Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice
Abstract Background Viral infection is implicated in development of autoimmunity. Parvovirus B19 (B19V) nonstructural protein, NS1, a helicase, covalently modifies self double-stranded deoxyribonucleic acid (dsDNA) and induces apoptosis. This study tested whether resulting apoptotic bodies (ApoBods)...
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| Veröffentlicht in: | The Journal of infectious diseases 2019-04, Vol.219 (9), p.1418-1429 |
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| creator | Puttaraksa, Kanoktip Pirttinen, Heidi Karvonen, Kati Nykky, Jonna Naides, Stanley J Gilbert, Leona |
| description | Abstract
Background
Viral infection is implicated in development of autoimmunity. Parvovirus B19 (B19V) nonstructural protein, NS1, a helicase, covalently modifies self double-stranded deoxyribonucleic acid (dsDNA) and induces apoptosis. This study tested whether resulting apoptotic bodies (ApoBods) containing virally modified dsDNA could induce autoimmunity in an animal model.
Methods
BALB/c mice were inoculated with (1) pristane-induced, (2) B19V NS1-induced, or (3) staurosporine-induced ApoBods. Serum was tested for dsDNA autoantibodies by Crithidia luciliae staining and enzyme-linked immunosorbent assay. Brain, heart, liver, and kidney pathology was examined. Deposition of self-antigens in glomeruli was examined by staining with antibodies to dsDNA, histones H1 and H4, and TATA-binding protein.
Results
The B19V NS1-induced ApoBod inoculation induced dsDNA autoantibodies in a dose-dependent fashion. Histopathological features of immune-mediated organ damage were evident in pristane-induced and NS1-induced ApoBod groups; severity scores were higher in these groups than in staurosporine-treated groups. Tissue damage was dependent on NS1-induced ApoBod dose. Nucleosomal antigens were deposited in target tissue from pristane-induced and NS1-induced ApoBod inoculated groups, but not in the staurosporine-induced ApoBod inoculated group.
Conclusions
This study demonstrated proof of principle in an animal model that virally modified dsDNA in apoptotic bodies could break tolerance to self dsDNA and induce dsDNA autoantibodies and end-organ damage.
Inoculation of normal mice with apoptotic bodies, generated by parvovirus B19V helicase NS1 expression, induces dsDNA antibodies and organ damage. This study provides proof of concept that viral modification of host cell DNA can lead to autoimmunity. |
| doi_str_mv | 10.1093/infdis/jiy614 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6468957</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/infdis/jiy614</oup_id><sourcerecordid>2179221507</sourcerecordid><originalsourceid>FETCH-LOGICAL-c448t-a7d88c435b83f44a74d752c7269f527810adea97fc75988ee09e3b3e0d20eb823</originalsourceid><addsrcrecordid>eNqFkc1u1DAUhSMEokNhyRZZYsMm1H-J7Q1S6RSoVNpKBbaWY98MHiX2YMcj5jF4YzKaUn42rK7k-_nTPTpV9Zzg1wQrduJD73w-WftdS_iDakEaJuq2JexhtcCY0ppIpY6qJzmvMcacteJxdcQw423TykX148akbdz6VDJ6S9QXdBVDnlKxU0lmQDcpTuADurol6CK4YiGjZSzdAPXtlExw4NAS4vdd8l0MxQ7gLTq13qHTMkUTpvnZ-fnTjKLz4OrrtDIBLc1oVoD24hjMTPpxLAHQR2_hafWoN0OGZ3fzuPr87vzT2Yf68vr9xdnpZW05l1NthJPSctZ0kvWcG8GdaKgVtFV9Q4Uk2DgwSvRWNEpKAKyAdQywoxg6Sdlx9ebg3ZRuBGchzIEGvUl-NGmno_H6703wX_UqbnXLW6kaMQte3QlS_FYgT3r02cIwmACxZE2JUJSSBu_Rl_-g61hSmONpyrlQbUMEman6QNkUc07Q3x9DsN6XrQ9l60PZM__izwT39K92f18Yy-Y_rp_V8rfo</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2447965171</pqid></control><display><type>article</type><title>Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice</title><source>MEDLINE</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>Alma/SFX Local Collection</source><creator>Puttaraksa, Kanoktip ; Pirttinen, Heidi ; Karvonen, Kati ; Nykky, Jonna ; Naides, Stanley J ; Gilbert, Leona</creator><creatorcontrib>Puttaraksa, Kanoktip ; Pirttinen, Heidi ; Karvonen, Kati ; Nykky, Jonna ; Naides, Stanley J ; Gilbert, Leona</creatorcontrib><description>Abstract
Background
Viral infection is implicated in development of autoimmunity. Parvovirus B19 (B19V) nonstructural protein, NS1, a helicase, covalently modifies self double-stranded deoxyribonucleic acid (dsDNA) and induces apoptosis. This study tested whether resulting apoptotic bodies (ApoBods) containing virally modified dsDNA could induce autoimmunity in an animal model.
Methods
BALB/c mice were inoculated with (1) pristane-induced, (2) B19V NS1-induced, or (3) staurosporine-induced ApoBods. Serum was tested for dsDNA autoantibodies by Crithidia luciliae staining and enzyme-linked immunosorbent assay. Brain, heart, liver, and kidney pathology was examined. Deposition of self-antigens in glomeruli was examined by staining with antibodies to dsDNA, histones H1 and H4, and TATA-binding protein.
Results
The B19V NS1-induced ApoBod inoculation induced dsDNA autoantibodies in a dose-dependent fashion. Histopathological features of immune-mediated organ damage were evident in pristane-induced and NS1-induced ApoBod groups; severity scores were higher in these groups than in staurosporine-treated groups. Tissue damage was dependent on NS1-induced ApoBod dose. Nucleosomal antigens were deposited in target tissue from pristane-induced and NS1-induced ApoBod inoculated groups, but not in the staurosporine-induced ApoBod inoculated group.
Conclusions
This study demonstrated proof of principle in an animal model that virally modified dsDNA in apoptotic bodies could break tolerance to self dsDNA and induce dsDNA autoantibodies and end-organ damage.
Inoculation of normal mice with apoptotic bodies, generated by parvovirus B19V helicase NS1 expression, induces dsDNA antibodies and organ damage. This study provides proof of concept that viral modification of host cell DNA can lead to autoimmunity.</description><identifier>ISSN: 0022-1899</identifier><identifier>ISSN: 1537-6613</identifier><identifier>EISSN: 1537-6613</identifier><identifier>DOI: 10.1093/infdis/jiy614</identifier><identifier>PMID: 30346568</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Animal models ; Animals ; Antibodies, Antinuclear - blood ; Antibodies, Antinuclear - metabolism ; Antigens ; Apoptosis ; Apoptosis - drug effects ; Autoantibodies ; Autoantigens ; Autoimmunity ; Brain - pathology ; Deoxyribonucleic acid ; DNA ; DNA - immunology ; DNA helicase ; Enzyme Inhibitors - pharmacology ; Enzyme-linked immunosorbent assay ; Extracellular Vesicles - immunology ; Female ; Glomerulonephritis - immunology ; Glomerulonephritis - pathology ; Histones ; Immunological tolerance ; Immunosuppressive Agents - pharmacology ; Inoculation ; Kidney Glomerulus - metabolism ; Kidney Glomerulus - pathology ; Kidneys ; Liver - pathology ; Major and Brief Reports ; Mice ; Myocardium - pathology ; Parvovirus B19, Human ; Parvoviruses ; Pristane ; Proteins ; Staurosporine ; Staurosporine - pharmacology ; TATA-binding protein ; Terpenes - pharmacology ; Viral Nonstructural Proteins - metabolism</subject><ispartof>The Journal of infectious diseases, 2019-04, Vol.219 (9), p.1418-1429</ispartof><rights>The Author(s) 2018. Published by Oxford University Press for the Infectious Diseases Society of America. 2018</rights><rights>The Author(s) 2018. Published by Oxford University Press for the Infectious Diseases Society of America.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c448t-a7d88c435b83f44a74d752c7269f527810adea97fc75988ee09e3b3e0d20eb823</citedby><cites>FETCH-LOGICAL-c448t-a7d88c435b83f44a74d752c7269f527810adea97fc75988ee09e3b3e0d20eb823</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30346568$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Puttaraksa, Kanoktip</creatorcontrib><creatorcontrib>Pirttinen, Heidi</creatorcontrib><creatorcontrib>Karvonen, Kati</creatorcontrib><creatorcontrib>Nykky, Jonna</creatorcontrib><creatorcontrib>Naides, Stanley J</creatorcontrib><creatorcontrib>Gilbert, Leona</creatorcontrib><title>Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice</title><title>The Journal of infectious diseases</title><addtitle>J Infect Dis</addtitle><description>Abstract
Background
Viral infection is implicated in development of autoimmunity. Parvovirus B19 (B19V) nonstructural protein, NS1, a helicase, covalently modifies self double-stranded deoxyribonucleic acid (dsDNA) and induces apoptosis. This study tested whether resulting apoptotic bodies (ApoBods) containing virally modified dsDNA could induce autoimmunity in an animal model.
Methods
BALB/c mice were inoculated with (1) pristane-induced, (2) B19V NS1-induced, or (3) staurosporine-induced ApoBods. Serum was tested for dsDNA autoantibodies by Crithidia luciliae staining and enzyme-linked immunosorbent assay. Brain, heart, liver, and kidney pathology was examined. Deposition of self-antigens in glomeruli was examined by staining with antibodies to dsDNA, histones H1 and H4, and TATA-binding protein.
Results
The B19V NS1-induced ApoBod inoculation induced dsDNA autoantibodies in a dose-dependent fashion. Histopathological features of immune-mediated organ damage were evident in pristane-induced and NS1-induced ApoBod groups; severity scores were higher in these groups than in staurosporine-treated groups. Tissue damage was dependent on NS1-induced ApoBod dose. Nucleosomal antigens were deposited in target tissue from pristane-induced and NS1-induced ApoBod inoculated groups, but not in the staurosporine-induced ApoBod inoculated group.
Conclusions
This study demonstrated proof of principle in an animal model that virally modified dsDNA in apoptotic bodies could break tolerance to self dsDNA and induce dsDNA autoantibodies and end-organ damage.
Inoculation of normal mice with apoptotic bodies, generated by parvovirus B19V helicase NS1 expression, induces dsDNA antibodies and organ damage. This study provides proof of concept that viral modification of host cell DNA can lead to autoimmunity.</description><subject>Animal models</subject><subject>Animals</subject><subject>Antibodies, Antinuclear - blood</subject><subject>Antibodies, Antinuclear - metabolism</subject><subject>Antigens</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Autoantibodies</subject><subject>Autoantigens</subject><subject>Autoimmunity</subject><subject>Brain - pathology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA - immunology</subject><subject>DNA helicase</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Extracellular Vesicles - immunology</subject><subject>Female</subject><subject>Glomerulonephritis - immunology</subject><subject>Glomerulonephritis - pathology</subject><subject>Histones</subject><subject>Immunological tolerance</subject><subject>Immunosuppressive Agents - pharmacology</subject><subject>Inoculation</subject><subject>Kidney Glomerulus - metabolism</subject><subject>Kidney Glomerulus - pathology</subject><subject>Kidneys</subject><subject>Liver - pathology</subject><subject>Major and Brief Reports</subject><subject>Mice</subject><subject>Myocardium - pathology</subject><subject>Parvovirus B19, Human</subject><subject>Parvoviruses</subject><subject>Pristane</subject><subject>Proteins</subject><subject>Staurosporine</subject><subject>Staurosporine - pharmacology</subject><subject>TATA-binding protein</subject><subject>Terpenes - pharmacology</subject><subject>Viral Nonstructural Proteins - metabolism</subject><issn>0022-1899</issn><issn>1537-6613</issn><issn>1537-6613</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFkc1u1DAUhSMEokNhyRZZYsMm1H-J7Q1S6RSoVNpKBbaWY98MHiX2YMcj5jF4YzKaUn42rK7k-_nTPTpV9Zzg1wQrduJD73w-WftdS_iDakEaJuq2JexhtcCY0ppIpY6qJzmvMcacteJxdcQw423TykX148akbdz6VDJ6S9QXdBVDnlKxU0lmQDcpTuADurol6CK4YiGjZSzdAPXtlExw4NAS4vdd8l0MxQ7gLTq13qHTMkUTpvnZ-fnTjKLz4OrrtDIBLc1oVoD24hjMTPpxLAHQR2_hafWoN0OGZ3fzuPr87vzT2Yf68vr9xdnpZW05l1NthJPSctZ0kvWcG8GdaKgVtFV9Q4Uk2DgwSvRWNEpKAKyAdQywoxg6Sdlx9ebg3ZRuBGchzIEGvUl-NGmno_H6703wX_UqbnXLW6kaMQte3QlS_FYgT3r02cIwmACxZE2JUJSSBu_Rl_-g61hSmONpyrlQbUMEman6QNkUc07Q3x9DsN6XrQ9l60PZM__izwT39K92f18Yy-Y_rp_V8rfo</recordid><startdate>20190416</startdate><enddate>20190416</enddate><creator>Puttaraksa, Kanoktip</creator><creator>Pirttinen, Heidi</creator><creator>Karvonen, Kati</creator><creator>Nykky, Jonna</creator><creator>Naides, Stanley J</creator><creator>Gilbert, Leona</creator><general>Oxford University Press</general><scope>TOX</scope><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>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20190416</creationdate><title>Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice</title><author>Puttaraksa, Kanoktip ; Pirttinen, Heidi ; Karvonen, Kati ; Nykky, Jonna ; Naides, Stanley J ; Gilbert, Leona</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c448t-a7d88c435b83f44a74d752c7269f527810adea97fc75988ee09e3b3e0d20eb823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animal models</topic><topic>Animals</topic><topic>Antibodies, Antinuclear - blood</topic><topic>Antibodies, Antinuclear - metabolism</topic><topic>Antigens</topic><topic>Apoptosis</topic><topic>Apoptosis - drug effects</topic><topic>Autoantibodies</topic><topic>Autoantigens</topic><topic>Autoimmunity</topic><topic>Brain - pathology</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA - immunology</topic><topic>DNA helicase</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Enzyme-linked immunosorbent assay</topic><topic>Extracellular Vesicles - immunology</topic><topic>Female</topic><topic>Glomerulonephritis - immunology</topic><topic>Glomerulonephritis - pathology</topic><topic>Histones</topic><topic>Immunological tolerance</topic><topic>Immunosuppressive Agents - pharmacology</topic><topic>Inoculation</topic><topic>Kidney Glomerulus - metabolism</topic><topic>Kidney Glomerulus - pathology</topic><topic>Kidneys</topic><topic>Liver - pathology</topic><topic>Major and Brief Reports</topic><topic>Mice</topic><topic>Myocardium - pathology</topic><topic>Parvovirus B19, Human</topic><topic>Parvoviruses</topic><topic>Pristane</topic><topic>Proteins</topic><topic>Staurosporine</topic><topic>Staurosporine - pharmacology</topic><topic>TATA-binding protein</topic><topic>Terpenes - pharmacology</topic><topic>Viral Nonstructural Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Puttaraksa, Kanoktip</creatorcontrib><creatorcontrib>Pirttinen, Heidi</creatorcontrib><creatorcontrib>Karvonen, Kati</creatorcontrib><creatorcontrib>Nykky, Jonna</creatorcontrib><creatorcontrib>Naides, Stanley J</creatorcontrib><creatorcontrib>Gilbert, Leona</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of infectious diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Puttaraksa, Kanoktip</au><au>Pirttinen, Heidi</au><au>Karvonen, Kati</au><au>Nykky, Jonna</au><au>Naides, Stanley J</au><au>Gilbert, Leona</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice</atitle><jtitle>The Journal of infectious diseases</jtitle><addtitle>J Infect Dis</addtitle><date>2019-04-16</date><risdate>2019</risdate><volume>219</volume><issue>9</issue><spage>1418</spage><epage>1429</epage><pages>1418-1429</pages><issn>0022-1899</issn><issn>1537-6613</issn><eissn>1537-6613</eissn><abstract>Abstract
Background
Viral infection is implicated in development of autoimmunity. Parvovirus B19 (B19V) nonstructural protein, NS1, a helicase, covalently modifies self double-stranded deoxyribonucleic acid (dsDNA) and induces apoptosis. This study tested whether resulting apoptotic bodies (ApoBods) containing virally modified dsDNA could induce autoimmunity in an animal model.
Methods
BALB/c mice were inoculated with (1) pristane-induced, (2) B19V NS1-induced, or (3) staurosporine-induced ApoBods. Serum was tested for dsDNA autoantibodies by Crithidia luciliae staining and enzyme-linked immunosorbent assay. Brain, heart, liver, and kidney pathology was examined. Deposition of self-antigens in glomeruli was examined by staining with antibodies to dsDNA, histones H1 and H4, and TATA-binding protein.
Results
The B19V NS1-induced ApoBod inoculation induced dsDNA autoantibodies in a dose-dependent fashion. Histopathological features of immune-mediated organ damage were evident in pristane-induced and NS1-induced ApoBod groups; severity scores were higher in these groups than in staurosporine-treated groups. Tissue damage was dependent on NS1-induced ApoBod dose. Nucleosomal antigens were deposited in target tissue from pristane-induced and NS1-induced ApoBod inoculated groups, but not in the staurosporine-induced ApoBod inoculated group.
Conclusions
This study demonstrated proof of principle in an animal model that virally modified dsDNA in apoptotic bodies could break tolerance to self dsDNA and induce dsDNA autoantibodies and end-organ damage.
Inoculation of normal mice with apoptotic bodies, generated by parvovirus B19V helicase NS1 expression, induces dsDNA antibodies and organ damage. This study provides proof of concept that viral modification of host cell DNA can lead to autoimmunity.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>30346568</pmid><doi>10.1093/infdis/jiy614</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | The Journal of infectious diseases, 2019-04, Vol.219 (9), p.1418-1429 |
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| source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | Animal models Animals Antibodies, Antinuclear - blood Antibodies, Antinuclear - metabolism Antigens Apoptosis Apoptosis - drug effects Autoantibodies Autoantigens Autoimmunity Brain - pathology Deoxyribonucleic acid DNA DNA - immunology DNA helicase Enzyme Inhibitors - pharmacology Enzyme-linked immunosorbent assay Extracellular Vesicles - immunology Female Glomerulonephritis - immunology Glomerulonephritis - pathology Histones Immunological tolerance Immunosuppressive Agents - pharmacology Inoculation Kidney Glomerulus - metabolism Kidney Glomerulus - pathology Kidneys Liver - pathology Major and Brief Reports Mice Myocardium - pathology Parvovirus B19, Human Parvoviruses Pristane Proteins Staurosporine Staurosporine - pharmacology TATA-binding protein Terpenes - pharmacology Viral Nonstructural Proteins - metabolism |
| title | Parvovirus B19V Nonstructural Protein NS1 Induces Double-Stranded Deoxyribonucleic Acid Autoantibodies and End-Organ Damage in Nonautoimmune Mice |
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