Phylogenetic and Molecular Epidemiological Studies Reveal Evidence of Multiple Past Recombination Events between Infectious Laryngotracheitis Viruses

Lee, Sang‐Won; Devlin, Joanne M.; Markham, John; Noormohammadi, Amir H.; Browning, Glenn F.; Ficorilli, Nino; Hartley, Carol A.; Markham, Philip F.

doi:10.1371/journal.pone.0055121

Cited by 36 publications

(55 citation statements)

References 41 publications

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“…High‐throughput genome sequencing has provided evidence of recombination between strains in other herpesviruses, namely HSV‐2, VZV, Marek's disease virus, HSV‐1, pseudorabies virus, human cytomegalovirus and infectious laryngotracheitis virus (Hughes & Rivailler, 2007; Kolb, Larsen, Cuellar, & Brandt, 2015; Lee et al., 2013; Norberg et al., 2011, 2015; Sijmons et al., 2015; Szpara et al., 2014; Szpara, Tafuri, et al., 2011; Zell et al., 2012). In the present study, network analysis suggested that recombination has also occurred between EHV‐1 strains.…”

Section: Discussionmentioning

confidence: 99%

Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks

Bryant

Wilkie

Russell

et al. 2018

Transbound Emerg Dis

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SummaryEquine herpesvirus 1 (EHV‐1) causes respiratory disease, abortion, neonatal death and neurological disease in equines and is endemic in most countries. The viral factors that influence EHV‐1 disease severity are poorly understood, and this has hampered vaccine development. However, the N752D substitution in the viral DNA polymerase catalytic subunit has been shown statistically to be associated with neurological disease. This has given rise to the term “neuropathic strain,” even though strains lacking the polymorphism have been recovered from cases of neurological disease. To broaden understanding of EHV‐1 diversity in the field, 78 EHV‐1 strains isolated over a period of 35 years were sequenced. The great majority of isolates originated from the United Kingdom and included in the collection were low passage isolates from respiratory, abortigenic and neurological outbreaks. Phylogenetic analysis of regions spanning 80% of the genome showed that up to 13 viral clades have been circulating in the United Kingdom and that most of these are continuing to circulate. Abortion isolates grouped into nine clades, and neurological isolates grouped into five. Most neurological isolates had the N752D substitution, whereas most abortion isolates did not, although three of the neurological isolates from linked outbreaks had a different polymorphism. Finally, bioinformatic analysis suggested that recombination has occurred between EHV‐1 clades, between EHV‐1 and equine herpesvirus 4, and between EHV‐1 and equine herpesvirus 8.

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Section: Discussionmentioning

confidence: 99%

Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks

Bryant

Wilkie

Russell

et al. 2018

Transbound Emerg Dis

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“…Even with the unequal numbers of isolates from the different geographical regions, higher rates of recombination were detected within Australian isolates. Vaccine strains, including the Serva, A20, and SA2 strains, were frequently involved in recombination events among the Australian isolates (2,34). In contrast, vaccine strains did not typically feature in the recombination events detected in the U.S. strains, although the Laryngovac strain was identified as a minor parent in one recombination event and some field strains, such as 1874c5 and J2, were involved in recombination events (Table 4).…”

Section: Discussionmentioning

confidence: 99%

Genetic Diversity of Infectious Laryngotracheitis Virus duringIn VivoCoinfection Parallels Viral Replication and Arises from Recombination Hot Spots within the Genome

Loncoman

Hartley

Coppo

et al. 2017

Appl Environ Microbiol

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Recombination is a feature of many alphaherpesviruses that infect people and animals. Infectious laryngotracheitis virus (ILTV; Gallid alphaherpesvirus 1) causes respiratory disease in chickens, resulting in significant production losses in poultry industries worldwide. Natural (field) ILTV recombination is widespread, particularly recombination between attenuated ILTV vaccine strains to create virulent viruses. These virulent recombinants have had a major impact on animal health. Recently, the development of a single nucleotide polymorphism (SNP) genotyping assay for ILTV has helped to understand ILTV recombination in laboratory settings. In this study, we applied this SNP genotyping assay to further examine ILTV recombination in the natural host. Following coinoculation of specific-pathogen-free chickens, we examined the resultant progeny for evidence of viral recombination and characterized the diversity of the recombinants over time. The results showed that ILTV replication and recombination are closely related and that the recombinant viral progeny are most diverse 4 days after coinoculation, which is the peak of viral replication. Further, the locations of recombination breakpoints in a selection of the recombinant progeny, and in field isolates of ILTV from different geographical regions, were examined following full-genome sequencing and used to identify recombination hot spots in the ILTV genome.IMPORTANCE Alphaherpesviruses are common causes of disease in people and animals. Recombination enables genome diversification in many different species of alphaherpesviruses, which can lead to the evolution of higher levels of viral virulence. Using the alphaherpesvirus infectious laryngotracheitis virus (ILTV), we performed coinfections in the natural host (chickens) to demonstrate high levels of virus recombination. Higher levels of diversity in the recombinant progeny coincided with the highest levels of virus replication. In the recombinant progeny, and in field isolates, recombination occurred at greater frequency in recombination hot spot regions of the virus genome. Our results suggest that control measures that aim to limit viral replication could offer the potential to limit virus recombination and thus the evolution of virulence. The development and use of vaccines that are focused on limiting virus replication, rather than vaccines that are focused more on limiting clinical disease, may be indicated in order to better control disease.

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“…In many alphaherpesviruses, recombination is increasingly being recognized as an important mechanism that plays a major role in evolution of viruses with an otherwise stable DNA genome that have low rates of nucleotide substitution (Lee et al, 2013(Lee et al, , 2012Thiry et al, 2005). Recent advances in high-throughput sequencing of complete viral genomes have allowed natural (field) recombination to be studied in a number of different alphaherpesviruses affecting animals and humans, including herpes simplex virus 1 (HSV-1), varicella-zoster virus (VZV) and infectious laryngotracheitis virus (ILTV) (Kolb et al, 2013;Lee et al, 2013;Norberg et al, 2015Norberg et al, , 2006Peters et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…Recent advances in high-throughput sequencing of complete viral genomes have allowed natural (field) recombination to be studied in a number of different alphaherpesviruses affecting animals and humans, including herpes simplex virus 1 (HSV-1), varicella-zoster virus (VZV) and infectious laryngotracheitis virus (ILTV) (Kolb et al, 2013;Lee et al, 2013;Norberg et al, 2015Norberg et al, , 2006Peters et al, 2006). Such studies provide insights into virus evolution and also allow the risk of recombination to be assessed in the context of attenuated vaccine use.…”

Section: Introductionmentioning

confidence: 99%

Evidence of widespread natural recombination among field isolates of equine herpesvirus 4 but not among field isolates of equine herpesvirus 1

Vaz

Horsington

Hartley

et al. 2016

Journal of General Virology

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Recombination in alphaherpesviruses allows evolution to occur in viruses that have an otherwise stable DNA genome with a low rate of nucleotide substitution. High-throughput sequencing of complete viral genomes has recently allowed natural (field) recombination to be studied in a number of different alphaherpesviruses, however, such studies have not been applied to equine herpesvirus 1 (EHV-1) or equine herpesvirus 4 (EHV-4). These two equine alphaherpesviruses are genetically similar, but differ in their pathogenesis and epidemiology. Both cause economically significant disease in horse populations worldwide. This study used highthroughput sequencing to determine the full genome sequences of EHV-1 and EHV-4 isolates (11 and 14 isolates, respectively) from Australian or New Zealand horses. These sequences were then analysed and examined for evidence of recombination. Evidence of widespread recombination was detected in the genomes of the EHV-4 isolates. Only one potential recombination event was detected in the genomes of the EHV-1 isolates, even when the genomes from an additional 11 international EHV-1 isolates were analysed. The results from this study reveal another fundamental difference between the biology of EHV-1 and EHV-4. The results may also be used to help inform the future safe use of attenuated equine herpesvirus vaccines.

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Phylogenetic and Molecular Epidemiological Studies Reveal Evidence of Multiple Past Recombination Events between Infectious Laryngotracheitis Viruses

Cited by 36 publications

References 41 publications

Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks

Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks

Genetic Diversity of Infectious Laryngotracheitis Virus duringIn VivoCoinfection Parallels Viral Replication and Arises from Recombination Hot Spots within the Genome

Evidence of widespread natural recombination among field isolates of equine herpesvirus 4 but not among field isolates of equine herpesvirus 1

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