Controlled human hookworm infection remodels plasmacytoid dendritic cells and regulatory T cells towards profiles seen in natural infections in endemic areas

Mikhael D. Manurung, Friederike Sonnet, Marie-Astrid Hoogerwerf, Jacqueline J. Janse, Yvonne Kruize, Laura de Bes-Roeleveld, Marion König, Alex Loukas, Benjamin G. Dewals, Taniawati Supali, Simon P. Jochems, Meta Roestenberg, Mariateresa Coppola and Maria Yazdanbakhsh ()
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Mikhael D. Manurung: Leiden University Medical Center
Friederike Sonnet: Leiden University Medical Center
Marie-Astrid Hoogerwerf: Leiden University Medical Center
Jacqueline J. Janse: Leiden University Medical Center
Yvonne Kruize: Leiden University Medical Center
Laura de Bes-Roeleveld: Leiden University Medical Center
Marion König: Leiden University Medical Center
Alex Loukas: James Cook University
Benjamin G. Dewals: University of Liège
Taniawati Supali: University of Indonesia
Simon P. Jochems: Leiden University Medical Center
Meta Roestenberg: Leiden University Medical Center
Mariateresa Coppola: Leiden University Medical Center
Maria Yazdanbakhsh: Leiden University Medical Center

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract Hookworm infection remains a significant public health concern, particularly in low- and middle-income countries, where mass drug administration has not stopped reinfection. Developing a vaccine is crucial to complement current control measures, which necessitates a thorough understanding of host immune responses. By leveraging controlled human infection models and high-dimensional immunophenotyping, here we investigated the immune remodeling following infection with 50 Necator americanus L3 hookworm larvae in four naïve volunteers over two years of follow-up and compared the profiles with naturally infected populations in endemic areas. Increased plasmacytoid dendritic cell frequency and diminished responsiveness to Toll-like receptor 7/8 ligand were observed in both controlled and natural infection settings. Despite the increased CD45RA+ regulatory T cell (Tregs) frequencies in both settings, markers of Tregs function, including inducible T-cell costimulatory (ICOS), tumor necrosis factor receptor 2 (TNFR2), and latency-associated peptide (LAP), as well as in vitro Tregs suppressive capacity were higher in natural infections. Taken together, this study provides unique insights into the immunological trajectories following a first-in-life hookworm infection compared to natural infections.

Date: 2024
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DOI: 10.1038/s41467-024-50313-0

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