A novel Australian flying-fox retrovirus shares an evolutionary ancestor with Koala, Gibbon and Melomys gamma-retroviruses

McMichael, Lee; Smith, Craig S.; Gordon, Anita N.; Agnihotri, Kalpana; Meers, J.; Oakey, Jane

doi:10.1007/s11262-019-01653-3

Cited by 17 publications

(19 citation statements)

References 18 publications

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“…Thus, given that HPGspecific sequences have been identified across several bat species, HPG is either an exogenous virus or is undergoing endogenization in real time. A possible example of the latter is FFRV1 (14), which was recently discovered in the brain tissue of a P. alecto bat but has not been identified within the genome of P. alecto or other bats. Serologic and nucleic acid analyses revealed that numerous individual bats across several species had been exposed to HPG and HPG-related viruses (SI Appendix, Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In particular, the habitat of such bats as the black flying fox, Pteropus alecto, overlap and connect the habitats of both gibbons and koalas, with bats being capable of traversing the bodies of water that separate the islands of Australia and Southeast Asia (22). In addition, bat gammaretroviral ERVs are widely distributed across the broader gammaretroviral phylogeny (23), with one recently discovered bat gammaretroviral ERV reportedly falling between KoRV and GALV on phylogenetic trees (14).…”

Section: Significancementioning

confidence: 99%

“…2) and "specific" primers designed to amplify only HPG (SI Appendix, Table S3). Notably, the HPG-specific forward primer binds to a site that is not present (i.e., lost through a deletion event) within the closely related ERV FFRV1 (14) and contains multiple nucleotide differences at the 3′ end of the primer compared with MmGRV and SaGRV. We first performed the RT-qPCR assay in such a way that both DNA and RNA would be amplified.…”

Section: Australian Bats Have Been Exposed To Hpg and Closely Relatedmentioning

confidence: 99%

“…Bats are reservoirs for many viruses from diverse viral families and are implicated in the transmission of numerous highly pathogenic viruses to humans and other mammals (10). Previous studies have revealed the presence of ERVs from the genera Betaretrovirus, Gammaretrovirus, and Deltaretrovirus within the genomes of bats (11)(12)(13)(14). Analyses of the evolutionary relationships between these bat ERVs and those from other mammals imply that bats have played a key role in the transmission of retroviruses between different mammalian species (15,16).…”

mentioning

confidence: 99%

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Infectious KoRV-related retroviruses circulating in Australian bats

Hayward

Tachedjian

Kohl

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Bats are reservoirs of emerging viruses that are highly pathogenic to other mammals, including humans. Despite the diversity and abundance of bat viruses, to date they have not been shown to harbor exogenous retroviruses. Here we report the discovery and characterization of a group of koala retrovirus-related (KoRV-related) gammaretroviruses in Australian and Asian bats. These include the Hervey pteropid gammaretrovirus (HPG), identified in the scat of the Australian black flying fox (Pteropus alecto), which is the first reproduction-competent retrovirus found in bats. HPG is a close relative of KoRV and the gibbon ape leukemia virus (GALV), with virion morphology and Mn2+-dependent virion-associated reverse transcriptase activity typical of a gammaretrovirus. In vitro, HPG is capable of infecting bat and human cells, but not mouse cells, and displays a similar pattern of cell tropism as KoRV-A and GALV. Population studies reveal the presence of HPG and KoRV-related sequences in several locations across northeast Australia, as well as serologic evidence for HPG in multiple pteropid bat species, while phylogenetic analysis places these bat viruses as the basal group within the KoRV-related retroviruses. Taken together, these results reveal bats to be important reservoirs of exogenous KoRV-related gammaretroviruses.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Section: Australian Bats Have Been Exposed To Hpg and Closely Relatedmentioning

confidence: 99%

mentioning

confidence: 99%

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Infectious KoRV-related retroviruses circulating in Australian bats

Hayward

Tachedjian

Kohl

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Retroviruses are RNA viruses that perform reverse transcription of their plus-sense RNA genomes and insert the resulting double-stranded cDNA into a host chromosome. Bat genomes contain endogenous retroviruses (ERVs) from the Betaretrovirus , Gammaretrovirus , and Deltaretrovirus genera ( 25 – 28 ), and an exogenous gammaretrovirus has also been identified ( 29 ). Germline endogenization represents the outcome of presumably very rare integrations into gametes or gamete progenitor cells.…”

Section: Introductionmentioning

confidence: 99%

A Potent Postentry Restriction to Primate Lentiviruses in a Yinpterochiropteran Bat

Morrison

Miller

Crameri

et al. 2020

mBio

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Bats are primary reservoirs for multiple lethal human viruses, such as Ebola, Nipah, Hendra, rabies, severe acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory syndrome-related coronavirus (MERS-CoV), and, most recently, SARS-CoV-2. The innate immune systems of these immensely abundant, anciently diverged mammals remain insufficiently characterized. While bat genomes contain many endogenous retroviral elements indicative of past exogenous infections, little is known about restrictions to extant retroviruses. Here, we describe a major postentry restriction in cells of the yinpterochiropteran bat Pteropus alecto. Primate lentiviruses (HIV-1, SIVmac) were potently blocked at early life cycle steps, with up to 1,000-fold decreases in infectivity. The block was specific, because nonprimate lentiviruses such as equine infectious anemia virus and feline immunodeficiency virus were unimpaired, as were foamy retroviruses. Interspecies heterokaryons demonstrated a dominant block consistent with restriction of incoming viruses. Several features suggested potential TRIM5 (tripartite motif 5) or myxovirus resistance protein 2 (MX2) protein restriction, including postentry action, cyclosporine sensitivity, and reversal by capsid cyclophilin A (CypA) binding loop mutations. Viral nuclear import was significantly reduced, and this deficit was substantially rescued by cyclosporine treatment. However, saturation with HIV-1 virus-like particles did not relieve the restriction at all. P. alecto TRIM5 was inactive against HIV-1 although it blocked the gammaretrovirus N-tropic murine leukemia virus. Despite major divergence in a critical N-terminal motif required for human MX2 activity, P. alecto MX2 had anti-HIV activity. However, this did not quantitatively account for the restriction and was independent of and synergistic with an additional CypA-dependent restriction. These results reveal a novel, specific restriction to primate lentiviruses in the Pteropodidae and advance understanding of bat innate immunity. IMPORTANCE The COVID-19 pandemic suggests that bat innate immune systems are insufficiently characterized relative to the medical importance of these animals. Retroviruses, e.g., HIV-1, can be severe pathogens when they cross species barriers, and bat restrictions corresponding to retroviruses are comparatively unstudied. Here, we compared the abilities of retroviruses from three genera (Lentivirus, Gammaretrovirus, and Spumavirus) to infect cells of the large fruit-eating bat P. alecto and other mammals. We identified a major, specific postentry restriction to primate lentiviruses. HIV-1 and SIVmac are potently blocked at early life cycle steps, but nonprimate lentiviruses and foamy retroviruses are entirely unrestricted. Despite acting postentry and in a CypA-dependent manner with features reminiscent of antiretroviral factors from other mammals, this restriction was not saturable with virus-like particles and was independent of P. alecto TRIM5, TRIM21, TRIM22, TRIM34, and MX2. These results identify a novel restriction and highlight cyclophilin-capsid interactions as ancient species-specific determinants of retroviral infection.

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Koala retrovirus and neoplasia: correlation and underlying mechanisms

Tarlinton,

Greenwood

2024

Current Opinion in Virology

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A novel Australian flying-fox retrovirus shares an evolutionary ancestor with Koala, Gibbon and Melomys gamma-retroviruses

Cited by 17 publications

References 18 publications

Infectious KoRV-related retroviruses circulating in Australian bats

Infectious KoRV-related retroviruses circulating in Australian bats

A Potent Postentry Restriction to Primate Lentiviruses in a Yinpterochiropteran Bat

Koala retrovirus and neoplasia: correlation and underlying mechanisms

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