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Ontogeny of Tissue-Resident Macrophages.

Hoeffel G, Ginhoux F - Front Immunol (2015)

Bottom Line: The origin of tissue-resident macrophages, crucial for homeostasis and immunity, has remained controversial until recently.These tissue-resident macrophages derive from sequential seeding of tissues by two precursors during embryonic development.Thus, hematopoietic stem cell-independent embryonic precursors transiently present in the YS and the FL give rise to long-lasting self-renewing macrophage populations.

View Article: PubMed Central - PubMed

Affiliation: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR) , Singapore , Singapore.

ABSTRACT
The origin of tissue-resident macrophages, crucial for homeostasis and immunity, has remained controversial until recently. Originally described as part of the mononuclear phagocyte system, macrophages were long thought to derive solely from adult blood circulating monocytes. However, accumulating evidence now shows that certain macrophage populations are in fact independent from monocyte and even from adult bone marrow hematopoiesis. These tissue-resident macrophages derive from sequential seeding of tissues by two precursors during embryonic development. Primitive macrophages generated in the yolk sac (YS) from early erythro-myeloid progenitors (EMPs), independently of the transcription factor c-Myb and bypassing monocytic intermediates, first give rise to microglia. Later, fetal monocytes, generated from c-Myb(+) EMPs that initially seed the fetal liver (FL), then give rise to the majority of other adult macrophages. Thus, hematopoietic stem cell-independent embryonic precursors transiently present in the YS and the FL give rise to long-lasting self-renewing macrophage populations.

No MeSH data available.


Related in: MedlinePlus

Transition between fetal and adult hematopoiesis. Hemogenic endothelial cells from extra and intra-embryonic hematopoietic tissues generate C-Myb-dependent multipotential progenitors, such as LMPs and pre-HSCs, between E9.0 and E10.5, culminating with the emergence of mature HSCs with long-term reconstitution-bearing potential. CD93 (AA4.1) expression is associated with the emergence of lymphoid potential, whereas Sca-1 is the hallmark of HSCs. These progenitors seed the fetal liver around E10/E11, expanding and giving rise to the various lineages of the hematopoietic system, including fetal monocytes. These late fetal monocytes continue to participate in the tissue-resident macrophage network until hematopoiesis switches completely from the fetal liver to the bone marrow. Once adult hematopoiesis begins to take place in the bone marrow generating monocytes, certain tissues, such as the dermis, heart peritoneum, and the gut, continue to recruit adult monocytes to generate resident macrophages and replace with time the embryonic-derived macrophages.
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Figure 4: Transition between fetal and adult hematopoiesis. Hemogenic endothelial cells from extra and intra-embryonic hematopoietic tissues generate C-Myb-dependent multipotential progenitors, such as LMPs and pre-HSCs, between E9.0 and E10.5, culminating with the emergence of mature HSCs with long-term reconstitution-bearing potential. CD93 (AA4.1) expression is associated with the emergence of lymphoid potential, whereas Sca-1 is the hallmark of HSCs. These progenitors seed the fetal liver around E10/E11, expanding and giving rise to the various lineages of the hematopoietic system, including fetal monocytes. These late fetal monocytes continue to participate in the tissue-resident macrophage network until hematopoiesis switches completely from the fetal liver to the bone marrow. Once adult hematopoiesis begins to take place in the bone marrow generating monocytes, certain tissues, such as the dermis, heart peritoneum, and the gut, continue to recruit adult monocytes to generate resident macrophages and replace with time the embryonic-derived macrophages.

Mentions: The complex hierarchy of stem and progenitor cells in the BM is first established during embryonic development starting with the emergence of small numbers of HSCs from the AGM at E10.5 in murine embryos or at 5 weeks in human embryos (71, 72). After E9.5 in the mouse, with the determination of the intra-embryonic mesoderm toward a hematopoietic lineage, new waves of hematopoietic progenitors emerge within the HE of the embryo proper (Figure 4), first in the P-Sp region and the umbilical and vitelline arterial regions of the embryo, then in the AGM region and the placenta (55, 73, 74). The hematopoietic activities of the P-Sp and AGM first generate immature HSCs and then mature HSCs, which are defined by their capacity to reconstitute adult conventional mice (long-term reconstitution; LTR). Both immature and mature HSCs seed the FL at approximately E10.5 (68, 71, 75, 76) to establish definitive hematopoiesis (40, 77, 78). A maturation step seems necessary for immature HSCs to express their LTR activity in full, which is then maintained until adulthood (68). However, further investigations using a fate-mapping system would be necessary to confirm this model.


Ontogeny of Tissue-Resident Macrophages.

Hoeffel G, Ginhoux F - Front Immunol (2015)

Transition between fetal and adult hematopoiesis. Hemogenic endothelial cells from extra and intra-embryonic hematopoietic tissues generate C-Myb-dependent multipotential progenitors, such as LMPs and pre-HSCs, between E9.0 and E10.5, culminating with the emergence of mature HSCs with long-term reconstitution-bearing potential. CD93 (AA4.1) expression is associated with the emergence of lymphoid potential, whereas Sca-1 is the hallmark of HSCs. These progenitors seed the fetal liver around E10/E11, expanding and giving rise to the various lineages of the hematopoietic system, including fetal monocytes. These late fetal monocytes continue to participate in the tissue-resident macrophage network until hematopoiesis switches completely from the fetal liver to the bone marrow. Once adult hematopoiesis begins to take place in the bone marrow generating monocytes, certain tissues, such as the dermis, heart peritoneum, and the gut, continue to recruit adult monocytes to generate resident macrophages and replace with time the embryonic-derived macrophages.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585135&req=5

Figure 4: Transition between fetal and adult hematopoiesis. Hemogenic endothelial cells from extra and intra-embryonic hematopoietic tissues generate C-Myb-dependent multipotential progenitors, such as LMPs and pre-HSCs, between E9.0 and E10.5, culminating with the emergence of mature HSCs with long-term reconstitution-bearing potential. CD93 (AA4.1) expression is associated with the emergence of lymphoid potential, whereas Sca-1 is the hallmark of HSCs. These progenitors seed the fetal liver around E10/E11, expanding and giving rise to the various lineages of the hematopoietic system, including fetal monocytes. These late fetal monocytes continue to participate in the tissue-resident macrophage network until hematopoiesis switches completely from the fetal liver to the bone marrow. Once adult hematopoiesis begins to take place in the bone marrow generating monocytes, certain tissues, such as the dermis, heart peritoneum, and the gut, continue to recruit adult monocytes to generate resident macrophages and replace with time the embryonic-derived macrophages.
Mentions: The complex hierarchy of stem and progenitor cells in the BM is first established during embryonic development starting with the emergence of small numbers of HSCs from the AGM at E10.5 in murine embryos or at 5 weeks in human embryos (71, 72). After E9.5 in the mouse, with the determination of the intra-embryonic mesoderm toward a hematopoietic lineage, new waves of hematopoietic progenitors emerge within the HE of the embryo proper (Figure 4), first in the P-Sp region and the umbilical and vitelline arterial regions of the embryo, then in the AGM region and the placenta (55, 73, 74). The hematopoietic activities of the P-Sp and AGM first generate immature HSCs and then mature HSCs, which are defined by their capacity to reconstitute adult conventional mice (long-term reconstitution; LTR). Both immature and mature HSCs seed the FL at approximately E10.5 (68, 71, 75, 76) to establish definitive hematopoiesis (40, 77, 78). A maturation step seems necessary for immature HSCs to express their LTR activity in full, which is then maintained until adulthood (68). However, further investigations using a fate-mapping system would be necessary to confirm this model.

Bottom Line: The origin of tissue-resident macrophages, crucial for homeostasis and immunity, has remained controversial until recently.These tissue-resident macrophages derive from sequential seeding of tissues by two precursors during embryonic development.Thus, hematopoietic stem cell-independent embryonic precursors transiently present in the YS and the FL give rise to long-lasting self-renewing macrophage populations.

View Article: PubMed Central - PubMed

Affiliation: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR) , Singapore , Singapore.

ABSTRACT
The origin of tissue-resident macrophages, crucial for homeostasis and immunity, has remained controversial until recently. Originally described as part of the mononuclear phagocyte system, macrophages were long thought to derive solely from adult blood circulating monocytes. However, accumulating evidence now shows that certain macrophage populations are in fact independent from monocyte and even from adult bone marrow hematopoiesis. These tissue-resident macrophages derive from sequential seeding of tissues by two precursors during embryonic development. Primitive macrophages generated in the yolk sac (YS) from early erythro-myeloid progenitors (EMPs), independently of the transcription factor c-Myb and bypassing monocytic intermediates, first give rise to microglia. Later, fetal monocytes, generated from c-Myb(+) EMPs that initially seed the fetal liver (FL), then give rise to the majority of other adult macrophages. Thus, hematopoietic stem cell-independent embryonic precursors transiently present in the YS and the FL give rise to long-lasting self-renewing macrophage populations.

No MeSH data available.


Related in: MedlinePlus