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Front. Cell Dev. Biol. | doi: 10.3389/fcell.2020.606642

Hematopoiesis: a layered organization across species Provisionally accepted The final, formatted version of the article will be published soon. Notify me

  • 1Institut Pasteur, France
  • 2Institute of Health Research and Innovation, University of Porto, Portugal
  • 3National Institute of Biomedical Engineering, Faculty of Engineering, University of Porto, Portugal
  • 4Université de Paris, France

The identification of distinct waves of progenitors during development, each corresponding to a specific time, space and function provided the basis for the concept of a “layered” organization in development. The concept of a layered hematopoiesis was established by classical embryology studies in birds and amphibians. Recent progress in generating reliable lineage tracing models together with transcriptional and proteomic analyses in single cells revealed that, also in mammals, the hematopoietic system evolves in successive waves of progenitors with distinct properties and fate.
During embryogenesis, sequential waves of hematopoietic progenitors emerge at different anatomic sites, generating specific cell types with distinct functions and tissue homing capacities. The first progenitors originate in the yolk sac before the emergence of hematopoietic stem cells, some giving rise to progenies that persist throughout life. Hematopoietic stem cell-derived cells that protect organisms against environmental pathogens follow the same sequential strategy, with subsets of lymphoid cells being only produced during embryonic development.
Growing evidence indicates that fetal immune cells contribute to the proper development of the organs they seed, and later ensure life-long tissue homeostasis and immune protection. They include macrophages, mast cells, some  T cells, B-1 B cells and innate lymphoid cells, which have “non-redundant” functions, and early perturbations in their development or function affect immunity in the adult. These observations challenged the view that all hematopoietic cells found in the adult result from constant and monotonous production from bone marrow-resident hematopoietic stem cells.
In this review, we evaluate evidence for a layered hematopoietic system across species. We discuss mechanisms and selective pressures leading to the temporal generation of different cell types. We elaborate on the consequences of disturbing fetal immune cells on tissues homeostasis and immune development later in life.

Keywords: hematopoieisis, Lymphopoieis, embryo, Evo devo biology, Layered

Received: 15 Sep 2020; Accepted: 19 Nov 2020.

Copyright: © 2020 Elsaid, Soares-Da-Silva, Peixoto, Amiri, Mackowski, Pereira, Bandeira and Cumano. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Antonio Bandeira, Institut Pasteur, Paris, 75015, Île-de-France, France,
Mx. ANa Cumano, Institut Pasteur, Paris, 75015, Île-de-France, France,