Deciphering the Differentiation Trajectory from Hematopoietic Stem Cells to Mast Cells

Overview

Journal Blood Adv

Specialty Hematology

Date 2018 Sep 13

PMID 30206100

Citations 30

Authors

Jennine Grootens

Johanna S Ungerstedt

Gunnar Nilsson

Joakim S Dahlin

Affiliations

Soon will be listed here.

Abstract

Hematopoietic stem cells differentiate into all types of blood cells, including peripheral tissue-resident mast cells. The early mast cell differentiation takes place in the bone marrow, after which the progenitor cells enter the circulation and mature once reaching their target organ. Early results from single-cell culture experiments and colony-forming assays have produced the classic hierarchical tree model of hematopoiesis. The introduction of high-throughput, single-cell RNA sequencing is now revolutionizing our understanding of the differentiation process, questioning the classic tree-based models. By integrating the results from early cell culture experiments with single-cell transcriptomics, we present a differentiation landscape model of hematopoiesis and discuss it with focus on mast cells. The review also describes how the hematologic neoplasm systemic mastocytosis can be used to model human hematopoiesis using naturally occurring cell barcoding by means of the common D816V mutation.

Citing Articles

Integrative deep immune profiling of the elderly reveals systems-level signatures of aging, sex, smoking, and clinical traits.

Riemann L, Gutierrez R, Odak I, Barros-Martins J, Roesner L, Leon Lara X EBioMedicine. 2025; 112:105558.

PMID: 39862806 PMC: 11873576. DOI: 10.1016/j.ebiom.2025.105558.

Deciphering the effect of UM171 on human hematopoietic progenitor cell fate through clonal analysis.

Coulombe P, Tomellini E, Chagraoui J, Mayotte N, Sauvageau G Nat Commun. 2025; 16(1):195.

PMID: 39747844 PMC: 11696577. DOI: 10.1038/s41467-024-55225-7.

ICU patient-on-a-chip emulating orchestration of mast cells and cerebral organoids in neuroinflammation.

Saglam-Metiner P, Yanasik S, Odabasi Y, Modamio J, Negwer M, Biray-Avci C Commun Biol. 2024; 7(1):1627.

PMID: 39639082 PMC: 11621364. DOI: 10.1038/s42003-024-07313-z.

Inducible pluripotent stem cells to study human mast cell trajectories.

Idelman G, Rizza C, Marella S, Sharma A, Chakraborty S, Tay H Mucosal Immunol. 2024; 17(5):1029-1044.

PMID: 39038754 PMC: 11801248. DOI: 10.1016/j.mucimm.2024.07.003.

Novel insights into the ontogeny of basophils.

Miyake K, Ito J, Karasuyama H Front Allergy. 2024; 5:1402841.

PMID: 38803659 PMC: 11128600. DOI: 10.3389/falgy.2024.1402841.

References

Ochi H, Hirani W, Yuan Q, Friend D, Austen K, Boyce J . T helper cell type 2 cytokine-mediated comitogenic responses and CCR3 expression during differentiation of human mast cells in vitro. J Exp Med. 1999; 190(2):267-80. PMC: 2195573. DOI: 10.1084/jem.190.2.267. View

Hallgren J, Jones T, Abonia J, Xing W, Humbles A, Austen K . Pulmonary CXCR2 regulates VCAM-1 and antigen-induced recruitment of mast cell progenitors. Proc Natl Acad Sci U S A. 2007; 104(51):20478-83. PMC: 2154456. DOI: 10.1073/pnas.0709651104. View

Toru H, Ra C, Nonoyama S, Suzuki K, Yata J, Nakahata T . Induction of the high-affinity IgE receptor (Fc epsilon RI) on human mast cells by IL-4. Int Immunol. 1996; 8(9):1367-73. DOI: 10.1093/intimm/8.9.1367. View

Escribano L, Orfao A, Villarrubia J, Cervero C, Lopez A, Marcos M . Indolent systemic mast cell disease in adults: immunophenotypic characterization of bone marrow mast cells and its diagnostic implications. Blood. 1998; 91(8):2731-6. View

Dahlin J, Heyman B, Hallgren J . Committed mast cell progenitors in mouse blood differ in maturity between Th1 and Th2 strains. Allergy. 2013; 68(10):1333-7. PMC: 4226387. DOI: 10.1111/all.12223. View

Jamur M, Moreno A, Mello L, Souza Junior D, Campos M, Pastor M . Mast cell repopulation of the peritoneal cavity: contribution of mast cell progenitors versus bone marrow derived committed mast cell precursors. BMC Immunol. 2010; 11:32. PMC: 2912243. DOI: 10.1186/1471-2172-11-32. View

Kanakura Y, Kuriu A, Waki N, Nakano T, Asai H, Yonezawa T . Changes in numbers and types of mast cell colony-forming cells in the peritoneal cavity of mice after injection of distilled water: evidence that mast cells suppress differentiation of bone marrow-derived precursors. Blood. 1988; 71(3):573-80. View

Bankova L, Dwyer D, Liu A, Austen K, Gurish M . Maturation of mast cell progenitors to mucosal mast cells during allergic pulmonary inflammation in mice. Mucosal Immunol. 2014; 8(3):596-606. PMC: 4390399. DOI: 10.1038/mi.2014.91. View

Garcia-Montero A, Jara-Acevedo M, Teodosio C, Sanchez M, Nunez R, Prados A . KIT mutation in mast cells and other bone marrow hematopoietic cell lineages in systemic mast cell disorders: a prospective study of the Spanish Network on Mastocytosis (REMA) in a series of 113 patients. Blood. 2006; 108(7):2366-72. DOI: 10.1182/blood-2006-04-015545. View

10.

Dahlin J, Ekoff M, Grootens J, Lof L, Amini R, Hagberg H . KIT signaling is dispensable for human mast cell progenitor development. Blood. 2017; 130(16):1785-1794. PMC: 5659818. DOI: 10.1182/blood-2017-03-773374. View

11.

Dahl C, Hoffmann H, Saito H, Schiotz P . Human mast cells express receptors for IL-3, IL-5 and GM-CSF; a partial map of receptors on human mast cells cultured in vitro. Allergy. 2004; 59(10):1087-96. DOI: 10.1111/j.1398-9995.2004.00606.x. View

12.

Sasaki H, Kurotaki D, Tamura T . Regulation of basophil and mast cell development by transcription factors. Allergol Int. 2016; 65(2):127-134. DOI: 10.1016/j.alit.2016.01.006. View

13.

Abonia J, Hallgren J, Jones T, Shi T, Xu Y, Koni P . Alpha-4 integrins and VCAM-1, but not MAdCAM-1, are essential for recruitment of mast cell progenitors to the inflamed lung. Blood. 2006; 108(5):1588-94. PMC: 1895513. DOI: 10.1182/blood-2005-12-012781. View

14.

Arinobu Y, Iwasaki H, Gurish M, Mizuno S, Shigematsu H, Ozawa H . Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. Proc Natl Acad Sci U S A. 2005; 102(50):18105-10. PMC: 1312421. DOI: 10.1073/pnas.0509148102. View

15.

Rodewald H, Dessing M, Dvorak A, Galli S . Identification of a committed precursor for the mast cell lineage. Science. 1996; 271(5250):818-22. DOI: 10.1126/science.271.5250.818. View

16.

Austen K, Gurish M . Resolution of a human mast cell development conundrum. Blood. 2017; 130(16):1777-1778. DOI: 10.1182/blood-2017-09-802173. View

17.

Gurish M, Tao H, Abonia J, Arya A, Friend D, Parker C . Intestinal mast cell progenitors require CD49dbeta7 (alpha4beta7 integrin) for tissue-specific homing. J Exp Med. 2001; 194(9):1243-52. PMC: 2195984. DOI: 10.1084/jem.194.9.1243. View

18.

Mitsui H, Furitsu T, Dvorak A, Irani A, Schwartz L, Inagaki N . Development of human mast cells from umbilical cord blood cells by recombinant human and murine c-kit ligand. Proc Natl Acad Sci U S A. 1993; 90(2):735-9. PMC: 45740. DOI: 10.1073/pnas.90.2.735. View

19.

Denburg J, Richardson M, Telizyn S, Bienenstock J . Basophil/mast cell precursors in human peripheral blood. Blood. 1983; 61(4):775-80. View

20.

Akashi K, Traver D, Miyamoto T, Weissman I . A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000; 404(6774):193-7. DOI: 10.1038/35004599. View