Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites

The identification of immune correlates of protection against infectious pathogens will accelerate the design and optimization of recombinant and subunit vaccines. Systematic analyses such as immunoprofiling including serological, cellular, and molecular assessments supported by computational tools...

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Main Authors: Marie Mura, Burook Misganaw, Aarti Gautam, Tanisha Robinson, Sidhartha Chaudhury, Neha Bansal, Andrew J. Martins, John Tsang, Rasha Hammamieh, Elke Bergmann-Leitner
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Human Vaccines & Immunotherapeutics
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Online Access:https://www.tandfonline.com/doi/10.1080/21645515.2023.2282693
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author Marie Mura
Burook Misganaw
Aarti Gautam
Tanisha Robinson
Sidhartha Chaudhury
Neha Bansal
Andrew J. Martins
John Tsang
Rasha Hammamieh
Elke Bergmann-Leitner
author_facet Marie Mura
Burook Misganaw
Aarti Gautam
Tanisha Robinson
Sidhartha Chaudhury
Neha Bansal
Andrew J. Martins
John Tsang
Rasha Hammamieh
Elke Bergmann-Leitner
author_sort Marie Mura
collection DOAJ
description The identification of immune correlates of protection against infectious pathogens will accelerate the design and optimization of recombinant and subunit vaccines. Systematic analyses such as immunoprofiling including serological, cellular, and molecular assessments supported by computational tools are key to not only identify correlates of protection but also biomarkers of disease susceptibility. The current study expands our previous cellular and serological profiling of vaccine-induced responses to a whole parasite malaria vaccine. The irradiated sporozoite model was chosen as it is considered the most effective vaccine against malaria. In contrast to whole blood transcriptomics analysis, we stimulated peripheral blood mononuclear cells (PBMC) with sporozoites and enriched for antigen-specific cells prior to conducting transcriptomics analysis. By focusing on transcriptional events triggered by antigen-specific stimulation, we were able to uncover quantitative and qualitative differences between protected and non-protected individuals to controlled human malaria infections and identified differentially expressed genes associated with sporozoite-specific responses. Further analyses including pathway and gene set enrichment analysis revealed that vaccination with irradiated sporozoites induced a transcriptomic profile associated with Th1-responses, Interferon-signaling, antigen-presentation, and inflammation. Analyzing longitudinal time points not only post-vaccination but also post-controlled human malaria infection further revealed that the transcriptomic profile of protected vs non-protected individuals was not static but continued to diverge over time. The results lay the foundation for comparing protective immune signatures induced by various vaccine platforms to uncover immune correlates of protection that are common across platforms.
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spelling doaj-art-3dbd74f968ee436faf72c29a5b48eac82025-08-20T02:31:56ZengTaylor & Francis GroupHuman Vaccines & Immunotherapeutics2164-55152164-554X2023-12-0119310.1080/21645515.2023.2282693Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bitesMarie Mura0Burook Misganaw1Aarti Gautam2Tanisha Robinson3Sidhartha Chaudhury4Neha Bansal5Andrew J. Martins6John Tsang7Rasha Hammamieh8Elke Bergmann-Leitner9Immunology Core, Biologics Research & Development, WRAIR-Walter Reed Army Institute of Research, Silver Spring, MD, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD, USAImmunology Core, Biologics Research & Development, WRAIR-Walter Reed Army Institute of Research, Silver Spring, MD, USACenter of Enabling Capabilties, WRAIR-Walter Reed Army Institute of Research, Silver Spring, MD, USAMultiscale Systems Biology Section, Laboratory of Immune System Biology, NIAID, NIH, Bethesda, MD, USAMultiscale Systems Biology Section, Laboratory of Immune System Biology, NIAID, NIH, Bethesda, MD, USAMultiscale Systems Biology Section, Laboratory of Immune System Biology, NIAID, NIH, Bethesda, MD, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD, USAImmunology Core, Biologics Research & Development, WRAIR-Walter Reed Army Institute of Research, Silver Spring, MD, USAThe identification of immune correlates of protection against infectious pathogens will accelerate the design and optimization of recombinant and subunit vaccines. Systematic analyses such as immunoprofiling including serological, cellular, and molecular assessments supported by computational tools are key to not only identify correlates of protection but also biomarkers of disease susceptibility. The current study expands our previous cellular and serological profiling of vaccine-induced responses to a whole parasite malaria vaccine. The irradiated sporozoite model was chosen as it is considered the most effective vaccine against malaria. In contrast to whole blood transcriptomics analysis, we stimulated peripheral blood mononuclear cells (PBMC) with sporozoites and enriched for antigen-specific cells prior to conducting transcriptomics analysis. By focusing on transcriptional events triggered by antigen-specific stimulation, we were able to uncover quantitative and qualitative differences between protected and non-protected individuals to controlled human malaria infections and identified differentially expressed genes associated with sporozoite-specific responses. Further analyses including pathway and gene set enrichment analysis revealed that vaccination with irradiated sporozoites induced a transcriptomic profile associated with Th1-responses, Interferon-signaling, antigen-presentation, and inflammation. Analyzing longitudinal time points not only post-vaccination but also post-controlled human malaria infection further revealed that the transcriptomic profile of protected vs non-protected individuals was not static but continued to diverge over time. The results lay the foundation for comparing protective immune signatures induced by various vaccine platforms to uncover immune correlates of protection that are common across platforms.https://www.tandfonline.com/doi/10.1080/21645515.2023.2282693Malariavaccinehuman controlled malaria infectionprotectiontranscriptomic
spellingShingle Marie Mura
Burook Misganaw
Aarti Gautam
Tanisha Robinson
Sidhartha Chaudhury
Neha Bansal
Andrew J. Martins
John Tsang
Rasha Hammamieh
Elke Bergmann-Leitner
Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
Human Vaccines & Immunotherapeutics
Malaria
vaccine
human controlled malaria infection
protection
transcriptomic
title Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
title_full Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
title_fullStr Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
title_full_unstemmed Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
title_short Human transcriptional signature of protection after Plasmodium falciparum immunization and infectious challenge via mosquito bites
title_sort human transcriptional signature of protection after plasmodium falciparum immunization and infectious challenge via mosquito bites
topic Malaria
vaccine
human controlled malaria infection
protection
transcriptomic
url https://www.tandfonline.com/doi/10.1080/21645515.2023.2282693
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