Hematopoiesis: A Layered Organization Across Chordate Species
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...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-12-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2020.606642/full |
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| author | Ramy Elsaid Ramy Elsaid Ramy Elsaid Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Dali Amiri Dali Amiri Dali Amiri Nathan Mackowski Nathan Mackowski Nathan Mackowski Pablo Pereira Pablo Pereira Pablo Pereira Antonio Bandeira Antonio Bandeira Antonio Bandeira Ana Cumano Ana Cumano Ana Cumano |
| author_facet | Ramy Elsaid Ramy Elsaid Ramy Elsaid Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Dali Amiri Dali Amiri Dali Amiri Nathan Mackowski Nathan Mackowski Nathan Mackowski Pablo Pereira Pablo Pereira Pablo Pereira Antonio Bandeira Antonio Bandeira Antonio Bandeira Ana Cumano Ana Cumano Ana Cumano |
| author_sort | Ramy Elsaid |
| collection | DOAJ |
| description | 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 γδ 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 tissue homeostasis and immune development later in life. |
| first_indexed | 2024-12-17T04:49:16Z |
| format | Article |
| id | doaj.art-69b310c353204defa5fb735fe180a2cd |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-17T04:49:16Z |
| publishDate | 2020-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-69b310c353204defa5fb735fe180a2cd2022-12-21T22:02:57ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-12-01810.3389/fcell.2020.606642606642Hematopoiesis: A Layered Organization Across Chordate SpeciesRamy Elsaid0Ramy Elsaid1Ramy Elsaid2Francisca Soares-da-Silva3Francisca Soares-da-Silva4Francisca Soares-da-Silva5Francisca Soares-da-Silva6Francisca Soares-da-Silva7Francisca Soares-da-Silva8Marcia Peixoto9Marcia Peixoto10Marcia Peixoto11Marcia Peixoto12Marcia Peixoto13Dali Amiri14Dali Amiri15Dali Amiri16Nathan Mackowski17Nathan Mackowski18Nathan Mackowski19Pablo Pereira20Pablo Pereira21Pablo Pereira22Antonio Bandeira23Antonio Bandeira24Antonio Bandeira25Ana Cumano26Ana Cumano27Ana Cumano28Unit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceI3S—Instituto de Investigação e Inovação em Saúde and INEB—Instituto Nacional de Engenharia Biomédica, Universidade do Porto, Porto, PortugalInstituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, PortugalGraduate Program in Areas of Basic and Applied Biology, Instituto de Ciências Biomeìdicas Abel Salazar, Universidade do Porto, Porto, PortugalUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceI3S—Instituto de Investigação e Inovação em Saúde and INEB—Instituto Nacional de Engenharia Biomédica, Universidade do Porto, Porto, PortugalInstituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, PortugalUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceUnit of Lymphocytes and Immunity, Immunology Department, Institut Pasteur, Paris, FranceINSERM U1223, Paris, FranceUniversité de Paris, Céllule Pasteur, Paris, FranceThe 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 γδ 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 tissue homeostasis and immune development later in life.https://www.frontiersin.org/articles/10.3389/fcell.2020.606642/fullhematopoieisislymphopoieisembryoevo devo biologylayered |
| spellingShingle | Ramy Elsaid Ramy Elsaid Ramy Elsaid Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Francisca Soares-da-Silva Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Marcia Peixoto Dali Amiri Dali Amiri Dali Amiri Nathan Mackowski Nathan Mackowski Nathan Mackowski Pablo Pereira Pablo Pereira Pablo Pereira Antonio Bandeira Antonio Bandeira Antonio Bandeira Ana Cumano Ana Cumano Ana Cumano Hematopoiesis: A Layered Organization Across Chordate Species Frontiers in Cell and Developmental Biology hematopoieisis lymphopoieis embryo evo devo biology layered |
| title | Hematopoiesis: A Layered Organization Across Chordate Species |
| title_full | Hematopoiesis: A Layered Organization Across Chordate Species |
| title_fullStr | Hematopoiesis: A Layered Organization Across Chordate Species |
| title_full_unstemmed | Hematopoiesis: A Layered Organization Across Chordate Species |
| title_short | Hematopoiesis: A Layered Organization Across Chordate Species |
| title_sort | hematopoiesis a layered organization across chordate species |
| topic | hematopoieisis lymphopoieis embryo evo devo biology layered |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2020.606642/full |
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