Origin and recent expansion of an endogenous gammaretroviral lineage in domestic and wild canids

Halo, Julia V.; Pendleton, Amanda L.; Jarosz, Abigail S.; Gifford, Robert J.; Day, Malika L.; Kidd, Jeffrey M.

doi:10.1186/s12977-019-0468-z

Cited by 12 publications

(35 citation statements)

References 111 publications

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“…Complementation is not uncommon between XRV and ERV [81, 82], is well established for murine Intracisternal A-type Particle (IAP) [83] and has been reported for ERV expansion in canids [84]. Complementation requires that two different retroviruses are co-expressed in the same cell [85].…”

Section: Discussionmentioning

confidence: 99%

“…However, because we have evidence for recent expansion of Lineage A and B recombinants, we considered an alternative explanation; that env -deficient Lineage B CrERV was complemented with an intact Lineage A CrERV envelope glycoprotein allowing for germline infection. Complementation is not uncommon between XRV and ERV (Hanafusa 1965; Evans et al 2009), is well established for murine Intracisternal A-type Particle (IAP) (Dewannieux et al 2004) and has been reported for ERV expansion in canids (Halo et al 2019). Complementation requires that two different retroviruses are co-expressed in the same cell (Ali et al 2016).…”

Section: Discussionmentioning

confidence: 99%

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Recombination marks the evolutionary dynamics of a recently endogenized retrovirus

Yang

Malhotra

Chikhi

et al. 2021

Preprint

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Background: All vertebrate genomes have been colonized by retroviruses along their evolutionary trajectory. Although it is clear that endogenous retroviruses (ERVs) can contribute important physiological functions to contemporary hosts, such benefits are attributed to long-term co-evolution of ERV and host. Newly colonized ERVs are thought unlikely to contribute to host genome evolution because germline infections are rare and because the host effectively silences them. The genomes of several outbred species including mule deer (Odocoileus hemionus) are currently being colonized by ERVs, which provides an opportunity to study ERV dynamics at a time when few are fixed. Here we investigate the history of cervid endogenous retrovirus (CrERV) acquisition and expansion in the mule deer genome to determine the potential impact of endogenizing retroviruses on host genomic diversity. Methods: A mule deer genome was de novo assembled from short and long insert mate pair reads. Scaffolds were further assembled using reference assisted chromosome assembly (RACA) to provide spatial orientation of CrERV insertion sites and to facilitate assembly of CrERV sequences. We applied phylogenetic and coalescent approaches to non-recombinant genomes to determine CrERV evolutionary history, augmenting ancestral divergence estimates with the prevalence of each CrERV locus in a population of mule deer. Recombination history was investigated on partial genome alignments. Results: The CrERV composition and diversity in the mule deer genome has recently measurably increased by horizontal acquisition of a new retroviruses lineage and because of recombination with existing CrERV. Resulting interlineage recombinants also endogenized and subsequently retrotransposed. CrERV loci are significantly closer to genes than expected if integration were random and gene proximity might explain the recent expansion by retrotransposition of one recombinant CrERV lineage. Conclusions: There has been a burst of CrERV integrations during a recent retrovirus epizootic that increased genomic CrERV burden and has resulted in extensive insertional polymorphism in contemporary mule deer genomes. Recombination is a defining feature of CrERV evolutionary dynamics driven by this colonization, increasing CrERV burden and CrERV genetic diversity. These data support that retroviral colonization during an epizootic provides a burst of genomic diversity to the host population.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Recombination marks the evolutionary dynamics of a recently endogenized retrovirus

Yang

Malhotra

Chikhi

et al. 2021

Preprint

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“…In cats infected by FeLV, a recombination between endogenous and exogenous viruses can generate strains with specific pathogenic capabilities (45). The canine genome displays only a low percentage (∼0.15%) of ERVs compared to other mammals (46,47), and this is mainly related to a low number of repetitive elements in the genome (48). Despite hematological malignancies are frequent in dogs, and retroviral particles have been reported both in lymphomas and cell lines (49,50), no exogenous retroviruses have been identified in dogs or any other canid so far.…”

Section: Discussionmentioning

confidence: 99%

“…The lack of exogenous retroviruses and the low number of ERVs are quite surprising mainly because canine cells are known to enable the replication of noncanid exogenous retroviruses, and the canine genome lacks the functional retroviral restriction factor TRIM5α (51). Recent studies have proposed that the expansion of an endogenous gammaretroviral lineage might originate from an infection in canid ancestors, thereby supporting the potential existence of canine exogenous retroviruses (46,52). Further studies are needed to confirm these findings.…”

Section: Discussionmentioning

confidence: 99%

A First NGS Investigation Suggests No Association Between Viruses and Canine Cancers

Giannuzzi

Aresu

2020

Front. Vet. Sci.

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Approximately 10-15% of worldwide human cancers are attributable to viral infection. When operating as carcinogenic elements, viruses may act with various mechanisms, but the most important is represented by viral integration into the host genome, causing chromosome instability, genomic mutations, and aberrations. In canine species, few reports have described an association between viral integration and canine cancers, but more comprehensive studies are needed. The advancement of next-generation sequencing and the cost reduction have resulted in a progressive increasing of sequencing data in veterinary oncology offering an opportunity to study virome in canine cancers. In this study, we have performed viral detection and integration analyses using VirusFinder2 software tool on available whole-genome and whole-exome sequencing data of different canine cancers. Several viral sequences were detected in lymphomas, hemangiosarcomas, melanomas, and osteosarcomas, but no reliable integration sites were identified. Even if with some limitations such as the depth and type of sequencing, a restricted number of available nonhuman genomes software, and a limited knowledge on endogenous retroviruses in the canine genome, results are compelling. However, further experiments are needed, and similarly to feline species, dedicated analysis tools for the identification of viral integration sites in canine cancers are required.

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“…The de-novo assembled reads resulted in 1,721,922 contigs, of which more than 90% (1,559,773) matched with the Canis lupus familiaris genome (Genbank assembly accession: with study suggesting that most canine ERVs lineages ceased replicating long ago (35)(36)(37)(38)(39).…”

Section: Rna Extraction From Purified Microbial Aliquots and Sequencingmentioning

confidence: 99%

Living infectious agents with the same organic wall assembly of Precambrian early-life fossils discovered in Canine Transmissible Venereal Tumour and human cancer: Giant viruses or living protocells? Evaluating the effects of an anti-cancer vaccine in stray dogs, while challenging the mysteries around the RNA world

Lusi

Caicci

Cristarella

et al. 2020

Preprint

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BackgroundCanine Transmissible Venereal Tumour (CTVT) along with Tasmanian Devil Facial Tumour and transmissible leukaemia in Mya Arenaria soft shell-clams are the only examples of contagious cancers occurring in nature. In particular, CTVT is the oldest contagious cancer present in the wild world, emerged 11,000 years ago.The attempts to detect a transmissible virus as a causative agent in these form of contagious cancer proved conflicting and the current consensus view is that a transformed cell itself is transmitted and starts the tumor in a new animal, as a parasitic allograft. We modify this perception and report for the first time the isolation of an acutely transforming microbial infectious agent from CTVT.MethodsGiant viral particles were successfully isolated from CTVT specimens through a sucrose gradient, examined at electron microscopy, fully sequenced, used for transformation tests on NIH-3T3 cells and tumorigenic experiments in dogs.ResultsThe particles isolated from CTVT are giant viral particles with 1.17MB mega-genome. They transformed NIH-3T3 cells in vitro and initiated the typical CTVT lesions in a healthy dog, just one week post-infection. Only the fraction containing the giant viral particles were able to reproduce the tumour, while a filtered supernatant did not. This ruled out the presence of classic filterable viruses.ConclusionsWe discovered an infectious microbial agent, acutely transforming in CTVT. The agent shares some of the features that apply to giant Mimiviruses, such as the gigantic size and the presence of a mega-genome. However, distinct from environmental giant Mimiviruses, this mammalian microbial entity has a transforming nature and does not require amoeba co-culture. The biological characteristics depict this large agent halfway in between a classic oncogenic virus and a self-governing microbial cell-like entity.A practical application of this finding could be a new vaccination plan to control the spreading of this contagious cancer among dogs in endemic area as well as a new approach to save the Tasmanian devils that share the same cancer’s tale with stray dogs.Significance StatementThe discovery of this infectious large agent in CTVT in dogs not only modifies our current beliefs on the origin of transmissible cancer in the wild, but offers alternative anti-cancer strategies that aim to eradicate an entire microbe and its mega-genome, carrying hundreds of proteins. Unlike conventional oncoviruses with a small genome and one or two transforming proteins, these transforming microbial entities are more similar to a self-governing cell, a sort of cell–like entity specialized in carcinogenesis, halfway in between a classic oncogenic virus and an eukaryotic cancer cell.The awareness, resulting from this finding, that contagious cancers may be more widespread than previously thought, opens the door to a preventive cancer vaccine in humans and in the wild, leading to the development of strategies to target an entire shuttling system of oncogenes, all enclosed in a single infectious microbe, and not just a solitary protein involved in carcinogenesis.

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Origin and recent expansion of an endogenous gammaretroviral lineage in domestic and wild canids

Cited by 12 publications

References 111 publications

Recombination marks the evolutionary dynamics of a recently endogenized retrovirus

Recombination marks the evolutionary dynamics of a recently endogenized retrovirus

A First NGS Investigation Suggests No Association Between Viruses and Canine Cancers

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