A Broad-Spectrum Chemokine-Binding Protein of Bovine Papular Stomatitis Virus Inhibits Neutrophil and Monocyte Infiltration in Inflammatory and Wound Models of Mouse Skin
Bovine papular stomatitis virus (BPSV) is a Parapoxvirus that induces acute pustular skin lesions in cattle and is transmissible to humans. Previous studies have shown that BPSV encodes a distinctive chemokine-binding protein (CBP). Chemokines are critically involved in the trafficking of immune cel...
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| description | Bovine papular stomatitis virus (BPSV) is a Parapoxvirus that induces acute pustular skin lesions in cattle and is transmissible to humans. Previous studies have shown that BPSV encodes a distinctive chemokine-binding protein (CBP). Chemokines are critically involved in the trafficking of immune cells to sites of inflammation and infected tissue, suggesting that the CBP plays a role in immune evasion by preventing immune cells reaching sites of infection. We hypothesised that the BPSV-CBP binds a wide range of inflammatory chemokines particularly those involved in BPSV skin infection, and inhibits the recruitment of immune cells from the blood into inflamed skin. Molecular analysis of the purified protein revealed that the BPSV-CBP is a homodimeric polypeptide with a MW of 82.4 kDa whilst a comprehensive screen of inflammatory chemokines by surface plasmon resonance showed high-affinity binding to a range of chemokines within the CXC, CC and XC subfamilies. Structural analysis of BPSV-CBP, based on the crystal structure of orf virus CBP, provided a probable explanation for these chemokine specificities at a molecular level. Functional analysis of the BPSV-CBP using transwell migration assays demonstrated that it potently inhibited chemotaxis of murine neutrophils and monocytes in response to CXCL1, CXCL2 as well as CCL2, CCL3 and CCL5 chemokines. In order to examine the effects of CBP in vivo, we used murine skin models to determine its impact on inflammatory cell recruitment such as that observed during BPSV infection. Intradermal injection of BPSV-CBP blocked the influx of neutrophils and monocytes in murine skin in which inflammation was induced with lipopolysaccharide. Furthermore, intradermal injection of BPSV-CBP into injured skin, which more closely mimics BPSV lesions, delayed the influx of neutrophils and reduced the recruitment of MHC-II+ immune cells to the wound bed. Our findings suggest that the CBP could be important in pathogenesis of BPSV infections. |
| doi_str_mv | 10.1371/journal.pone.0168007 |
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Previous studies have shown that BPSV encodes a distinctive chemokine-binding protein (CBP). Chemokines are critically involved in the trafficking of immune cells to sites of inflammation and infected tissue, suggesting that the CBP plays a role in immune evasion by preventing immune cells reaching sites of infection. We hypothesised that the BPSV-CBP binds a wide range of inflammatory chemokines particularly those involved in BPSV skin infection, and inhibits the recruitment of immune cells from the blood into inflamed skin. Molecular analysis of the purified protein revealed that the BPSV-CBP is a homodimeric polypeptide with a MW of 82.4 kDa whilst a comprehensive screen of inflammatory chemokines by surface plasmon resonance showed high-affinity binding to a range of chemokines within the CXC, CC and XC subfamilies. Structural analysis of BPSV-CBP, based on the crystal structure of orf virus CBP, provided a probable explanation for these chemokine specificities at a molecular level. Functional analysis of the BPSV-CBP using transwell migration assays demonstrated that it potently inhibited chemotaxis of murine neutrophils and monocytes in response to CXCL1, CXCL2 as well as CCL2, CCL3 and CCL5 chemokines. In order to examine the effects of CBP in vivo, we used murine skin models to determine its impact on inflammatory cell recruitment such as that observed during BPSV infection. Intradermal injection of BPSV-CBP blocked the influx of neutrophils and monocytes in murine skin in which inflammation was induced with lipopolysaccharide. Furthermore, intradermal injection of BPSV-CBP into injured skin, which more closely mimics BPSV lesions, delayed the influx of neutrophils and reduced the recruitment of MHC-II+ immune cells to the wound bed. Our findings suggest that the CBP could be important in pathogenesis of BPSV infections.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0168007</identifier><identifier>PMID: 27936239</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Analysis ; Animal models ; Animals ; Anticoagulants ; Biology and Life Sciences ; Bovine papular stomatitis ; Cattle diseases ; CCL3 protein ; Cell migration ; Chemokine-binding protein ; Chemokines ; Chemokines - metabolism ; Chemotaxis ; Chemotaxis, Leukocyte - physiology ; Chromatography ; Crystal structure ; Dimerization ; Disease Models, Animal ; Functional analysis ; Genetic aspects ; Immune system ; Immunology ; In vivo methods and tests ; Infections ; Infiltration ; Inflammation ; Inflammation - pathology ; Influenza ; Injection ; Lesions ; Leukocyte migration ; Leukocytes (neutrophilic) ; Lipopolysaccharides ; Major histocompatibility complex ; Medicine and Health Sciences ; Mice ; Monocyte chemoattractant protein 1 ; Monocytes ; Monocytes - pathology ; Neutrophils ; Neutrophils - pathology ; Orf ; Orf virus ; Parapoxvirus - metabolism ; Pathogenesis ; Poxviridae ; Protein Conformation ; Proteins ; Sequence Homology, Amino Acid ; Skin ; Skin diseases ; Stomatitis ; Structural analysis ; Surface Plasmon Resonance ; Viral infections ; Viral Proteins - chemistry ; Viral Proteins - physiology ; Viruses ; Wounds ; Wounds and Injuries - pathology</subject><ispartof>PloS one, 2016-12, Vol.11 (12), p.e0168007-e0168007</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Sharif et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Sharif et al 2016 Sharif et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-cae2eeacda0de57044424c24a59a86f130e282a4df26e275c1087470b624d7303</citedby><cites>FETCH-LOGICAL-c725t-cae2eeacda0de57044424c24a59a86f130e282a4df26e275c1087470b624d7303</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5148066/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5148066/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27936239$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Proost, Paul</contributor><creatorcontrib>Sharif, Saeed</creatorcontrib><creatorcontrib>Nakatani, Yoshio</creatorcontrib><creatorcontrib>Wise, Lyn</creatorcontrib><creatorcontrib>Corbett, Michael</creatorcontrib><creatorcontrib>Real, Nicola C</creatorcontrib><creatorcontrib>Stuart, Gabriella S</creatorcontrib><creatorcontrib>Lateef, Zabeen</creatorcontrib><creatorcontrib>Krause, Kurt</creatorcontrib><creatorcontrib>Mercer, Andrew A</creatorcontrib><creatorcontrib>Fleming, Stephen B</creatorcontrib><title>A Broad-Spectrum Chemokine-Binding Protein of Bovine Papular Stomatitis Virus Inhibits Neutrophil and Monocyte Infiltration in Inflammatory and Wound Models of Mouse Skin</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Bovine papular stomatitis virus (BPSV) is a Parapoxvirus that induces acute pustular skin lesions in cattle and is transmissible to humans. Previous studies have shown that BPSV encodes a distinctive chemokine-binding protein (CBP). Chemokines are critically involved in the trafficking of immune cells to sites of inflammation and infected tissue, suggesting that the CBP plays a role in immune evasion by preventing immune cells reaching sites of infection. We hypothesised that the BPSV-CBP binds a wide range of inflammatory chemokines particularly those involved in BPSV skin infection, and inhibits the recruitment of immune cells from the blood into inflamed skin. Molecular analysis of the purified protein revealed that the BPSV-CBP is a homodimeric polypeptide with a MW of 82.4 kDa whilst a comprehensive screen of inflammatory chemokines by surface plasmon resonance showed high-affinity binding to a range of chemokines within the CXC, CC and XC subfamilies. Structural analysis of BPSV-CBP, based on the crystal structure of orf virus CBP, provided a probable explanation for these chemokine specificities at a molecular level. Functional analysis of the BPSV-CBP using transwell migration assays demonstrated that it potently inhibited chemotaxis of murine neutrophils and monocytes in response to CXCL1, CXCL2 as well as CCL2, CCL3 and CCL5 chemokines. In order to examine the effects of CBP in vivo, we used murine skin models to determine its impact on inflammatory cell recruitment such as that observed during BPSV infection. Intradermal injection of BPSV-CBP blocked the influx of neutrophils and monocytes in murine skin in which inflammation was induced with lipopolysaccharide. Furthermore, intradermal injection of BPSV-CBP into injured skin, which more closely mimics BPSV lesions, delayed the influx of neutrophils and reduced the recruitment of MHC-II+ immune cells to the wound bed. Our findings suggest that the CBP could be important in pathogenesis of BPSV infections.</description><subject>Amino Acid Sequence</subject><subject>Analysis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Anticoagulants</subject><subject>Biology and Life Sciences</subject><subject>Bovine papular stomatitis</subject><subject>Cattle diseases</subject><subject>CCL3 protein</subject><subject>Cell migration</subject><subject>Chemokine-binding protein</subject><subject>Chemokines</subject><subject>Chemokines - metabolism</subject><subject>Chemotaxis</subject><subject>Chemotaxis, Leukocyte - physiology</subject><subject>Chromatography</subject><subject>Crystal structure</subject><subject>Dimerization</subject><subject>Disease Models, Animal</subject><subject>Functional analysis</subject><subject>Genetic aspects</subject><subject>Immune system</subject><subject>Immunology</subject><subject>In vivo methods and tests</subject><subject>Infections</subject><subject>Infiltration</subject><subject>Inflammation</subject><subject>Inflammation - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sharif, Saeed</au><au>Nakatani, Yoshio</au><au>Wise, Lyn</au><au>Corbett, Michael</au><au>Real, Nicola C</au><au>Stuart, Gabriella S</au><au>Lateef, Zabeen</au><au>Krause, Kurt</au><au>Mercer, Andrew A</au><au>Fleming, Stephen B</au><au>Proost, Paul</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Broad-Spectrum Chemokine-Binding Protein of Bovine Papular Stomatitis Virus Inhibits Neutrophil and Monocyte Infiltration in Inflammatory and Wound Models of Mouse Skin</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-12-09</date><risdate>2016</risdate><volume>11</volume><issue>12</issue><spage>e0168007</spage><epage>e0168007</epage><pages>e0168007-e0168007</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Bovine papular stomatitis virus (BPSV) is a Parapoxvirus that induces acute pustular skin lesions in cattle and is transmissible to humans. Previous studies have shown that BPSV encodes a distinctive chemokine-binding protein (CBP). Chemokines are critically involved in the trafficking of immune cells to sites of inflammation and infected tissue, suggesting that the CBP plays a role in immune evasion by preventing immune cells reaching sites of infection. We hypothesised that the BPSV-CBP binds a wide range of inflammatory chemokines particularly those involved in BPSV skin infection, and inhibits the recruitment of immune cells from the blood into inflamed skin. Molecular analysis of the purified protein revealed that the BPSV-CBP is a homodimeric polypeptide with a MW of 82.4 kDa whilst a comprehensive screen of inflammatory chemokines by surface plasmon resonance showed high-affinity binding to a range of chemokines within the CXC, CC and XC subfamilies. Structural analysis of BPSV-CBP, based on the crystal structure of orf virus CBP, provided a probable explanation for these chemokine specificities at a molecular level. Functional analysis of the BPSV-CBP using transwell migration assays demonstrated that it potently inhibited chemotaxis of murine neutrophils and monocytes in response to CXCL1, CXCL2 as well as CCL2, CCL3 and CCL5 chemokines. In order to examine the effects of CBP in vivo, we used murine skin models to determine its impact on inflammatory cell recruitment such as that observed during BPSV infection. Intradermal injection of BPSV-CBP blocked the influx of neutrophils and monocytes in murine skin in which inflammation was induced with lipopolysaccharide. Furthermore, intradermal injection of BPSV-CBP into injured skin, which more closely mimics BPSV lesions, delayed the influx of neutrophils and reduced the recruitment of MHC-II+ immune cells to the wound bed. Our findings suggest that the CBP could be important in pathogenesis of BPSV infections.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27936239</pmid><doi>10.1371/journal.pone.0168007</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2016-12, Vol.11 (12), p.e0168007-e0168007 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1847563948 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amino Acid Sequence Analysis Animal models Animals Anticoagulants Biology and Life Sciences Bovine papular stomatitis Cattle diseases CCL3 protein Cell migration Chemokine-binding protein Chemokines Chemokines - metabolism Chemotaxis Chemotaxis, Leukocyte - physiology Chromatography Crystal structure Dimerization Disease Models, Animal Functional analysis Genetic aspects Immune system Immunology In vivo methods and tests Infections Infiltration Inflammation Inflammation - pathology Influenza Injection Lesions Leukocyte migration Leukocytes (neutrophilic) Lipopolysaccharides Major histocompatibility complex Medicine and Health Sciences Mice Monocyte chemoattractant protein 1 Monocytes Monocytes - pathology Neutrophils Neutrophils - pathology Orf Orf virus Parapoxvirus - metabolism Pathogenesis Poxviridae Protein Conformation Proteins Sequence Homology, Amino Acid Skin Skin diseases Stomatitis Structural analysis Surface Plasmon Resonance Viral infections Viral Proteins - chemistry Viral Proteins - physiology Viruses Wounds Wounds and Injuries - pathology |
| title | A Broad-Spectrum Chemokine-Binding Protein of Bovine Papular Stomatitis Virus Inhibits Neutrophil and Monocyte Infiltration in Inflammatory and Wound Models of Mouse Skin |
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