IFNs Drive Development of Novel IL-15-Responsive Macrophages

J Immunol. 2020 Aug 15;205(4):1113-1124. doi: 10.4049/jimmunol.2000184. Epub 2020 Jul 20.

Abstract

Disruption in homeostasis of IL-15 is linked to poor maternal and fetal outcomes during pregnancy. The only cells described to respond to IL-15 at the early maternal-fetal interface have been NK cells. We now show a novel population of macrophages, evident in several organs but enriched in the uterus of mice and humans, expressing the β-chain of the IL-15R complex (CD122) and responding to IL-15. CD122+ macrophages (CD122+Macs) are morphologic, phenotypic, and transcriptomic macrophages that can derive from bone marrow monocytes. CD122+Macs develop in the uterus and placenta with kinetics that mirror IFN activity at the maternal-fetal interface. M-CSF permits macrophages to express CD122, and IFNs are sufficient to drive expression of CD122 on macrophages. Neither type I nor type II IFNs are required to generate CD122+Macs, however. In response to IL-15, CD122+Macs activate the ERK signaling cascade and enhance production of proinflammatory cytokines after stimulation with the TLR9 agonist CpG. Finally, we provide evidence of human cells that phenocopy murine CD122+Macs in secretory phase endometrium during the implantation window and in first-trimester uterine decidua. Our data support a model wherein IFNs local to the maternal-fetal interface direct novel IL-15-responsive macrophages with the potential to mediate IL-15 signals critical for optimal outcomes of pregnancy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • CpG Islands / physiology
  • Cytokines / metabolism
  • Decidua / metabolism
  • Female
  • Humans
  • Inflammation / metabolism
  • Interferons / metabolism*
  • Interleukin-15 / metabolism*
  • Interleukin-2 Receptor beta Subunit / metabolism
  • Killer Cells, Natural / metabolism
  • MAP Kinase Signaling System / physiology
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / metabolism
  • Placenta / metabolism
  • Pregnancy
  • Pregnancy Trimester, First / metabolism
  • Signal Transduction / physiology
  • Toll-Like Receptor 9 / metabolism
  • Transcriptome / physiology
  • Young Adult

Substances

  • Cytokines
  • IL15 protein, human
  • Interleukin-15
  • Interleukin-2 Receptor beta Subunit
  • Toll-Like Receptor 9
  • Interferons