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Special Issue "Spumaretroviruses"

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: 31 August 2019.

Special Issue Editors

Guest Editor
Dr. Arifa S. Khan

Center for Biologics Research and Evaluation, U. S. Food and Drug Administration, 10903 New Hampshire Ave, Bldg. 72–52, Room 1216, Silver Spring, Maryland, 20993-0002, USA
Website | E-Mail
Fax: +301 496 1810
Interests: retrovirus biology and genomics; in vitro models for virus-host interactions; SIV monkey models; viral vaccines; high-throughput sequencing; bioinformatics; novel virus discovery
Guest Editor
Prof. Dr. Dirk Lindemann

Institute of Virology, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
Website | E-Mail
Interests: virus—host interactions; molecular and cellular biology of retroviruses; development and application of retroviral vector systems
Guest Editor
Prof. Dr. Martin Löchelt

German Cancer Research Center (DKFZ), Research Program Infection, Inflammation and Cancer, Dept. Molecular Diagnostics of Oncogenic Infections (F020), Im Neuenheimer Feld 242, D-69120 Heidelberg, Germany
Website | E-Mail
Fax: +49 6221 42 4932
Interests: virus—host interactions; molecular and cellular biology of retroviruses in vitro and in vivo; foamy virus vector systems for gene delivery and antigen presentation; infection, inflammation, and cancer

Special Issue Information

Dear Colleagues,

Foamy Viruses (FVs) of the sub-family Spumaretrovirnae are unconventional retroviruses with several unique features in their replication that distinguish them from Orthoretrovirinae. Evolutionary studies revealed that FVs are the most ancient retroviruses, with endogenous elements present in species ranging from fish to mammals. Exogenous FVs circulate and co-speciate with their mammalian hosts such as non-human primates, bovines, equines, and felines, and inter-species infections can occur. Furthermore, cross-species infections may occur in humans through exposure to infected non-human primates. FV infections are considered apathogenic upon natural, experimental, or zoonotic transmission. This co-existence of FVs with their hosts and the potential of FVs as co-pathogens are topics of intense investigations, as well as the interactions of FVs with innate immunity and immune recognition and evasion.

FV molecular biology is unique and provides exciting insights into the breadth of retrovirus replication strategies. Additionally, FVs are an excellent model organism for retroviruses in general; in fact, the first atomic structure of the intasome complex containing full-length retroviral integrase was from a prototype FV and serves as a blueprint for corresponding investigations in other retroelements. Due to their apparent lack of pathogenicity and other features such as their broad tropism, FVs are engineered as novel vectors for gene therapy, vaccine antigen expression, and targeted protein and RNA transfer.

This Special Issue aims to provide new insights and a comprehensive overview of all aspects of FV biology including molecular and cellular biology, virus-host interactions, molecular evolution, epidemiology, structural biology, gene therapy vectors, and translational research. We cordially invite you to contribute original papers and review articles on these and related topics to highlight recent advances in spumaretrovirus research.

Dr. Arifa S. Khan
Prof. Dr. Dirk Lindemann
Prof. Dr. Martin Löchelt
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1800 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • spumaretroviruses
  • foamy viruses
  • complex retroviruses
  • ancient retroviruses
  • natural infections
  • zoonoses
  • foamy virus prevalence
  • nonhuman primates and non primates
  • foamy virus-host interactions
  • molecular biology and replication
  • viral proteins
  • restriction factors
  • virus detection assays
  • antivirals
  • foamy virus vectors

Published Papers (9 papers)

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Research

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Open AccessArticle
Feline Foamy Virus Infection: Characterization of Experimental Infection and Prevalence of Natural Infection in Domestic Cats with and without Chronic Kidney Disease
Viruses 2019, 11(7), 662; https://doi.org/10.3390/v11070662
Received: 25 June 2019 / Revised: 11 July 2019 / Accepted: 13 July 2019 / Published: 19 July 2019
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Abstract
Foamy viruses (FVs) are globally prevalent retroviruses that establish apparently apathogenic lifelong infections. Feline FV (FFV) has been isolated from domestic cats with concurrent diseases, including urinary syndromes. We experimentally infected five cats with FFV to study viral kinetics and tropism, peripheral blood [...] Read more.
Foamy viruses (FVs) are globally prevalent retroviruses that establish apparently apathogenic lifelong infections. Feline FV (FFV) has been isolated from domestic cats with concurrent diseases, including urinary syndromes. We experimentally infected five cats with FFV to study viral kinetics and tropism, peripheral blood mononuclear cell (PBMC) phenotype, urinary parameters, and histopathology. A persistent infection of primarily lymphoid tropism was detected with no evidence of immunological or hematologic perturbations. One cat with a significant negative correlation between lymphocytes and PBMC proviral load displayed an expanded FFV tissue tropism. Significantly increased blood urea nitrogen and ultrastructural kidney changes were noted in all experimentally infected cats, though chemistry parameters were not outside of normal ranges. Histopathological changes were observed in the brain, large intestine, and other tissues. In order to determine if there is an association of FFV with Chronic Kidney Disease, we additionally screened 125 Australian pet cats with and without CKD for FFV infection and found that FFV is highly prevalent in older cats, particularly in males with CKD, though this difference was not statistically significant compared to controls. Acute FFV infection was clinically silent, and while some measures indicated mild changes, there was no overt association of FFV infection with renal disease. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
The First Co-Opted Endogenous Foamy Viruses and the Evolutionary History of Reptilian Foamy Viruses
Viruses 2019, 11(7), 641; https://doi.org/10.3390/v11070641
Received: 9 May 2019 / Revised: 1 July 2019 / Accepted: 4 July 2019 / Published: 12 July 2019
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Abstract
A recent study reported the discovery of an endogenous reptilian foamy virus (FV), termed ERV-Spuma-Spu, found in the genome of tuatara. Here, we report two novel reptilian foamy viruses also identified as endogenous FVs (EFVs) in the genomes of panther gecko (ERV-Spuma-Ppi) and [...] Read more.
A recent study reported the discovery of an endogenous reptilian foamy virus (FV), termed ERV-Spuma-Spu, found in the genome of tuatara. Here, we report two novel reptilian foamy viruses also identified as endogenous FVs (EFVs) in the genomes of panther gecko (ERV-Spuma-Ppi) and Schlegel’s Japanese gecko (ERV-Spuma-Gja). Their presence indicates that FVs are capable of infecting reptiles in addition to mammals, amphibians, and fish. Numerous copies of full length ERV-Spuma-Spu elements were found in the tuatara genome littered with in-frame stop codons and transposable elements, suggesting that they are indeed endogenous and are not functional. ERV-Spuma-Ppi and ERV-Spuma-Gja, on the other hand, consist solely of a foamy virus-like env gene. Examination of host flanking sequences revealed that they are orthologous, and despite being more than 96 million years old, their env reading frames are fully coding competent with evidence for strong purifying selection to maintain expression and for them likely being transcriptionally active. These make them the oldest EFVs discovered thus far and the first documented EFVs that may have been co-opted for potential cellular functions. Phylogenetic analyses revealed a complex virus–host co-evolutionary history and cross-species transmission routes of ancient FVs. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
Isolation of an Equine Foamy Virus and Sero-Epidemiology of the Viral Infection in Horses in Japan
Viruses 2019, 11(7), 613; https://doi.org/10.3390/v11070613
Received: 10 June 2019 / Revised: 2 July 2019 / Accepted: 3 July 2019 / Published: 5 July 2019
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Abstract
An equine foamy virus (EFV) was isolated for the first time in Japan from peripheral blood mononuclear cells of a broodmare that showed wobbler syndrome after surgery for intestinal volvulus and the isolate was designated as EFVeca_LM. Complete nucleotide sequences of EFVeca_LM were [...] Read more.
An equine foamy virus (EFV) was isolated for the first time in Japan from peripheral blood mononuclear cells of a broodmare that showed wobbler syndrome after surgery for intestinal volvulus and the isolate was designated as EFVeca_LM. Complete nucleotide sequences of EFVeca_LM were determined. Nucleotide sequence analysis of the long terminal repeat (LTR) region, gag, pol, env, tas, and bel2 genes revealed that EFVeca_LM and the EFV reference strain had 97.2% to 99.1% identities. For a sero-epidemiological survey, indirect immunofluorescent antibody tests were carried out using EFVeca_LM-infected cells as an antigen against 166 sera of horses in five farms collected in 2001 to 2002 and 293 sera of horses in eight farms collected in 2014 to 2016 in Hokkaido, Japan. All of the farms had EFV antibody-positive horses, and average positive rates were 24.6% in sera obtained in 2001 to 2002 and 25.6% in sera obtained in 2014 to 2016 from broodmare farms. The positive rate in a stallion farm (Farm A) in 2002 was 10.7%, and the positive rates in two stallion farms, Farms A and B, in 2015 were 40.9% and 13.3%, respectively. The results suggested that EFV infection is maintained widely in horses in Japan. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
Molecular Analysis of the Complete Genome of a Simian Foamy Virus Infecting Hylobates pileatus (pileated gibbon) Reveals Ancient Co-Evolution with Lesser Apes
Viruses 2019, 11(7), 605; https://doi.org/10.3390/v11070605
Received: 1 April 2019 / Revised: 27 June 2019 / Accepted: 30 June 2019 / Published: 3 July 2019
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Abstract
Foamy viruses (FVs) are complex retroviruses present in many mammals, including nonhuman primates, where they are called simian foamy viruses (SFVs). SFVs can zoonotically infect humans, but very few complete SFV genomes are available, hampering the design of diagnostic assays. Gibbons are lesser [...] Read more.
Foamy viruses (FVs) are complex retroviruses present in many mammals, including nonhuman primates, where they are called simian foamy viruses (SFVs). SFVs can zoonotically infect humans, but very few complete SFV genomes are available, hampering the design of diagnostic assays. Gibbons are lesser apes widespread across Southeast Asia that can be infected with SFV, but only two partial SFV sequences are currently available. We used a metagenomics approach with next-generation sequencing of nucleic acid extracted from the cell culture of a blood specimen from a lesser ape, the pileated gibbon (Hylobates pileatus), to obtain the complete SFVhpi_SAM106 genome. We used Bayesian analysis to co-infer phylogenetic relationships and divergence dates. SFVhpi_SAM106 is ancestral to other ape SFVs with a divergence date of ~20.6 million years ago, reflecting ancient co-evolution of the host and SFVhpi_SAM106. Analysis of the complete SFVhpi_SAM106 genome shows that it has the same genetic architecture as other SFVs but has the longest recorded genome (13,885-nt) due to a longer long terminal repeat region (2,071 bp). The complete sequence of the SFVhpi_SAM106 genome fills an important knowledge gap in SFV genetics and will facilitate future studies of FV infection, transmission, and evolutionary history. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
Feline Foamy Virus is Highly Prevalent in Free-Ranging Puma concolor from Colorado, Florida and Southern California
Viruses 2019, 11(4), 359; https://doi.org/10.3390/v11040359
Received: 7 March 2019 / Revised: 15 April 2019 / Accepted: 17 April 2019 / Published: 19 April 2019
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Abstract
Feline foamy virus (FFV) is a retrovirus that has been detected in multiple feline species, including domestic cats (Felis catus) and pumas (Puma concolor). FFV results in persistent infection but is generally thought to be apathogenic. Sero-prevalence in domestic [...] Read more.
Feline foamy virus (FFV) is a retrovirus that has been detected in multiple feline species, including domestic cats (Felis catus) and pumas (Puma concolor). FFV results in persistent infection but is generally thought to be apathogenic. Sero-prevalence in domestic cat populations has been documented in several countries, but the extent of viral infections in nondomestic felids has not been reported. In this study, we screened sera from 348 individual pumas from Colorado, Southern California and Florida for FFV exposure by assessing sero-reactivity using an FFV anti-Gag ELISA. We documented a sero-prevalence of 78.6% across all sampled subpopulations, representing 69.1% in Southern California, 77.3% in Colorado, and 83.5% in Florida. Age was a significant risk factor for FFV infection when analyzing the combined populations. This high prevalence in geographically distinct populations reveals widespread exposure of puma to FFV and suggests efficient shedding and transmission in wild populations. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
The Influence of Envelope C-Terminus Amino Acid Composition on the Ratio of Cell-Free to Cell-Cell Transmission for Bovine Foamy Virus
Viruses 2019, 11(2), 130; https://doi.org/10.3390/v11020130
Received: 12 November 2018 / Revised: 26 January 2019 / Accepted: 29 January 2019 / Published: 31 January 2019
Cited by 1 | PDF Full-text (3499 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Foamy viruses (FVs) have extensive cell tropism in vitro, special replication features, and no clinical pathogenicity in naturally or experimentally infected animals, which distinguish them from orthoretroviruses. Among FVs, bovine foamy virus (BFV) has undetectable or extremely low levels of cell-free transmission in [...] Read more.
Foamy viruses (FVs) have extensive cell tropism in vitro, special replication features, and no clinical pathogenicity in naturally or experimentally infected animals, which distinguish them from orthoretroviruses. Among FVs, bovine foamy virus (BFV) has undetectable or extremely low levels of cell-free transmission in the supernatants of infected cells and mainly spreads by cell-to-cell transmission, which deters its use as a gene transfer vector. Here, using an in vitro virus evolution system, we successfully isolated high-titer cell-free BFV strains from the original cell-to-cell transmissible BFV3026 strain and further constructed an infectious cell-free BFV clone called pBS-BFV-Z1. Following sequence alignment with a cell-associated clone pBS-BFV-B, we identified a number of changes in the genome of pBS-BFV-Z1. Extensive mutagenesis analysis revealed that the C-terminus of envelope protein, especially the K898 residue, controls BFV cell-free transmission by enhancing cell-free virus entry but not the virus release capacity. Taken together, our data show the genetic determinants that regulate cell-to-cell and cell-free transmission of BFV. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Open AccessArticle
Clinical and Molecular Features of Feline Foamy Virus and Feline Leukemia Virus Co-Infection in Naturally-Infected Cats
Viruses 2018, 10(12), 702; https://doi.org/10.3390/v10120702
Received: 14 October 2018 / Revised: 6 December 2018 / Accepted: 7 December 2018 / Published: 11 December 2018
Cited by 3 | PDF Full-text (3248 KB) | HTML Full-text | XML Full-text
Abstract
Feline foamy virus (FFV) and feline leukemia virus (FeLV) belong to the Retroviridae family. While disease has not been reported for FFV infection, FeLV infection can cause anemia and immunosuppression (progressive infection). Co-infection with FFV/FeLV allows evaluation of the pathogenic potential and epidemiology [...] Read more.
Feline foamy virus (FFV) and feline leukemia virus (FeLV) belong to the Retroviridae family. While disease has not been reported for FFV infection, FeLV infection can cause anemia and immunosuppression (progressive infection). Co-infection with FFV/FeLV allows evaluation of the pathogenic potential and epidemiology of FFV infection in cats with FeLV pathology. Blood and buccal swab samples from 81 cats were collected in Rio de Janeiro. Plasma was serologically tested for FeLV. DNA extracted from peripheral blood mononuclear cells and buccal swabs was used to PCR detect FFV and FeLV. A qPCR was developed to detect and measure FFV proviral loads (pVLs) in cats. FeLV qPCR was performed using previous methods. The median log10 pVL of FFV mono-infected individuals was lower than found in FFV/FeLV co-infected cats in buccal swabs (p = 0.003). We found 78% of cats had detectable buccal FFV DNA in FFV mono-infected and FFV co-infected FeLV-progressive cats, while in FeLV-regressive cats (those without signs of disease) 22% of cats had detectable buccal FFV DNA (p = 0.004). Our results suggest that regressive FeLV infection may reduce FFV saliva transmission, the main mode of FV transmission. We did not find evidence of differences in pathogenicity in FFV mono- and -dually infected cats. In summary, we show that FVs may interact with FeLV within the same host. Our study supports the utility of cats naturally co-infected with retroviruses as a model to investigate the impact of FV on immunocompromised mammalian hosts. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Review

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Open AccessReview
Structural and Functional Aspects of Foamy Virus Protease-Reverse Transcriptase
Viruses 2019, 11(7), 598; https://doi.org/10.3390/v11070598
Received: 12 June 2019 / Revised: 28 June 2019 / Accepted: 29 June 2019 / Published: 2 July 2019
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Abstract
Reverse transcription describes the process of the transformation of single-stranded RNA into double-stranded DNA via an RNA/DNA duplex intermediate, and is catalyzed by the viral enzyme reverse transcriptase (RT). This event is a pivotal step in the life cycle of all retroviruses. In [...] Read more.
Reverse transcription describes the process of the transformation of single-stranded RNA into double-stranded DNA via an RNA/DNA duplex intermediate, and is catalyzed by the viral enzyme reverse transcriptase (RT). This event is a pivotal step in the life cycle of all retroviruses. In contrast to orthoretroviruses, the domain structure of the mature RT of foamy viruses is different, i.e., it harbors the protease (PR) domain at its N-terminus, thus being a PR-RT. This structural feature has consequences on PR activation, since the enzyme is monomeric in solution and retroviral PRs are only active as dimers. This review focuses on the structural and functional aspects of simian and prototype foamy virus reverse transcription and reverse transcriptase, as well as special features of reverse transcription that deviate from orthoretroviral processes, e.g., PR activation. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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Other

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Open AccessMeeting Report
Twelfth International Foamy Virus Conference—Meeting Report
Viruses 2019, 11(2), 134; https://doi.org/10.3390/v11020134
Received: 25 January 2019 / Accepted: 29 January 2019 / Published: 1 February 2019
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Abstract
The 12th International Foamy Virus Conference took place on 30–31 August 2018 at the Technische Universität Dresden, Dresden, Germany. The meeting included presentations on current research on non-human primate and non-primate foamy viruses (FVs; also called spumaretroviruses) as well as keynote talks on [...] Read more.
The 12th International Foamy Virus Conference took place on 30–31 August 2018 at the Technische Universität Dresden, Dresden, Germany. The meeting included presentations on current research on non-human primate and non-primate foamy viruses (FVs; also called spumaretroviruses) as well as keynote talks on related research areas in retroviruses. The taxonomy of foamy viruses was updated earlier this year to create five new genera in the subfamily, Spumaretrovirinae, based on their animal hosts. Research on viruses from different genera was presented on topics of potential relevance to human health, such as natural infections and cross-species transmission, replication, and viral-host interactions in particular with the immune system, dual retrovirus infections, virus structure and biology, and viral vectors for gene therapy. This article provides an overview of the current state-of-the-field, summarizes the meeting highlights, and presents some important questions that need to be addressed in the future. Full article
(This article belongs to the Special Issue Spumaretroviruses)
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