Differential evolution of antigenic regions of porcine reproductive and respiratory syndrome virus 1 before and after vaccine introduction

Kwon, Taehyun; Yoo, Sang‐Jo; Lee, Dong Uk; Sunwoo, Sun Young; Je, Sang H.; Park, Jun Woo; Myung-Hyee, Kim; Park, Choi‐Kyu; Lyoo, Young S.

doi:10.1016/j.virusres.2018.11.004

Cited by 13 publications

(15 citation statements)

References 43 publications

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“…While the observational nature of our data makes causality of sub-lineage emergence difficult to assess, the findings of this study support hypothesis generation on processes that lead to the observed turnover in sub-lineages through time. Taken together, our results support the idea that PRRSV evolution and continued endemicity in the U.S. is characterized by multi-strain dynamics driven at least partly by immune-mediated interactions [23,53].…”

Section: Discussionsupporting

confidence: 85%

Phylogenetic Structure and Sequential Dominance of Sub-Lineages of PRRSV Type-2 Lineage 1 in the United States

et al. 2021

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The genetic diversity and frequent emergence of novel genetic variants of porcine reproductive and respiratory syndrome virus type-2 (PRRSV) hinders control efforts, yet drivers of macro-evolutionary patterns of PRRSV remain poorly documented. Utilizing a comprehensive database of >20,000 orf5 sequences, our objective was to classify variants according to the phylogenetic structure of PRRSV co-circulating in the U.S., quantify evolutionary dynamics of sub-lineage emergence, and describe potential antigenic differences among sub-lineages. We subdivided the most prevalent lineage (Lineage 1, accounting for approximately 60% of available sequences) into eight sub-lineages. Bayesian coalescent SkyGrid models were used to estimate each sub-lineage’s effective population size over time. We show that a new sub-lineage emerged every 1 to 4 years and that the time between emergence and peak population size was 4.5 years on average (range: 2–8 years). A pattern of sequential dominance of different sub-lineages was identified, with a new dominant sub-lineage replacing its predecessor approximately every 3 years. Consensus amino acid sequences for each sub-lineage differed in key GP5 sites related to host immunity, suggesting that sub-lineage turnover may be linked to immune-mediated competition. This has important implications for understanding drivers of genetic diversity and emergence of new PRRSV variants in the U.S.

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Section: Discussionsupporting

confidence: 85%

Phylogenetic Structure and Sequential Dominance of Sub-Lineages of PRRSV Type-2 Lineage 1 in the United States

et al. 2021

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“…For PRRSV, recent research demonstrates that antibodies can exert a strong selective pressure to viral pathogens by targeting specific viral sub-populations, while allowing for the establishment of other sub-populations (Wang, 2016). When comparing PRRSV genetic diversity before and after vaccine adoption in South Korea, PRRSV vaccination was suggested to increase viral genetic heterogeneity and the emergence of new glycosylation sites in viral populations (Kwon et al, 2019). However, the extent in which PRRSV immunity, whether from natural infection or vaccination, can potentially drive the evolution of the virus in the field remains largely unanswered.…”

Section: Discussionmentioning

confidence: 99%

Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus

et al. 2019

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Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) is the most important endemic pathogen in the U.S. swine industry. Despite control efforts involving improved biosecurity and different vaccination protocols, the virus continues to circulate and evolve. One of the foremost challenges in its control is high levels of genetic and antigenic diversity. Here, we quantify the co-circulation, emergence and sequential turnover of multiple PRRSV lineages in a single swine-producing region in the United States over a span of 9 years (2009–2017). By classifying over 4,000 PRRSV sequences (open-reading frame 5) into phylogenetic lineages and sub-lineages, we document the ongoing diversification and temporal dynamics of the PRRSV population, including the rapid emergence of a novel sub-lineage that appeared to be absent globally pre-2008. In addition, lineage 9 was the most prevalent lineage from 2009 to 2010, but its occurrence fell to 0.5% of all sequences identified per year after 2014, coinciding with the emergence or re-emergence of lineage 1 as the dominant lineage. The sequential dominance of different lineages, as well as three different sub-lineages within lineage 1, is consistent with the immune-mediated selection hypothesis for the sequential turnover in the dominant lineage. As host populations build immunity through natural infection or vaccination toward the most common variant, this dominant (sub-) lineage may be replaced by an emerging variant to which the population is more susceptible. An analysis of patterns of non- synonymous and synonymous mutations revealed evidence of positive selection on immunologically important regions of the genome, further supporting the potential that immune-mediated selection shapes the evolutionary and epidemiological dynamics for this virus. This has important implications for patterns of emergence and re-emergence of genetic variants of PRRSV that have negative impacts on the swine industry. Constant surveillance on PRRSV occurrence is crucial to a better understanding of the epidemiological and evolutionary dynamics of co-circulating viral lineages. Further studies utilizing whole genome sequencing and exploring the extent of cross-immunity between heterologous PRRS viruses could shed further light on PRRSV immunological response and aid in developing strategies that might be able to diminish disease impact.

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“…However, the origin and genetic characteristics of these novel lineages remain unclear due to the limited available whole-genome information, as only 12 PRRSV whole-genome sequences are available in the GenBank database. Furthermore, recent reports of recombinant strains in Korea indicate that ORF5 sequencing is no longer sufficient for the complete identification or classification of PRRSV isolates [ 21 , 47 , 61 , 66 ]. Thus, the purposes of this study were to establish a WGS method for retrieving PRRSV whole-genome sequences and to analyze the PRRSV genetic diversity in Korea at the whole-genome level.…”

Section: Discussionmentioning

confidence: 99%

“…2 b), which is consistent with previous studies [ 18 , 19 ]. As PRRSV1 continued to become increasingly prevalent and to impose an enormous economic burden in Korea, two PRRSV1 MLVs [Unistrain PRRS (Amervac) and Porcilis PRRS)] were introduced in Korea in 2014 [ 66 ]. A vaccine-like strain (subtype 1C) isolated in this study (strain JB15-E-M17-JB) shares > 99% nucleotide homology with the Unistrain PRRS or SHE strain at the whole-genome level (Fig.…”

Section: Discussionmentioning

confidence: 99%

Whole-genome sequencing and genetic characteristics of representative porcine reproductive and respiratory syndrome virus (PRRSV) isolates in Korea

Kim

Moon

Jeong

et al. 2022

Virol J

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Background Porcine reproductive and respiratory syndrome virus (PRRSV) is a macrophage-tropic arterivirus with extremely high genetic and pathogenic heterogeneity that causes significant economic losses in the swine industry worldwide. PRRSV can be divided into two species [PRRSV1 (European) and PRRSV2 (North American)] and is usually diagnosed and genetically differentiated into several lineages based on the ORF5 gene, which constitutes only 5% of the whole genome. This study was conducted to achieve nonselective amplification and whole-genome sequencing (WGS) based on a simplified sequence-independent, single-primer amplification (SISPA) technique with next-generation sequencing (NGS), and to genetically characterize Korean PRRSV field isolates at the whole genome level. Methods The SISPA-NGS method coupled with a bioinformatics pipeline was utilized to retrieve full length PRRSV genomes of 19 representative Korean PRRSV strains by de novo assembly. Phylogenetic analysis, analysis of the insertion and deletion (INDEL) pattern of nonstructural protein 2 (NSP2), and recombination analysis were conducted. Results Nineteen complete PRRSV genomes were obtained with a high depth of coverage by the SISPA-NGS method. Korean PRRSV1 belonged to the Korean-specific subtype 1A and vaccine-related subtype 1C lineages, showing no evidence of recombination and divergent genetic heterogeneity with conserved NSP2 deletion patterns. Among Korean PRRSV2 isolates, modified live vaccine (MLV)-related lineage 5 viruses, lineage 1 viruses, and nation-specific Korean lineages (KOR A, B and C) could be identified. The NSP2 deletion pattern of the Korean lineages was consistent with that of the MN-184 strain (lineage 1), which indicates the common ancestor and independent evolution of Korean lineages. Multiple recombination signals were detected from Korean-lineage strains isolated in the 2010s, suggesting natural interlineage recombination between circulating KOR C and MLV strains. Interestingly, the Korean strain GGYC45 was identified as a recombinant KOR C and MLV strain harboring the KOR B ORF5 gene and might be the ancestor of currently circulating KOR B strains. Additionally, two novel lineage 1 recombinants of NADC30-like and NADC34-like viruses were detected. Conclusion Genome-wide analysis of Korean PRRSV isolates retrieved by the SISPA-NGS method and de novo assembly, revealed complex evolution and recombination in the field. Therefore, continuous surveillance of PRRSV at the whole genome level should be conducted, and new vaccine strategies for more efficient control of the virus are needed.

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Differential evolution of antigenic regions of porcine reproductive and respiratory syndrome virus 1 before and after vaccine introduction

Cited by 13 publications

References 43 publications

Phylogenetic Structure and Sequential Dominance of Sub-Lineages of PRRSV Type-2 Lineage 1 in the United States

Phylogenetic Structure and Sequential Dominance of Sub-Lineages of PRRSV Type-2 Lineage 1 in the United States

Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus

Whole-genome sequencing and genetic characteristics of representative porcine reproductive and respiratory syndrome virus (PRRSV) isolates in Korea

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