An archaic HLA class I receptor allele diversifies natural killer cell-driven immunity in First Nations peoples of Oceania

Journal article


Loh, Liyen, Saunders, Philippa M., Faoro, Camilla, Font-Porterias, Neus, Nemat-Gorgani, Neda, Harrison, Genelle F., Sadeeq, Suraju, Hensen, Luca, Wong, Shu Cheng, Widjaja, Jacqueline, Clemens, E. Bridie, Zhu, Shiying, Kichula, Katherine M., Tao, Sudan, Zhu, Faming, Montero-Martin, Gonzalo, Fernandez-Vina, Marcelo, Guethlein, Lisbeth A., Vivian, Julian P., ... Norman, Paul J.. (2024). An archaic HLA class I receptor allele diversifies natural killer cell-driven immunity in First Nations peoples of Oceania. Cell. 187(24), pp. 7008-7024. https://doi.org/10.1016/j.cell.2024.10.005
AuthorsLoh, Liyen, Saunders, Philippa M., Faoro, Camilla, Font-Porterias, Neus, Nemat-Gorgani, Neda, Harrison, Genelle F., Sadeeq, Suraju, Hensen, Luca, Wong, Shu Cheng, Widjaja, Jacqueline, Clemens, E. Bridie, Zhu, Shiying, Kichula, Katherine M., Tao, Sudan, Zhu, Faming, Montero-Martin, Gonzalo, Fernandez-Vina, Marcelo, Guethlein, Lisbeth A., Vivian, Julian P., Davies, Jane, Mentzer, Alexander J., Oppenheimer, Stephen J., Pomat, William, Ioannidis, Alexander G., Barberena-Jonas, Carmina, Oceanian Genome Variation Project Consortium, Moreno-Estrada, Andrés, Miller, Adrian, Parham, Peter, Rossjohn, Jamie, Tong, Steven Y. C., Kedzierska, Katherine, Brooks, Andrew G. and Norman, Paul J.
Abstract

Genetic variation in host immunity impacts the disproportionate burden of infectious diseases that can be experienced by First Nations peoples. Polymorphic human leukocyte antigen (HLA) class I and killer cell immunoglobulin-like receptors (KIRs) are key regulators of natural killer (NK) cells, which mediate early infection control. How this variation impacts their responses across populations is unclear. We show that HLA-A∗24:02 became the dominant ligand for inhibitory KIR3DL1 in First Nations peoples across Oceania, through positive natural selection. We identify KIR3DL1∗114, widespread across and unique to Oceania, as an allele lineage derived from archaic humans. KIR3DL1∗114+NK cells from First Nations Australian donors are inhibited through binding HLA-A∗24:02. The KIR3DL1∗114 lineage is defined by phenylalanine at residue 166. Structural and binding studies show phenylalanine 166 forms multiple unique contacts with HLA-peptide complexes, increasing both affinity and specificity. Accordingly, assessing immunogenetic variation and the functional implications for immunity are fundamental toward understanding population-based disease associations.

Year2024
JournalCell
Journal citation187 (24), pp. 7008-7024
PublisherCell Press
ISSN0092-8674
Digital Object Identifier (DOI)https://doi.org/10.1016/j.cell.2024.10.005
PubMed ID39476840
Scopus EID2-s2.0-85209832524
PubMed Central IDPMC11606752
Open accessPublished as ‘gold’ (paid) open access
Page range7008-7024
FunderAustralian Research Council (ARC)
National Health and Medical Research Council (NHMRC)
National Institutes of Health (NIH), United States of America
Victorian Cancer Agency
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
Online27 Nov 2024
Publication process dates
Accepted03 Oct 2024
Deposited03 Apr 2025
Supplemental file
License
File Access Level
Open
ARC Funded ResearchThis output has been funded, wholly or partially, under the Australian Research Council Act 2001
Grant IDDP190103282
1042662
1122524
1145033
R01 AI17892
R01 AI151549
1173871
1091516
P30 DK116073
Additional information

© 2024 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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