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Fetal‐derived immune cells at the roots of lifelong pathophysiology

Mass, Elvira, Gentek, Rebecca·2021·Frontiers in Cell and Developmental Biology
DOI 10.3389/fcell.2021.648313PMC PMC7940384
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Abstract

Tissue-resident innate immune cells exert a wide range of functions in both adult homeostasis and pathology. Our understanding of when and how these cellular networks are established has dramatically changed with the recognition that many lineages originate at least in part from fetal sources and self-maintain independently from hematopoietic stem cells. Indeed, fetal-derived immune cells are found in most organs and serous cavities of our body, where they reside throughout the entire lifespan. At the same time, there is a growing appreciation that pathologies manifesting in adulthood may be caused by adverse early life events, a concept known as “developmental origins of health and disease” (DOHaD). Yet, whether fetal-derived immune cells are mechanistically involved in DOHaD remains elusive. In this review, we summarize our knowledge of fetal hematopoiesis and its contribution to adult immune compartments, which results in a “layered immune system.” Based on their ontogeny, we argue that fetal-derived immune cells are prime transmitters of long-term consequences of prenatal adversities. In addition to increasing disease susceptibility, these may also directly cause inflammatory, degenerative, and metabolic disorders. We explore this notion for cells generated from erythro-myeloid progenitors (EMP) produced in the extra-embryonic yolk sac. Focusing on macrophages and mast cells, we present emerging evidence implicating them in lifelong disease by either somatic mutations or developmental programming events resulting from maternal and early environmental perturbations.

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FIGURE 1 Layered hematopoiesis. The primitive and transient-definitive waves in the yolk sac (YS) give rise to erythro-myeloid progenitors (EMP) that will colonize the fetal liver (FL) consecutively. EMP arising at early stages will differentiate into macrophages and probably mast cells in tissues developing early during embryogenesis (brain, liver), while EMPs at later stages remain in the FL and will give rise to the same cell types driven by the demand of later developing tissues, such as the lung and skin. Hematopoietic stem cells (HSC) develop in the aorta-gonad-mesonephros (AGM) region before colonizing the FL. After the formation of the bone marrow (BM), HSC migrate to the BM cavity where they will constantly give rise to short-lived macrophages and mast cells. The cell of origin for mast cells and macrophages is color-indicated. For simplicity, blood-circulating intermediate precursor stages between EMP and macrophages are not depicted. Created with BioRender.com.
FIGURE 1 Layered hematopoiesis. The primitive and transient-definitive waves in the yolk sac (YS) give rise to erythro-myeloid progenitors (EMP) that will colonize the fetal liver (FL) consecutively. EMP arising at early stages will differentiate into macrophages and probably mast cells in tissues developing early during embryogenesis (brain, liver), while EMPs at later stages remain in the FL and will give rise to the same cell types driven by the demand of later developing tissues, such as the lung and skin. Hematopoietic stem cells (HSC) develop in the aorta-gonad-mesonephros (AGM) region before colonizing the FL. After the formation of the bone marrow (BM), HSC migrate to the BM cavity where they will constantly give rise to short-lived macrophages and mast cells. The cell of origin for mast cells and macrophages is color-indicated. For simplicity, blood-circulating intermediate precursor stages between EMP and macrophages are not depicted. Created with BioRender.com.CC BY · PubMed Central
FIGURE 2 Genetic and developmental programming of fetal-derived immune cells. Perturbation of the maternal environment e.g., by nutrition, smoking, and infection, leads to the production of mediators such as cytokines and lipids that will lead to epigenetic alterations in EMP and thereby, chronic activation of EMP-derived immune cells after birth. This switch from a homeostatic to a pro-inflammatory state due to developmental programming may cause or contribute to different diseases. In addition to naturally occurring somatic mutations in proliferating EMP and their progeny, maternal-derived hazardous materials may lead to DNA damage, which could eventually lead to a change in transcriptional programs and chronic activation of tissue-resident immune cells. Created with BioRender.com.
FIGURE 2 Genetic and developmental programming of fetal-derived immune cells. Perturbation of the maternal environment e.g., by nutrition, smoking, and infection, leads to the production of mediators such as cytokines and lipids that will lead to epigenetic alterations in EMP and thereby, chronic activation of EMP-derived immune cells after birth. This switch from a homeostatic to a pro-inflammatory state due to developmental programming may cause or contribute to different diseases. In addition to naturally occurring somatic mutations in proliferating EMP and their progeny, maternal-derived hazardous materials may lead to DNA damage, which could eventually lead to a change in transcriptional programs and chronic activation of tissue-resident immune cells. Created with BioRender.com.CC BY · PubMed Central

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Metadata

Authors
Mass, E., & Gentek, R.
Venue
Frontiers in Cell and Developmental Biology
Publisher
Frontiers Media SA
Published
2021-02-23
Volume
9
ISSN
2296-634X
DOI
10.3389/fcell.2021.648313
PMC
PMC7940384
Cited by
47
References
31
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Deutsche Forschungsgemeinschaft (EXC2151-390873048)
  • Fritz Thyssen Stiftung
  • Daimler und Benz Stiftung
  • Kennedy Trust for Rheumatology Research

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