Compartmentalization of innate immune responses in the central nervous system during cryptococcal meningitis/HIV coinfection
The role of innate immunity in the pathogenesis of cryptococcal meningitis is unclear. We hypothesized that natural killer (NK) cell and monocyte responses show central nervous system (CNS) compartment-specific profiles, and are altered by antifungal therapy and combination antiretroviral therapy (c...
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| Veröffentlicht in: | AIDS (London) 2014-03, Vol.28 (5), p.657-666 |
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| creator | Naranbhai, Vivek Chang, Christina C Durgiah, Raveshni Omarjee, Saleha Lim, Andrew Moosa, Mahomed-Yunus S Elliot, Julian H Ndung'u, Thumbi Lewin, Sharon R French, Martyn A Carr, William H |
| description | The role of innate immunity in the pathogenesis of cryptococcal meningitis is unclear. We hypothesized that natural killer (NK) cell and monocyte responses show central nervous system (CNS) compartment-specific profiles, and are altered by antifungal therapy and combination antiretroviral therapy (cART) during cryptococcal meningitis/HIV coinfection.
Substudy of a prospective cohort study of adults with cryptococcal meningitis/HIV coinfection in Durban, South Africa.
We used multiparametric flow cytometry to study compartmentalization of subsets, CD69 (a marker of activation), CXCR3 and CX3CR1 expression, and cytokine secretion of NK cells and monocytes in freshly collected blood and cerebrospinal fluid (CSF) at diagnosis (n = 23), completion of antifungal therapy induction (n = 19), and after a further 4 weeks of cART (n = 9).
Relative to blood, CSF was enriched with CD56(bright) (immunoregulatory) NK cells (P = 0.0004). At enrolment, CXCR3 expression was more frequent among blood CD56(bright) than either blood CD56(dim) (P < 0.0001) or CSF CD56(bright) (P = 0.0002) NK cells. Antifungal therapy diminished blood (P < 0.05), but not CSF CXCR3(pos) NK-cell proportions nor CX3CR1(pos) NK-cell proportions. CD56(bright) and CD56(dim) NK cells were more activated in CSF than blood (P < 0.0001). Antifungal therapy induction reduced CD56(dim) NK-cell activation in CSF (P = 0.02). Activation of blood CD56(bright) and CD56(dim) NK cells was diminished following cART commencement (P < 0.0001, P = 0.03). Immunoregulatory NK cells in CSF tended to secrete higher levels of CXCL10 (P = 0.06) and lower levels of tumor necrosis factor α (P = 0.06) than blood immunoregulatory NK cells. CSF was enriched with nonclassical monocytes (P = 0.001), but antifungal therapy restored proportions of classical monocytes (P = 0.007).
These results highlight CNS activation, trafficking, and function of NK cells and monocytes in cryptococcal meningitis/HIV and implicate immunoregulatory NK cells and proinflammatory monocytes as potential modulators of cryptococcal meningitis pathogenesis during HIV coinfection. |
| doi_str_mv | 10.1097/QAD.0000000000000200 |
| format | Article |
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Substudy of a prospective cohort study of adults with cryptococcal meningitis/HIV coinfection in Durban, South Africa.
We used multiparametric flow cytometry to study compartmentalization of subsets, CD69 (a marker of activation), CXCR3 and CX3CR1 expression, and cytokine secretion of NK cells and monocytes in freshly collected blood and cerebrospinal fluid (CSF) at diagnosis (n = 23), completion of antifungal therapy induction (n = 19), and after a further 4 weeks of cART (n = 9).
Relative to blood, CSF was enriched with CD56(bright) (immunoregulatory) NK cells (P = 0.0004). At enrolment, CXCR3 expression was more frequent among blood CD56(bright) than either blood CD56(dim) (P < 0.0001) or CSF CD56(bright) (P = 0.0002) NK cells. Antifungal therapy diminished blood (P < 0.05), but not CSF CXCR3(pos) NK-cell proportions nor CX3CR1(pos) NK-cell proportions. CD56(bright) and CD56(dim) NK cells were more activated in CSF than blood (P < 0.0001). Antifungal therapy induction reduced CD56(dim) NK-cell activation in CSF (P = 0.02). Activation of blood CD56(bright) and CD56(dim) NK cells was diminished following cART commencement (P < 0.0001, P = 0.03). Immunoregulatory NK cells in CSF tended to secrete higher levels of CXCL10 (P = 0.06) and lower levels of tumor necrosis factor α (P = 0.06) than blood immunoregulatory NK cells. CSF was enriched with nonclassical monocytes (P = 0.001), but antifungal therapy restored proportions of classical monocytes (P = 0.007).
These results highlight CNS activation, trafficking, and function of NK cells and monocytes in cryptococcal meningitis/HIV and implicate immunoregulatory NK cells and proinflammatory monocytes as potential modulators of cryptococcal meningitis pathogenesis during HIV coinfection.</description><identifier>ISSN: 0269-9370</identifier><identifier>EISSN: 1473-5571</identifier><identifier>DOI: 10.1097/QAD.0000000000000200</identifier><identifier>PMID: 24451162</identifier><language>eng</language><publisher>England</publisher><subject>Adult ; AIDS/HIV ; Antigens, CD - analysis ; Antigens, Differentiation, T-Lymphocyte - analysis ; Blood Cells ; Central Nervous System - immunology ; Cerebrospinal Fluid - cytology ; Cohort Studies ; Coinfection - immunology ; Cryptococcus ; Cytokines - secretion ; Female ; Flow Cytometry ; HIV Infections - complications ; Humans ; Immunity, Innate ; Killer Cells, Natural - chemistry ; Killer Cells, Natural - immunology ; Lectins, C-Type - analysis ; Lentivirus ; Male ; Meningitis, Cryptococcal - immunology ; Middle Aged ; Monocytes - chemistry ; Monocytes - immunology ; Prospective Studies ; Receptors, CXCR3 - analysis ; Receptors, Interleukin-8A - analysis ; Retroviridae ; South Africa ; Young Adult</subject><ispartof>AIDS (London), 2014-03, Vol.28 (5), p.657-666</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c386t-25ed7aca8e872f344308023d7a10c7534c2e3784dbe5810f2292f8347b36f1903</citedby><cites>FETCH-LOGICAL-c386t-25ed7aca8e872f344308023d7a10c7534c2e3784dbe5810f2292f8347b36f1903</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24451162$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Naranbhai, Vivek</creatorcontrib><creatorcontrib>Chang, Christina C</creatorcontrib><creatorcontrib>Durgiah, Raveshni</creatorcontrib><creatorcontrib>Omarjee, Saleha</creatorcontrib><creatorcontrib>Lim, Andrew</creatorcontrib><creatorcontrib>Moosa, Mahomed-Yunus S</creatorcontrib><creatorcontrib>Elliot, Julian H</creatorcontrib><creatorcontrib>Ndung'u, Thumbi</creatorcontrib><creatorcontrib>Lewin, Sharon R</creatorcontrib><creatorcontrib>French, Martyn A</creatorcontrib><creatorcontrib>Carr, William H</creatorcontrib><title>Compartmentalization of innate immune responses in the central nervous system during cryptococcal meningitis/HIV coinfection</title><title>AIDS (London)</title><addtitle>AIDS</addtitle><description>The role of innate immunity in the pathogenesis of cryptococcal meningitis is unclear. We hypothesized that natural killer (NK) cell and monocyte responses show central nervous system (CNS) compartment-specific profiles, and are altered by antifungal therapy and combination antiretroviral therapy (cART) during cryptococcal meningitis/HIV coinfection.
Substudy of a prospective cohort study of adults with cryptococcal meningitis/HIV coinfection in Durban, South Africa.
We used multiparametric flow cytometry to study compartmentalization of subsets, CD69 (a marker of activation), CXCR3 and CX3CR1 expression, and cytokine secretion of NK cells and monocytes in freshly collected blood and cerebrospinal fluid (CSF) at diagnosis (n = 23), completion of antifungal therapy induction (n = 19), and after a further 4 weeks of cART (n = 9).
Relative to blood, CSF was enriched with CD56(bright) (immunoregulatory) NK cells (P = 0.0004). At enrolment, CXCR3 expression was more frequent among blood CD56(bright) than either blood CD56(dim) (P < 0.0001) or CSF CD56(bright) (P = 0.0002) NK cells. Antifungal therapy diminished blood (P < 0.05), but not CSF CXCR3(pos) NK-cell proportions nor CX3CR1(pos) NK-cell proportions. CD56(bright) and CD56(dim) NK cells were more activated in CSF than blood (P < 0.0001). Antifungal therapy induction reduced CD56(dim) NK-cell activation in CSF (P = 0.02). Activation of blood CD56(bright) and CD56(dim) NK cells was diminished following cART commencement (P < 0.0001, P = 0.03). Immunoregulatory NK cells in CSF tended to secrete higher levels of CXCL10 (P = 0.06) and lower levels of tumor necrosis factor α (P = 0.06) than blood immunoregulatory NK cells. CSF was enriched with nonclassical monocytes (P = 0.001), but antifungal therapy restored proportions of classical monocytes (P = 0.007).
These results highlight CNS activation, trafficking, and function of NK cells and monocytes in cryptococcal meningitis/HIV and implicate immunoregulatory NK cells and proinflammatory monocytes as potential modulators of cryptococcal meningitis pathogenesis during HIV coinfection.</description><subject>Adult</subject><subject>AIDS/HIV</subject><subject>Antigens, CD - analysis</subject><subject>Antigens, Differentiation, T-Lymphocyte - analysis</subject><subject>Blood Cells</subject><subject>Central Nervous System - immunology</subject><subject>Cerebrospinal Fluid - cytology</subject><subject>Cohort Studies</subject><subject>Coinfection - immunology</subject><subject>Cryptococcus</subject><subject>Cytokines - secretion</subject><subject>Female</subject><subject>Flow Cytometry</subject><subject>HIV Infections - complications</subject><subject>Humans</subject><subject>Immunity, Innate</subject><subject>Killer Cells, Natural - chemistry</subject><subject>Killer Cells, Natural - immunology</subject><subject>Lectins, C-Type - analysis</subject><subject>Lentivirus</subject><subject>Male</subject><subject>Meningitis, Cryptococcal - immunology</subject><subject>Middle Aged</subject><subject>Monocytes - chemistry</subject><subject>Monocytes - immunology</subject><subject>Prospective Studies</subject><subject>Receptors, CXCR3 - analysis</subject><subject>Receptors, Interleukin-8A - analysis</subject><subject>Retroviridae</subject><subject>South Africa</subject><subject>Young Adult</subject><issn>0269-9370</issn><issn>1473-5571</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU9rGzEQxUVJaBy33yAUHXPZRH9X2qNx0sRgCIG010WWZ1uFXWkraQMu_fCRsVNKLp3LwOM384Z5CF1QckVJo64fFzdX5N9ihHxAMyoUr6RU9ATNCKubquGKnKHzlJ4LI4nWH9EZE0JSWrMZ-rMMw2hiHsBn07vfJrvgceiw895kwG4YJg84QhqDT5CKjvNPwLbw0fTYQ3wJU8JplzIMeDtF539gG3djDjZYW5Cyumguu3R9v_qObXC-A7v3-YROO9Mn-Hzsc_Tt6-3T8r5aP9ytlot1Zbmuc8UkbJWxRoNWrONCcKIJ40WjxCrJhWXAlRbbDUhNScdYwzrNhdrwuqMN4XN0edg7xvBrgpTbwSULfW88lONbqmrZ1A2l8v-oFKwuluXLcyQOqI0hpQhdO0Y3mLhrKWn3EbUlovZ9RGXsy9Fh2gyw_Tv0lgl_BeFFjZ4</recordid><startdate>20140313</startdate><enddate>20140313</enddate><creator>Naranbhai, Vivek</creator><creator>Chang, Christina C</creator><creator>Durgiah, Raveshni</creator><creator>Omarjee, Saleha</creator><creator>Lim, Andrew</creator><creator>Moosa, Mahomed-Yunus S</creator><creator>Elliot, Julian H</creator><creator>Ndung'u, Thumbi</creator><creator>Lewin, Sharon R</creator><creator>French, Martyn A</creator><creator>Carr, William H</creator><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>7X8</scope><scope>7T2</scope><scope>7T5</scope><scope>7U2</scope><scope>7U9</scope><scope>C1K</scope><scope>H94</scope><scope>M7N</scope></search><sort><creationdate>20140313</creationdate><title>Compartmentalization of innate immune responses in the central nervous system during cryptococcal meningitis/HIV coinfection</title><author>Naranbhai, Vivek ; Chang, Christina C ; Durgiah, Raveshni ; Omarjee, Saleha ; Lim, Andrew ; Moosa, Mahomed-Yunus S ; Elliot, Julian H ; Ndung'u, Thumbi ; Lewin, Sharon R ; French, Martyn A ; Carr, William H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c386t-25ed7aca8e872f344308023d7a10c7534c2e3784dbe5810f2292f8347b36f1903</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Adult</topic><topic>AIDS/HIV</topic><topic>Antigens, CD - analysis</topic><topic>Antigens, Differentiation, T-Lymphocyte - analysis</topic><topic>Blood Cells</topic><topic>Central Nervous System - immunology</topic><topic>Cerebrospinal Fluid - cytology</topic><topic>Cohort Studies</topic><topic>Coinfection - immunology</topic><topic>Cryptococcus</topic><topic>Cytokines - secretion</topic><topic>Female</topic><topic>Flow Cytometry</topic><topic>HIV Infections - complications</topic><topic>Humans</topic><topic>Immunity, Innate</topic><topic>Killer Cells, Natural - chemistry</topic><topic>Killer Cells, Natural - immunology</topic><topic>Lectins, C-Type - analysis</topic><topic>Lentivirus</topic><topic>Male</topic><topic>Meningitis, Cryptococcal - immunology</topic><topic>Middle Aged</topic><topic>Monocytes - chemistry</topic><topic>Monocytes - immunology</topic><topic>Prospective Studies</topic><topic>Receptors, CXCR3 - analysis</topic><topic>Receptors, Interleukin-8A - analysis</topic><topic>Retroviridae</topic><topic>South Africa</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Naranbhai, Vivek</creatorcontrib><creatorcontrib>Chang, Christina C</creatorcontrib><creatorcontrib>Durgiah, Raveshni</creatorcontrib><creatorcontrib>Omarjee, Saleha</creatorcontrib><creatorcontrib>Lim, Andrew</creatorcontrib><creatorcontrib>Moosa, Mahomed-Yunus S</creatorcontrib><creatorcontrib>Elliot, Julian H</creatorcontrib><creatorcontrib>Ndung'u, Thumbi</creatorcontrib><creatorcontrib>Lewin, Sharon R</creatorcontrib><creatorcontrib>French, Martyn A</creatorcontrib><creatorcontrib>Carr, William H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Health and Safety Science Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Safety Science and Risk</collection><collection>Virology and AIDS Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><jtitle>AIDS (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Naranbhai, Vivek</au><au>Chang, Christina C</au><au>Durgiah, Raveshni</au><au>Omarjee, Saleha</au><au>Lim, Andrew</au><au>Moosa, Mahomed-Yunus S</au><au>Elliot, Julian H</au><au>Ndung'u, Thumbi</au><au>Lewin, Sharon R</au><au>French, Martyn A</au><au>Carr, William H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Compartmentalization of innate immune responses in the central nervous system during cryptococcal meningitis/HIV coinfection</atitle><jtitle>AIDS (London)</jtitle><addtitle>AIDS</addtitle><date>2014-03-13</date><risdate>2014</risdate><volume>28</volume><issue>5</issue><spage>657</spage><epage>666</epage><pages>657-666</pages><issn>0269-9370</issn><eissn>1473-5571</eissn><abstract>The role of innate immunity in the pathogenesis of cryptococcal meningitis is unclear. We hypothesized that natural killer (NK) cell and monocyte responses show central nervous system (CNS) compartment-specific profiles, and are altered by antifungal therapy and combination antiretroviral therapy (cART) during cryptococcal meningitis/HIV coinfection.
Substudy of a prospective cohort study of adults with cryptococcal meningitis/HIV coinfection in Durban, South Africa.
We used multiparametric flow cytometry to study compartmentalization of subsets, CD69 (a marker of activation), CXCR3 and CX3CR1 expression, and cytokine secretion of NK cells and monocytes in freshly collected blood and cerebrospinal fluid (CSF) at diagnosis (n = 23), completion of antifungal therapy induction (n = 19), and after a further 4 weeks of cART (n = 9).
Relative to blood, CSF was enriched with CD56(bright) (immunoregulatory) NK cells (P = 0.0004). At enrolment, CXCR3 expression was more frequent among blood CD56(bright) than either blood CD56(dim) (P < 0.0001) or CSF CD56(bright) (P = 0.0002) NK cells. Antifungal therapy diminished blood (P < 0.05), but not CSF CXCR3(pos) NK-cell proportions nor CX3CR1(pos) NK-cell proportions. CD56(bright) and CD56(dim) NK cells were more activated in CSF than blood (P < 0.0001). Antifungal therapy induction reduced CD56(dim) NK-cell activation in CSF (P = 0.02). Activation of blood CD56(bright) and CD56(dim) NK cells was diminished following cART commencement (P < 0.0001, P = 0.03). Immunoregulatory NK cells in CSF tended to secrete higher levels of CXCL10 (P = 0.06) and lower levels of tumor necrosis factor α (P = 0.06) than blood immunoregulatory NK cells. CSF was enriched with nonclassical monocytes (P = 0.001), but antifungal therapy restored proportions of classical monocytes (P = 0.007).
These results highlight CNS activation, trafficking, and function of NK cells and monocytes in cryptococcal meningitis/HIV and implicate immunoregulatory NK cells and proinflammatory monocytes as potential modulators of cryptococcal meningitis pathogenesis during HIV coinfection.</abstract><cop>England</cop><pmid>24451162</pmid><doi>10.1097/QAD.0000000000000200</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | AIDS (London), 2014-03, Vol.28 (5), p.657-666 |
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| subjects | Adult AIDS/HIV Antigens, CD - analysis Antigens, Differentiation, T-Lymphocyte - analysis Blood Cells Central Nervous System - immunology Cerebrospinal Fluid - cytology Cohort Studies Coinfection - immunology Cryptococcus Cytokines - secretion Female Flow Cytometry HIV Infections - complications Humans Immunity, Innate Killer Cells, Natural - chemistry Killer Cells, Natural - immunology Lectins, C-Type - analysis Lentivirus Male Meningitis, Cryptococcal - immunology Middle Aged Monocytes - chemistry Monocytes - immunology Prospective Studies Receptors, CXCR3 - analysis Receptors, Interleukin-8A - analysis Retroviridae South Africa Young Adult |
| title | Compartmentalization of innate immune responses in the central nervous system during cryptococcal meningitis/HIV coinfection |
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