{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T04:28:26Z","timestamp":1790137706692,"version":"4.0.1"},"reference-count":62,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2021,12,8]],"date-time":"2021-12-08T00:00:00Z","timestamp":1638921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009139","name":"Deutsches Zentrum f\u00fcr Infektionsforschung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009139","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,4,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Relatively little is known about the ex vivo frequency and phenotype of the Plasmodium falciparum-specific CD4+ T-cell response in humans. The exported protein 1 (EXP1) is expressed by plasmodia at both, the liver stage and blood stage, of infection making it a potential target for CD4+ and CD8+ effector T cells. Here, a fluorochrome-labelled HLA-DRB1\u221711:01-restriced MHC class II tetramer derived from the P. falciparum EXP1 (aa62-74) was established for ex vivo tetramer analysis and magnetic bead enrichment in 10 patients with acute malaria. EXP1-specific CD4+ T cells were detectable in 9 out of 10 (90%) malaria patients expressing the HLA-DRB1\u221711 molecule with an average ex vivo frequency of 0.11% (0\u20130.22%) of total CD4+ T cells. The phenotype of EXP1-specific CD4+ T cells was further assessed using co-staining with activation (CD38, HLA-DR, CD26), differentiation (CD45RO, CCR7, KLRG1, CD127), senescence (CD57), and co-inhibitory (PD-1, TIGIT, LAG-3, TIM-3) markers as well as the ectonucleotidases CD39 and CD73. EXP1-specific tetramer+ CD4+ T cells had a distinct phenotype compared to bulk CD4+ T cells and displayed a highly activated effector memory phenotype with elevated levels of co-inhibitory receptors and activation markers: EXP1-specific CD4+ T cells universally expressed the co-inhibitory receptors PD-1 and TIGIT as well as the activation marker CD38 and showed elevated frequencies of CD39. These results demonstrate that MHC class II tetramer enrichment is a sensitive approach to investigate ex vivo antigen-specific CD4+ T cells in malaria patients that will aid further analysis of the role of CD4+ T cells during malaria.<\/jats:p>","DOI":"10.1093\/cei\/uxab027","type":"journal-article","created":{"date-parts":[[2022,1,12]],"date-time":"2022-01-12T18:52:56Z","timestamp":1642013576000},"page":"227-236","source":"Crossref","is-referenced-by-count":9,"title":["Deciphering the <i>Plasmodium falciparum<\/i> malaria-specific CD4+ T-cell response: <i>ex vivo<\/i> detection of high frequencies of PD-1+TIGIT+ EXP1-specific CD4+ T cells using a novel HLA-DR11-restricted MHC class II tetramer"],"prefix":"10.1093","volume":"207","author":[{"given":"Sophia","family":"Schulte","sequence":"first","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janna","family":"Heide","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christin","family":"Ackermann","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sven","family":"Peine","sequence":"additional","affiliation":[{"name":"Department of Transfusion Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Ramharter","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"},{"name":"Department of Tropical Medicine, Bernhard-Nocht-Institute for Tropical Medicine (BNITM), Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Sophia","family":"Mackroth","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"},{"name":"Department of Tropical Medicine, Bernhard-Nocht-Institute for Tropical Medicine (BNITM), Hamburg, Germany"},{"name":"Protozoa Immunology, Bernhard-Nocht-Institute for Tropical Medicine (BNITM), Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robin","family":"Woost","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Jacobs","sequence":"additional","affiliation":[{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"},{"name":"Protozoa Immunology, Bernhard-Nocht-Institute for Tropical Medicine (BNITM), Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5033-1938","authenticated-orcid":false,"given":"Julian","family":"Schulze zur Wiesch","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany"},{"name":"German Center for Infection Research (DZIF), Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, Hamburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,12,8]]},"reference":[{"key":"2022040512173821300_CIT0001","doi-asserted-by":"crossref","first-page":"1931","DOI":"10.1126\/science.8100366","article-title":"The role of TH1 and TH2 cells in a rodent malaria infection.","volume":"260","author":"Taylor-Robinson","year":"1993","journal-title":"Science"},{"key":"2022040512173821300_CIT0002","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1111\/j.1365-3024.1993.tb00614.x","article-title":"Protective CD4+ T-cell lines raised against Plasmodium chabaudi show characteristics of either Th1 or Th2 cells.","volume":"15","author":"Taylor-Robinson","year":"1993","journal-title":"Parasite Immunol"},{"key":"2022040512173821300_CIT0003","doi-asserted-by":"crossref","first-page":"3081","DOI":"10.1128\/iai.56.12.3081-3088.1988","article-title":"Roles of CD4- and CD8-bearing T lymphocytes in the immune response to the erythrocytic stages of Plasmodium chabaudi.","volume":"56","author":"S\u00fcss","year":"1988","journal-title":"Infect Immun"},{"key":"2022040512173821300_CIT0004","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1111\/imr.12804","article-title":"The regulation of CD4+ T cells during malaria.","volume":"293","author":"Kumar","year":"2020","journal-title":"Immunol Rev"},{"key":"2022040512173821300_CIT0005","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1038\/nature21060","article-title":"Sterile protection against human malaria by chemoattenuated PfSPZ 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plasmodium vivax malaria impairs cytokine production.","volume":"212","author":"Costa","year":"2015","journal-title":"J Infect Dis"},{"key":"2022040512173821300_CIT0012","doi-asserted-by":"crossref","first-page":"576743","DOI":"10.3389\/fimmu.2020.576743","article-title":"Blockade of LAG-3 in PD-L1-deficient mice enhances clearance of blood stage malaria independent of humoral responses.","volume":"11","author":"Furtado","year":"2020","journal-title":"Front Immunol"},{"key":"2022040512173821300_CIT0013","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1002\/eji.200324477","article-title":"CTLA-4-dependent mechanisms prevent T cell induced-liver pathology during the erythrocyte stage of Plasmodium berghei malaria.","volume":"34","author":"Jacobs","year":"2004","journal-title":"Eur J Immunol"},{"key":"2022040512173821300_CIT0014","doi-asserted-by":"crossref","first-page":"e12723","DOI":"10.1111\/pim.12723","article-title":"Combinatorial Tim-3 and PD-1 activity sustains antigen-specific Th1 cell numbers during blood-stage malaria.","volume":"42","author":"Dookie","year":"2020","journal-title":"Parasite Immunol"},{"key":"2022040512173821300_CIT0015","doi-asserted-by":"crossref","first-page":"10624","DOI":"10.1038\/s41598-019-47024-8","article-title":"HCV-specific CD4+ T cells of patients with acute and chronic HCV infection display high expression of TIGIT and other co-inhibitory molecules.","volume":"9","author":"Ackermann","year":"2019","journal-title":"Sci Rep"},{"key":"2022040512173821300_CIT0016","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/nature05115","article-title":"PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression.","volume":"443","author":"Day","year":"2006","journal-title":"Nature"},{"key":"2022040512173821300_CIT0017","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1172\/JCI126277","article-title":"Hepatitis C virus-specific CD4+ T cell phenotype and function 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