cap modified nucleotides in the unicellular eukaryote Trichomonas vaginalis

Lookup NU author(s): Professor Robert HirtORCiD

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Abstract

The cap structure of eukaryotic messenger RNAs is initially elaborated through three enzymatic reactions: hydrolysis of the 5'-triphosphate, transfer of guanosine through a 5'-5' triphosphate linkage and N7-methylation of the guanine cap. Three distinctive enzymes catalyze each reaction in various microbial eukaryotes, whereas the first two enzymes are fused into a single polypeptide in metazoans and plants. In addition to the guanosine cap, adjacent nucleotides are 2'-O-ribose methylated in metazoa and plants, but not in yeast. Analyses of various cap structures have suggested a linear phylogenetic trend of complexity. These findings have led to a model in which plants and metazoa evolved a two-component capping apparatus and modification of adjacent nucleotides while many microbial eukaryotes maintained the three-component system and did not develop modification of adjacent nucleotides. Here, we have characterized a bifunctional capping enzyme in the divergent microbial eukaryote Trichomonas vaginalis using biochemical and phylogenetic analyses. This unicellular parasite was found to harbor a metazoan/plant-like capping apparatus that is represented by a two-domain polypeptide containing a C-terminus guanylyltransferase and a cysteinyl phosphatase triphosphatase, distinct from its counterpart in other microbial eukaryotes. In addition, T. vaginalis mRNAs contain a cap 1 structure represented by m(7)GpppAmpUp or m(7)GpppCmpUp; a feature typical of metazoan and plant mRNAs but absent in yeast mRNAs. Phylogenetic and biochemical analyses of the origin of the T. vaginalis capping enzyme suggests a complex evolutionary model where differential gene loss and/or acquisition occurred in the development of the RNA capping apparatus and cap modified nucleotides during eukaryote diversification.


Publication metadata

Author(s): Simoes-Barbosa A, Hirt RP, Johnson PJ

Publication type: Article

Publication status: Published

Journal: PLoS Pathogens

Year: 2010

Volume: 6

Issue: 7

Print publication date: 15/07/2010

Date deposited: 01/09/2010

ISSN (print): 1553-7366

ISSN (electronic): 1553-7374

Publisher: Public Library of Science

URL: http://dx.doi.org/10.1371/journal.ppat.1000999

DOI: 10.1371/journal.ppat.1000999


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Funding

Funder referenceFunder name
AI30537National Institutes of Health

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