Distinctive phenotypes and functions of innate lymphoid cells in human decidua during early pregnancy

Oisín Huhn, Martin A. Ivarsson, Lucy Gardner, Mike Hollinshead, Jane C Stinchcombe, Puran Chen, Norman Shreeve, Olympe Chazara, Lydia E. Farrell, Jakob Theorell, Hormas Ghadially, Peter Parham, Gillian Griffiths, Amir Horowitz, Ashley Moffett, Andrew M. Sharkey () and Francesco Colucci ()
Additional contact information
Oisín Huhn: National Institute for Health Research Cambridge Biomedical Research Centre
Martin A. Ivarsson: University of Cambridge
Lucy Gardner: University of Cambridge
Mike Hollinshead: University of Cambridge
Jane C Stinchcombe: University of Cambridge
Puran Chen: Karolinska University Hospital
Norman Shreeve: National Institute for Health Research Cambridge Biomedical Research Centre
Olympe Chazara: University of Cambridge
Lydia E. Farrell: University of Cambridge
Jakob Theorell: University of Oxford
Hormas Ghadially: Oncology R&D
Peter Parham: Stanford University School of Medicine
Gillian Griffiths: University of Cambridge
Amir Horowitz: Tisch Cancer Institute Icahn School of Medicine at Mount Sinai
Ashley Moffett: University of Cambridge
Andrew M. Sharkey: University of Cambridge
Francesco Colucci: National Institute for Health Research Cambridge Biomedical Research Centre

Nature Communications, 2020, vol. 11, issue 1, 1-14

Abstract: Abstract During early pregnancy, decidual innate lymphoid cells (dILCs) interact with surrounding maternal cells and invading fetal extravillous trophoblasts (EVT). Here, using mass cytometry, we characterise five main dILC subsets: decidual NK cells (dNK)1–3, ILC3s and proliferating NK cells. Following stimulation, dNK2 and dNK3 produce more chemokines than dNK1 including XCL1 which can act on both maternal dendritic cells and fetal EVT. In contrast, dNK1 express receptors including Killer-cell Immunoglobulin-like Receptors (KIR), indicating they respond to HLA class I ligands on EVT. Decidual NK have distinctive organisation and content of granules compared with peripheral blood NK cells. Acquisition of KIR correlates with higher granzyme B levels and increased chemokine production in response to KIR activation, suggesting a link between increased granule content and dNK1 responsiveness. Our analysis shows that dILCs are unique and provide specialised functions dedicated to achieving placental development and successful reproduction.

Date: 2020
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DOI: 10.1038/s41467-019-14123-z

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