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Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF

Martin Guilliams UGent, Ismé De Kleer UGent, Sandrine Henri, Sijranke Post UGent, Leen Vanhoutte UGent, Sofie De Prijck UGent, Kim Deswarte UGent, Bernard Malissen, Hamida Hammad UGent and Bart Lambrecht UGent (2013) JOURNAL OF EXPERIMENTAL MEDICINE. 210(10). p.1977-1992
abstract
Tissue-resident macrophages can develop from circulating adult monocytes or from primitive yolk sac-derived macrophages. The precise ontogeny of alveolar macrophages (AMFs) is unknown. By performing BrdU labeling and parabiosis experiments in adult mice, we found that circulating monocytes contributed minimally to the steady-state AMF pool. Mature AMFs were undetectable before birth and only fully colonized the alveolar space by 3 d after birth. Before birth, F4/80(hi)CD11b(lo) primitive macrophages and Ly6C(hi)CD11b(hi) fetal monocytes sequentially colonized the developing lung around E12.5 and E16.5, respectively. The first signs of AMF differentiation appeared around the saccular stage of lung development (E18.5). Adoptive transfer identified fetal monocytes, and not primitive macrophages, as the main precursors of AMFs. Fetal monocytes transferred to the lung of neonatal mice acquired an AMF phenotype via defined developmental stages over the course of one week, and persisted for at least three months. Early AMF commitment from fetal monocytes was absent in GM-CSF-deficient mice, whereas short-term perinatal intrapulmonary GM-CSF therapy rescued AMF development for weeks, although the resulting AMFs displayed an immature phenotype. This demonstrates that tissue-resident macrophages can also develop from fetal monocytes that adopt a stable phenotype shortly after birth in response to instructive cytokines, and then self-maintain throughout life.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
LANGERHANS CELLS, DEFICIENT MICE, DENDRITIC CELLS, TISSUE MACROPHAGES, LUNG MACROPHAGES, BLOOD MONOCYTES, LYMPHOID ORGANS, KUPFFER CELLS, SELF-RENEWAL, BONE-MARROW
journal title
JOURNAL OF EXPERIMENTAL MEDICINE
J. Exp. Med.
volume
210
issue
10
pages
1977 - 1992
Web of Science type
Article
Web of Science id
000324813000009
JCR category
MEDICINE, RESEARCH & EXPERIMENTAL
JCR impact factor
13.912 (2013)
JCR rank
4/124 (2013)
JCR quartile
1 (2013)
ISSN
0022-1007
DOI
10.1084/jem.20131199
project
Ghent researchers on unfolded proteins in inflammatory disease (GROUP-ID)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
4178862
handle
http://hdl.handle.net/1854/LU-4178862
date created
2013-11-05 11:10:13
date last changed
2016-12-19 15:43:48
@article{4178862,
  abstract     = {Tissue-resident macrophages can develop from circulating adult monocytes or from primitive yolk sac-derived macrophages. The precise ontogeny of alveolar macrophages (AMFs) is unknown. By performing BrdU labeling and parabiosis experiments in adult mice, we found that circulating monocytes contributed minimally to the steady-state AMF pool. Mature AMFs were undetectable before birth and only fully colonized the alveolar space by 3 d after birth. Before birth, F4/80(hi)CD11b(lo) primitive macrophages and Ly6C(hi)CD11b(hi) fetal monocytes sequentially colonized the developing lung around E12.5 and E16.5, respectively. The first signs of AMF differentiation appeared around the saccular stage of lung development (E18.5). Adoptive transfer identified fetal monocytes, and not primitive macrophages, as the main precursors of AMFs. Fetal monocytes transferred to the lung of neonatal mice acquired an AMF phenotype via defined developmental stages over the course of one week, and persisted for at least three months. Early AMF commitment from fetal monocytes was absent in GM-CSF-deficient mice, whereas short-term perinatal intrapulmonary GM-CSF therapy rescued AMF development for weeks, although the resulting AMFs displayed an immature phenotype. This demonstrates that tissue-resident macrophages can also develop from fetal monocytes that adopt a stable phenotype shortly after birth in response to instructive cytokines, and then self-maintain throughout life.},
  author       = {Guilliams, Martin and De Kleer, Ism{\'e} and Henri, Sandrine and Post, Sijranke and Vanhoutte, Leen and De Prijck, Sofie and Deswarte, Kim and Malissen, Bernard and Hammad, Hamida and Lambrecht, Bart},
  issn         = {0022-1007},
  journal      = {JOURNAL OF EXPERIMENTAL MEDICINE},
  keyword      = {LANGERHANS CELLS,DEFICIENT MICE,DENDRITIC CELLS,TISSUE MACROPHAGES,LUNG MACROPHAGES,BLOOD MONOCYTES,LYMPHOID ORGANS,KUPFFER CELLS,SELF-RENEWAL,BONE-MARROW},
  language     = {eng},
  number       = {10},
  pages        = {1977--1992},
  title        = {Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF},
  url          = {http://dx.doi.org/10.1084/jem.20131199},
  volume       = {210},
  year         = {2013},
}

Chicago
Guilliams, Martin, Ismé De Kleer, Sandrine Henri, Sijranke Post, Leen Vanhoutte, Sofie De Prijck, Kim Deswarte, Bernard Malissen, Hamida Hammad, and Bart Lambrecht. 2013. “Alveolar Macrophages Develop from Fetal Monocytes That Differentiate into Long-lived Cells in the First Week of Life via GM-CSF.” Journal of Experimental Medicine 210 (10): 1977–1992.
APA
Guilliams, M., De Kleer, I., Henri, S., Post, S., Vanhoutte, L., De Prijck, S., Deswarte, K., et al. (2013). Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. JOURNAL OF EXPERIMENTAL MEDICINE, 210(10), 1977–1992.
Vancouver
1.
Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. JOURNAL OF EXPERIMENTAL MEDICINE. 2013;210(10):1977–92.
MLA
Guilliams, Martin, Ismé De Kleer, Sandrine Henri, et al. “Alveolar Macrophages Develop from Fetal Monocytes That Differentiate into Long-lived Cells in the First Week of Life via GM-CSF.” JOURNAL OF EXPERIMENTAL MEDICINE 210.10 (2013): 1977–1992. Print.