Primitive haematopoiesis in the human placenta gives rise to macrophages with epigenetically silenced HLA-DR

Jake R. Thomas, Anna Appios, Emily F. Calderbank, Nagisa Yoshida, Xiaohui Zhao, Russell S. Hamilton, Ashley Moffett, Andrew Sharkey, Elisa Laurenti, Courtney W. Hanna () and Naomi McGovern ()
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Jake R. Thomas: University of Cambridge
Anna Appios: University of Cambridge
Emily F. Calderbank: University of Cambridge
Nagisa Yoshida: University of Cambridge
Xiaohui Zhao: University of Cambridge
Russell S. Hamilton: University of Cambridge
Ashley Moffett: University of Cambridge
Andrew Sharkey: University of Cambridge
Elisa Laurenti: University of Cambridge
Courtney W. Hanna: University of Cambridge
Naomi McGovern: University of Cambridge

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The earliest macrophages are generated during embryonic development from erythro-myeloid progenitors (EMPs) via primitive haematopoiesis. Although this process is thought to be spatially restricted to the yolk sac in the mouse, in humans, it remains poorly understood. Human foetal placental macrophages, or Hofbauer cells (HBC), arise during the primitive haematopoietic wave ~18 days post conception and lack expression of human leukocyte antigen (HLA) class II. Here, we identify a population of placental erythro-myeloid progenitors (PEMPs) in the early human placenta that have conserved features of primitive yolk sac EMPs, including the lack of HLF expression. Using in vitro culture experiments we demonstrate that PEMP generate HBC-like cells lacking HLA-DR expression. We find the absence of HLA-DR in primitive macrophages is mediated via epigenetic silencing of class II transactivator, CIITA, the master regulator of HLA class II gene expression. These findings establish the human placenta as an additional site of primitive haematopoiesis.

Date: 2023
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DOI: 10.1038/s41467-023-37383-2

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