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Human Term Pregnancy Decidual NK Cells Generate Distinct Cytotoxic Responses

Ricardo de Mendonça Vieira, Ava Meagher, Ângela C. Crespo, Sarika K. Kshirsagar, Vidya Iyer, Errol R. Norwitz, Jack L. Strominger and Tamara Tilburgs
J Immunol May 6, 2020, ji1901435; DOI: https://doi.org/10.4049/jimmunol.1901435
Ricardo de Mendonça Vieira
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
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Ava Meagher
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
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Ângela C. Crespo
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
†Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115;
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Sarika K. Kshirsagar
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
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Vidya Iyer
‡Department of Obstetrics and Gynecology, Tufts Medical Center, Boston, MA 02111;
§Mother Infant Research Institute, Tufts Medical Center, Boston, MA 02111;
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Errol R. Norwitz
‡Department of Obstetrics and Gynecology, Tufts Medical Center, Boston, MA 02111;
§Mother Infant Research Institute, Tufts Medical Center, Boston, MA 02111;
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Jack L. Strominger
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
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Tamara Tilburgs
*Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138;
¶Division of Immunobiology, Center for Inflammation and Tolerance, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229; and
‖Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229
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Key Points

  • Term pregnancy dNK generate distinct cytolytic responses to K562, PMA/I, and HCMV.

  • Unlike first trimester dNK, term pregnancy dNK are not skewed to recognize HLA-C.

  • Protein and mRNA profiles suggest term pregnancy dNK are a distinct type of NK cell.

Abstract

Decidual NK cells (dNK) are the main lymphocyte population in early pregnancy decidual mucosa. Although dNK decrease during pregnancy, they remain present in decidual tissues at term. First trimester dNK facilitate trophoblast invasion, provide protection against infections, and were shown to have many differences in their expression of NKRs, cytokines, and cytolytic capacity compared with peripheral blood NK cells (pNK). However, only limited data are available on the phenotype and function of term pregnancy dNK. In this study, dNK from human term pregnancy decidua basalis and decidua parietalis tissues were compared with pNK and first trimester dNK. Profound differences were found, including: 1) term pregnancy dNK have an increased degranulation response to K562 and PMA/ionomycin but lower capacity to respond to human CMV–infected cells; 2) term pregnancy dNK are not skewed toward recognition of HLA-C, as was previously shown for first trimester dNK; and 3) protein and gene expression profiles identified multiple differences between pNK, first trimester, and term pregnancy dNK, suggesting term pregnancy dNK are a distinct type of NK cells. Understanding the role of dNK throughout pregnancy is of high clinical relevance for studies aiming to prevent placental inflammatory disorders as well as maternal-to-fetal transmission of pathogens.

Footnotes

  • This work was supported by National Institute of Allergy and Infectious Diseases, National Institutes of Health Grant R01-AI145862 and Strominger laboratory departmental grants.

  • The online version of this article contains supplemental material.

  • Received December 3, 2019.
  • Accepted April 14, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Human Term Pregnancy Decidual NK Cells Generate Distinct Cytotoxic Responses
Ricardo de Mendonça Vieira, Ava Meagher, Ângela C. Crespo, Sarika K. Kshirsagar, Vidya Iyer, Errol R. Norwitz, Jack L. Strominger, Tamara Tilburgs
The Journal of Immunology May 6, 2020, ji1901435; DOI: 10.4049/jimmunol.1901435

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Human Term Pregnancy Decidual NK Cells Generate Distinct Cytotoxic Responses
Ricardo de Mendonça Vieira, Ava Meagher, Ângela C. Crespo, Sarika K. Kshirsagar, Vidya Iyer, Errol R. Norwitz, Jack L. Strominger, Tamara Tilburgs
The Journal of Immunology May 6, 2020, ji1901435; DOI: 10.4049/jimmunol.1901435
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Print ISSN 0022-1767        Online ISSN 1550-6606