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Dr. Joana Abrantes
Research Centre in Biodiversity and Genetic Resources (CIBIO), Research Network in Biodiversity and Evolutionary Biology (InBIO), University of Porto, Portugal; Department of Biology, Faculty of Sciences, University of Porto, Porto, Portugal

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0 Immunogenetics
0 Virus Evolution
0 RNA viruses
0 Rabbit hemorrhagic disease virus
0 Virus recombination

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Rabbit hemorrhagic disease virus
Species jump
Virus Evolution
RNA viruses

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Review
Published: 30 April 2021 in Microorganisms
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Since the early 1980s, the European rabbit (Oryctolagus cuniculus) has been threatened by the rabbit hemorrhagic disease (RHD). The disease is caused by a lagovirus of the family Caliciviridae, the rabbit hemorrhagic disease virus (RHDV). The need for detection, identification and further characterization of RHDV led to the development of several diagnostic tests. Owing to the lack of an appropriate cell culture system for in vitro propagation of the virus, much of the methods involved in these tests contributed to our current knowledge on RHD and RHDV and to the development of vaccines to contain the disease. Here, we provide a comprehensive review of the RHDV diagnostic tests used since the first RHD outbreak and that include molecular, histological and serological techniques, ranging from simpler tests initially used, such as the hemagglutination test, to the more recent and sophisticated high-throughput sequencing, along with an overview of their potential and their limitations.

ACS Style

Joana Abrantes; Ana Lopes. A Review on the Methods Used for the Detection and Diagnosis of Rabbit Hemorrhagic Disease Virus (RHDV). Microorganisms 2021, 9, 972 .

AMA Style

Joana Abrantes, Ana Lopes. A Review on the Methods Used for the Detection and Diagnosis of Rabbit Hemorrhagic Disease Virus (RHDV). Microorganisms. 2021; 9 (5):972.

Chicago/Turabian Style

Joana Abrantes; Ana Lopes. 2021. "A Review on the Methods Used for the Detection and Diagnosis of Rabbit Hemorrhagic Disease Virus (RHDV)." Microorganisms 9, no. 5: 972.

Short communication
Published: 04 February 2021 in Molecular Immunology
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Guanylate binding proteins (GBPs) are major players in the host immunity, providing defense against bacterial and viral invaders. Multigene families may suffer different processes of evolution. Gene families related to the immune system usually follow the birth-and-death evolution process, where duplicated genes can be deleted, gain new functions or become non-functional. We analyzed publicly available primate GBP sequences and their genomic organization and observed that GBP7 genes appear to have emerged from a duplication of GBP4 and seem to be only present in primates. Furthermore, GBP3 genes are only present in Simiiformes and probably originated from GBP1 genes. Finally, a duplication event occurred in the GBP6 in Tarsiiformes and became functional which might also explain the duplication of GBP6 in New World monkeys and Cercopithecidae. Taken together, this study provides new knowledge on the evolution of GBPs in primates and suggests that a revision of the GBPs nomenclature is necessary.

ACS Style

João Vasco Côrte-Real; Hanna-Mari Baldauf; Joana Abrantes; Pedro José Esteves. Evolution of the guanylate binding protein (GBP) genes: Emergence of GBP7 genes in primates and further acquisition of a unique GBP3 gene in simians. Molecular Immunology 2021, 132, 79 -81.

AMA Style

João Vasco Côrte-Real, Hanna-Mari Baldauf, Joana Abrantes, Pedro José Esteves. Evolution of the guanylate binding protein (GBP) genes: Emergence of GBP7 genes in primates and further acquisition of a unique GBP3 gene in simians. Molecular Immunology. 2021; 132 ():79-81.

Chicago/Turabian Style

João Vasco Côrte-Real; Hanna-Mari Baldauf; Joana Abrantes; Pedro José Esteves. 2021. "Evolution of the guanylate binding protein (GBP) genes: Emergence of GBP7 genes in primates and further acquisition of a unique GBP3 gene in simians." Molecular Immunology 132, no. : 79-81.

Journal article
Published: 02 September 2020 in Scientific Reports
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Rabbit haemorrhagic disease is a viral disease that emerged in the 1980s and causes high mortality and morbidity in the European rabbit (Oryctolagus cuniculus). In 2010, a new genotype of the rabbit haemorrhagic disease virus emerged and replaced the former circulating Lagovirus europaeus/GI.1 strains. Several recombination events have been reported for the new genotype Lagovirus europaeus/GI.2, with pathogenic (variants GI.1a and GI.1b) and benign (genotype GI.4) strains that served as donors for the non-structural part while GI.2 composed the structural part; another recombination event has also been described at the p16/p23 junction involving GI.4 strains. In this study, we analysed new complete coding sequences of four benign GI.3 strains and four GI.2 strains. Phylogenetic and recombination detection analyses revealed that the first GI.2 strains, considered as non-recombinant, resulted from a recombination event between GI.3 and GI.2, with GI.3 as the major donor for the non-structural part and GI.2 for the structural part. Our results indicate that recombination contributed to the emergence, persistence and dissemination of GI.2 as a pathogenic form and that all described GI.2 strains so far are the product of recombination. This highlights the need to study full-genomic sequences of lagoviruses to understand their emergence and evolution.

ACS Style

Joana Abrantes; Clément Droillard; Ana M. Lopes; Evelyne Lemaitre; Pierrick Lucas; Yannick Blanchard; Stéphane Marchandeau; Pedro J. Esteves; Ghislaine Le Gall-Reculé. Recombination at the emergence of the pathogenic rabbit haemorrhagic disease virus Lagovirus europaeus/GI.2. Scientific Reports 2020, 10, 1 -11.

AMA Style

Joana Abrantes, Clément Droillard, Ana M. Lopes, Evelyne Lemaitre, Pierrick Lucas, Yannick Blanchard, Stéphane Marchandeau, Pedro J. Esteves, Ghislaine Le Gall-Reculé. Recombination at the emergence of the pathogenic rabbit haemorrhagic disease virus Lagovirus europaeus/GI.2. Scientific Reports. 2020; 10 (1):1-11.

Chicago/Turabian Style

Joana Abrantes; Clément Droillard; Ana M. Lopes; Evelyne Lemaitre; Pierrick Lucas; Yannick Blanchard; Stéphane Marchandeau; Pedro J. Esteves; Ghislaine Le Gall-Reculé. 2020. "Recombination at the emergence of the pathogenic rabbit haemorrhagic disease virus Lagovirus europaeus/GI.2." Scientific Reports 10, no. 1: 1-11.

Journal article
Published: 09 August 2020 in Genes
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Recombination is one of the major sources of genetic variation in viruses. RNA viruses, such as rabbit hemorrhagic disease virus (RHDV), are among the viruses with the highest recombination rates. Several recombination events have been described for RHDV, mostly as a consequence of their genomic architecture. Here, we undertook phylogenetic and recombination analyses of French and Swedish RHDV strains from 1994 to 2016 and uncovered a new intergenotypic recombination event. This event occurred in the late 1990s/early 2000s and involved nonpathogenic GI.3 strains as donors for the nonstructural part of the genome of these recombinants, while pathogenic GI.1d strains contributed to the structural part. These GI.3P–GI.1d recombinant strains did not entirely replace GI.1d (nonrecombinant) strains, but became the dominant strains in France and Sweden, likely due to a fitness advantage associated with this genomic architecture. GI.3P–GI.1d (P stands for polymerase) strains persisted until 2013 and 2016 in Sweden and France, respectively, and cocirculated with the new genotype GI.2 in France. Since strains from the first GI.2 outbreaks were GI.3P–GI.2, we hypothesize that GI.3P–GI.1d could be the parental strain. Our results confirm the outstanding recombination ability of RHDV and its importance in the evolution of lagoviruses, which was only revealed by studying complete genomic sequences.

ACS Style

Joana Abrantes; Ana M. Lopes; Evelyne Lemaitre; Harri Ahola; Fereshteh Banihashem; Clément Droillard; Stéphane Marchandeau; Pedro J. Esteves; Aleksija Neimanis; Ghislaine Le Gall-Reculé. Retrospective Analysis Shows That Most RHDV GI.1 Strains Circulating Since the Late 1990s in France and Sweden Were Recombinant GI.3P–GI.1d Strains. Genes 2020, 11, 910 .

AMA Style

Joana Abrantes, Ana M. Lopes, Evelyne Lemaitre, Harri Ahola, Fereshteh Banihashem, Clément Droillard, Stéphane Marchandeau, Pedro J. Esteves, Aleksija Neimanis, Ghislaine Le Gall-Reculé. Retrospective Analysis Shows That Most RHDV GI.1 Strains Circulating Since the Late 1990s in France and Sweden Were Recombinant GI.3P–GI.1d Strains. Genes. 2020; 11 (8):910.

Chicago/Turabian Style

Joana Abrantes; Ana M. Lopes; Evelyne Lemaitre; Harri Ahola; Fereshteh Banihashem; Clément Droillard; Stéphane Marchandeau; Pedro J. Esteves; Aleksija Neimanis; Ghislaine Le Gall-Reculé. 2020. "Retrospective Analysis Shows That Most RHDV GI.1 Strains Circulating Since the Late 1990s in France and Sweden Were Recombinant GI.3P–GI.1d Strains." Genes 11, no. 8: 910.

Letter
Published: 23 July 2020 in Science
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ACS Style

Carlos Rouco; Joana Abrantes; Miguel Delibes-Mateos. Lessons from viruses that affect lagomorphs. Science 2020, 369, 386 -386.

AMA Style

Carlos Rouco, Joana Abrantes, Miguel Delibes-Mateos. Lessons from viruses that affect lagomorphs. Science. 2020; 369 (6502):386-386.

Chicago/Turabian Style

Carlos Rouco; Joana Abrantes; Miguel Delibes-Mateos. 2020. "Lessons from viruses that affect lagomorphs." Science 369, no. 6502: 386-386.

Letter to the editors
Published: 29 June 2020 in Transboundary and Emerging Diseases
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An original article has recently been published in Transboundary and Emerging Diseases entitled “Absence of Hepatitis E virus circulation in wild rabbits (Oryctolagus cuniculus ) and Iberian hares (Lepus granatensis ) in Mediterranean ecosystems in Spain” by Caballero‐Gómez and others (https://doi.org/10.1111/tbed.13478; Caballero‐Gómez et al., 2020), to which we have some comments.

ACS Style

Ana M. Lopes; Joana Abrantes. Hepatitis E virus is likely circulating in wild rabbits from Iberian Peninsula. Transboundary and Emerging Diseases 2020, 1 .

AMA Style

Ana M. Lopes, Joana Abrantes. Hepatitis E virus is likely circulating in wild rabbits from Iberian Peninsula. Transboundary and Emerging Diseases. 2020; ():1.

Chicago/Turabian Style

Ana M. Lopes; Joana Abrantes. 2020. "Hepatitis E virus is likely circulating in wild rabbits from Iberian Peninsula." Transboundary and Emerging Diseases , no. : 1.

Rapid communication
Published: 17 May 2020 in Transboundary and Emerging Diseases
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Adenoviruses (AdV) are pathogens capable of infecting animals and humans leading to a wide spectrum of diseases. They have a widespread geographical dissemination and infect several species, including red squirrels (Sciurus vulgaris ). In the Iberian Peninsula, there are no reports of infection of red squirrels by AdV. In this study, we report for the first time the detection of squirrel AdV in a red squirrel trapped in central Portugal. The phylogenetic analysis shows that the sequences obtained for the hexon and the penton base genes were similar to the Korean squirrel AdV strain and strongly divergent from the strains present in red squirrels in Europe. These findings indicate the emergence of a new strain circulating in Europe and raise concerns regarding the conservation of the red squirrel.

ACS Style

João Vasco Côrte-Real; Ana Margarida Lopes; Hugo Rebelo; João Paulo Lopes; Francisco Amorim; Ricardo Pita; Jorge Correia; Pedro Melo; Pedro Beja; Pedro José Esteves; Joana Abrantes. Adenovirus emergence in a red squirrel ( Sciurus vulgaris ) in Iberian Peninsula. Transboundary and Emerging Diseases 2020, 67, 2300 -2306.

AMA Style

João Vasco Côrte-Real, Ana Margarida Lopes, Hugo Rebelo, João Paulo Lopes, Francisco Amorim, Ricardo Pita, Jorge Correia, Pedro Melo, Pedro Beja, Pedro José Esteves, Joana Abrantes. Adenovirus emergence in a red squirrel ( Sciurus vulgaris ) in Iberian Peninsula. Transboundary and Emerging Diseases. 2020; 67 (6):2300-2306.

Chicago/Turabian Style

João Vasco Côrte-Real; Ana Margarida Lopes; Hugo Rebelo; João Paulo Lopes; Francisco Amorim; Ricardo Pita; Jorge Correia; Pedro Melo; Pedro Beja; Pedro José Esteves; Joana Abrantes. 2020. "Adenovirus emergence in a red squirrel ( Sciurus vulgaris ) in Iberian Peninsula." Transboundary and Emerging Diseases 67, no. 6: 2300-2306.

Journal article
Published: 02 December 2019 in BMC Evolutionary Biology
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Background Toll-like receptors (TLRs) are the most widely studied innate immunity receptors responsible for recognition of invading pathogens. Among the TLR family, TLR5 is the only that senses and recognizes flagellin, the major protein of bacterial flagella. TLR5 has been reported to be under overall purifying selection in mammals, with a small proportion of codons under positive selection. However, the variation of substitution rates among major mammalian groups has been neglected. Here, we studied the evolution of TLR5 in mammals, comparing the substitution rates among groups. Results In this study we analysed the TLR5 substitution rates in Euungulata, Carnivora, Chiroptera, Primata, Rodentia and Lagomorpha, groups. For that, Tajima’s relative rate test, Bayesian inference of evolutionary rates and genetic distances were estimated with CODEML’s branch model and RELAX. The combined results showed that in the Lagomorpha, Rodentia, Carnivora and Chiroptera lineages TLR5 is evolving at a higher substitution rate. The RELAX analysis further suggested a significant relaxation of selective pressures for the Lagomorpha (K = 0.22,p < 0.01), Rodentia (K = 0.58,p < 0.01) and Chiroptera (K = 0.65,p < 0.01) lineages and for the Carnivora ancestral branches (K = 0.13,p < 0.01). Conclusions Our results show that the TLR5 substitution rate is not uniform among mammals. In fact, among the different mammal groups studied, the Lagomorpha, Rodentia, Carnivora and Chiroptera are evolving faster. This evolutionary pattern could be explained by 1) the acquisition of new functions of TLR5 in the groups with higher substitution rate, i.e. TLR5 neofunctionalization, 2) by the beginning of a TLR5 pseudogenization in these groups due to some redundancy between the TLRs genes, or 3) an arms race between TLR5 and species-specific parasites.

ACS Style

Ana Pinheiro; Ana Águeda-Pinto; José Melo-Ferreira; Fabiana Neves; Joana Abrantes; Pedro Esteves. Analysis of substitution rates showed that TLR5 is evolving at different rates among mammalian groups. BMC Evolutionary Biology 2019, 19, 1 -9.

AMA Style

Ana Pinheiro, Ana Águeda-Pinto, José Melo-Ferreira, Fabiana Neves, Joana Abrantes, Pedro Esteves. Analysis of substitution rates showed that TLR5 is evolving at different rates among mammalian groups. BMC Evolutionary Biology. 2019; 19 (1):1-9.

Chicago/Turabian Style

Ana Pinheiro; Ana Águeda-Pinto; José Melo-Ferreira; Fabiana Neves; Joana Abrantes; Pedro Esteves. 2019. "Analysis of substitution rates showed that TLR5 is evolving at different rates among mammalian groups." BMC Evolutionary Biology 19, no. 1: 1-9.

Original research article
Published: 29 May 2019 in Frontiers in Veterinary Science
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Trichomonas gallinae is a pathogen of conservation relevance, whose main maintenance hosts are Columbiformes, but spillover to avian predators has been described. The goal of this study was to characterize the epidemiology of Trichomonas spp. in a community of free-ranging domestic and wild Columbiformes and an endangered predator, Bonelli's eagle Aquila fasciata. We surveyed 253 live-captured Rock doves, 16 nestling Bonelli's eagles and 41 hunted Columbiformes. Oro-esophageal swabs were incubated in culture media and Trichomonas spp. isolated from Bonelli's eagle (6.3%, CI95 1.1-28.3), Turtle dove Streptopelia turtur (56.3%, CI95 39.3–71.8), Wood pigeon Columba palumbus (83.3%, CI95 43.7–97.0) and Rock dove Columba livia (68.4%, CI95 62.4–73.8). Infected Rock doves showed significantly poorer body condition than uninfected ones (p = 0.022). From a subset of 32 isolates, 18S and ITS1/5.8S/ITS2 rRNA genes were sequenced and Maximum-Likelihood trees inferred. Four ribotypes of Trichomonas spp. were identified. In this study area Trichomonas spp. seem to persist in a multi-host system involving several species of Columbiformes. Conservation actions aimed at increasing the availability of trophic resources for Bonelli's eagles through Rock dove restocking should consider the risk of pathogen transmission and of introduction of alien strains.

ACS Style

Nuno Santos; José Jambas; António Monteiro; Jorge Amaral; Nuno Martins; Javier Garcia; Ana Martinez Fernández; Kevin Tyler; Tereza Almeida; Joana Abrantes; Pedro Esteves. Trichomonas Infection in a Community of Free-Ranging Domestic and Wild Columbiformes and Bonelli's Eagle (Aquila fasciata). Frontiers in Veterinary Science 2019, 6, 1 .

AMA Style

Nuno Santos, José Jambas, António Monteiro, Jorge Amaral, Nuno Martins, Javier Garcia, Ana Martinez Fernández, Kevin Tyler, Tereza Almeida, Joana Abrantes, Pedro Esteves. Trichomonas Infection in a Community of Free-Ranging Domestic and Wild Columbiformes and Bonelli's Eagle (Aquila fasciata). Frontiers in Veterinary Science. 2019; 6 ():1.

Chicago/Turabian Style

Nuno Santos; José Jambas; António Monteiro; Jorge Amaral; Nuno Martins; Javier Garcia; Ana Martinez Fernández; Kevin Tyler; Tereza Almeida; Joana Abrantes; Pedro Esteves. 2019. "Trichomonas Infection in a Community of Free-Ranging Domestic and Wild Columbiformes and Bonelli's Eagle (Aquila fasciata)." Frontiers in Veterinary Science 6, no. : 1.

Short communication
Published: 29 March 2019 in Transboundary and Emerging Diseases
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We describe the extremely rapid worldwide spread of the Lagovirus europaeus/GI.2/RHDV2/b (henceforth GI.2), the causative infectious agent of the so-called 'novel' rabbit haemorrhagic disease of the European rabbit (Oryctolagus cuniculus). We tracked down all novel confirmed detections of GI.2 between May 2010 and November 2018 by carrying out a two-step in-depth review. We suggest that such spread would not have been possible without anthropogenic involvement. Our results also point out the importance of reviewing and adapting the protocols of virus detection and management in order to control, mitigate and contain properly, not only GI.2, but also new viruses that may emerge in the future.

ACS Style

Carlos Rouco; Juan Antonio Aguayo‐Adán; Simone Santoro; Joana Abrantes; Miguel Delibes‐Mateos. Worldwide rapid spread of the novel rabbit haemorrhagic disease virus (GI.2/RHDV2/b). Transboundary and Emerging Diseases 2019, 66, 1762 -1764.

AMA Style

Carlos Rouco, Juan Antonio Aguayo‐Adán, Simone Santoro, Joana Abrantes, Miguel Delibes‐Mateos. Worldwide rapid spread of the novel rabbit haemorrhagic disease virus (GI.2/RHDV2/b). Transboundary and Emerging Diseases. 2019; 66 (4):1762-1764.

Chicago/Turabian Style

Carlos Rouco; Juan Antonio Aguayo‐Adán; Simone Santoro; Joana Abrantes; Miguel Delibes‐Mateos. 2019. "Worldwide rapid spread of the novel rabbit haemorrhagic disease virus (GI.2/RHDV2/b)." Transboundary and Emerging Diseases 66, no. 4: 1762-1764.

Short communication
Published: 14 March 2019 in Immunogenetics
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Toll-like receptors (TLRs) are one of the first lines of defense against pathogens and are crucial for triggering an appropriate immune response. Among TLRs, TLR2 is functional in all vertebrates and has high ability in detecting bacterial and viral pathogen ligands. The mammals' phylogenetic tree of TLR2 showed longer branches for the Lagomorpha clade, raising the hypothesis that lagomorphs experienced an acceleration of the mutation rate. This hypothesis was confirmed by (i) Tajima's test of neutrality that revealed different evolutionary rates between lagomorphs and the remaining mammals with lagomorphs presenting higher nucleotide diversity; (ii) genetic distances were similar among lagomorphs and between lagomorphs and other mammals; and (iii) branch models reinforced the existence of an acceleration of the mutation rate in lagomorphs. These results suggest that the lagomorph TLR2 has been strongly involved in pathogen recognition, which probably caused a host-pathogen arms race that led to the observed acceleration of the mutation rate.

ACS Style

Fabiana Neves; Ana Águeda-Pinto; Ana Pinheiro; Joana Abrantes; Pedro J. Esteves. Strong selection of the TLR2 coding region among the Lagomorpha suggests an evolutionary history that differs from other mammals. Immunogenetics 2019, 71, 437 -443.

AMA Style

Fabiana Neves, Ana Águeda-Pinto, Ana Pinheiro, Joana Abrantes, Pedro J. Esteves. Strong selection of the TLR2 coding region among the Lagomorpha suggests an evolutionary history that differs from other mammals. Immunogenetics. 2019; 71 (5-6):437-443.

Chicago/Turabian Style

Fabiana Neves; Ana Águeda-Pinto; Ana Pinheiro; Joana Abrantes; Pedro J. Esteves. 2019. "Strong selection of the TLR2 coding region among the Lagomorpha suggests an evolutionary history that differs from other mammals." Immunogenetics 71, no. 5-6: 437-443.

Journal article
Published: 01 March 2019 in Virus Research
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RERV-H was first identified in human tissues and mistaken for a human exogenous retrovirus. However, the integration sites carried by this virus showed that it was instead a European rabbit (Oryctolagus cuniculus) endogenous retrovirus. The first clones retrieved from European rabbit samples represented defective proviruses, although estimation of proviral copy numbers found in the European rabbit genome ranged from hundreds to thousands. Screening for the presence of RERV-H showed the absence of the virus in two other lagomorphs, pika (Ochotona) and hares (Lepus), which diverged from rabbits about 35 and 12 million years ago, respectively. Using a PCR-based approach, samples of seven different Lagomorph genera were tested for the presence of RERV-H. It was possible to amplify a proviral fragment corresponding to RNaseH from Oryctolagus, Bunolagus and Pentalagus genomic samples. The amplification of proviral DNA in species other than Oryctolagus revealed that this virus was endogenized in their common ancestor, roughly 9 million years ago. Using the European rabbit genome sequence OryCun2.0, it was possible to find multiple copies spread throughout the genome and several complete proviral genomes were retrieved. Some copies contained full open reading frames for all viral components. The lack of a complete genome in the other Lagomorph species did not allow further analyses of the provirus, although more deleterious mutations were found in Bunolagus and Pentalagus than in Oryctolagus RNaseH-amplified sequences. To what extent RERV-H and other endogenous viruses might have had an impact on the rabbit genome and its immune system remains elusive.

ACS Style

Patrícia Pereira; Joana Abrantes; Hanna-Mari Baldauf; Pedro José Esteves. Evolutionary studies on the betaretrovirus RERV-H in the Leporidae family reveal an endogenization in the ancestor of Oryctolagus, Bunolagus and Pentalagus at 9 million years ago. Virus Research 2019, 262, 24 -29.

AMA Style

Patrícia Pereira, Joana Abrantes, Hanna-Mari Baldauf, Pedro José Esteves. Evolutionary studies on the betaretrovirus RERV-H in the Leporidae family reveal an endogenization in the ancestor of Oryctolagus, Bunolagus and Pentalagus at 9 million years ago. Virus Research. 2019; 262 ():24-29.

Chicago/Turabian Style

Patrícia Pereira; Joana Abrantes; Hanna-Mari Baldauf; Pedro José Esteves. 2019. "Evolutionary studies on the betaretrovirus RERV-H in the Leporidae family reveal an endogenization in the ancestor of Oryctolagus, Bunolagus and Pentalagus at 9 million years ago." Virus Research 262, no. : 24-29.

Journal article
Published: 20 February 2019 in BMC Evolutionary Biology
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The C-C motif chemokine ligand 16 (CCL16) is a potent pro-inflammatory chemokine and a chemoattractant for monocytes and lymphocytes. In normal plasma, it is present at high concentrations and elicits its effects on cells by interacting with cell surface chemokine receptors. In the European rabbit and in rodents such as mouse, rat and guinea pig, CCL16 was identified as a pseudogene, while in the thirteen-lined ground squirrel it appears to be potentially functional. To gain insight into the evolution of this gene in the superorder Glires (rodents and lagomorphs), we amplified the CCL16 gene from eleven Leporidae and seven Ochotonidae species. We compared our sequences with CCL16 sequences of twelve rodent species retrieved from public databases. The data show that for all leporid species studied CCL16 is a pseudogene. This is primarily due to mutations at the canonical Cys Cys motif, creating either premature stop codons, or disrupting amino acid replacements. In the Mexican cottontail, CCL16 is pseudogenized due to a frameshift deletion. Additionally, in the exon 1 (signal peptide), there are frameshift deletions present in all leporids studied. In contrast, in Ochotona species, CCL16 is potentially functional, except for an allele in Hoffmann’s pika. In rodents, CCL16 is functional in a number of species, but patterns of pseudogenization similar to those observed in lagomorphs also exist. Our results suggest that while functional in the Glires ancestor, CCL16 underwent pseudogenization in some species. This process occurred stochastically or in specific lineages at different moments in the evolution of Glires. These observations suggest that the CCL16 had different evolutionary constrains in the Glires group that could be associated with the CCL16 biological function.

ACS Style

Fabiana Neves; Joana Abrantes; Ana M. Lopes; Luciana A. Fusinatto; Maria J. Magalhães; Wessel Van Der Loo; Pedro J. Esteves. Evolution of CCL16 in Glires (Rodentia and Lagomorpha) shows an unusual random pseudogenization pattern. BMC Evolutionary Biology 2019, 19, 59 .

AMA Style

Fabiana Neves, Joana Abrantes, Ana M. Lopes, Luciana A. Fusinatto, Maria J. Magalhães, Wessel Van Der Loo, Pedro J. Esteves. Evolution of CCL16 in Glires (Rodentia and Lagomorpha) shows an unusual random pseudogenization pattern. BMC Evolutionary Biology. 2019; 19 (1):59.

Chicago/Turabian Style

Fabiana Neves; Joana Abrantes; Ana M. Lopes; Luciana A. Fusinatto; Maria J. Magalhães; Wessel Van Der Loo; Pedro J. Esteves. 2019. "Evolution of CCL16 in Glires (Rodentia and Lagomorpha) shows an unusual random pseudogenization pattern." BMC Evolutionary Biology 19, no. 1: 59.

Journal article
Published: 01 February 2019 in Journal of General Virology
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A first step towards the development of a human immunodeficiency virus (HIV) animal model has been the identification and surmounting of species-specific barriers encountered by HIV along its replication cycle in cells from small animals. Serine incorporator proteins 3 (SERINC3) and 5 (SERINC5) were recently identified as restriction factors that reduce HIV-1 infectivity. Here, we compared the antiviral activity of SERINC3 and SERINC5 among mice, rats and rabbits, and their susceptibility to viral counteraction to their human counterparts. In the absence of viral antagonists, rodent and lagomorph SERINC3 and SERINC5 displayed anti-HIV activity in a similar range to human controls. Vesicular stomatitis virus G protein (VSV-G) pseudotyped virions were considerably less sensitive to restriction by all SERINC3/5 orthologs. Interestingly, HIV-1 Nef, murine leukemia virus (MLV) GlycoGag and equine infectious anemia virus (EIAV) S2 counteracted the antiviral activity of all SERINC3/5 orthologs with similar efficiency. Our results demonstrate that the antiviral activity of SERINC3/5 proteins is conserved in rodents and rabbits, and can be overcome by all three previously reported viral antagonists.

ACS Style

Patrícia De Sousa-Pereira; Joana Abrantes; Stefan Bauernfried; Virginia Pierini; Pedro José Esteves; Oliver T. Keppler; Massimo Pizzato; Veit Hornung; Oliver T. Fackler; Hanna-Mari Baldauf. The antiviral activity of rodent and lagomorph SERINC3 and SERINC5 is counteracted by known viral antagonists. Journal of General Virology 2019, 100, 278 -288.

AMA Style

Patrícia De Sousa-Pereira, Joana Abrantes, Stefan Bauernfried, Virginia Pierini, Pedro José Esteves, Oliver T. Keppler, Massimo Pizzato, Veit Hornung, Oliver T. Fackler, Hanna-Mari Baldauf. The antiviral activity of rodent and lagomorph SERINC3 and SERINC5 is counteracted by known viral antagonists. Journal of General Virology. 2019; 100 (2):278-288.

Chicago/Turabian Style

Patrícia De Sousa-Pereira; Joana Abrantes; Stefan Bauernfried; Virginia Pierini; Pedro José Esteves; Oliver T. Keppler; Massimo Pizzato; Veit Hornung; Oliver T. Fackler; Hanna-Mari Baldauf. 2019. "The antiviral activity of rodent and lagomorph SERINC3 and SERINC5 is counteracted by known viral antagonists." Journal of General Virology 100, no. 2: 278-288.

Journal article
Published: 26 November 2018 in BMC Veterinary Research
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Prior to 2010, the lagoviruses that cause rabbit hemorrhagic disease (RHD) in European rabbits (Oryctolagus cuniculus) and European brown hare syndrome (EBHS) in hares (Lepus spp.) were generally genus-specific. However, in 2010, rabbit hemorrhagic disease virus 2 (RHDV2), also known as Lagovirus europaeus GI.2, emerged and had the distinguishing ability to cause disease in both rabbits and certain hare species. The mountain hare (Lepus timidus) is native to Sweden and is susceptible to European brown hare syndrome virus (EBHSV), also called Lagovirus europaeus GII.1. While most mountain hare populations are found on the mainland, isolated populations also exist on islands. Here we investigate a mortality event in mountain hares on the small island of Hallands Väderö where other leporid species, including rabbits, are absent. Post-mortem and microscopic examination of three mountain hare carcasses collected from early November 2016 to mid-March 2017 revealed acute hepatic necrosis consistent with pathogenic lagovirus infection. Using immunohistochemistry, lagoviral capsid antigen was visualized within lesions, both in hepatocytes and macrophages. Genotyping and immunotyping of the virus independently confirmed infection with L. europaeus GI.2, not GII.1. Phylogenetic analyses of the vp60 gene grouped mountain hare strains together with a rabbit strain from an outbreak of GI.2 in July 2016, collected approximately 50 km away on the mainland. This is the first documented infection of GI.2 in mountain hares and further expands the host range of GI.2. Lesions and tissue distribution mimic those of GII.1 in mountain hares. The virus was most likely initially introduced from a concurrent, large-scale GI.2 outbreak in rabbits on the adjacent mainland, providing another example of how readily this virus can spread. The mortality event in mountain hares lasted for at least 4.5 months in the absence of rabbits, which would have required virus circulation among mountain hares, environmental persistence and/or multiple introductions. This marks the fourth Lepus species that can succumb to GI.2 infection, suggesting that susceptibility to GI.2 may be common in Lepus species. Measures to minimize the spread of GI.2 to vulnerable Lepus populations therefore are prudent.

ACS Style

Aleksija S. Neimanis; Harri Ahola; Ulrika Larsson Pettersson; Ana M. Lopes; Joana Abrantes; Siamak Zohari; Pedro J. Esteves; Dolores Gavier-Widén. Overcoming species barriers: an outbreak of Lagovirus europaeus GI.2/RHDV2 in an isolated population of mountain hares (Lepus timidus). BMC Veterinary Research 2018, 14, 1 -12.

AMA Style

Aleksija S. Neimanis, Harri Ahola, Ulrika Larsson Pettersson, Ana M. Lopes, Joana Abrantes, Siamak Zohari, Pedro J. Esteves, Dolores Gavier-Widén. Overcoming species barriers: an outbreak of Lagovirus europaeus GI.2/RHDV2 in an isolated population of mountain hares (Lepus timidus). BMC Veterinary Research. 2018; 14 (1):1-12.

Chicago/Turabian Style

Aleksija S. Neimanis; Harri Ahola; Ulrika Larsson Pettersson; Ana M. Lopes; Joana Abrantes; Siamak Zohari; Pedro J. Esteves; Dolores Gavier-Widén. 2018. "Overcoming species barriers: an outbreak of Lagovirus europaeus GI.2/RHDV2 in an isolated population of mountain hares (Lepus timidus)." BMC Veterinary Research 14, no. 1: 1-12.

Brief report
Published: 04 October 2018 in Archives of Virology
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Rabbit hemorrhagic disease virus (RHDV) is highly lethal to the European rabbit (Oryctolagus cuniculus). It was first reported in 1984 in China, but in 2010, a new variant of the virus was detected (GI.2) in France. Several recombination events with pathogenic and non-pathogenic strains have been described. Here, we report the first sequences of RHDV in Africa, isolated from Moroccan rabbits, and these resemble GI.1b/GI.1b/GI.2 recombinants found in the Iberian Peninsula. Monitoring and characterization of strains from future outbreaks are advised to guarantee the success of current programs on small-rabbit production for poverty alleviation in African countries.

ACS Style

Ana M. Lopes; Carlos Rouco; Pedro J. Esteves; Joana Abrantes. GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa. Archives of Virology 2018, 164, 279 -283.

AMA Style

Ana M. Lopes, Carlos Rouco, Pedro J. Esteves, Joana Abrantes. GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa. Archives of Virology. 2018; 164 (1):279-283.

Chicago/Turabian Style

Ana M. Lopes; Carlos Rouco; Pedro J. Esteves; Joana Abrantes. 2018. "GI.1b/GI.1b/GI.2 recombinant rabbit hemorrhagic disease virus 2 (Lagovirus europaeus/GI.2) in Morocco, Africa." Archives of Virology 164, no. 1: 279-283.

Review article
Published: 22 May 2018 in Experimental & Molecular Medicine
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Studies using the European rabbit Oryctolagus cuniculus contributed to elucidating numerous fundamental aspects of antibody structure and diversification mechanisms and continue to be valuable for the development and testing of therapeutic humanized polyclonal and monoclonal antibodies. Additionally, during the last two decades, the use of the European rabbit as an animal model has been increasingly extended to many human diseases. This review documents the continuing wide utility of the rabbit as a reliable disease model for development of therapeutics and vaccines and studies of the cellular and molecular mechanisms underlying many human diseases. Examples include syphilis, tuberculosis, HIV-AIDS, acute hepatic failure and diseases caused by noroviruses, ocular herpes, and papillomaviruses. The use of rabbits for vaccine development studies, which began with Louis Pasteur’s rabies vaccine in 1881, continues today with targets that include the potentially blinding HSV-1 virus infection and HIV-AIDS. Additionally, two highly fatal viral diseases, rabbit hemorrhagic disease and myxomatosis, affect the European rabbit and provide unique models to understand co-evolution between a vertebrate host and viral pathogens. Rabbits offer a powerful complement to rodents as a model for studying human immunology, disease pathology, and responses to infectious disease. A review from Pedro Esteves at the University of Porto, Portugal, Rose Mage of the National Institute of Allergy and Infectious Disease, Bethesda, USA and colleagues highlights some of the areas of research where rabbits offer an edge over rats and mice. Rabbits have a particularly sophisticated adaptive immune system, which could provide useful insights into human biology and produce valuable research and clinical reagents. They are also excellent models for studying - infectious diseases such as syphilis and tuberculosis, which produce pathology that closely resembles that of human patients. Rabbit-specific infections such as myxomatosis are giving researchers insights into how pathogens and hosts can shape each other’s evolution.

ACS Style

Pedro J. Esteves; Joana Abrantes; Hanna-Mari Baldauf; Lbachir BenMohamed; Yuxing Chen; Neil Christensen; Javier González-Gallego; Lorenzo Giacani; Jiafen Hu; Gilla Kaplan; Oliver T. Keppler; Katherine L. Knight; Xiang-Peng Kong; Dennis K. Lanning; Jacques Le Pendu; Ana Lemos De Matos; Jia Liu; Shuying Liu; Ana Lopes; Shan Lu; Sheila Lukehart; Yukari C. Manabe; Fabiana Neves; Grant McFadden; Ruimin Pan; Xuwen Peng; Patrícia Pereira; Ana Pinheiro; Masmudur Rahman; Natalie Ruvoën-Clouet; Selvakumar Subbian; María Jesús Tuñón; Wessel Van Der Loo; Michael Vaine; Laura Via; Shixia Wang; Rose Mage. The wide utility of rabbits as models of human diseases. Experimental & Molecular Medicine 2018, 50, 1 -10.

AMA Style

Pedro J. Esteves, Joana Abrantes, Hanna-Mari Baldauf, Lbachir BenMohamed, Yuxing Chen, Neil Christensen, Javier González-Gallego, Lorenzo Giacani, Jiafen Hu, Gilla Kaplan, Oliver T. Keppler, Katherine L. Knight, Xiang-Peng Kong, Dennis K. Lanning, Jacques Le Pendu, Ana Lemos De Matos, Jia Liu, Shuying Liu, Ana Lopes, Shan Lu, Sheila Lukehart, Yukari C. Manabe, Fabiana Neves, Grant McFadden, Ruimin Pan, Xuwen Peng, Patrícia Pereira, Ana Pinheiro, Masmudur Rahman, Natalie Ruvoën-Clouet, Selvakumar Subbian, María Jesús Tuñón, Wessel Van Der Loo, Michael Vaine, Laura Via, Shixia Wang, Rose Mage. The wide utility of rabbits as models of human diseases. Experimental & Molecular Medicine. 2018; 50 (5):1-10.

Chicago/Turabian Style

Pedro J. Esteves; Joana Abrantes; Hanna-Mari Baldauf; Lbachir BenMohamed; Yuxing Chen; Neil Christensen; Javier González-Gallego; Lorenzo Giacani; Jiafen Hu; Gilla Kaplan; Oliver T. Keppler; Katherine L. Knight; Xiang-Peng Kong; Dennis K. Lanning; Jacques Le Pendu; Ana Lemos De Matos; Jia Liu; Shuying Liu; Ana Lopes; Shan Lu; Sheila Lukehart; Yukari C. Manabe; Fabiana Neves; Grant McFadden; Ruimin Pan; Xuwen Peng; Patrícia Pereira; Ana Pinheiro; Masmudur Rahman; Natalie Ruvoën-Clouet; Selvakumar Subbian; María Jesús Tuñón; Wessel Van Der Loo; Michael Vaine; Laura Via; Shixia Wang; Rose Mage. 2018. "The wide utility of rabbits as models of human diseases." Experimental & Molecular Medicine 50, no. 5: 1-10.

Journal article
Published: 15 February 2018 in Journal of Virology
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Rabbit hemorrhagic disease virus (RHDV) and European brown hare syndrome virus (EBHSV) are two lagoviruses from the family Caliciviridae that cause fatal diseases in two leporid genera, Oryctolagus and Lepus , respectively. In the last few years, several examples of host jumps of lagoviruses among leporids were recorded. In addition, a new pathogenic genotype of RHDV emerged, and many nonpathogenic strains of lagoviruses have been described. The molecular mechanisms behind host shifts and the emergence of virulence are unknown. Since RHDV uses glycans of the histo-blood group antigen type as attachment factors to initiate infection, we studied if glycan specificities of the new pathogenic RHDV genotype, nonpathogenic lagoviruses, and EBHSV potentially play a role in determining the host range and virulence of lagoviruses. We observed binding to A, B, or H antigens of the histo-blood group family for all strains known to primarily infect European rabbits ( Oryctolagus cuniculus ), which have recently been classified as GI strains. However, we could not explain the emergence of virulence, since similar glycan specificities were found in several pathogenic and nonpathogenic strains. In contrast, EBHSV, recently classified as GII.1, bound to terminal β-linked N -acetylglucosamine residues of O-glycans. Expression of these attachment factors in the upper respiratory and digestive tracts in three lagomorph species ( Oryctolagus cuniculus , Lepus europaeus , and Sylvilagus floridanus ) showed species-specific patterns regarding susceptibility to infection by these viruses, indicating that species-specific glycan expression is likely a major contributor to lagovirus host specificity and range. IMPORTANCE Lagoviruses constitute a genus of the family Caliciviridae comprising highly pathogenic viruses, RHDV and EBHSV, that infect rabbits and hares, respectively. Recently, nonpathogenic strains were discovered and new pathogenic strains have emerged. In addition, host jumps between lagomorphs have been observed. The mechanisms responsible for the emergence of pathogenicity and host species range are unknown. Previous studies showed that RHDV strains attach to glycans expressed in the upper respiratory and digestive tracts of rabbits, the likely portals of virus entry. Here, we studied the glycan-binding properties of novel pathogenic and nonpathogenic strains looking for a link between glycan binding and virulence or between glycan specificity and host range. We found that glycan binding did not correlate with virulence. However, expression of glycan motifs in the upper respiratory and digestive tracts of lagomorphs revealed species-specific patterns associated with the host ranges of the virus strains, suggesting that glycan diversity contributes to lagovirus host ranges.

ACS Style

Ana M. Lopes; Adrien Breiman; Mónica Lora; Béatrice Le Moullac-Vaidye; Oxana Galanina; Kristina Nyström; Stephane Marchandeau; Ghislaine Le Gall-Reculé; Tanja Strive; Aleksija Neimanis; Nicolai V. Bovin; Nathalie Ruvoën-Clouet; Pedro J. Esteves; Joana Abrantes; Jacques Le Pendu. Host-Specific Glycans Are Correlated with Susceptibility to Infection by Lagoviruses, but Not with Their Virulence. Journal of Virology 2018, 92, 1 .

AMA Style

Ana M. Lopes, Adrien Breiman, Mónica Lora, Béatrice Le Moullac-Vaidye, Oxana Galanina, Kristina Nyström, Stephane Marchandeau, Ghislaine Le Gall-Reculé, Tanja Strive, Aleksija Neimanis, Nicolai V. Bovin, Nathalie Ruvoën-Clouet, Pedro J. Esteves, Joana Abrantes, Jacques Le Pendu. Host-Specific Glycans Are Correlated with Susceptibility to Infection by Lagoviruses, but Not with Their Virulence. Journal of Virology. 2018; 92 (4):1.

Chicago/Turabian Style

Ana M. Lopes; Adrien Breiman; Mónica Lora; Béatrice Le Moullac-Vaidye; Oxana Galanina; Kristina Nyström; Stephane Marchandeau; Ghislaine Le Gall-Reculé; Tanja Strive; Aleksija Neimanis; Nicolai V. Bovin; Nathalie Ruvoën-Clouet; Pedro J. Esteves; Joana Abrantes; Jacques Le Pendu. 2018. "Host-Specific Glycans Are Correlated with Susceptibility to Infection by Lagoviruses, but Not with Their Virulence." Journal of Virology 92, no. 4: 1.

Original article
Published: 11 February 2018 in Transboundary and Emerging Diseases
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Rabbit haemorrhagic disease (RHD) is a viral disease that affects the European rabbit. RHD was detected in 1984 in China and rapidly disseminated worldwide causing a severe decline in wild rabbit populations. The aetiological agent, rabbit haemorrhagic disease virus (RHDV), is an RNA virus of the family Caliciviridae, genus Lagovirus. Pathogenic (G1‐G6 or variants GI.1a‐GI.1d) and non‐pathogenic strains (GI.4) have been characterized. In 2010, a new variant of RHDV, RHDV2/RHDVb/GI.2, was detected in France. GI.2 arrived to the Iberian Peninsula in 2011, and several recombination events were reported. Here, we sequenced full genomes of 19 samples collected in Portugal between 2014 and 2016. New GI.2 recombinant strains were detected, including triple recombinants. These recombinants possess a non‐structural protein p16 related to a non‐pathogenic strain. Evolutionary analyses were conducted on GI.2 VP60 sequences. Estimated time to the most recent common ancestor (tMRCA) suggests an emergence of GI.2 in July 2008, not distant from its first detection in 2010. This is the first study on GI.2 evolution and highlights the need of continued monitoring and characterization of complete genome sequences when studying lagoviruses’ evolution.

ACS Style

Diogo Silvério; Ana Lopes; José Melo-Ferreira; M. J. Magalhães; P. Monterroso; A. Serronha; E. Maio; Paulo Célio Alves; P. J. Esteves; J. Abrantes. Insights into the evolution of the new variant rabbit haemorrhagic disease virus (GI.2) and the identification of novel recombinant strains. Transboundary and Emerging Diseases 2018, 65, 983 -992.

AMA Style

Diogo Silvério, Ana Lopes, José Melo-Ferreira, M. J. Magalhães, P. Monterroso, A. Serronha, E. Maio, Paulo Célio Alves, P. J. Esteves, J. Abrantes. Insights into the evolution of the new variant rabbit haemorrhagic disease virus (GI.2) and the identification of novel recombinant strains. Transboundary and Emerging Diseases. 2018; 65 (4):983-992.

Chicago/Turabian Style

Diogo Silvério; Ana Lopes; José Melo-Ferreira; M. J. Magalhães; P. Monterroso; A. Serronha; E. Maio; Paulo Célio Alves; P. J. Esteves; J. Abrantes. 2018. "Insights into the evolution of the new variant rabbit haemorrhagic disease virus (GI.2) and the identification of novel recombinant strains." Transboundary and Emerging Diseases 65, no. 4: 983-992.

Article
Published: 18 November 2017 in Virus Genes
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A recent publication by Carvalho et al. in “Virus Genes” (June 2017) reported the presence of the new variant of rabbit hemorrhagic disease virus (RHDV2) in the two larger islands of the archipelago of Madeira. Based on the capsid protein sequence, the authors suggested that the high sequence identity, along with the short time spanning between outbreaks, points to dissemination from Porto Santo to Madeira. By including information of the full RHDV2 genome of strains from Azores, Madeira, and the Canary Islands, we confirm the results obtained by Carvalho et al., but further show that several subtypes of RHDV2 circulate in these islands: non-recombinant RHDV2 in the Canary Islands, G1/RHDV2 in Azores, Porto Santo and Madeira, and NP/RHDV2 also in Madeira. Here we conclude that RHDV2 has been independently introduced in these archipelagos, and that in Madeira at least two independent introductions must have occurred. We provide additional information on the dynamics of RHDV2 in the Macaronesian archipelagos of Azores, Madeira, and the Canary Islands and highlight the importance of analyzing RHDV2 complete genome.

ACS Style

Ana Lopes; Jose A Blanco-Aguiar; Aaron Martín-Alonso; Manuel Leitão; Pilar Foronda; Marco Mendes; David Afonso Rocha Gonçalves; Joana Abrantes; Pedro J. Esteves. Full genome sequences are key to disclose RHDV2 emergence in the Macaronesian islands. Virus Genes 2017, 54, 1 -4.

AMA Style

Ana Lopes, Jose A Blanco-Aguiar, Aaron Martín-Alonso, Manuel Leitão, Pilar Foronda, Marco Mendes, David Afonso Rocha Gonçalves, Joana Abrantes, Pedro J. Esteves. Full genome sequences are key to disclose RHDV2 emergence in the Macaronesian islands. Virus Genes. 2017; 54 (1):1-4.

Chicago/Turabian Style

Ana Lopes; Jose A Blanco-Aguiar; Aaron Martín-Alonso; Manuel Leitão; Pilar Foronda; Marco Mendes; David Afonso Rocha Gonçalves; Joana Abrantes; Pedro J. Esteves. 2017. "Full genome sequences are key to disclose RHDV2 emergence in the Macaronesian islands." Virus Genes 54, no. 1: 1-4.