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Transcriptome-based profiling reveals a macrophage pedigree and identifies Irf8 as pivotal for macrophage homeostasis and function

ABSTRACT: Recent studies have shown that tissue macrophages (MF) arise from embryonic progenitors of the yolk sac (YS) and fetal liver and colonize the tissues before birth. Further studies have proposed that developmentally distinct tissue MF can be identified based on the differential expression of F4/80 and CD11b, but whether a characteristic transcriptional profile exists is largely unknown. Here, we established an inducible fate mapping system that facilitated the identification of A2 progenitors of the YS as source of F4/80hi but not CD11bhi MF. Large-scale transcriptional profiling of MF precursors from the YS until adulthood allowed the description of a complex MF pedigree. We further identified a distinct molecular signature of F4/80hi and CD11bhi MF and found that Irf8 was vital for MF maturation and the innate immune response. Our data provide new cellular and molecular insights into the origin and developmental pathways of tissue MF.

ORGANISM(S): Mus musculus

PROVIDER: GSE73125 | GEO | 2016/07/28

SECONDARY ACCESSION(S): PRJNA296084

REPOSITORIES: GEO

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Transcriptome-based profiling reveals a macrophage pedigree and identifies Irf8 as pivotal for macrophage homeostasis and function

Project description:Recent studies have shown that tissue macrophages (MF) arise from embryonic progenitors of the yolk sac (YS) and fetal liver and colonize the tissues before birth. Further studies have proposed that developmentally distinct tissue MF can be identified based on the differential expression of F4/80 and CD11b, but whether a characteristic transcriptional profile exists is largely unknown. Here, we established an inducible fate mapping system that facilitated the identification of A2 progenitors of the YS as source of F4/80hi but not CD11bhi MF. Large-scale transcriptional profiling of MF precursors from the YS until adulthood allowed the description of a complex MF pedigree. We further identified a distinct molecular signature of F4/80hi and CD11bhi MF and found that Irf8 was vital for MF maturation and the innate immune response. Our data provide new cellular and molecular insights into the origin and developmental pathways of tissue MF. All samples are from mouse tissue at early developmental stages (E8, E9.5, E14) and from adulthood (6 weeks old). For the early developmental time points timed matings were performed. Macrophage populations were isolated from each tissue. RNA was isolated using Arcturus PicoPure isolation kit from yolk sac, brain, liver, kidney and skin samples after FACS sorting. Three replicates per cell population were included. Wildtype and Irf8 knockout samples were analyzed.

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Project description:Most resident macrophages (MF) populations in adult tissues arise from MF progenitors populations that emerge during ontogeny, either from haematopoietic stem cells (HSC), or from Yolk Sac (YS) progenitors produced prior to HSC development. The YS generates two populations of MF progenitors. In the earliest one, called primitive, MF progenitors arise from monopotent/uni-lineage progenitors, while in the second one they derive from multipotent erythro-myeloid progenitors. These two populations soon mix in the blood circulation, and as they are highly similar in phenotype, the specific features and function of the two MF progenitors populations are still unclear. When investigating the function of the bHLH transcription factor Lyl-1 during the development of blood cells in mouse embryos, we observed that Lyl-1 expression marks YS primitive MF progenitors. Lyl-1 bHLH disruption leads to an increased production and a defective differentiation of primitive MF progenitors. To gain a better insight into primitive MF progenitors specificity and function, we performed a RNA-seq analysis of these progenitors sorted from the YS at embryonic day (E) 9, when the YS only contains primitive MF progenitors, and at E10, when it contains both primitive MF progenitors and those produced by erythro-myeloid progenitors. At both stages, MF progenitors were collected from the YS of either wild-type or Lyl-1-deficient embryos, to better understand the role of Lyl-1 in the development of Lyl-1-expressing resident macrophage populations.

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