C-Myb+ Erythro-Myeloid Progenitor-Derived Fetal Monocytes Give Rise to Adult Tissue-Resident Macrophages

被引:835
作者
Hoeffel, Guillaume [1 ]
Chen, Jinmiao [1 ]
Lavin, Yonit [2 ,3 ]
Low, Donovan [1 ]
Almeida, Francisca F. [1 ]
See, Peter [1 ]
Beaudin, Anna E. [4 ]
Lum, Josephine [1 ]
Low, Ivy [1 ]
Forsberg, E. Camilla [4 ]
Poidinger, Michael [1 ]
Zolezzi, Francesca [1 ]
Larbi, Anis [1 ]
Ng, Lai Guan [1 ]
Chan, Jerry K. Y. [1 ,5 ,6 ,7 ]
Greter, Melanie [8 ]
Becher, Burkhard [8 ]
Samokhvalov, Igor M. [9 ]
Merad, Miriam [2 ,3 ]
Ginhoux, Florent [1 ]
机构
[1] ASTAR, Singapore Immunol Network SIgN, BIOPOLIS, Singapore 138648, Singapore
[2] Tisch Canc Inst, Dept Oncol Sci, New York, NY 10029 USA
[3] Icahn Sch Med Mt Sinai, Inst Immunol, New York, NY 10029 USA
[4] Univ Calif Santa Cruz, Inst Biol Stem Cells, Dept Biomol Engn, Santa Cruz, CA 95064 USA
[5] Natl Univ Singapore, Yong Loo Lin Sch Med, Expt Fetal Med Grp, Singapore 119228, Singapore
[6] KK Womens & Childrens Hosp, Reprod Med, Singapore 229899, Singapore
[7] Duke NUS Grad Med Sch, Singapore & Canc & Stem Cell Biol Program, Singapore 169857, Singapore
[8] Univ Zurich, Inst Expt Immunol, CH-8057 Zurich, Switzerland
[9] Chinese Acad Sci, Guangzhou Inst Biomed & Hlth, Guangzhou 510530, Guangdong, Peoples R China
关键词
HEMATOPOIETIC STEM-CELLS; MOUSE YOLK-SAC; CIRCULATING MONOCYTES; ALVEOLAR MACROPHAGES; STEADY-STATE; GM-CSF; DIFFERENTIATION; MYB; SYSTEM; BLOOD;
D O I
10.1016/j.immuni.2015.03.011
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Although classified as hematopoietic cells, tissue-resident macrophages (MFs) arise from embryonic precursors that seed the tissues prior to birth to generate a self-renewing population, which is maintained independently of adult hematopoiesis. Here we reveal the identity of these embryonic precursors using an in utero MF-depletion strategy and fate-mapping of yolk sac (YS) and fetal liver (FL) hematopoiesis. We show that YS MFs are the main precursors of microglia, while most other MFs derive from fetal monocytes (MOs). Both YS MFs and fetal MOs arise from erythro-myeloid progenitors (EMPs) generated in the YS. In the YS, EMPs gave rise to MFs without monocytic intermediates, while EMP seeding the FL upon the establishment of blood circulation acquired c-Myb expression and gave rise to fetal MOs that then seeded embryonic tissues and differentiated into MFs. Thus, adult tissue-resident MFs established from hematopoietic stem cell-independent embryonic precursors arise from two distinct developmental programs.
引用
收藏
页码:665 / 678
页数:14
相关论文
共 52 条
  • [1] Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice
    Bain, Calum C.
    Bravo-Blas, Alberto
    Scott, Charlotte L.
    Perdiguero, Elisa Gomez
    Geissmann, Frederic
    Henri, Sandrine
    Malissen, Bernard
    Osborne, Lisa C.
    Artis, David
    Mowat, Allan Mci
    [J]. NATURE IMMUNOLOGY, 2014, 15 (10) : 929 - U236
  • [2] Three pathways to mature macrophages in the early mouse yolk sac
    Bertrand, JY
    Jalil, A
    Klaine, M
    Jung, S
    Cumano, A
    Godin, I
    [J]. BLOOD, 2005, 106 (09) : 3004 - 3011
  • [3] TGF-β signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia
    Bhowmick, NA
    Chytil, A
    Plieth, D
    Gorska, AE
    Dumont, N
    Shappell, S
    Washington, MK
    Neilson, EG
    Moses, HL
    [J]. SCIENCE, 2004, 303 (5659) : 848 - 851
  • [4] Lymphomyeloid Contribution of an Immune-Restricted Progenitor Emerging Prior to Definitive Hematopoietic Stem Cells
    Boiers, Charlotta
    Carrelha, Joana
    Lutteropp, Michael
    Luc, Sidinh
    Green, Joanna C. A.
    Azzoni, Emanuele
    Woll, Petter S.
    Mead, Adam J.
    Hultquist, Anne
    Swiers, Gemma
    Perdiguero, Elisa Gomez
    Macaulay, Iain C.
    Melchiori, Luca
    Luis, Tiago C.
    Kharazi, Shabnam
    Bouriez-Jones, Tiphaine
    Deng, Qiaolin
    Ponten, Annica
    Atkinson, Deborah
    Jensen, Christina T.
    Sitnicka, Ewa
    Geissmann, Frederic
    Godin, Isabelle
    Sandberg, Rickard
    de Bruijn, Marella F. T. R.
    Jacobsen, Sten Eirik W.
    [J]. CELL STEM CELL, 2013, 13 (05) : 535 - 548
  • [5] All Hematopoietic Cells Develop from Hematopoietic Stem Cells through Flk2/Flt3-Positive Progenitor Cells
    Boyer, Scott W.
    Schroeder, Aaron V.
    Smith-Berdan, Stephanie
    Forsberg, E. Camilla
    [J]. CELL STEM CELL, 2011, 9 (01) : 64 - 73
  • [6] FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells
    Buza-Vidas, Natalija
    Woll, Petter
    Hultquist, Anne
    Duarte, Sara
    Lutteropp, Michael
    Bouriez-Jones, Tiphaine
    Ferry, Helen
    Luc, Sidinh
    Jacobsen, Sten Eirik Waelgaard
    [J]. BLOOD, 2011, 118 (06) : 1544 - 1548
  • [7] Circulation and chemotaxis of fetal hematopoietic stem cells
    Christensen, JL
    Wright, DE
    Wagers, AJ
    Weissman, IL
    [J]. PLOS BIOLOGY, 2004, 2 (03): : 368 - 377
  • [8] In vitro differentiation of c-myb-/- ES cells reveals that the colony forming capacity of unilineage macrophage precursors and myeloid progenitor commitment are c-Myb independent
    Clarke, D
    Vegiopoulos, A
    Crawford, A
    Mucenski, M
    Bonifer, C
    Frampton, J
    [J]. ONCOGENE, 2000, 19 (30) : 3343 - 3351
  • [9] Pericytes are required for blood-brain barrier integrity during embryogenesis
    Daneman, Richard
    Zhou, Lu
    Kebede, Amanuel A.
    Barres, Ben A.
    [J]. NATURE, 2010, 468 (7323) : 562 - U238
  • [10] Of lineage and legacy: the development of mammalian hematopoietic stem cells
    Dzierzak, Elaine
    Speck, Nancy A.
    [J]. NATURE IMMUNOLOGY, 2008, 9 (02) : 129 - 136