Mayaro virus pathogenesis and immunity in rhesus macaques
Mayaro virus (MAYV) is a mosquito-transmitted alphavirus that causes debilitating and persistent arthritogenic disease. While MAYV was previously reported to infect non-human primates (NHP), characterization of MAYV pathogenesis is currently lacking. Therefore, in this study we characterized MAYV in...
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| Veröffentlicht in: | PLoS neglected tropical diseases 2023-11, Vol.17 (11), p.e0011742-e0011742 |
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| creator | Weber, Whitney C Labriola, Caralyn S Kreklywich, Craig N Ray, Karina Haese, Nicole N Andoh, Takeshi F Denton, Michael Medica, Samuel Streblow, Magdalene M Smith, Patricia P Mizuno, Nobuyo Frias, Nina Fisher, Miranda B Barber-Axthelm, Aaron M Chun, Kimberly Uttke, Samantha Whitcomb, Danika DeFilippis, Victor Rakshe, Shauna Fei, Suzanne S Axthelm, Michael K Smedley, Jeremy V Streblow, Daniel N |
| description | Mayaro virus (MAYV) is a mosquito-transmitted alphavirus that causes debilitating and persistent arthritogenic disease. While MAYV was previously reported to infect non-human primates (NHP), characterization of MAYV pathogenesis is currently lacking. Therefore, in this study we characterized MAYV infection and immunity in rhesus macaques. To inform the selection of a viral strain for NHP experiments, we evaluated five MAYV strains in C57BL/6 mice and showed that MAYV strain BeAr505411 induced robust tissue dissemination and disease. Three male rhesus macaques were subcutaneously challenged with 10.sup.5 plaque-forming units of this strain into the arms. Peak plasma viremia occurred at 2 days post-infection (dpi). NHPs were taken to necropsy at 10 dpi to assess viral dissemination, which included the muscles and joints, lymphoid tissues, major organs, male reproductive tissues, as well as peripheral and central nervous system tissues. Histological examination demonstrated that MAYV infection was associated with appendicular joint and muscle inflammation as well as presence of perivascular inflammation in a wide variety of tissues. One animal developed a maculopapular rash and two NHP had viral RNA detected in upper torso skin samples, which was associated with the presence of perivascular and perifollicular lymphocytic aggregation. Analysis of longitudinal peripheral blood samples indicated a robust innate and adaptive immune activation, including the presence of anti-MAYV neutralizing antibodies with activity against related Una virus and chikungunya virus. Inflammatory cytokines and monocyte activation also peaked coincident with viremia, which was well supported by our transcriptomic analysis highlighting enrichment of interferon signaling and other antiviral processes at 2 days post MAYV infection. The rhesus macaque model of MAYV infection recapitulates many of the aspects of human infection and is poised to facilitate the evaluation of novel therapies and vaccines targeting this re-emerging virus. |
| doi_str_mv | 10.1371/journal.pntd.0011742 |
| format | Article |
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While MAYV was previously reported to infect non-human primates (NHP), characterization of MAYV pathogenesis is currently lacking. Therefore, in this study we characterized MAYV infection and immunity in rhesus macaques. To inform the selection of a viral strain for NHP experiments, we evaluated five MAYV strains in C57BL/6 mice and showed that MAYV strain BeAr505411 induced robust tissue dissemination and disease. Three male rhesus macaques were subcutaneously challenged with 10.sup.5 plaque-forming units of this strain into the arms. Peak plasma viremia occurred at 2 days post-infection (dpi). NHPs were taken to necropsy at 10 dpi to assess viral dissemination, which included the muscles and joints, lymphoid tissues, major organs, male reproductive tissues, as well as peripheral and central nervous system tissues. Histological examination demonstrated that MAYV infection was associated with appendicular joint and muscle inflammation as well as presence of perivascular inflammation in a wide variety of tissues. One animal developed a maculopapular rash and two NHP had viral RNA detected in upper torso skin samples, which was associated with the presence of perivascular and perifollicular lymphocytic aggregation. Analysis of longitudinal peripheral blood samples indicated a robust innate and adaptive immune activation, including the presence of anti-MAYV neutralizing antibodies with activity against related Una virus and chikungunya virus. Inflammatory cytokines and monocyte activation also peaked coincident with viremia, which was well supported by our transcriptomic analysis highlighting enrichment of interferon signaling and other antiviral processes at 2 days post MAYV infection. The rhesus macaque model of MAYV infection recapitulates many of the aspects of human infection and is poised to facilitate the evaluation of novel therapies and vaccines targeting this re-emerging virus.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0011742</identifier><identifier>PMID: 37983245</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Aggregation ; Analysis ; Animal experimentation ; Antibodies ; Antiviral agents ; Aquatic insects ; Biological response modifiers ; Biology and life sciences ; Body organs ; Cell activation ; Central nervous system ; Chikungunya virus ; Cytokines ; Dengue fever ; Diagnosis ; Disease transmission ; Epidemics ; Evaluation ; Forests ; Genotype & phenotype ; Health aspects ; Immune response ; Immunity ; Infection ; Infections ; Inflammation ; Joint diseases ; Lymphoid tissue ; Males ; Medical research ; Medicine and Health Sciences ; Medicine, Experimental ; Microbiological strains ; Monoclonal antibodies ; Monocytes ; Muscles ; Necropsy ; Nervous tissues ; Pathogenesis ; Peripheral blood ; Research and Analysis Methods ; Rhesus monkey ; Risk factors ; RNA ; RNA viruses ; Robustness ; Skin ; Tissue ; Torso ; Transcriptomics ; Vaccines ; Vector-borne diseases ; Viral antibodies ; Viremia ; Virus diseases ; Viruses ; Zika virus</subject><ispartof>PLoS neglected tropical diseases, 2023-11, Vol.17 (11), p.e0011742-e0011742</ispartof><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Weber 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>2023 Weber et al 2023 Weber et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c551t-9cba356b0fe96bfa0c3c68516987ba2e63fb4698cad9054694447b7c070bba0b3</cites><orcidid>0000-0002-6828-2492</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10695392/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10695392/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids></links><search><creatorcontrib>Weber, Whitney C</creatorcontrib><creatorcontrib>Labriola, Caralyn S</creatorcontrib><creatorcontrib>Kreklywich, Craig N</creatorcontrib><creatorcontrib>Ray, Karina</creatorcontrib><creatorcontrib>Haese, Nicole N</creatorcontrib><creatorcontrib>Andoh, Takeshi F</creatorcontrib><creatorcontrib>Denton, Michael</creatorcontrib><creatorcontrib>Medica, Samuel</creatorcontrib><creatorcontrib>Streblow, Magdalene M</creatorcontrib><creatorcontrib>Smith, Patricia P</creatorcontrib><creatorcontrib>Mizuno, Nobuyo</creatorcontrib><creatorcontrib>Frias, Nina</creatorcontrib><creatorcontrib>Fisher, Miranda B</creatorcontrib><creatorcontrib>Barber-Axthelm, Aaron M</creatorcontrib><creatorcontrib>Chun, Kimberly</creatorcontrib><creatorcontrib>Uttke, Samantha</creatorcontrib><creatorcontrib>Whitcomb, Danika</creatorcontrib><creatorcontrib>DeFilippis, Victor</creatorcontrib><creatorcontrib>Rakshe, Shauna</creatorcontrib><creatorcontrib>Fei, Suzanne S</creatorcontrib><creatorcontrib>Axthelm, Michael K</creatorcontrib><creatorcontrib>Smedley, Jeremy V</creatorcontrib><creatorcontrib>Streblow, Daniel N</creatorcontrib><title>Mayaro virus pathogenesis and immunity in rhesus macaques</title><title>PLoS neglected tropical diseases</title><description>Mayaro virus (MAYV) is a mosquito-transmitted alphavirus that causes debilitating and persistent arthritogenic disease. While MAYV was previously reported to infect non-human primates (NHP), characterization of MAYV pathogenesis is currently lacking. Therefore, in this study we characterized MAYV infection and immunity in rhesus macaques. To inform the selection of a viral strain for NHP experiments, we evaluated five MAYV strains in C57BL/6 mice and showed that MAYV strain BeAr505411 induced robust tissue dissemination and disease. Three male rhesus macaques were subcutaneously challenged with 10.sup.5 plaque-forming units of this strain into the arms. Peak plasma viremia occurred at 2 days post-infection (dpi). NHPs were taken to necropsy at 10 dpi to assess viral dissemination, which included the muscles and joints, lymphoid tissues, major organs, male reproductive tissues, as well as peripheral and central nervous system tissues. Histological examination demonstrated that MAYV infection was associated with appendicular joint and muscle inflammation as well as presence of perivascular inflammation in a wide variety of tissues. One animal developed a maculopapular rash and two NHP had viral RNA detected in upper torso skin samples, which was associated with the presence of perivascular and perifollicular lymphocytic aggregation. Analysis of longitudinal peripheral blood samples indicated a robust innate and adaptive immune activation, including the presence of anti-MAYV neutralizing antibodies with activity against related Una virus and chikungunya virus. Inflammatory cytokines and monocyte activation also peaked coincident with viremia, which was well supported by our transcriptomic analysis highlighting enrichment of interferon signaling and other antiviral processes at 2 days post MAYV infection. The rhesus macaque model of MAYV infection recapitulates many of the aspects of human infection and is poised to facilitate the evaluation of novel therapies and vaccines targeting this re-emerging virus.</description><subject>Aggregation</subject><subject>Analysis</subject><subject>Animal experimentation</subject><subject>Antibodies</subject><subject>Antiviral agents</subject><subject>Aquatic insects</subject><subject>Biological response modifiers</subject><subject>Biology and life sciences</subject><subject>Body organs</subject><subject>Cell activation</subject><subject>Central nervous system</subject><subject>Chikungunya virus</subject><subject>Cytokines</subject><subject>Dengue fever</subject><subject>Diagnosis</subject><subject>Disease transmission</subject><subject>Epidemics</subject><subject>Evaluation</subject><subject>Forests</subject><subject>Genotype & phenotype</subject><subject>Health aspects</subject><subject>Immune response</subject><subject>Immunity</subject><subject>Infection</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Joint diseases</subject><subject>Lymphoid tissue</subject><subject>Males</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Medicine, Experimental</subject><subject>Microbiological strains</subject><subject>Monoclonal antibodies</subject><subject>Monocytes</subject><subject>Muscles</subject><subject>Necropsy</subject><subject>Nervous tissues</subject><subject>Pathogenesis</subject><subject>Peripheral blood</subject><subject>Research and Analysis Methods</subject><subject>Rhesus monkey</subject><subject>Risk factors</subject><subject>RNA</subject><subject>RNA viruses</subject><subject>Robustness</subject><subject>Skin</subject><subject>Tissue</subject><subject>Torso</subject><subject>Transcriptomics</subject><subject>Vaccines</subject><subject>Vector-borne diseases</subject><subject>Viral 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virus pathogenesis and immunity in rhesus macaques</title><author>Weber, Whitney C ; Labriola, Caralyn S ; Kreklywich, Craig N ; Ray, Karina ; Haese, Nicole N ; Andoh, Takeshi F ; Denton, Michael ; Medica, Samuel ; Streblow, Magdalene M ; Smith, Patricia P ; Mizuno, Nobuyo ; Frias, Nina ; Fisher, Miranda B ; Barber-Axthelm, Aaron M ; Chun, Kimberly ; Uttke, Samantha ; Whitcomb, Danika ; DeFilippis, Victor ; Rakshe, Shauna ; Fei, Suzanne S ; Axthelm, Michael K ; Smedley, Jeremy V ; Streblow, Daniel N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c551t-9cba356b0fe96bfa0c3c68516987ba2e63fb4698cad9054694447b7c070bba0b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Aggregation</topic><topic>Analysis</topic><topic>Animal experimentation</topic><topic>Antibodies</topic><topic>Antiviral agents</topic><topic>Aquatic insects</topic><topic>Biological response modifiers</topic><topic>Biology and life sciences</topic><topic>Body organs</topic><topic>Cell activation</topic><topic>Central nervous system</topic><topic>Chikungunya virus</topic><topic>Cytokines</topic><topic>Dengue fever</topic><topic>Diagnosis</topic><topic>Disease transmission</topic><topic>Epidemics</topic><topic>Evaluation</topic><topic>Forests</topic><topic>Genotype & phenotype</topic><topic>Health aspects</topic><topic>Immune response</topic><topic>Immunity</topic><topic>Infection</topic><topic>Infections</topic><topic>Inflammation</topic><topic>Joint diseases</topic><topic>Lymphoid tissue</topic><topic>Males</topic><topic>Medical research</topic><topic>Medicine and Health Sciences</topic><topic>Medicine, Experimental</topic><topic>Microbiological strains</topic><topic>Monoclonal antibodies</topic><topic>Monocytes</topic><topic>Muscles</topic><topic>Necropsy</topic><topic>Nervous tissues</topic><topic>Pathogenesis</topic><topic>Peripheral blood</topic><topic>Research and Analysis Methods</topic><topic>Rhesus monkey</topic><topic>Risk factors</topic><topic>RNA</topic><topic>RNA viruses</topic><topic>Robustness</topic><topic>Skin</topic><topic>Tissue</topic><topic>Torso</topic><topic>Transcriptomics</topic><topic>Vaccines</topic><topic>Vector-borne diseases</topic><topic>Viral antibodies</topic><topic>Viremia</topic><topic>Virus diseases</topic><topic>Viruses</topic><topic>Zika virus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Weber, Whitney C</creatorcontrib><creatorcontrib>Labriola, Caralyn S</creatorcontrib><creatorcontrib>Kreklywich, Craig N</creatorcontrib><creatorcontrib>Ray, Karina</creatorcontrib><creatorcontrib>Haese, Nicole N</creatorcontrib><creatorcontrib>Andoh, Takeshi F</creatorcontrib><creatorcontrib>Denton, Michael</creatorcontrib><creatorcontrib>Medica, Samuel</creatorcontrib><creatorcontrib>Streblow, Magdalene M</creatorcontrib><creatorcontrib>Smith, Patricia 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M</au><au>Chun, Kimberly</au><au>Uttke, Samantha</au><au>Whitcomb, Danika</au><au>DeFilippis, Victor</au><au>Rakshe, Shauna</au><au>Fei, Suzanne S</au><au>Axthelm, Michael K</au><au>Smedley, Jeremy V</au><au>Streblow, Daniel N</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mayaro virus pathogenesis and immunity in rhesus macaques</atitle><jtitle>PLoS neglected tropical diseases</jtitle><date>2023-11-01</date><risdate>2023</risdate><volume>17</volume><issue>11</issue><spage>e0011742</spage><epage>e0011742</epage><pages>e0011742-e0011742</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>Mayaro virus (MAYV) is a mosquito-transmitted alphavirus that causes debilitating and persistent arthritogenic disease. While MAYV was previously reported to infect non-human primates (NHP), characterization of MAYV pathogenesis is currently lacking. Therefore, in this study we characterized MAYV infection and immunity in rhesus macaques. To inform the selection of a viral strain for NHP experiments, we evaluated five MAYV strains in C57BL/6 mice and showed that MAYV strain BeAr505411 induced robust tissue dissemination and disease. Three male rhesus macaques were subcutaneously challenged with 10.sup.5 plaque-forming units of this strain into the arms. Peak plasma viremia occurred at 2 days post-infection (dpi). NHPs were taken to necropsy at 10 dpi to assess viral dissemination, which included the muscles and joints, lymphoid tissues, major organs, male reproductive tissues, as well as peripheral and central nervous system tissues. Histological examination demonstrated that MAYV infection was associated with appendicular joint and muscle inflammation as well as presence of perivascular inflammation in a wide variety of tissues. One animal developed a maculopapular rash and two NHP had viral RNA detected in upper torso skin samples, which was associated with the presence of perivascular and perifollicular lymphocytic aggregation. Analysis of longitudinal peripheral blood samples indicated a robust innate and adaptive immune activation, including the presence of anti-MAYV neutralizing antibodies with activity against related Una virus and chikungunya virus. Inflammatory cytokines and monocyte activation also peaked coincident with viremia, which was well supported by our transcriptomic analysis highlighting enrichment of interferon signaling and other antiviral processes at 2 days post MAYV infection. The rhesus macaque model of MAYV infection recapitulates many of the aspects of human infection and is poised to facilitate the evaluation of novel therapies and vaccines targeting this re-emerging virus.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>37983245</pmid><doi>10.1371/journal.pntd.0011742</doi><orcidid>https://orcid.org/0000-0002-6828-2492</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1935-2735 |
| ispartof | PLoS neglected tropical diseases, 2023-11, Vol.17 (11), p.e0011742-e0011742 |
| issn | 1935-2735 1935-2727 1935-2735 |
| language | eng |
| recordid | cdi_plos_journals_3069183229 |
| source | Public Library of Science (PLoS) Journals Open Access; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; PubMed Central Open Access |
| subjects | Aggregation Analysis Animal experimentation Antibodies Antiviral agents Aquatic insects Biological response modifiers Biology and life sciences Body organs Cell activation Central nervous system Chikungunya virus Cytokines Dengue fever Diagnosis Disease transmission Epidemics Evaluation Forests Genotype & phenotype Health aspects Immune response Immunity Infection Infections Inflammation Joint diseases Lymphoid tissue Males Medical research Medicine and Health Sciences Medicine, Experimental Microbiological strains Monoclonal antibodies Monocytes Muscles Necropsy Nervous tissues Pathogenesis Peripheral blood Research and Analysis Methods Rhesus monkey Risk factors RNA RNA viruses Robustness Skin Tissue Torso Transcriptomics Vaccines Vector-borne diseases Viral antibodies Viremia Virus diseases Viruses Zika virus |
| title | Mayaro virus pathogenesis and immunity in rhesus macaques |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T02%3A24%3A46IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Mayaro%20virus%20pathogenesis%20and%20immunity%20in%20rhesus%20macaques&rft.jtitle=PLoS%20neglected%20tropical%20diseases&rft.au=Weber,%20Whitney%20C&rft.date=2023-11-01&rft.volume=17&rft.issue=11&rft.spage=e0011742&rft.epage=e0011742&rft.pages=e0011742-e0011742&rft.issn=1935-2735&rft.eissn=1935-2735&rft_id=info:doi/10.1371/journal.pntd.0011742&rft_dat=%3Cgale_plos_%3EA775219147%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3069183229&rft_id=info:pmid/37983245&rft_galeid=A775219147&rft_doaj_id=oai_doaj_org_article_9deed2140f2e40a9aabdd1d8e7593a3d&rfr_iscdi=true |