Molecular characteristics and pathogenic assessment of porcine epidemic diarrhoea virus isolates from the 2018 endemic outbreaks on Jeju Island, South Korea

Since the 2013–2014 incursion of the virulent G2b porcine epidemic diarrhoea virus (PEDV) pandemic strains in South Korea, frequent moderate‐scale regional outbreaks have recurred. In particular, areas of Jeju Island with extensive swine production have faced repeated epidemics since the re‐emergenc...

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Veröffentlicht in:Transboundary and emerging diseases 2019-09, Vol.66 (5), p.1894-1909
Hauptverfasser: Lee, Sunhee, Lee, Dong‐Uk, Noh, Yun‐Hee, Lee, Seung‐Chul, Choi, Hwan‐Won, Yang, Hyoung‐Seok, Seol, Jun‐Ho, Mun, Seong Hwan, Kang, Won‐Myoung, Yoo, Hyekyung, Lee, Changhee
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container_issue 5
container_start_page 1894
container_title Transboundary and emerging diseases
container_volume 66
creator Lee, Sunhee
Lee, Dong‐Uk
Noh, Yun‐Hee
Lee, Seung‐Chul
Choi, Hwan‐Won
Yang, Hyoung‐Seok
Seol, Jun‐Ho
Mun, Seong Hwan
Kang, Won‐Myoung
Yoo, Hyekyung
Lee, Changhee
description Since the 2013–2014 incursion of the virulent G2b porcine epidemic diarrhoea virus (PEDV) pandemic strains in South Korea, frequent moderate‐scale regional outbreaks have recurred. In particular, areas of Jeju Island with extensive swine production have faced repeated epidemics since the re‐emergence in 2014. The current study reports the complete genome sequences and molecular characterization of the representative PEDV strains responsible for the 2018 endemic outbreaks on Jeju Island. All isolates were determined to belong genetically to the highly pathogenic pandemic G2b group. Full‐length genome sizes of four isolates differed from that of the G2b epidemic field strain due to insertion or deletion (DEL) mutations in the non‐structural protein (nsp)‐ or spike (S) protein‐coding regions. The 2018 Jeju isolates shared 96.7%–98.7% and 98.5%–99.4% identity at the S gene and whole‐genome levels, respectively, compared to global G2b PEDV strains. Genetic and phylogenetic analyses indicated that the 2018 isolates were closest to the 2014 G2b re‐emergent Jeju strains, but appeared to have undergone substantial rapid independent evolution. Among the isolates, a notable nsp3 DEL variant strain, KOR/KNU‐1807/2018, was isolated and propagated by continuous passages in Vero cells, and displayed typical PEDV‐induced syncytia formation. Genomic sequencing identified a unique 8‐nt DEL in the extreme C‐terminal region of the S gene at the 4th passage (KNU‐1807‐P4) compared to its original sample. This DEL resulted in the premature termination of S by nine amino acid residues (EVFEKVHVQ), which contained a KxHxx motif that is a potential endoplasmic reticulum retrieval signal. In vivo animal studies showed that variant strain KNU‐1807 had decreased virulence in suckling piglets. These results advance our knowledge regarding the genetic variation and pathogenicity of the G2b PEDV endemic strains prevalent in Jeju swine herds in South Korea.
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In particular, areas of Jeju Island with extensive swine production have faced repeated epidemics since the re‐emergence in 2014. The current study reports the complete genome sequences and molecular characterization of the representative PEDV strains responsible for the 2018 endemic outbreaks on Jeju Island. All isolates were determined to belong genetically to the highly pathogenic pandemic G2b group. Full‐length genome sizes of four isolates differed from that of the G2b epidemic field strain due to insertion or deletion (DEL) mutations in the non‐structural protein (nsp)‐ or spike (S) protein‐coding regions. The 2018 Jeju isolates shared 96.7%–98.7% and 98.5%–99.4% identity at the S gene and whole‐genome levels, respectively, compared to global G2b PEDV strains. Genetic and phylogenetic analyses indicated that the 2018 isolates were closest to the 2014 G2b re‐emergent Jeju strains, but appeared to have undergone substantial rapid independent evolution. Among the isolates, a notable nsp3 DEL variant strain, KOR/KNU‐1807/2018, was isolated and propagated by continuous passages in Vero cells, and displayed typical PEDV‐induced syncytia formation. Genomic sequencing identified a unique 8‐nt DEL in the extreme C‐terminal region of the S gene at the 4th passage (KNU‐1807‐P4) compared to its original sample. This DEL resulted in the premature termination of S by nine amino acid residues (EVFEKVHVQ), which contained a KxHxx motif that is a potential endoplasmic reticulum retrieval signal. In vivo animal studies showed that variant strain KNU‐1807 had decreased virulence in suckling piglets. 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In particular, areas of Jeju Island with extensive swine production have faced repeated epidemics since the re‐emergence in 2014. The current study reports the complete genome sequences and molecular characterization of the representative PEDV strains responsible for the 2018 endemic outbreaks on Jeju Island. All isolates were determined to belong genetically to the highly pathogenic pandemic G2b group. Full‐length genome sizes of four isolates differed from that of the G2b epidemic field strain due to insertion or deletion (DEL) mutations in the non‐structural protein (nsp)‐ or spike (S) protein‐coding regions. The 2018 Jeju isolates shared 96.7%–98.7% and 98.5%–99.4% identity at the S gene and whole‐genome levels, respectively, compared to global G2b PEDV strains. Genetic and phylogenetic analyses indicated that the 2018 isolates were closest to the 2014 G2b re‐emergent Jeju strains, but appeared to have undergone substantial rapid independent evolution. Among the isolates, a notable nsp3 DEL variant strain, KOR/KNU‐1807/2018, was isolated and propagated by continuous passages in Vero cells, and displayed typical PEDV‐induced syncytia formation. Genomic sequencing identified a unique 8‐nt DEL in the extreme C‐terminal region of the S gene at the 4th passage (KNU‐1807‐P4) compared to its original sample. This DEL resulted in the premature termination of S by nine amino acid residues (EVFEKVHVQ), which contained a KxHxx motif that is a potential endoplasmic reticulum retrieval signal. In vivo animal studies showed that variant strain KNU‐1807 had decreased virulence in suckling piglets. These results advance our knowledge regarding the genetic variation and pathogenicity of the G2b PEDV endemic strains prevalent in Jeju swine herds in South Korea.</description><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Chlorocebus aethiops</subject><subject>Clonal deletion</subject><subject>Coronavirus Infections - veterinary</subject><subject>Coronavirus Infections - virology</subject><subject>Diarrhea</subject><subject>endemic outbreaks</subject><subject>Endoplasmic reticulum</subject><subject>Epidemics</subject><subject>Gene deletion</subject><subject>Gene sequencing</subject><subject>Genetic analysis</subject><subject>Genetic diversity</subject><subject>genome analysis</subject><subject>Genome, Viral - genetics</subject><subject>Genomes</subject><subject>In vivo methods and tests</subject><subject>Insertion</subject><subject>Mutation</subject><subject>Original</subject><subject>Outbreaks</subject><subject>Pandemics</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>PEDV</subject><subject>Phylogeny</subject><subject>Porcine epidemic diarrhea virus - genetics</subject><subject>Porcine epidemic diarrhea virus - pathogenicity</subject><subject>Proteins</subject><subject>Republic of Korea</subject><subject>S gene</subject><subject>Sequence Alignment</subject><subject>Spike Glycoprotein, Coronavirus - chemistry</subject><subject>Spike Glycoprotein, Coronavirus - genetics</subject><subject>Spike Glycoprotein, Coronavirus - metabolism</subject><subject>Strains (organisms)</subject><subject>Suckling behavior</subject><subject>Sus scrofa</subject><subject>Swine</subject><subject>Swine Diseases - virology</subject><subject>Swine production</subject><subject>Syncytia</subject><subject>Vero Cells</subject><subject>Virulence</subject><subject>virus isolation</subject><subject>Viruses</subject><issn>1865-1674</issn><issn>1865-1682</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1u1TAQhSMEoj-w4QGQJTYIcYvt2I6zQYJSoFDEgrK2HHvS-JLEwZO06rvwsLikXAELvLGl8-l4zpyieMToEcvnxdyAP2IlZ_WdYp9pJTdMaX53967EXnGAuKVU0VrJ-8VeyaiUWsv94sen2INbepuI62yyboYUcA4OiR09mezcxQsYgyMWERAHGGcSWzLF5MIIBKbgYciyDzalLoIllyEtSALG3s6ApE1xIHMHhFOmCYwrHpe5SWC_IYkj-QDbhZxin398Tr5kqSMfY1YfFPda2yM8vL0Pi69vT86P32_OPr87PX51tnFC6HrDqfBeOF82tfVSeV3xSjtVAzTeiUaBbWWrvKKy9ZY1svGVc0rYmtZcWunKw-Ll6jstzQDe5YzJ9mZKYbDp2kQbzN_KGDpzES9NlRcthc4GT28NUvy-AM5mCOigz4kgLmg4LznVQpRVRp_8g27jksYcL1Naap47qjP1bKVciogJ2t0wjJqb0s1N6eZX6Rl-_Of4O_R3yxlgK3AVerj-j5U5f33yZjX9CZXsu68</recordid><startdate>201909</startdate><enddate>201909</enddate><creator>Lee, Sunhee</creator><creator>Lee, Dong‐Uk</creator><creator>Noh, Yun‐Hee</creator><creator>Lee, Seung‐Chul</creator><creator>Choi, Hwan‐Won</creator><creator>Yang, Hyoung‐Seok</creator><creator>Seol, Jun‐Ho</creator><creator>Mun, Seong Hwan</creator><creator>Kang, Won‐Myoung</creator><creator>Yoo, Hyekyung</creator><creator>Lee, Changhee</creator><general>Hindawi Limited</general><general>John Wiley and Sons Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5930-5461</orcidid></search><sort><creationdate>201909</creationdate><title>Molecular characteristics and pathogenic assessment of porcine epidemic diarrhoea virus isolates from the 2018 endemic outbreaks on Jeju Island, South Korea</title><author>Lee, Sunhee ; Lee, Dong‐Uk ; Noh, Yun‐Hee ; Lee, Seung‐Chul ; Choi, Hwan‐Won ; Yang, Hyoung‐Seok ; Seol, Jun‐Ho ; Mun, Seong Hwan ; Kang, Won‐Myoung ; Yoo, Hyekyung ; Lee, Changhee</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4489-204dd4cd3b9ad56d87278c69eebdc4b6eaf5f6d605fda1b5bd7cc64a90925a5c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Chlorocebus aethiops</topic><topic>Clonal deletion</topic><topic>Coronavirus Infections - veterinary</topic><topic>Coronavirus Infections - virology</topic><topic>Diarrhea</topic><topic>endemic outbreaks</topic><topic>Endoplasmic reticulum</topic><topic>Epidemics</topic><topic>Gene deletion</topic><topic>Gene sequencing</topic><topic>Genetic analysis</topic><topic>Genetic diversity</topic><topic>genome analysis</topic><topic>Genome, Viral - genetics</topic><topic>Genomes</topic><topic>In vivo methods and tests</topic><topic>Insertion</topic><topic>Mutation</topic><topic>Original</topic><topic>Outbreaks</topic><topic>Pandemics</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>PEDV</topic><topic>Phylogeny</topic><topic>Porcine epidemic diarrhea virus - genetics</topic><topic>Porcine epidemic diarrhea virus - pathogenicity</topic><topic>Proteins</topic><topic>Republic of Korea</topic><topic>S gene</topic><topic>Sequence Alignment</topic><topic>Spike Glycoprotein, Coronavirus - chemistry</topic><topic>Spike Glycoprotein, Coronavirus - genetics</topic><topic>Spike Glycoprotein, Coronavirus - metabolism</topic><topic>Strains (organisms)</topic><topic>Suckling behavior</topic><topic>Sus scrofa</topic><topic>Swine</topic><topic>Swine Diseases - virology</topic><topic>Swine production</topic><topic>Syncytia</topic><topic>Vero Cells</topic><topic>Virulence</topic><topic>virus isolation</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Sunhee</creatorcontrib><creatorcontrib>Lee, Dong‐Uk</creatorcontrib><creatorcontrib>Noh, Yun‐Hee</creatorcontrib><creatorcontrib>Lee, Seung‐Chul</creatorcontrib><creatorcontrib>Choi, Hwan‐Won</creatorcontrib><creatorcontrib>Yang, Hyoung‐Seok</creatorcontrib><creatorcontrib>Seol, Jun‐Ho</creatorcontrib><creatorcontrib>Mun, Seong Hwan</creatorcontrib><creatorcontrib>Kang, Won‐Myoung</creatorcontrib><creatorcontrib>Yoo, Hyekyung</creatorcontrib><creatorcontrib>Lee, Changhee</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Transboundary and emerging diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Sunhee</au><au>Lee, Dong‐Uk</au><au>Noh, Yun‐Hee</au><au>Lee, Seung‐Chul</au><au>Choi, Hwan‐Won</au><au>Yang, Hyoung‐Seok</au><au>Seol, Jun‐Ho</au><au>Mun, Seong Hwan</au><au>Kang, Won‐Myoung</au><au>Yoo, Hyekyung</au><au>Lee, Changhee</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular characteristics and pathogenic assessment of porcine epidemic diarrhoea virus isolates from the 2018 endemic outbreaks on Jeju Island, South Korea</atitle><jtitle>Transboundary and emerging diseases</jtitle><addtitle>Transbound Emerg Dis</addtitle><date>2019-09</date><risdate>2019</risdate><volume>66</volume><issue>5</issue><spage>1894</spage><epage>1909</epage><pages>1894-1909</pages><issn>1865-1674</issn><eissn>1865-1682</eissn><abstract>Since the 2013–2014 incursion of the virulent G2b porcine epidemic diarrhoea virus (PEDV) pandemic strains in South Korea, frequent moderate‐scale regional outbreaks have recurred. In particular, areas of Jeju Island with extensive swine production have faced repeated epidemics since the re‐emergence in 2014. The current study reports the complete genome sequences and molecular characterization of the representative PEDV strains responsible for the 2018 endemic outbreaks on Jeju Island. All isolates were determined to belong genetically to the highly pathogenic pandemic G2b group. Full‐length genome sizes of four isolates differed from that of the G2b epidemic field strain due to insertion or deletion (DEL) mutations in the non‐structural protein (nsp)‐ or spike (S) protein‐coding regions. The 2018 Jeju isolates shared 96.7%–98.7% and 98.5%–99.4% identity at the S gene and whole‐genome levels, respectively, compared to global G2b PEDV strains. Genetic and phylogenetic analyses indicated that the 2018 isolates were closest to the 2014 G2b re‐emergent Jeju strains, but appeared to have undergone substantial rapid independent evolution. Among the isolates, a notable nsp3 DEL variant strain, KOR/KNU‐1807/2018, was isolated and propagated by continuous passages in Vero cells, and displayed typical PEDV‐induced syncytia formation. Genomic sequencing identified a unique 8‐nt DEL in the extreme C‐terminal region of the S gene at the 4th passage (KNU‐1807‐P4) compared to its original sample. This DEL resulted in the premature termination of S by nine amino acid residues (EVFEKVHVQ), which contained a KxHxx motif that is a potential endoplasmic reticulum retrieval signal. In vivo animal studies showed that variant strain KNU‐1807 had decreased virulence in suckling piglets. 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subjects Amino Acid Sequence
Amino acids
Animals
Chlorocebus aethiops
Clonal deletion
Coronavirus Infections - veterinary
Coronavirus Infections - virology
Diarrhea
endemic outbreaks
Endoplasmic reticulum
Epidemics
Gene deletion
Gene sequencing
Genetic analysis
Genetic diversity
genome analysis
Genome, Viral - genetics
Genomes
In vivo methods and tests
Insertion
Mutation
Original
Outbreaks
Pandemics
Pathogenicity
Pathogens
PEDV
Phylogeny
Porcine epidemic diarrhea virus - genetics
Porcine epidemic diarrhea virus - pathogenicity
Proteins
Republic of Korea
S gene
Sequence Alignment
Spike Glycoprotein, Coronavirus - chemistry
Spike Glycoprotein, Coronavirus - genetics
Spike Glycoprotein, Coronavirus - metabolism
Strains (organisms)
Suckling behavior
Sus scrofa
Swine
Swine Diseases - virology
Swine production
Syncytia
Vero Cells
Virulence
virus isolation
Viruses
title Molecular characteristics and pathogenic assessment of porcine epidemic diarrhoea virus isolates from the 2018 endemic outbreaks on Jeju Island, South Korea
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