Molecular Properties and Evolutionary Origins of a Parvovirus-Derived Myosin Fusion Gene in Guinea Pigs

Valencia-Herrera, Ignacio; Faunes, Fernando; Cena-Ahumada, Eduardo; Ibarra-Karmy, Rodrigo; Gifford, Robert J.; Arriagada, Gloria

doi:10.1128/jvi.00404-19

Cited by 6 publications

(25 citation statements)

References 31 publications

(39 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Previous studies have shown that some EPV loci express RNA with the potential to encode polypeptide gene products, either as unspliced viral RNA [ 17 , 37 , 38 ] or as fusion genes comprising RNA sequences derived from both host and viral sources [ 39 ]. We examined all EPV loci identified in our study to determine their coding potential.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates

Campbell¹,

Loncar

Kotin

et al. 2022

PLoS Biol

Self Cite

View full text Add to dashboard Cite

Parvoviruses (family Parvoviridae) are small DNA viruses that cause numerous diseases of medical, veterinary, and agricultural significance and have important applications in gene and anticancer therapy. DNA sequences derived from ancient parvoviruses are common in animal genomes and analysis of these endogenous parvoviral elements (EPVs) has demonstrated that the family, which includes twelve vertebrate-specific genera, arose in the distant evolutionary past. So far, however, such “paleovirological” analysis has only provided glimpses into the biology of ancient parvoviruses and their long-term evolutionary interactions with hosts. Here, we comprehensively map EPV diversity in 752 published vertebrate genomes, revealing defining aspects of ecology and evolution within individual parvovirus genera. We identify 364 distinct EPV sequences and show these represent approximately 200 unique germline incorporation events, involving at least five distinct parvovirus genera, which took place at points throughout the Cenozoic Era. We use the spatiotemporal and host range calibrations provided by these sequences to infer defining aspects of long-term evolution within individual parvovirus genera, including mammalian vicariance for genus Protoparvovirus, and interclass transmission for genus Dependoparvovirus. Moreover, our findings support a model of virus evolution in which the long-term cocirculation of multiple parvovirus genera in vertebrates reflects the adaptation of each viral genus to fill a distinct ecological niche. Our findings show that efforts to develop parvoviruses as therapeutic tools can be approached from a rational foundation based on comparative evolutionary analysis. To support this, we published our data in the form of an open, extensible, and cross-platform database designed to facilitate the wider utilisation of evolution-related domain knowledge in parvovirus research.

show abstract

Section: Resultsmentioning

confidence: 99%

“… f VP shown in bold. *EPV–gene fusion products predicted [ 25 ] or confirmed [ 39 ]—length shown is for viral portion only. …”

Section: Resultsmentioning

confidence: 99%

Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates

Campbell¹,

Loncar

Kotin

et al. 2022

PLoS Biol

Self Cite

View full text Add to dashboard Cite

show abstract

“…Previous studies have shown that some EPV loci express RNA with the potential to encode polypeptide gene products, either as unspliced viral RNA [17, 40, 41], or as fusion genes comprising RNA sequences derived from both host and viral sources [42]. We examined all EPV loci identified in our study to determine their coding potential.…”

Section: Resultsmentioning

confidence: 99%

“…We recovered the complete repertoire of EPV sequences in WGS data representing 752 vertebrate species. While previous studies have reported a sampling of EPV diversity in vertebrates [12-18, 22, 32, 35, 40, 42, 43], our investigation is an order of magnitude larger in scale: we identify 364 sequences representing nearly 200 discrete germline incorporation events that took place during the Cenozoic Era ( Fig. 2, Table S1 ).…”

Section: Discussionmentioning

confidence: 96%

See 1 more Smart Citation

Comparative analysis reveals the long-term co-evolutionary history of parvoviruses and vertebrates

Campbell

Loncar

Kotin

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Parvoviruses (family Parvoviridae) are small, non-enveloped DNA viruses that infect a broad range of animal species. Comparative studies, supported by experimental evidence, show that many vertebrate species contain sequences derived from ancient parvoviruses embedded in their genomes. These endogenous parvoviral elements (EPVs), which arose via recombination-based mechanisms in infected germline cells of ancestral organisms, constitute a form of molecular fossil record that can be used to investigate the origin and evolution of the parvovirus family. Here, we use comparative approaches to investigate 198 EPV loci, represented by 470 EPV sequences identified in a comprehensive in silico screen of 752 published vertebrate genomes. We investigated EPV loci by constructing an open resource that contains the data items required for comparative sequence analysis of parvoviruses and uses a relational database to represent the complex semantic relationships between them. We used this standardised framework to implement reproducible comparative phylogenetic analysis of combined EPV and virus data. Our analysis reveals that viruses closely related to contemporary parvoviruses have circulated among vertebrates since the Late Cretaceous epoch (100-66 million years ago). We present evidence that the subfamily Parvovirinae, which includes ten vertebrate-specific genera, has evolved in broad congruence with the emergence and diversification of major vertebrate groups. Furthermore, we infer defining aspects of evolution within individual parvovirus genera - mammalian vicariance for protoparvoviruses (genus Protoparvovirus), and inter-class transmission for dependoparvoviruses (genus Dependoparvovirus) - thereby establishing an ecological and evolutionary perspective through which to approach analysis of these virus groups. We also identify evidence of EPV expression at RNA level and show that EPV coding sequences have frequently been maintained during evolution, adding to a growing body of evidence that EPV loci have been co-opted or exapted by vertebrate species, and especially by mammals. Our findings offer fundamental insights into parvovirus evolution. In addition, we establish novel genomic resources that can advance the development of parvovirus-related research - including both therapeutics and disease prevention efforts - by enabling more efficient dissemination and utilisation of relevant, evolution-related domain knowledge.

show abstract

A novel approach to exploring the dark genome and its application to mapping of the vertebrate virus ‘fossil record’

Blanco-Melo,

Campbell,

Zhu

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Background: Genomic regions that remain poorly understood, often referred to as the "dark genome," contain a variety of functionally relevant and biologically informative genome features. These include endogenous viral elements (EVEs) - virus-derived sequences that can dramatically impact host biology and serve as a virus "fossil record". In this study, we introduce a database-integrated genome screening (DIGS) approach to investigating the dark genome in silico, focusing on EVEs found within vertebrate genomes. Results: Using DIGS on 874 vertebrate species genomes, we uncovered approximately 1.1 million EVE sequences, with over 99% originating from endogenous retroviruses or transposable elements that contain EVE DNA. We show that the remaining 6038 sequences represent over a thousand distinct horizontal gene transfer events across ten virus families, including some that have not previously been reported as EVEs. We explore the genomic and phylogenetic characteristics of non-retroviral EVEs and determine their rates of acquisition during vertebrate evolution. Our study uncovers novel virus diversity and broadens our knowledge of virus distribution among vertebrate hosts. It also provides new insights into the long-term evolution of highly pathogenic filoviruses. Conclusions: We comprehensively catalogue and analyse EVEs within 874 vertebrate genomes, shedding light on the distribution, diversity and long-term evolution of viruses, and revealing their extensive impact on vertebrate genome evolution. Our results demonstrate the power of linking a relational database management system to a similarity search-based screening pipeline for in silico exploration of the dark genome.

show abstract

Molecular Properties and Evolutionary Origins of a Parvovirus-Derived Myosin Fusion Gene in Guinea Pigs

Cited by 6 publications

References 31 publications

Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates

Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates

Comparative analysis reveals the long-term co-evolutionary history of parvoviruses and vertebrates

A novel approach to exploring the dark genome and its application to mapping of the vertebrate virus ‘fossil record’

Contact Info

Product

Resources

About