Parvovirus-Derived Endogenous Viral Elements in Two South American Rodent Genomes

Arriagada, Gloria; Gifford, Robert J.

doi:10.1128/jvi.01173-14

Cited by 23 publications

(47 citation statements)

References 19 publications

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“…In addition to the possibly endogenized PRSs identified in these 31 invertebrate species, PRSs were also identified in the genomes of 16 animal species for which potential parvovirus endogenization has been previously reported (including nine arthropods, six chordates and one platyhelminthes; Fig. 3)202131323334.…”

Section: Resultsmentioning

confidence: 90%

Discovery of parvovirus-related sequences in an unexpected broad range of animals

François

Filloux

Bigot

et al. 2016

Sci Rep

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Our knowledge of the genetic diversity and host ranges of viruses is fragmentary. This is particularly true for the Parvoviridae family. Genetic diversity studies of single stranded DNA viruses within this family have been largely focused on arthropod- and vertebrate-infecting species that cause diseases of humans and our domesticated animals: a focus that has biased our perception of parvovirus diversity. While metagenomics approaches could help rectify this bias, so too could transcriptomics studies. Large amounts of transcriptomic data are available for a diverse array of animal species and whenever this data has inadvertently been gathered from virus-infected individuals, it could contain detectable viral transcripts. We therefore performed a systematic search for parvovirus-related sequences (PRSs) within publicly available transcript, genome and protein databases and eleven new transcriptome datasets. This revealed 463 PRSs in the transcript databases of 118 animals. At least 41 of these PRSs are likely integrated within animal genomes in that they were also found within genomic sequence databases. Besides illuminating the ubiquity of parvoviruses, the number of parvoviral sequences discovered within public databases revealed numerous previously unknown parvovirus-host combinations; particularly in invertebrates. Our findings suggest that the host-ranges of extant parvoviruses might span the entire animal kingdom.

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Section: Resultsmentioning

confidence: 90%

Discovery of parvovirus-related sequences in an unexpected broad range of animals

François

Filloux

Bigot

et al. 2016

Sci Rep

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“…Unlike AAV Rep and other EPVs containing intact ORFs encoding complete or nearly complete Rep proteins (e.g. the Odegus4 element in the genome of the degu [ Octodon degus ]) [13], the enREP-Myo9 sequence does not contain nuclear localization signals. We cloned and expressed the Odegus4 element, demonstrating that this transcript can express a protein (Fig 3A).…”

Section: Resultsmentioning

confidence: 99%

“…We compared the localization of enRep-Myo9 with another EPV-encoded Rep protein: Odegus4, encoded by a dependoparvoviruses-derived EPV in the degu genome. We previously reported that this EPV is specifically transcribed in degu liver [13]. The predicted gene product contains at least two NLS, as it is expected for Rep proteins (which must locate to the nucleus to allow replication of parvoviral DNA).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, the presence of numerous independently acquired, fixed EPV insertions in mammalian genomes is unexpected, and suggests that selective pressures may have occasionally favored retention of EPV genes during mammalian evolution. Intriguingly, several EPV loci contain open reading frames (ORFs) capable of expressing complete or almost complete proteins [13, 14], and recent studies have shown that Rep-encoding EPV loci in rodents and elephants exhibit a similar, distinctive pattern of tissue-specific expression (being specifically transcribed in the liver) despite having been acquired in entirely independent germline incorporation events [14].…”

Section: Introductionmentioning

confidence: 99%

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Molecular properties and evolutionary origins of a parvovirus-derived myosin fusion gene in guinea pigs

Valencia-Herrera

Cena-Ahumada

Faunes

et al. 2019

Preprint

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word count: 239 17 Text word count: 3128 18 2 Abstract 19Sequences derived from parvoviruses (family Parvoviridae) are relatively common in 20 animal genomes, but the functional significance of these endogenous parvoviral element (EPV) 21 sequences remains unclear. In this study we use a combination of in silico and molecular 22 biological approaches to investigate a fusion gene encoded by guinea pigs (genus Cavia) that is 23 partially derived from an EPV. This gene, named enRep-Myo9, encodes a predicted polypeptide 24 gene product comprising a partial myosin9 (Myo9)-like gene fused to a 3' truncated, EPV-25 encoded replicase. We first examined the genomic and phylogenetic characteristics of the EPV 26 locus that encodes the viral portions of enRep-Myo9. We show that this locus, named enRep, is 27 specific to guinea pigs and derives from an ancient representative of the parvoviral genus 28 Dependoparvovirus that integrated into the guinea pig germline 22-35 million years ago. Despite 29 these ancient origins, however, the regions of enRep that are incorporated into the coding 30 sequence of the enRep-Myo9 gene are conserved across multiple species in the family Caviidae 31 (guinea pigs and cavies) consistent with purifying selection. Using molecular biological 32 approaches, we further demonstrate that: (i) enRep-Myo9 mRNA is broadly transcribed in guinea 33 pig cells; (ii) the cloned enRep-Myo9 transcript can express a protein of the expected size in 34 guinea pig cells in vitro, and; (iii) the expressed protein localizes to the cytosol. Our findings 35 demonstrate that, consistent with a functional role, the enRep-Myo9 fusion gene is evolutionarily 36 conserved, broadly transcribed, and capable of expressing protein. 37 38 Importance 39DNA from viruses has been 'horizontally transferred' to mammalian genomes during 40 evolution, but the impact of this process on mammalian biology remains poorly understood. The 41 3 findings of our study indicate that in guinea pigs a novel gene has evolved through fusion of host 42 and virus genes. 43 44

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“…Sequences derived from parvoviruses occur relatively frequently in animal genomes (13, 14, 17, 25, 26). However, these sequences overwhelmingly derive from a small proportion of parvovirus lineages.…”

Section: Discussionmentioning

confidence: 99%

An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

Pénzes

Souza

Agbandje‐McKenna

et al. 2019

Preprint

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2Chapparvoviruses are a highly divergent group of parvoviruses (family 3 Parvoviridae) first identified in 2013. Interest in these poorly characterized 4 viruses has been raised by recent studies indicating that they are the cause of 5 chronic kidney disease that arises spontaneously in laboratory mice. In this 6 study, we investigate the biological and evolutionary characteristics of 7 chapparvoviruses via comparative analysis of genome sequence data. Our 8 analysis, which incorporates sequences derived from endogenous viral 9 elements (EVEs) as well as exogenous viruses, reveals that 10 chapparvoviruses are an ancient lineage within the family Parvoviridae, 11 clustering separately from members of both currently established parvoviral 12 subfamilies. Consistent with this, they exhibit a number of characteristic 13 genomic and structural features, i.e. a large number of putative auxiliary 14 protein-encoding genes, capsid protein genes non-homologous to any hitherto 15 parvoviral cap, as well as a putative capsid structure lacking the canonical fifth 16 strand of the ABIDG sheet comprising the luminal side of the jelly roll. Our 17 findings demonstrate that the chapparvovirus lineage infects an exceptionally 18 broad range of host species, including both vertebrates and invertebrates.19Furthermore, we observe that chapparvoviruses found in fish are more closely 20 related to those from invertebrates than they are to those that infect amniote 21 vertebrates. This suggests that transmission between distantly related host 22 species may have occurred in the past. Our study provides the first integrated 23 overview of the chapparvovirus group, and revises current views of parvovirus 24 evolution 25 26 AUTHOR SUMMARY 27 Chapparvoviruses are a recently identified group of viruses about 28 which relatively little is known. However, recent studies have shown that these 29 viruses cause disease in laboratory mice and are prevalent in the fecal virome 30 of pigs and poultry, raising interest in their potential impact as pathogens, and 31 utility as experimental tools. We examined the genomes of chapparvoviruses 32 and endogenous viral elements ('fossilized' virus sequences derived from 33 ancestral viruses) using a variety of bioinformatics-based approaches. We 3 1 show that the chapparvoviruses have an ancient origin and are evolutionarily 2 distinct from all other related viruses. Accordingly, their genomes and virions 3 exhibit a range of distinct characteristic features. We examine the distribution 4 of these features in the light of chapparvovirus evolutionary history (which we 5 can also infer from genomic data), revealing new insights into chapparvovirus 6 biology. 7 8

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Parvovirus-Derived Endogenous Viral Elements in Two South American Rodent Genomes

Cited by 23 publications

References 19 publications

Discovery of parvovirus-related sequences in an unexpected broad range of animals

Discovery of parvovirus-related sequences in an unexpected broad range of animals

Molecular properties and evolutionary origins of a parvovirus-derived myosin fusion gene in guinea pigs

An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

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