Cancer, Warts, or Asymptomatic Infections: Clinical Presentation Matches Codon Usage Preferences in Human Papillomaviruses

Félez-Sánchez, Marta; Trösemeier, Jan-Hendrik; Bedhomme, Stéphanie; González-Bravo, M. Isabel; Kamp, Christel; Bravo, Ignacio G.

doi:10.1093/gbe/evv129

Cited by 17 publications

(28 citation statements)

References 84 publications

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“…This result is consistent with the hypothesis suggesting that the proto-PV was composed by the E1, E2, L2 and L1 genes, the core region of the genome, while the E6 and E7 were incorporated later, providing with dispensable transforming capacities [ 66 ]. Further, this clustering matches well differences in codon usage preferences between different PV genes, which are similar for genes expressed at similar stages of the natural history of the PV infection [ 81 ].…”

Section: Discussionsupporting

confidence: 56%

Assessing parallel gene histories in viral genomes

Mengual‐Chuliá¹,

Bedhomme²,

Lafforgue³

et al. 2016

BMC Evol Biol

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BackgroundThe increasing abundance of sequence data has exacerbated a long known problem: gene trees and species trees for the same terminal taxa are often incongruent. Indeed, genes within a genome have not all followed the same evolutionary path due to events such as incomplete lineage sorting, horizontal gene transfer, gene duplication and deletion, or recombination. Considering conflicts between gene trees as an obstacle, numerous methods have been developed to deal with these incongruences and to reconstruct consensus evolutionary histories of species despite the heterogeneity in the history of their genes. However, inconsistencies can also be seen as a source of information about the specific evolutionary processes that have shaped genomes.ResultsThe goal of the approach here proposed is to exploit this conflicting information: we have compiled eleven variables describing phylogenetic relationships and evolutionary pressures and submitted them to dimensionality reduction techniques to identify genes with similar evolutionary histories. To illustrate the applicability of the method, we have chosen two viral datasets, namely papillomaviruses and Turnip mosaic virus (TuMV) isolates, largely dissimilar in genome, evolutionary distance and biology. Our method pinpoints viral genes with common evolutionary patterns. In the case of papillomaviruses, gene clusters match well our knowledge on viral biology and life cycle, illustrating the potential of our approach. For the less known TuMV, our results trigger new hypotheses about viral evolution and gene interaction.ConclusionsThe approach here presented allows turning phylogenetic inconsistencies into evolutionary information, detecting gene assemblies with similar histories, and could be a powerful tool for comparative pathogenomics.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0605-4) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 56%

Assessing parallel gene histories in viral genomes

Mengual‐Chuliá¹,

Bedhomme²,

Lafforgue³

et al. 2016

BMC Evol Biol

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“…This is likely due to the degenerate nature of the genetic code (Betts and Russell 2003). Interestingly, it has been demonstrated that HPV genomes have a pronounced codon usage bias when compared with host genes (Bravo and Muller 2005; Cladel, Bertotto, and Christensen, 2010; Félez-Sánchez et al 2015). This study may begin to shed light unto why papillomavirus genomes have evolved to use sub-optimal codons.…”

Section: Discussionmentioning

confidence: 99%

Role of the host restriction factor APOBEC3 on papillomavirus evolution

Warren

Doorslaer

Pandey³

et al. 2015

Virus Evol

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More than 270 different types of papillomaviruses have been discovered in a wide array of animal species. Despite the great diversity of papillomaviruses, little is known about the evolutionary processes that drive host tropism and the emergence of oncogenic genotypes. Although host defense mechanisms have evolved to interfere with various aspects of a virus life cycle, viruses have also coevolved copious strategies to avoid host antiviral restriction. Our and other studies have shown that the cytidine deaminase APOBEC3 family members edit HPV genomes and restrict virus infectivity. Thus, we hypothesized that host restriction by APOBEC3 served as selective pressure during papillomavirus evolution. To test this hypothesis, we analyzed the relative abundance of all dinucleotide sequences in full-length genomes of 274 papillomavirus types documented in the Papillomavirus Episteme database (PaVE). Here, we report that TC dinucleotides, the preferred target sequence of several human APOBEC3 proteins (hA3A, hA3B, hA3F, and hA3H), are highly depleted in papillomavirus genomes. Given that HPV infection is highly tissue-specific, the expression levels of APOBEC3 family members were analyzed. The basal expression levels of all APOBEC3 isoforms, excluding hA3B, are significantly higher in mucosal skin compared with cutaneous skin. Interestingly, we reveal that Alphapapillomaviruses (alpha-PVs), a majority of which infects anogenital mucosa, display the most dramatic reduction in TC dinucleotide content. Computer modeling and reconstruction of ancestral alpha-PV genomes suggest that TC depletion occurred after the alpha-PVs diverged from their most recent common ancestor. In addition, we found that TC depletion in alpha-PVs is greatly affected by protein coding potential. Taken together, our results suggest that PVs replicating in tissues with high APOBEC3 levels may have evolved to evade restriction by selecting for variants that contain reduced APOBEC3 target sites in their genomes.

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“…A recent study suggested that, following the exit from Nigeria, LASV evolved towards a higher virulence possibly driven by an increase in CAI (Andersen et al., ). Indeed, changes in CAI in other viral species have been associated with different disease presentation or virulence (Cladel, Budgeon, Hu, Balogh, & Christensen, ; Felez‐Sanchez et al., ; Tello, Vergara, & Spencer, ; Wirblich & Schnell, ).…”

Section: Resultsmentioning

confidence: 99%

“…Within viral species or genera, differences in CAI have been associated with viral phenotypes. For instance, clinical presentation is an important explanatory factor for codon usage preferences in papillomaviruses (Cladel et al., ; Felez‐Sanchez et al., ), and CAI correlates with the virulence of infectious salmon anaemia virus isolates (Tello et al., ). Nonetheless, the effects of CAI changes in viral sequences are often difficult to predict.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary analysis of Old World arenaviruses reveals a major adaptive contribution of the viral polymerase

et al. 2017

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The Old World (OW) arenavirus complex includes several species of rodent-borne viruses, some of which (i.e., Lassa virus, LASV and Lymphocytic choriomeningitis virus, LCMV) cause human diseases. Most LCMV and LASV infections are caused by rodent-to-human transmissions. Thus, viral evolution is largely determined by events that occur in the wildlife reservoirs. We used a set of human- and rodent-derived viral sequences to investigate the evolutionary history underlying OW arenavirus speciation, as well as the more recent selective events that accompanied LASV spread in West Africa. We show that the viral RNA polymerase (L protein) was a major positive selection target in OW arenaviruses and during LASV out-of-Nigeria migration. No evidence of selection was observed for the glycoprotein, whereas positive selection acted on the nucleoprotein (NP) during LCMV speciation. Positively selected sites in L and NP are surrounded by highly conserved residues, and the bulk of the viral genome evolves under purifying selection. Several positively selected sites are likely to modulate viral replication/transcription. In both L and NP, structural features (solvent exposed surface area) are important determinants of site-wise evolutionary rate variation. By incorporating several rodent-derived sequences, we also performed an analysis of OW arenavirus codon adaptation to the human host. Results do not support a previously hypothesized role of codon adaptation in disease severity for non-Nigerian strains. In conclusion, L and NP represent the major selection targets and possible determinants of disease presentation; these results suggest that field surveys and experimental studies should primarily focus on these proteins.

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Cancer, Warts, or Asymptomatic Infections: Clinical Presentation Matches Codon Usage Preferences in Human Papillomaviruses

Cited by 17 publications

References 84 publications

Assessing parallel gene histories in viral genomes

Assessing parallel gene histories in viral genomes

Role of the host restriction factor APOBEC3 on papillomavirus evolution

Evolutionary analysis of Old World arenaviruses reveals a major adaptive contribution of the viral polymerase

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