Sterile immunity to malaria after DNA prime/adenovirus boost immunization is associated with effector memory CD8+T cells targeting AMA1 class I epitopes
Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controll...
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| Published in | PloS one Vol. 9; no. 9; p. e106241 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
11.09.2014
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection.
We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans.
We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. |
|---|---|
| AbstractList | Background Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. Methodology/Principal Findings We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. Conclusions/Significance We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. Background Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-[gamma] activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. Methodology/Principal Findings We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-[gamma] responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-[gamma] responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-[gamma], TNF-[alpha] and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. Conclusions/Significance We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-[gamma] activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-[gamma] responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-[gamma] responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-[gamma], TNF-[alpha] and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection.We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans.We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. Background Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. Methodology/Principal Findings We sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. Conclusions/Significance We suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. BACKGROUNDFifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1) and boosted with human adenovirus-5 (Ad) expressing the same antigens (DNA/Ad). Four volunteers (27%) demonstrated sterile immunity to controlled human malaria infection and, overall, protection was statistically significantly associated with ELISpot and CD8+ T cell IFN-γ activities to AMA1 but not CSP. DNA priming was required for protection, as 18 additional subjects immunized with Ad alone (AdCA) did not develop sterile protection. METHODOLOGY/PRINCIPAL FINDINGSWe sought to identify correlates of protection, recognizing that DNA-priming may induce different responses than AdCA alone. Among protected volunteers, two and three had higher ELISpot and CD8+ T cell IFN-γ responses to CSP and AMA1, respectively, than non-protected volunteers. Unexpectedly, non-protected volunteers in the AdCA trial showed ELISpot and CD8+ T cell IFN-γ responses to AMA1 equal to or higher than the protected volunteers. T cell functionality assessed by intracellular cytokine staining for IFN-γ, TNF-α and IL-2 likewise did not distinguish protected from non-protected volunteers across both trials. However, three of the four protected volunteers showed higher effector to central memory CD8+ T cell ratios to AMA1, and one of these to CSP, than non-protected volunteers for both antigens. These responses were focused on discrete regions of CSP and AMA1. Class I epitopes restricted by A*03 or B*58 supertypes within these regions of AMA1 strongly recalled responses in three of four protected volunteers. We hypothesize that vaccine-induced effector memory CD8+ T cells recognizing a single class I epitope can confer sterile immunity to P. falciparum in humans. CONCLUSIONS/SIGNIFICANCEWe suggest that better understanding of which epitopes within malaria antigens can confer sterile immunity and design of vaccine approaches that elicit responses to these epitopes will increase the potency of next generation gene-based vaccines. |
| Audience | Academic |
| Author | Villasante, Eileen Kim, Yohan Richie, Thomas L Sedegah, Martha Peters, Bjoern Chuang, Ilin Epstein, Judith E Tamminga, Cindy Farooq, Fouzia Abot, Esteban Belmonte, Maria Sette, Alessandro Shi, Meng Huang, Jun McGrath, Shannon Soisson, Lorraine Limbach, Keith Ganeshan, Harini Diggs, Carter Hollingdale, Michael R |
| AuthorAffiliation | Institut de Recherche pour le Développement, France 2 La Jolla Institute for Allergy and Immunology, La Jolla, California, United States of America 1 US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America 3 Division of Medical, Audio, Visual, Library and Statistical Services, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America 4 USAID, Washington, DC, United States of America |
| AuthorAffiliation_xml | – name: Institut de Recherche pour le Développement, France – name: 2 La Jolla Institute for Allergy and Immunology, La Jolla, California, United States of America – name: 4 USAID, Washington, DC, United States of America – name: 1 US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – name: 3 Division of Medical, Audio, Visual, Library and Statistical Services, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America |
| Author_xml | – sequence: 1 givenname: Martha surname: Sedegah fullname: Sedegah, Martha organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 2 givenname: Michael R surname: Hollingdale fullname: Hollingdale, Michael R organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 3 givenname: Fouzia surname: Farooq fullname: Farooq, Fouzia organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 4 givenname: Harini surname: Ganeshan fullname: Ganeshan, Harini organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 5 givenname: Maria surname: Belmonte fullname: Belmonte, Maria organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 6 givenname: Yohan surname: Kim fullname: Kim, Yohan organization: La Jolla Institute for Allergy and Immunology, La Jolla, California, United States of America – sequence: 7 givenname: Bjoern surname: Peters fullname: Peters, Bjoern organization: La Jolla Institute for Allergy and Immunology, La Jolla, California, United States of America – sequence: 8 givenname: Alessandro surname: Sette fullname: Sette, Alessandro organization: La Jolla Institute for Allergy and Immunology, La Jolla, California, United States of America – sequence: 9 givenname: Jun surname: Huang fullname: Huang, Jun organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 10 givenname: Shannon surname: McGrath fullname: McGrath, Shannon organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 11 givenname: Esteban surname: Abot fullname: Abot, Esteban organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 12 givenname: Keith surname: Limbach fullname: Limbach, Keith organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 13 givenname: Meng surname: Shi fullname: Shi, Meng organization: Division of Medical, Audio, Visual, Library and Statistical Services, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America – sequence: 14 givenname: Lorraine surname: Soisson fullname: Soisson, Lorraine organization: USAID, Washington, DC, United States of America – sequence: 15 givenname: Carter surname: Diggs fullname: Diggs, Carter organization: USAID, Washington, DC, United States of America – sequence: 16 givenname: Ilin surname: Chuang fullname: Chuang, Ilin organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 17 givenname: Cindy surname: Tamminga fullname: Tamminga, Cindy organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 18 givenname: Judith E surname: Epstein fullname: Epstein, Judith E organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 19 givenname: Eileen surname: Villasante fullname: Villasante, Eileen organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America – sequence: 20 givenname: Thomas L surname: Richie fullname: Richie, Thomas L organization: US Military Malaria Vaccine Program, Naval Medical Research Center, Silver Spring, Maryland, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25211344$$D View this record in MEDLINE/PubMed |
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| Copyright_xml | – notice: COPYRIGHT 2014 Public Library of Science – notice: 2014. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2014 |
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| DOI | 10.1371/journal.pone.0106241 |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 Conceived and designed the experiments: M. Sedegah. Performed the experiments: FF SM KL M. Sedegah HG JH MB EA. Analyzed the data: M. Sedegah MRH FF SM MB JH M. Shi. Contributed reagents/materials/analysis tools: AS YK BP. Contributed to the writing of the manuscript: M. Sedegah MRH TLR. Intellectual contributions: EV LS CD. Served as principal investigators and performed clinical trials: IC CT JE. Competing Interests: CD and LS from USAID (funders) played a role in study design. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials. |
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| RelatedPersons | Yang, Cindy |
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| Snippet | Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1 (AMA1)... Background Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane... BACKGROUNDFifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane antigen-1... Background Fifteen volunteers were immunized with three doses of plasmid DNA encoding P. falciparum circumsporozoite protein (CSP) and apical membrane... |
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| SubjectTerms | Adenoviridae - immunology Adenoviruses Adult Antigenic determinants Antigens Antigens, Protozoan - administration & dosage Antigens, Protozoan - immunology Biology and life sciences CD8 antigen CD8-Positive T-Lymphocytes - immunology Circumsporozoite protein Comparative analysis Deoxyribonucleic acid DNA DNA - administration & dosage DNA - immunology Effector cells Enzyme-linked immunosorbent assay Epitopes Epitopes - immunology Health aspects Humans Immunity Immunization Immunologic Memory Immunological memory Immunology Infection Infections Interferon Interferon-gamma - immunology Interleukin 2 Interleukin-2 - immunology Liver Lymphocytes Lymphocytes T Malaria Malaria Vaccines - administration & dosage Malaria Vaccines - immunology Malaria, Falciparum - immunology Malaria, Falciparum - parasitology Malaria, Falciparum - pathology Medical research Membrane proteins Membrane Proteins - administration & dosage Membrane Proteins - immunology Memory cells Plasmids Plasmodium falciparum Plasmodium falciparum - immunology Plasmodium falciparum - pathogenicity Priming Proteins Protozoan Proteins - administration & dosage Protozoan Proteins - immunology T cells Tumor Necrosis Factor-alpha - immunology Tumor necrosis factor-α Vaccines Vector-borne diseases Vectors (Biology) Volunteers Yang, Cindy γ-Interferon |
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| Title | Sterile immunity to malaria after DNA prime/adenovirus boost immunization is associated with effector memory CD8+T cells targeting AMA1 class I epitopes |
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