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Innate immune responses to malaria-infected erythrocytes in pregnant women: Effects of gravidity, malaria infection, and geographic location
Malaria in pregnancy causes maternal, fetal and neonatal morbidity and mortality, and maternal innate immune responses are implicated in pathogenesis of these complications. The effects of malaria exposure and obstetric and demographic factors on the early maternal immune response are poorly underst...
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Published in: | PloS one 2020-07, Vol.15 (7), p.e0236375-e0236375 |
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description | Malaria in pregnancy causes maternal, fetal and neonatal morbidity and mortality, and maternal innate immune responses are implicated in pathogenesis of these complications. The effects of malaria exposure and obstetric and demographic factors on the early maternal immune response are poorly understood. Peripheral blood mononuclear cell responses to Plasmodium falciparum-infected erythrocytes and phytohemagglutinin were compared between pregnant women from Papua New Guinea (malaria-exposed) with and without current malaria infection and from Australia (unexposed). Elicited levels of inflammatory cytokines at 48 h and 24 h (interferon [gamma], IFN-[gamma] only) and the cellular sources of IFN-[gamma] were analysed. Among Papua New Guinean women, microscopic malaria at enrolment did not alter peripheral blood mononuclear cell responses. Compared to samples from Australia, cells from Papua New Guinean women secreted more inflammatory cytokines tumor necrosis factor-[alpha], interleukin 1[beta], interleukin 6 and IFN-[gamma]; p |
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The effects of malaria exposure and obstetric and demographic factors on the early maternal immune response are poorly understood. Peripheral blood mononuclear cell responses to Plasmodium falciparum-infected erythrocytes and phytohemagglutinin were compared between pregnant women from Papua New Guinea (malaria-exposed) with and without current malaria infection and from Australia (unexposed). Elicited levels of inflammatory cytokines at 48 h and 24 h (interferon [gamma], IFN-[gamma] only) and the cellular sources of IFN-[gamma] were analysed. Among Papua New Guinean women, microscopic malaria at enrolment did not alter peripheral blood mononuclear cell responses. Compared to samples from Australia, cells from Papua New Guinean women secreted more inflammatory cytokines tumor necrosis factor-[alpha], interleukin 1[beta], interleukin 6 and IFN-[gamma]; p<0.001 for all assays, and more natural killer cells produced IFN-[gamma] in response to infected erythrocytes and phytohemagglutinin. In both populations, cytokine responses were not affected by gravidity, except that in the Papua New Guinean cohort multigravid women had higher IFN-[gamma] secretion at 24 h (p = 0.029) and an increased proportion of IFN-[gamma].sup.+ V[delta]2 [gamma][delta] T cells (p = 0.003). Cytokine levels elicited by a pregnancy malaria-specific CSA binding parasite line, CS2, were broadly similar to those elicited by CD36-binding line P6A1. Geographic location and, to some extent, gravidity influence maternal innate immunity to malaria.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0236375</identifier><identifier>PMID: 32726331</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Anemia ; Binding ; Biology and Life Sciences ; Blood ; CD36 antigen ; Complications ; Cytokines ; Development and progression ; Diagnosis ; Erythrocytes ; Ethics ; Fetuses ; Geographical locations ; Health aspects ; Hospitals ; Immune response ; Immune system ; Infections ; Inflammation ; Innate immunity ; Interferon ; Interleukin 6 ; Lymphocytes ; Lymphocytes T ; Malaria ; Medical research ; Medicine ; Medicine and Health Sciences ; Microscopy ; Morbidity ; Natural killer cells ; Neonates ; Parasites ; Pathogenesis ; Peripheral blood ; Plasmodium falciparum ; Pregnancy ; Pregnancy complications ; Pregnant women ; Proteins ; Red blood cells ; Tumor necrosis factor-TNF ; Tumor necrosis factor-α ; Vector-borne diseases ; Vectors (Biology) ; Womens health ; γ-Interferon</subject><ispartof>PloS one, 2020-07, Vol.15 (7), p.e0236375-e0236375</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Jabbarzare 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>2020 Jabbarzare et al 2020 Jabbarzare et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c618t-e482b0f035565e3f6d0d60ae89221e8c24c541c4a469c8ea34cfd8906ed4e74b3</cites><orcidid>0000-0001-7369-9463</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2428409981/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2428409981?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids></links><search><contributor>Carvalho, Luzia Helena</contributor><creatorcontrib>Jabbarzare, Marzieh</creatorcontrib><creatorcontrib>Njie, Madi</creatorcontrib><creatorcontrib>Jaworowski, Anthony</creatorcontrib><creatorcontrib>Umbers, Alexandra J</creatorcontrib><creatorcontrib>Ome-Kaius, Maria</creatorcontrib><creatorcontrib>Hasang, Wina</creatorcontrib><creatorcontrib>Randall, Louise M</creatorcontrib><creatorcontrib>Kalionis, Bill</creatorcontrib><creatorcontrib>Rogerson, Stephen J</creatorcontrib><title>Innate immune responses to malaria-infected erythrocytes in pregnant women: Effects of gravidity, malaria infection, and geographic location</title><title>PloS one</title><description>Malaria in pregnancy causes maternal, fetal and neonatal morbidity and mortality, and maternal innate immune responses are implicated in pathogenesis of these complications. The effects of malaria exposure and obstetric and demographic factors on the early maternal immune response are poorly understood. Peripheral blood mononuclear cell responses to Plasmodium falciparum-infected erythrocytes and phytohemagglutinin were compared between pregnant women from Papua New Guinea (malaria-exposed) with and without current malaria infection and from Australia (unexposed). Elicited levels of inflammatory cytokines at 48 h and 24 h (interferon [gamma], IFN-[gamma] only) and the cellular sources of IFN-[gamma] were analysed. Among Papua New Guinean women, microscopic malaria at enrolment did not alter peripheral blood mononuclear cell responses. Compared to samples from Australia, cells from Papua New Guinean women secreted more inflammatory cytokines tumor necrosis factor-[alpha], interleukin 1[beta], interleukin 6 and IFN-[gamma]; p<0.001 for all assays, and more natural killer cells produced IFN-[gamma] in response to infected erythrocytes and phytohemagglutinin. In both populations, cytokine responses were not affected by gravidity, except that in the Papua New Guinean cohort multigravid women had higher IFN-[gamma] secretion at 24 h (p = 0.029) and an increased proportion of IFN-[gamma].sup.+ V[delta]2 [gamma][delta] T cells (p = 0.003). Cytokine levels elicited by a pregnancy malaria-specific CSA binding parasite line, CS2, were broadly similar to those elicited by CD36-binding line P6A1. Geographic location and, to some extent, gravidity influence maternal innate immunity to malaria.</description><subject>Anemia</subject><subject>Binding</subject><subject>Biology and Life Sciences</subject><subject>Blood</subject><subject>CD36 antigen</subject><subject>Complications</subject><subject>Cytokines</subject><subject>Development and progression</subject><subject>Diagnosis</subject><subject>Erythrocytes</subject><subject>Ethics</subject><subject>Fetuses</subject><subject>Geographical locations</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interferon</subject><subject>Interleukin 6</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Malaria</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Microscopy</subject><subject>Morbidity</subject><subject>Natural killer cells</subject><subject>Neonates</subject><subject>Parasites</subject><subject>Pathogenesis</subject><subject>Peripheral blood</subject><subject>Plasmodium falciparum</subject><subject>Pregnancy</subject><subject>Pregnancy complications</subject><subject>Pregnant women</subject><subject>Proteins</subject><subject>Red blood cells</subject><subject>Tumor necrosis factor-TNF</subject><subject>Tumor necrosis factor-α</subject><subject>Vector-borne diseases</subject><subject>Vectors (Biology)</subject><subject>Womens 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immune responses to malaria-infected erythrocytes in pregnant women: Effects of gravidity, malaria infection, and geographic location</title><author>Jabbarzare, Marzieh ; Njie, Madi ; Jaworowski, Anthony ; Umbers, Alexandra J ; Ome-Kaius, Maria ; Hasang, Wina ; Randall, Louise M ; Kalionis, Bill ; Rogerson, Stephen J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c618t-e482b0f035565e3f6d0d60ae89221e8c24c541c4a469c8ea34cfd8906ed4e74b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Anemia</topic><topic>Binding</topic><topic>Biology and Life Sciences</topic><topic>Blood</topic><topic>CD36 antigen</topic><topic>Complications</topic><topic>Cytokines</topic><topic>Development and progression</topic><topic>Diagnosis</topic><topic>Erythrocytes</topic><topic>Ethics</topic><topic>Fetuses</topic><topic>Geographical locations</topic><topic>Health 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one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jabbarzare, Marzieh</au><au>Njie, Madi</au><au>Jaworowski, Anthony</au><au>Umbers, Alexandra J</au><au>Ome-Kaius, Maria</au><au>Hasang, Wina</au><au>Randall, Louise M</au><au>Kalionis, Bill</au><au>Rogerson, Stephen J</au><au>Carvalho, Luzia Helena</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Innate immune responses to malaria-infected erythrocytes in pregnant women: Effects of gravidity, malaria infection, and geographic location</atitle><jtitle>PloS one</jtitle><date>2020-07-29</date><risdate>2020</risdate><volume>15</volume><issue>7</issue><spage>e0236375</spage><epage>e0236375</epage><pages>e0236375-e0236375</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Malaria in pregnancy causes maternal, fetal and neonatal morbidity and mortality, and maternal innate immune responses are implicated in pathogenesis of these complications. The effects of malaria exposure and obstetric and demographic factors on the early maternal immune response are poorly understood. Peripheral blood mononuclear cell responses to Plasmodium falciparum-infected erythrocytes and phytohemagglutinin were compared between pregnant women from Papua New Guinea (malaria-exposed) with and without current malaria infection and from Australia (unexposed). Elicited levels of inflammatory cytokines at 48 h and 24 h (interferon [gamma], IFN-[gamma] only) and the cellular sources of IFN-[gamma] were analysed. Among Papua New Guinean women, microscopic malaria at enrolment did not alter peripheral blood mononuclear cell responses. Compared to samples from Australia, cells from Papua New Guinean women secreted more inflammatory cytokines tumor necrosis factor-[alpha], interleukin 1[beta], interleukin 6 and IFN-[gamma]; p<0.001 for all assays, and more natural killer cells produced IFN-[gamma] in response to infected erythrocytes and phytohemagglutinin. In both populations, cytokine responses were not affected by gravidity, except that in the Papua New Guinean cohort multigravid women had higher IFN-[gamma] secretion at 24 h (p = 0.029) and an increased proportion of IFN-[gamma].sup.+ V[delta]2 [gamma][delta] T cells (p = 0.003). Cytokine levels elicited by a pregnancy malaria-specific CSA binding parasite line, CS2, were broadly similar to those elicited by CD36-binding line P6A1. Geographic location and, to some extent, gravidity influence maternal innate immunity to malaria.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>32726331</pmid><doi>10.1371/journal.pone.0236375</doi><tpages>e0236375</tpages><orcidid>https://orcid.org/0000-0001-7369-9463</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anemia Binding Biology and Life Sciences Blood CD36 antigen Complications Cytokines Development and progression Diagnosis Erythrocytes Ethics Fetuses Geographical locations Health aspects Hospitals Immune response Immune system Infections Inflammation Innate immunity Interferon Interleukin 6 Lymphocytes Lymphocytes T Malaria Medical research Medicine Medicine and Health Sciences Microscopy Morbidity Natural killer cells Neonates Parasites Pathogenesis Peripheral blood Plasmodium falciparum Pregnancy Pregnancy complications Pregnant women Proteins Red blood cells Tumor necrosis factor-TNF Tumor necrosis factor-α Vector-borne diseases Vectors (Biology) Womens health γ-Interferon |
title | Innate immune responses to malaria-infected erythrocytes in pregnant women: Effects of gravidity, malaria infection, and geographic location |
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