Identification of a Novel Subgroup of Koala Retrovirus from Koalas in Japanese Zoos

Shojima, Takayuki; Yoshikawa, Rokusuke; Hoshino, Shigeki; Shimode, Sayumi; Nakagawa, So; Ohata, Takuji; Nakaoka, Rie; Miyazawa, Takayuki

doi:10.1128/jvi.01385-13

Cited by 68 publications

(117 citation statements)

References 31 publications

(36 reference statements)

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“…In both cases it has been posited that these variants of KoRV are recently evolved strains that are exogenous (23,36,67). The concentration of selection in the env gene is consistent with analysis of historical koala KoRV-A derived sequences that suggest that the env gene is one of the few genes under longer-term selection, although weak (23,68).…”

Section: Discussionsupporting

confidence: 65%

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Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Alfano

Kolokotronis

Tsangaras

et al. 2016

J Virol

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Gibbon ape leukemia viruses (GALVs) are part of a larger group of pathogenic gammaretroviruses present across phylogenetically diverse host species of Australasian mammals. Despite the biomedical utility of GALVs as viral vectors and in cancer gene therapy, full genome sequences have not been determined for all of the five identified GALV strains, nor has a comprehensive evolutionary analysis been performed. We therefore generated complete genomic sequences for each GALV strain using hybridization capture and high-throughput sequencing. The four strains of GALV isolated from gibbons formed a monophyletic clade that was closely related to the woolly monkey virus (WMV), which is a GALV strain that likely originated in a gibbon host. The GALV-WMV clade in turn formed a sister group to the koala retroviruses (KoRVs). Genomic signatures of episodic diversifying selection were detected among the gammaretroviruses with concentration in the env gene across the GALV strains that were particularly oncogenic and KoRV strains that were potentially exogenous, likely reflecting their adaptation to the host immune system. In vitro studies involving vectors chimeric between GALV and KoRV-B established that variable regions A and B of the surface unit of the envelope determine which receptor is used by a viral strain to enter host cells. IMPORTANCEThe gibbon ape leukemia viruses (GALVs) are among the most medically relevant retroviruses due to their use as viral vectors for gene transfer and in cancer gene therapy. Despite their importance, full genome sequences have not been determined for the majority of primate isolates, nor has comprehensive evolutionary analysis been performed, despite evidence that the viruses are facing complex selective pressures associated with cross-species transmission. Using hybridization capture and high-throughput sequencing, we report here the full genome sequences of all the GALV strains and demonstrate that diversifying selection is acting on them, particularly in the envelope gene in functionally important domains, suggesting that host immune pressure is shaping GALV evolution. G ibbon ape leukemia virus (GALV) is an exogenous gammaretrovirus associated with hematopoietic neoplasms in captive colonies of white-handed gibbon (Hylobates lar). Five strains of GALV have been isolated from gibbons. The first was isolated from an animal with lymphocytic leukemia in a colony at the San Francisco Medical Center (strain SF) (1, 2). GALV was later isolated from gibbons displaying malignant tumors, notably an individual gibbon with granulocytic leukemia, at the Southeast Asia Treaty Organization Medical Research Laboratory in Bangkok, Thailand (strain SEATO) (3, 4), and another gibbon with lymphocytic leukemia from a colony on Hall's Island, near Bermuda (strain GALV-H) (5, 6). The Brain strain was isolated from two healthy gibbons injected with brain extracts from human patients with kuru and from an uninoculated cage mate (7). The SEATO strain has been shown to cause chronic myelogenous leukemia...

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Section: Discussionsupporting

confidence: 65%

“…The only KoRVs exhibiting episodic diversifying selection are those associated with greater pathogenicity and which have switched receptor usage from Pit-1 to THTR1 (36,67). In both cases it has been posited that these variants of KoRV are recently evolved strains that are exogenous (23,36,67).…”

Section: Discussionmentioning

confidence: 99%

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Alfano

Kolokotronis

Tsangaras

et al. 2016

J Virol

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“…The resulting melt curves from this qPCR, coupled with appropriate controls, can be used to distinguish detected Chlamydia species (Fig. S1, housekeeping gene b-actin was utilized to standardize genome copy numbers detected in each sample, as described previously (Shojima et al, 2013). Each sample was standardized based on the number of 16S rRNA copies per b-actin copies in the extracted liquid sample.…”

Section: Methodsmentioning

confidence: 99%

Identification of unusual Chlamydia pecorum genotypes in Victorian koalas (Phascolarctos cinereus) and clinical variables associated with infection

Legione

Patterson

Whiteley

et al. 2016

Journal of Medical Microbiology

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“…Five subtypes of KoRV, denoted KoRV-A, -B/J, -C, -D, and -E, have been reported to date; they differ primarily in sequences encoding the envelope protein, particularly within a hypervariable region of the receptor binding domain (RBD) (amino acids [aa] 91 to 135 [KoRV-A numbering]) (14,(16)(17)(18)(19)(20)(21). KoRV-A was first identified in wild and captive Australian koala populations (16) and is the most commonly identified subtype (6,14,18,20,(22)(23)(24).…”

mentioning

confidence: 99%

Phylogenetic Diversity of Koala Retrovirus within a Wild Koala Population

Chappell

Brealey

Amarilla

et al. 2017

J Virol

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Koala populations are in serious decline across many areas of mainland Australia, with infectious disease a contributing factor. Koala retrovirus (KoRV) is a gammaretrovirus present in most wild koala populations and captive colonies. Five subtypes of KoRV (A to E) have been identified based on amino acid sequence divergence in a hypervariable region of the receptor binding domain of the envelope protein. However, analysis of viral genetic diversity has been conducted primarily on KoRV in captive koalas housed in zoos in Japan, the United States, and Germany. Wild koalas within Australia have not been comparably assessed. Here we report a detailed analysis of KoRV genetic diversity in samples collected from 18 wild koalas from southeast Queensland. By employing deep sequencing we identified 108 novel KoRV envelope sequences and determined their phylogenetic diversity. Genetic diversity in KoRV was abundant and fell into three major groups; two comprised the previously identified subtypes A and B, while the third contained the remaining hypervariable region subtypes (C, D, and E) as well as four hypervariable region subtypes that we newly define here (F, G, H, and I). In addition to the ubiquitous presence of KoRV-A, which may represent an exclusively endogenous variant, subtypes B, D, and F were found to be at high prevalence, while subtypes G, H, and I were present in a smaller number of animals. IMPORTANCE Koala retrovirus (KoRV) is thought to be a significant contributor to koala disease and population decline across mainland Australia. This study is the first to determine KoRV subtype prevalence among a wild koala population, and it significantly expands the total number of KoRV sequences available, providing a more precise picture of genetic diversity. This understanding of KoRV subtype prevalence and genetic diversity will be important for conservation efforts attempting to limit the spread of KoRV. Furthermore, KoRV is one of the only retroviruses shown to exist in both endogenous (transmitted vertically to offspring in the germ line DNA) and exogenous (horizontally transmitted between infected individuals) forms, a division of fundamental evolutionary importance.

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Identification of a Novel Subgroup of Koala Retrovirus from Koalas in Japanese Zoos

Cited by 68 publications

References 31 publications

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Episodic Diversifying Selection Shaped the Genomes of Gibbon Ape Leukemia Virus and Related Gammaretroviruses

Identification of unusual Chlamydia pecorum genotypes in Victorian koalas (Phascolarctos cinereus) and clinical variables associated with infection

Phylogenetic Diversity of Koala Retrovirus within a Wild Koala Population

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