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Adult connective tissue‐resident mast cells originate from late erythro‐myeloid progenitors
Abstract
Tissue-resident mast cells are associated with many inflammatory and physiological processes. Although mast cells arise from the yolk sac, the exact ontogeny of adult mast cells remains unclear. Here we have investigated the hematopoietic origin of mast cells using fate-mapping systems. We have shown that early erythro-myeloid progenitors (EMPs), late EMPs, and definitive hematopoietic stem cells (HSCs) each gave rise to mast cells in succession via an intermediate integrin β7 + progenitor. From late embryogenesis to adult, early EMP-derived mast cells were largely replaced by late EMP-derived cells in most connective tissues except adipose and pleural cavity. Thus, mast cells with distinct origin displayed tissue-location preferences: early EMP-derived cells were limited to adipose and pleural cavity and late EMP-derived cells dominated most connective tissues, while HSC-derived cells were a main group in mucosa. Therefore, embryonic origin shapes the heterogeneity of adult mast cells, with diverse functions in immunity and development.
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“At E11.5, EMP‐derived mast cell progenitors expressing integrin α4β7 are also already present in the fetal circulation and body. 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“As introduced above, mast cell replenishment from BM transferred into lethally irradiated mice is restricted to mucosal sites like the cecum and stomach, in which approximately 50% of resident mast cells are of donor BM origin after 8 months. 23 , 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“Three different fate mapping approaches unequivocally established that in vivo and under physiological conditions, the first mast cells are produced from YS EMPs. 53 , 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“In support of this notion, progenitors with mast cell potential can be found in the fetal liver from E11.5 onwards, and these progenitors give rise to mast cells when transferred into fetal or newborn recipients. 54 , 69”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“Moreover, others failed to detect them until E16.5 in mouse skin. 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“The first mast cell progenitors arise from the erythro‐myeloid progenitors (EMPs) produced in the extra‐embryonic yolk sac starting at embryonic day 8.25 (E8.25).”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“Indeed, integrin α4β7 is expressed by EMP‐derived progenitors that can be found in the fetal liver at E11.5. 53 , 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“These do not yet have granules but express cardinal markers of mast cells such as Kit, as well as several mast cell proteases, at least on transcriptional level. 54 , 59 , 60”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“Committed progenitors with an immature mast cell phenotype can be found in the circulation and peripheral tissues of developing mice and rats from E11.5 onwards. 54 , 56”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“These progenitors phenotypically still resemble EMPs, 66 except for the lack of CD93 expression. 54”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“The frequency of EMP‐derived mast cells gradually declines over time, although sizeable populations are retained in adult connective tissues, such as the body skin, as well as adipose tissues.”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“While surface expression of FcεR1 is only upregulated perinatally, 53 , 63 fetal mast cells express other receptors through which they can sense the environment, such as the IL‐33 receptor. 53 , 54 , 63 They can also respond to environmental signals and stressors already in utero. 63”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“At least on transcript level, fetal mast cells also express key effectors like proteases. 53 , 54 , 63 This is also true for human fetal mast cells, which express, for example, TPSAB1, the gene encoding tryptase, and carry granules. 59 , 60 , 63”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
In the citing paper
“Mast cells can also be found in the developing brain of mice 54 and rats, 119 including the pre‐optic area. 120 This brain region is essential for male copulatory behavior, which is marked by a higher synaptic density compared to females. Late fetal and early postnatal stages are critical for sexual differentiation in this region. At these stages, mast cell numbers are higher in the pre‐optic area”
From Mast cell ontogeny: From fetal development to life‐long health and disease (2023) · cites this paper as [54]
Citations
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Weinstock, L. B., Pace, L. A., Rezaie, A., Afrin, L. B., & Molderings, G. J. (2021) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06264-9 · Cited by 59
Mast cell ontogeny: From fetal development to life‐long health and disease
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Metadata
- Authors
- Li, Z., Liu, S., Xu, J., Zhang, X., Han, D., Liu, J., Xia, M., Yi, L., Shen, Q., Xu, S., Lu, L., & Cao, X.
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 49
- Issue
- 4
- Pages
- 640-653.e5
- ISSN
- 1074-7613
- Cited by
- 198
- References
- 6
- Language
- en
- Licence
- Funders
- National Key Research and Development Program of China (2018YFA0507403, 2015CB964403)
- Chinese Academy of Meteorological Sciences (2016-12M-1-003)
- RIKEN
- National Natural Science Foundation of China (81788101, 91542000, 31870878, 91642000, 31470858)
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