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Age-dependent changes in circulating Tfh cells influence development of functional malaria antibodies in children

Author

Listed:
  • Jo-Anne Chan

    (Burnet Institute
    Monash University
    The University of Melbourne)

  • Jessica R. Loughland

    (QIMR-Berghofer Medical Research Institute
    Menzies School of Health Research)

  • Lauren de la Parte

    (Stanford University)

  • Satomi Okano

    (QIMR-Berghofer Medical Research Institute)

  • Isaac Ssewanyana

    (Infectious Diseases Research Collaboration
    London School of Hygiene and Tropical Medicine)

  • Mayimuna Nalubega

    (QIMR-Berghofer Medical Research Institute
    Infectious Diseases Research Collaboration
    University of Queensland)

  • Felistas Nankya

    (Infectious Diseases Research Collaboration)

  • Kenneth Musinguzi

    (Infectious Diseases Research Collaboration)

  • John Rek

    (Infectious Diseases Research Collaboration)

  • Emmanuel Arinaitwe

    (Infectious Diseases Research Collaboration)

  • Peta Tipping

    (Menzies School of Health Research)

  • Peter Bourke

    (Cairns Hospital)

  • Dean Andrew

    (QIMR-Berghofer Medical Research Institute)

  • Nicholas Dooley

    (QIMR-Berghofer Medical Research Institute
    Griffith University)

  • Arya SheelaNair

    (QIMR-Berghofer Medical Research Institute)

  • Bruce D. Wines

    (Burnet Institute
    Monash University
    The University of Melbourne)

  • P. Mark Hogarth

    (Burnet Institute
    Monash University
    The University of Melbourne)

  • James G. Beeson

    (Burnet Institute
    The University of Melbourne
    Monash University)

  • Bryan Greenhouse

    (University of California San Francisco)

  • Grant Dorsey

    (University of California San Francisco)

  • Moses Kamya

    (Infectious Diseases Research Collaboration)

  • Gunter Hartel

    (QIMR-Berghofer Medical Research Institute)

  • Gabriela Minigo

    (Menzies School of Health Research
    Charles Darwin University)

  • Margaret Feeney

    (University of California San Francisco)

  • Prasanna Jagannathan

    (Stanford University)

  • Michelle J. Boyle

    (Burnet Institute
    QIMR-Berghofer Medical Research Institute
    Menzies School of Health Research
    University of Queensland)

Abstract

T-follicular helper (Tfh) cells are key drivers of antibodies that protect from malaria. However, little is known regarding the host and parasite factors that influence Tfh and functional antibody development. Here, we use samples from a large cross-sectional study of children residing in an area of high malaria transmission in Uganda to characterize Tfh cells and functional antibodies to multiple parasites stages. We identify a dramatic re-distribution of the Tfh cell compartment with age that is independent of malaria exposure, with Th2-Tfh cells predominating in early childhood, while Th1-Tfh cell gradually increase to adult levels over the first decade of life. Functional antibody acquisition is age-dependent and hierarchical acquired based on parasite stage, with merozoite responses followed by sporozoite and gametocyte antibodies. Antibodies are boosted in children with current infection, and are higher in females. The children with the very highest antibody levels have increased Tfh cell activation and proliferation, consistent with a key role of Tfh cells in antibody development. Together, these data reveal a complex relationship between the circulating Tfh compartment, antibody development and protection from malaria.

Suggested Citation

  • Jo-Anne Chan & Jessica R. Loughland & Lauren de la Parte & Satomi Okano & Isaac Ssewanyana & Mayimuna Nalubega & Felistas Nankya & Kenneth Musinguzi & John Rek & Emmanuel Arinaitwe & Peta Tipping & Pe, 2022. "Age-dependent changes in circulating Tfh cells influence development of functional malaria antibodies in children," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31880-6
    DOI: 10.1038/s41467-022-31880-6
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    References listed on IDEAS

    as
    1. Gaoqian Feng & Bruce D. Wines & Liriye Kurtovic & Jo-Anne Chan & Philippe Boeuf & Vanessa Mollard & Anton Cozijnsen & Damien R. Drew & Rob J. Center & Daniel L. Marshall & Sandra Chishimba & Geoffrey , 2021. "Mechanisms and targets of Fcγ-receptor mediated immunity to malaria sporozoites," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Friedman, Jerome H. & Hastie, Trevor & Tibshirani, Rob, 2010. "Regularization Paths for Generalized Linear Models via Coordinate Descent," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i01).
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