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      The ontogenesis and heterogeneity of basophils

      review-article
      ,
      Discovery Immunology
      Oxford University Press
      basophil, ontogenesis, hematopoiesis, heterogeneity

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          Summary

          Basophils are the rarest leukocytes, but they have essential roles in protection against helminths, allergic disorders, autoimmune diseases, and some cancers. For years, the clinical significance of basophils has been neglected because of the lack of proper experimental tools to study them. The development of basophil-specific antibodies and animal models, along with genomic advances like single-cell transcriptomics, has greatly enhanced our understanding of basophil biology. Recent discoveries regarding basophils prompted us to write this review, emphasizing the basophil developmental pathway. In it, we chronologically examine the steps of basophil development in various species, which reveals the apparent advent of basophils predating IgE and basophil’s IgE-independent regulatory role in primitive vertebrates. Then, we cover studies of basophil development in adult bone marrow, and compare those of murine and human basophils, introducing newly identified basophil progenitors and mature basophil subsets, as well as the transcription factors that regulate the transitions between them. Last, we discuss the heterogeneity of tissue-resident basophils, which may develop through extramedullary hematopoiesis. We expect that this review will contribute to a deeper understanding of basophil biology from the intricate aspects of basophil development and differentiation, offering valuable insights for both researchers and clinicians.

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          Most cited references147

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          Tissue-Resident Macrophage Ontogeny and Homeostasis.

          Defining the origins and developmental pathways of tissue-resident macrophages should help refine our understanding of the role of these cells in various disease settings and enable the design of novel macrophage-targeted therapies. In recent years the long-held belief that macrophage populations in the adult are continuously replenished by monocytes from the bone marrow (BM) has been overturned with the advent of new techniques to dissect cellular ontogeny. The new paradigm suggests that several tissue-resident macrophage populations are seeded during waves of embryonic hematopoiesis and self-maintain independently of BM contribution during adulthood. However, the exact nature of the embryonic progenitors that give rise to adult tissue-resident macrophages is still debated, and the mechanisms enabling macrophage population maintenance in the adult are undefined. Here, we review the emergence of these concepts and discuss current controversies and future directions in macrophage biology.
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            A lineage of myeloid cells independent of Myb and hematopoietic stem cells.

            Macrophages and dendritic cells (DCs) are key components of cellular immunity and are thought to originate and renew from hematopoietic stem cells (HSCs). However, some macrophages develop in the embryo before the appearance of definitive HSCs. We thus reinvestigated macrophage development. We found that the transcription factor Myb was required for development of HSCs and all CD11b(high) monocytes and macrophages, but was dispensable for yolk sac (YS) macrophages and for the development of YS-derived F4/80(bright) macrophages in several tissues, such as liver Kupffer cells, epidermal Langerhans cells, and microglia--cell populations that all can persist in adult mice independently of HSCs. These results define a lineage of tissue macrophages that derive from the YS and are genetically distinct from HSC progeny.
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              Identification of clonogenic common lymphoid progenitors in mouse bone marrow.

              The existence of a common lymphoid progenitor that can only give rise to T cells, B cells, and natural killer (NK) cells remains controversial and constitutes an important gap in the hematopoietic lineage maps. Here, we report that the Lin(-)IL-7R(+)Thy-1(-)Sca-1loc-Kit(lo) population from adult mouse bone marrow possessed a rapid lymphoid-restricted (T, B, and NK) reconstitution capacity in vivo but completely lacked myeloid differentiation potential either in vivo or in vitro. A single Lin(-)IL-7R(+)Thy-1(-)Sca-1loc-Kit(lo) cell could generate at least both T and B cells. These data provide direct evidence for the existence of common lymphoid progenitors in sites of early hematopoiesis.
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                Author and article information

                Contributors
                Journal
                Discov Immunol
                Discov Immunol
                discovimmunology
                Discovery Immunology
                Oxford University Press (US )
                2754-2483
                2024
                02 February 2024
                02 February 2024
                : 3
                : 1
                : kyae003
                Affiliations
                Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea
                Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea
                Author notes
                Correspondence: Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea. Email: suk-jo.kang@ 123456kaist.ac.kr
                Author information
                https://orcid.org/0000-0003-2653-576X
                Article
                kyae003
                10.1093/discim/kyae003
                10941320
                38567293
                85e004a5-b48b-4da1-9093-454845d68839
                © The Author(s) 2024. Published by Oxford University Press on behalf of the British Society for Immunology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 04 November 2023
                : 02 January 2024
                : 31 January 2024
                : 15 March 2024
                Page count
                Pages: 15
                Funding
                Funded by: National Research Foundation, DOI 10.13039/501100001321;
                Award ID: RS-2023-00220369
                Award ID: RS-2023-00248457
                Categories
                Mononuclear Cells
                Review
                AcademicSubjects/MED00010
                AcademicSubjects/MED00770
                AcademicSubjects/MED00730

                basophil,ontogenesis,hematopoiesis,heterogeneity
                basophil, ontogenesis, hematopoiesis, heterogeneity

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