A Primitive Endogenous Lentivirus in a Colugo: Insights into the Early Evolution of Lentiviruses

Han, Guan-Zhu; Worobey, Michael

doi:10.1093/molbev/msu297

Cited by 22 publications

(23 citation statements)

References 28 publications

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“…Then the insertion times for the two complete ERVs are approximately 75 and 54.5 million years ago, respectively. However, these estimates should be taken with cautions [ 14 ], given that I am not sure whether LTRs evolve at a neutral manner and what the actual neutral rate for the elephant shark is. Nevertheless, these results suggest these retroviruses were infecting the elephant shark millions of years ago.…”

Section: Resultsmentioning

confidence: 99%

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Extensive retroviral diversity in shark

Han

2015

Retrovirology

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BackgroundRetroviruses infect a wide range of vertebrates. However, little is known about the diversity of retroviruses in basal vertebrates. Endogenous retrovirus (ERV) provides a valuable resource to study the ecology and evolution of retrovirus.FindingsI performed a genome-scale screening for ERVs in the elephant shark (Callorhinchus milii) and identified three complete or nearly complete ERVs and many short ERV fragments. I designate these retroviral elements “C. milli ERVs” (CmiERVs). Phylogenetic analysis shows that the CmiERVs form three distinct lineages. The genome invasions by these retroviruses are estimated to take place more than 50 million years ago.ConclusionsMy results reveal the extensive retroviral diversity in the elephant shark. Diverse retroviruses appear to have been associated with cartilaginous fishes for millions of years. These findings have important implications in understanding the diversity and evolution of retroviruses.Electronic supplementary materialThe online version of this article (doi:10.1186/s12977-015-0158-4) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

“…To date, only a limited number of exogenous/endogenous retroviruses have been identified in fishes [ 1 - 5 , 14 ]. My results reveal the unexpectedly extensive retroviral diversity of the elephant shark.…”

Section: Resultsmentioning

confidence: 99%

Extensive retroviral diversity in shark

Han

2015

Retrovirology

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“…The key role of GBP2 and GBP5 in the defense against invading pathogens is further highlighted by our finding that they prevent the activation of the envelope glycoprotein of HERV-K (HML-2). This ancient retrovirus integrated into the germ line multiple times between 35 and one million years ago ( 95 ), when also ERV9 entered the genome ( 53 , 83 , 84 ) and primate lentiviruses were already circulating ( 96 , 97 ). Notably, the LTR12 elements upstream of GBP2 and GBP5 are most likely the result of two independent integration events since the common GBP ancestor duplicated before the fixation of LTR12C repeats in primates ( 53 , 63 , 83 , 84 ).…”

Section: Discussionmentioning

confidence: 99%

HIV-1 infection activates endogenous retroviral promoters regulating antiviral gene expression

Badarinarayan

Shcherbakova

Langer

et al. 2020

Nucleic Acids Research

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Although endogenous retroviruses (ERVs) are known to harbor cis-regulatory elements, their role in modulating cellular immune responses remains poorly understood. Using an RNA-seq approach, we show that several members of the ERV9 lineage, particularly LTR12C elements, are activated upon HIV-1 infection of primary CD4+ T cells. Intriguingly, HIV-1-induced ERVs harboring transcription start sites are primarily found in the vicinity of immunity genes. For example, HIV-1 infection activates LTR12C elements upstream of the interferon-inducible genes GBP2 and GBP5 that encode for broad-spectrum antiviral factors. Reporter assays demonstrated that these LTR12C elements drive gene expression in primary CD4+ T cells. In line with this, HIV-1 infection triggered the expression of a unique GBP2 transcript variant by activating a cryptic transcription start site within LTR12C. Furthermore, stimulation with HIV-1-induced cytokines increased GBP2 and GBP5 expression in human cells, but not in macaque cells that naturally lack the GBP5 gene and the LTR12C element upstream of GBP2. Finally, our findings suggest that GBP2 and GBP5 have already been active against ancient viral pathogens as they suppress the maturation of the extinct retrovirus HERV-K (HML-2). In summary, our findings uncover how human cells can exploit remnants of once-infectious retroviruses to regulate antiviral gene expression.

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“…Based on their relationships with exogenous retroviruses, ERVs are roughly classified into three classes: class I ERVs are closely related to gammaretroviruses and epsilonretroviruses, class II ERVs are closely related to betaretroviruses, and class III ERVs are closely related to foamy viruses [ 3 , 7 ]. However, the ERV classification system has not been well designed and has many practical problems: i) the term “Class” ranks above the term “Family” in traditional taxonomy [ 3 , 7 ]; ii) the classification systems for exogenous retroviruses and ERVs were developed separately and have been poorly incorporated; iii) some ERVs arose from recent endogenization events and nest within the diversity of exogenous retroviruses, such as endogenous lentiviruses identified recently in mammals [ 8 – 11 ], thus those ERVs cannot be readily classified into a certain ERV class.…”

Section: Introductionmentioning

confidence: 99%

Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses

Zhao

Gong

et al. 2018

PLoS Pathog

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The deep history and early diversification of retroviruses remains elusive, largely because few retroviruses have been characterized in vertebrates other than mammals and birds. Endogenous retroviruses (ERVs) documented past retroviral infections and thus provide ‘molecular fossils’ for studying the deep history of retroviruses. Here we perform a comprehensive phylogenomic analysis of ERVs within the genomes of 92 non-avian/mammalian vertebrates, including 72 fishes, 4 amphibians, and 16 reptiles. We find that ERVs are present in all the genomes of jawed vertebrates, revealing the ubiquitous presence of ERVs in jawed vertebrates. We identify a total of >8,000 ERVs and reconstruct ~450 complete or partial ERV genomes, which dramatically expands the phylogenetic diversity of retroviruses and suggests that the diversity of exogenous retroviruses might be much underestimated in non-avian/mammalian vertebrates. Phylogenetic analyses show that retroviruses cluster into five major groups with different host distributions, providing important insights into the classification and diversification of retroviruses. Moreover, we find retroviruses mainly underwent frequent host switches in non-avian/mammalian vertebrates, with exception of spumavirus-related viruses that codiverged with their ray-finned fish hosts. Interestingly, ray-finned fishes and turtles appear to serve as unappreciated hubs for the transmission of retroviruses. Finally, we find retroviruses underwent many independent water-land transmissions, indicating the water-land interface is not a strict barrier for retrovirus transmission. Our analyses provide unprecedented insights into and valuable resources for studying the diversification, key evolutionary transitions, and macroevolution of retroviruses.

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A Primitive Endogenous Lentivirus in a Colugo: Insights into the Early Evolution of Lentiviruses

Cited by 22 publications

References 28 publications

Extensive retroviral diversity in shark

Extensive retroviral diversity in shark

HIV-1 infection activates endogenous retroviral promoters regulating antiviral gene expression

Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses

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