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Porcine reproductive and respiratory syndrome type 1 viruses induce hypoplasia of erythroid cells and myeloid cell hyperplasia in the bone marrow of experimentally infected piglets independently of the viral load and virulence
•PRRSV-1 strains of differing virulence induce pathology in the bone marrow of infected pigs.•Bone marrow changes were independent of the viral load and strain virulence.•Erythroid hypoplasia, myeloid hyperplasia and increased M:E ratio were detected.•These changes were associated with an increased...
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Published in: | Veterinary microbiology 2017-03, Vol.201, p.126-135 |
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creator | Amarilla, Shyrley Paola Gómez-Laguna, Jaime Carrasco, Librado Rodríguez-Gómez, Irene M. Caridad y Ocerín, José M. Graham, Simon P. Frossard, Jean-Pierre Steinbach, Falko Salguero, Francisco J. |
description | •PRRSV-1 strains of differing virulence induce pathology in the bone marrow of infected pigs.•Bone marrow changes were independent of the viral load and strain virulence.•Erythroid hypoplasia, myeloid hyperplasia and increased M:E ratio were detected.•These changes were associated with an increased expression of IL-1α, IL-6 and TNF-α.
Porcine reproductive and respiratory syndrome viruses (PRRSV) present a wide phenotypic and genetic diversity. Experimental infections have demonstrated viral replication, including highly pathogenic strains (HP-PRRSV), in primary lymphoid organs such as the thymus. However, studies of the bone marrow are scarce but necessary to help elucidate the immunobiology of PRRSV strains of differing virulence. In this study, whereas viral RNA was detected within the bone marrow of animals experimentally infected with both low virulent Lelystad (LV) and 215-06 PRRSV-1 strains and with the highly virulent SU1-bel strain, PRRSV positive cells were only occasionally detected in one SU1-bel infected animal. PRRSV RNA levels were associated to circulating virus with the highest levels detected in LV-infected pigs. At 3 dpi, a decrease in the proportion of haematopoietic tissue and number of erythroid cells in all infected groups was associated with an increase in TUNEL or cleaved caspase 3 labelling and higher counts of myeloid cells compared to control. The expression of IL-1α and IL-6 was elevated at the beginning of the infection in all infected animals. The expression of TNF-α was increased at the end of the study in all infected groups with respect to control. Different PRRSV-1 strains induced, presummably by indirect mechanisms and independently of viral load and strain virulence, moderate and sustained hypoplasia of erythroid cells and myeloid cell hyperplasia at early stages of infection. These changes were paralleled by a peak in the local expression of IL-1α, IL-6 and TNF-α in all infected groups. |
doi_str_mv | 10.1016/j.vetmic.2016.12.040 |
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Porcine reproductive and respiratory syndrome viruses (PRRSV) present a wide phenotypic and genetic diversity. Experimental infections have demonstrated viral replication, including highly pathogenic strains (HP-PRRSV), in primary lymphoid organs such as the thymus. However, studies of the bone marrow are scarce but necessary to help elucidate the immunobiology of PRRSV strains of differing virulence. In this study, whereas viral RNA was detected within the bone marrow of animals experimentally infected with both low virulent Lelystad (LV) and 215-06 PRRSV-1 strains and with the highly virulent SU1-bel strain, PRRSV positive cells were only occasionally detected in one SU1-bel infected animal. PRRSV RNA levels were associated to circulating virus with the highest levels detected in LV-infected pigs. At 3 dpi, a decrease in the proportion of haematopoietic tissue and number of erythroid cells in all infected groups was associated with an increase in TUNEL or cleaved caspase 3 labelling and higher counts of myeloid cells compared to control. The expression of IL-1α and IL-6 was elevated at the beginning of the infection in all infected animals. The expression of TNF-α was increased at the end of the study in all infected groups with respect to control. Different PRRSV-1 strains induced, presummably by indirect mechanisms and independently of viral load and strain virulence, moderate and sustained hypoplasia of erythroid cells and myeloid cell hyperplasia at early stages of infection. These changes were paralleled by a peak in the local expression of IL-1α, IL-6 and TNF-α in all infected groups.</description><identifier>ISSN: 0378-1135</identifier><identifier>EISSN: 1873-2542</identifier><identifier>DOI: 10.1016/j.vetmic.2016.12.040</identifier><identifier>PMID: 28284598</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Bone marrow ; Bone Marrow - pathology ; Bone Marrow - virology ; Caspase ; Caspase-3 ; Cytokine ; Cytokines - immunology ; Erythroid and myeloid cells ; Erythroid cells ; Erythroid Cells - pathology ; Erythroid Cells - virology ; Gene expression ; Genetic diversity ; Genotype & phenotype ; Hogs ; Hyperplasia ; Hyperplasia - pathology ; Hyperplasia - veterinary ; Hyperplasia - virology ; Hypoplasia ; Infections ; Interleukin 6 ; Labeling ; Male ; Myeloid cells ; Myeloid Cells - pathology ; Myeloid Cells - virology ; Organs ; Porcine Reproductive and Respiratory Syndrome - pathology ; Porcine Reproductive and Respiratory Syndrome - virology ; Porcine respiratory and reproductive syndrome virus - pathogenicity ; Porcine respiratory and reproductive syndrome virus - physiology ; PRRSV-1 ; Respiratory diseases ; Ribonucleic acid ; RNA ; Strains (organisms) ; Studies ; Swine ; Thymus ; Tumor necrosis factor-α ; Viral Load ; Virulence ; Virus Replication ; Viruses</subject><ispartof>Veterinary microbiology, 2017-03, Vol.201, p.126-135</ispartof><rights>2017 Elsevier B.V.</rights><rights>Copyright © 2017 Elsevier B.V. All rights reserved.</rights><rights>Copyright Elsevier BV Mar 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c436t-126fe65c67f312e49b18d7c4fdc1b372bd37c50f2d75a73053d1b7ae30f6aef03</citedby><cites>FETCH-LOGICAL-c436t-126fe65c67f312e49b18d7c4fdc1b372bd37c50f2d75a73053d1b7ae30f6aef03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28284598$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Amarilla, Shyrley Paola</creatorcontrib><creatorcontrib>Gómez-Laguna, Jaime</creatorcontrib><creatorcontrib>Carrasco, Librado</creatorcontrib><creatorcontrib>Rodríguez-Gómez, Irene M.</creatorcontrib><creatorcontrib>Caridad y Ocerín, José M.</creatorcontrib><creatorcontrib>Graham, Simon P.</creatorcontrib><creatorcontrib>Frossard, Jean-Pierre</creatorcontrib><creatorcontrib>Steinbach, Falko</creatorcontrib><creatorcontrib>Salguero, Francisco J.</creatorcontrib><title>Porcine reproductive and respiratory syndrome type 1 viruses induce hypoplasia of erythroid cells and myeloid cell hyperplasia in the bone marrow of experimentally infected piglets independently of the viral load and virulence</title><title>Veterinary microbiology</title><addtitle>Vet Microbiol</addtitle><description>•PRRSV-1 strains of differing virulence induce pathology in the bone marrow of infected pigs.•Bone marrow changes were independent of the viral load and strain virulence.•Erythroid hypoplasia, myeloid hyperplasia and increased M:E ratio were detected.•These changes were associated with an increased expression of IL-1α, IL-6 and TNF-α.
Porcine reproductive and respiratory syndrome viruses (PRRSV) present a wide phenotypic and genetic diversity. Experimental infections have demonstrated viral replication, including highly pathogenic strains (HP-PRRSV), in primary lymphoid organs such as the thymus. However, studies of the bone marrow are scarce but necessary to help elucidate the immunobiology of PRRSV strains of differing virulence. In this study, whereas viral RNA was detected within the bone marrow of animals experimentally infected with both low virulent Lelystad (LV) and 215-06 PRRSV-1 strains and with the highly virulent SU1-bel strain, PRRSV positive cells were only occasionally detected in one SU1-bel infected animal. PRRSV RNA levels were associated to circulating virus with the highest levels detected in LV-infected pigs. At 3 dpi, a decrease in the proportion of haematopoietic tissue and number of erythroid cells in all infected groups was associated with an increase in TUNEL or cleaved caspase 3 labelling and higher counts of myeloid cells compared to control. The expression of IL-1α and IL-6 was elevated at the beginning of the infection in all infected animals. The expression of TNF-α was increased at the end of the study in all infected groups with respect to control. Different PRRSV-1 strains induced, presummably by indirect mechanisms and independently of viral load and strain virulence, moderate and sustained hypoplasia of erythroid cells and myeloid cell hyperplasia at early stages of infection. These changes were paralleled by a peak in the local expression of IL-1α, IL-6 and TNF-α in all infected groups.</description><subject>Animals</subject><subject>Bone marrow</subject><subject>Bone Marrow - pathology</subject><subject>Bone Marrow - virology</subject><subject>Caspase</subject><subject>Caspase-3</subject><subject>Cytokine</subject><subject>Cytokines - immunology</subject><subject>Erythroid and myeloid cells</subject><subject>Erythroid cells</subject><subject>Erythroid Cells - pathology</subject><subject>Erythroid Cells - virology</subject><subject>Gene expression</subject><subject>Genetic diversity</subject><subject>Genotype & phenotype</subject><subject>Hogs</subject><subject>Hyperplasia</subject><subject>Hyperplasia - pathology</subject><subject>Hyperplasia - veterinary</subject><subject>Hyperplasia - virology</subject><subject>Hypoplasia</subject><subject>Infections</subject><subject>Interleukin 6</subject><subject>Labeling</subject><subject>Male</subject><subject>Myeloid cells</subject><subject>Myeloid Cells - pathology</subject><subject>Myeloid Cells - virology</subject><subject>Organs</subject><subject>Porcine Reproductive and Respiratory Syndrome - pathology</subject><subject>Porcine Reproductive and Respiratory Syndrome - virology</subject><subject>Porcine respiratory and reproductive syndrome virus - pathogenicity</subject><subject>Porcine respiratory and reproductive syndrome virus - physiology</subject><subject>PRRSV-1</subject><subject>Respiratory diseases</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Strains (organisms)</subject><subject>Studies</subject><subject>Swine</subject><subject>Thymus</subject><subject>Tumor necrosis factor-α</subject><subject>Viral Load</subject><subject>Virulence</subject><subject>Virus Replication</subject><subject>Viruses</subject><issn>0378-1135</issn><issn>1873-2542</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNp9ksuO1DAQRSMEYnoG_gAhS2zYJPiR5wYJjWBAGgkWsLYcu0K75cTBdhryu3wJle4eFizY2LJ96lb5VmXZC0YLRln95lAcIY1WFxxPBeMFLemjbMfaRuS8KvnjbEdF0-aMieoqu47xQCktu5o-za54y9uy6tpd9vuLD9pOQALMwZtFJ3sEoiaDF3G2QSUfVhLXyQQ_AknrDISRow1LhEjshBFA9uvsZ6eiVcQPBMKa9sFbQzQ4F09i4wru4WbDIVx4O5G0B9J7LGFUIfifJ4lfSNgRpqScWxEaQCcwZLbfHaRTXpgBlynhMwZsGliUcsR5ZU4ptxodTBqeZU8G5SI8v-w32bcP77_efszvP999un13n-tS1ClnvB6grnTdDIJxKLuetabR5WA060XDeyMaXdGBm6ZSjaCVMKxvFAg61AoGKm6y12ddNPLHAjHJ0cbtw2oCv0SJnalbVnddieirf9CDX8KE1UnW1QI71nabYHmmdPAxBhjkjKaosEpG5TYD8iDPMyC3GZCMS5wBDHt5EV_6EczfoIemI_D2DAC6cbQQZNR2c8rYgD5L4-3_M_wBrNDLug</recordid><startdate>201703</startdate><enddate>201703</enddate><creator>Amarilla, Shyrley Paola</creator><creator>Gómez-Laguna, Jaime</creator><creator>Carrasco, Librado</creator><creator>Rodríguez-Gómez, Irene M.</creator><creator>Caridad y Ocerín, José M.</creator><creator>Graham, Simon P.</creator><creator>Frossard, Jean-Pierre</creator><creator>Steinbach, Falko</creator><creator>Salguero, Francisco J.</creator><general>Elsevier B.V</general><general>Elsevier BV</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>7U9</scope><scope>H94</scope><scope>M7N</scope><scope>7X8</scope></search><sort><creationdate>201703</creationdate><title>Porcine reproductive and respiratory syndrome type 1 viruses induce hypoplasia of erythroid cells and myeloid cell hyperplasia in the bone marrow of experimentally infected piglets independently of the viral load and virulence</title><author>Amarilla, Shyrley Paola ; Gómez-Laguna, Jaime ; Carrasco, Librado ; Rodríguez-Gómez, Irene M. ; Caridad y Ocerín, José M. ; Graham, Simon P. ; Frossard, Jean-Pierre ; Steinbach, Falko ; Salguero, Francisco J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c436t-126fe65c67f312e49b18d7c4fdc1b372bd37c50f2d75a73053d1b7ae30f6aef03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Bone marrow</topic><topic>Bone Marrow - pathology</topic><topic>Bone Marrow - virology</topic><topic>Caspase</topic><topic>Caspase-3</topic><topic>Cytokine</topic><topic>Cytokines - immunology</topic><topic>Erythroid and myeloid cells</topic><topic>Erythroid cells</topic><topic>Erythroid Cells - pathology</topic><topic>Erythroid Cells - virology</topic><topic>Gene expression</topic><topic>Genetic diversity</topic><topic>Genotype & phenotype</topic><topic>Hogs</topic><topic>Hyperplasia</topic><topic>Hyperplasia - pathology</topic><topic>Hyperplasia - veterinary</topic><topic>Hyperplasia - virology</topic><topic>Hypoplasia</topic><topic>Infections</topic><topic>Interleukin 6</topic><topic>Labeling</topic><topic>Male</topic><topic>Myeloid cells</topic><topic>Myeloid Cells - pathology</topic><topic>Myeloid Cells - virology</topic><topic>Organs</topic><topic>Porcine Reproductive and Respiratory Syndrome - pathology</topic><topic>Porcine Reproductive and Respiratory Syndrome - virology</topic><topic>Porcine respiratory and reproductive syndrome virus - pathogenicity</topic><topic>Porcine respiratory and reproductive syndrome virus - physiology</topic><topic>PRRSV-1</topic><topic>Respiratory diseases</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Strains (organisms)</topic><topic>Studies</topic><topic>Swine</topic><topic>Thymus</topic><topic>Tumor necrosis factor-α</topic><topic>Viral Load</topic><topic>Virulence</topic><topic>Virus Replication</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Amarilla, Shyrley Paola</creatorcontrib><creatorcontrib>Gómez-Laguna, Jaime</creatorcontrib><creatorcontrib>Carrasco, Librado</creatorcontrib><creatorcontrib>Rodríguez-Gómez, Irene M.</creatorcontrib><creatorcontrib>Caridad y Ocerín, José M.</creatorcontrib><creatorcontrib>Graham, Simon P.</creatorcontrib><creatorcontrib>Frossard, Jean-Pierre</creatorcontrib><creatorcontrib>Steinbach, Falko</creatorcontrib><creatorcontrib>Salguero, Francisco J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>MEDLINE - Academic</collection><jtitle>Veterinary microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Amarilla, Shyrley Paola</au><au>Gómez-Laguna, Jaime</au><au>Carrasco, Librado</au><au>Rodríguez-Gómez, Irene M.</au><au>Caridad y Ocerín, José M.</au><au>Graham, Simon P.</au><au>Frossard, Jean-Pierre</au><au>Steinbach, Falko</au><au>Salguero, Francisco J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Porcine reproductive and respiratory syndrome type 1 viruses induce hypoplasia of erythroid cells and myeloid cell hyperplasia in the bone marrow of experimentally infected piglets independently of the viral load and virulence</atitle><jtitle>Veterinary microbiology</jtitle><addtitle>Vet Microbiol</addtitle><date>2017-03</date><risdate>2017</risdate><volume>201</volume><spage>126</spage><epage>135</epage><pages>126-135</pages><issn>0378-1135</issn><eissn>1873-2542</eissn><abstract>•PRRSV-1 strains of differing virulence induce pathology in the bone marrow of infected pigs.•Bone marrow changes were independent of the viral load and strain virulence.•Erythroid hypoplasia, myeloid hyperplasia and increased M:E ratio were detected.•These changes were associated with an increased expression of IL-1α, IL-6 and TNF-α.
Porcine reproductive and respiratory syndrome viruses (PRRSV) present a wide phenotypic and genetic diversity. Experimental infections have demonstrated viral replication, including highly pathogenic strains (HP-PRRSV), in primary lymphoid organs such as the thymus. However, studies of the bone marrow are scarce but necessary to help elucidate the immunobiology of PRRSV strains of differing virulence. In this study, whereas viral RNA was detected within the bone marrow of animals experimentally infected with both low virulent Lelystad (LV) and 215-06 PRRSV-1 strains and with the highly virulent SU1-bel strain, PRRSV positive cells were only occasionally detected in one SU1-bel infected animal. PRRSV RNA levels were associated to circulating virus with the highest levels detected in LV-infected pigs. At 3 dpi, a decrease in the proportion of haematopoietic tissue and number of erythroid cells in all infected groups was associated with an increase in TUNEL or cleaved caspase 3 labelling and higher counts of myeloid cells compared to control. The expression of IL-1α and IL-6 was elevated at the beginning of the infection in all infected animals. The expression of TNF-α was increased at the end of the study in all infected groups with respect to control. Different PRRSV-1 strains induced, presummably by indirect mechanisms and independently of viral load and strain virulence, moderate and sustained hypoplasia of erythroid cells and myeloid cell hyperplasia at early stages of infection. These changes were paralleled by a peak in the local expression of IL-1α, IL-6 and TNF-α in all infected groups.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>28284598</pmid><doi>10.1016/j.vetmic.2016.12.040</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bone marrow Bone Marrow - pathology Bone Marrow - virology Caspase Caspase-3 Cytokine Cytokines - immunology Erythroid and myeloid cells Erythroid cells Erythroid Cells - pathology Erythroid Cells - virology Gene expression Genetic diversity Genotype & phenotype Hogs Hyperplasia Hyperplasia - pathology Hyperplasia - veterinary Hyperplasia - virology Hypoplasia Infections Interleukin 6 Labeling Male Myeloid cells Myeloid Cells - pathology Myeloid Cells - virology Organs Porcine Reproductive and Respiratory Syndrome - pathology Porcine Reproductive and Respiratory Syndrome - virology Porcine respiratory and reproductive syndrome virus - pathogenicity Porcine respiratory and reproductive syndrome virus - physiology PRRSV-1 Respiratory diseases Ribonucleic acid RNA Strains (organisms) Studies Swine Thymus Tumor necrosis factor-α Viral Load Virulence Virus Replication Viruses |
title | Porcine reproductive and respiratory syndrome type 1 viruses induce hypoplasia of erythroid cells and myeloid cell hyperplasia in the bone marrow of experimentally infected piglets independently of the viral load and virulence |
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