Induction of differentiation of human mast cells from bone marrow and peripheral blood mononuclear cells by recombinant human stem cell factor/kit-ligand in long-term culture.

In the murine system, a number of cytokines (including interleukin-3 [IL-3], IL-4, and stem cell factor [SCF]) promote the growth of mast cells (MCs). However, so far little is known about factors controlling differentiation of human MCs. Recent data suggest that human MCs express receptors (R) for SCF. The aim of the present study was to investigate whether recombinant human (rh) SCF induces differentiation of human MCs from their precursor cells. For this purpose, bone marrow (BM; normal donors, n = 6) and peripheral blood (PB; normal donors, n = 11) mononuclear cells (MNC) were cultured in the presence of rhSCF, rhIL-3, rhIL-4, rhIL-9, recombinant human macrophage colony-stimulating factor (rhM-CSF), or control medium in long-term (8 weeks) suspension cultures. After 4 weeks, up to 5% of the MNC (BM and PB) cultured in the presence of rhSCF, but not in the presence of other cytokines, were found to exhibit the characteristics of MCs. These MCs expressed the YB5.B8-reactive domain of the SCF R as well as IgE R, as determined by combined toluidine blue/immunofluorescence staining. Myeloid antigens, likewise expressed on human basophils (ie, CD11b, CDw65, and Bsp-1), could not be detected on these cells. Furthermore, rhSCF, but not rhIL-3, rhIL-4, rhIL-9, or rhM-CSF, induced dose- and time-dependent increases in the formation of cellular tryptase (an MC-specific enzyme) (rhSCF [100 ng/mL], 1,308 +/- 679 ng/mL v control medium, 18 +/- 6 ng/mL tryptase on day 35 of PB cell cultures), as well as an increase in cellular histamine. After 6 to 8 weeks, when other mature hematopoietic cells decreased, MCs still could be detected in culture, with up to 40% of all cells being MCs. To test whether rhSCF also activates tissue MCs, we performed histamine release experiments (dispersed tissue; lung, n = 3; uterus, n = 3). SCF was found to enhance (by up to 3.4-fold) the capacity of the MCs to release histamine upon cross-linkage of IgE R with anti-IgE. Together, these observations suggest that rhSCF induces in vitro differentiation of human MCs from their BM and PB precursor cells in long-term culture and upregulates MC releasability.

[1]  S. Bischoff,et al.  c-kit ligand: a unique potentiator of mediator release by human lung mast cells , 1992, The Journal of experimental medicine.

[2]  E. Morii,et al.  Characterization of Ws mutant allele of rats: a 12-base deletion in tyrosine kinase domain of c-kit gene. , 1991, Blood.

[3]  J. Warner,et al.  Human uterine mast cells. Isolation, purification, characterization, ultrastructure, and pharmacology. , 1991, Journal of immunology.

[4]  M. Tsai,et al.  Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[5]  L. Ashman,et al.  Expression of the YB5.B8 antigen (c-kit proto-oncogene product) in normal human bone marrow. , 1991, Blood.

[6]  Y. Kitamura,et al.  Nerve growth factor induces development of connective tissue-type mast cells in vitro from murine bone marrow cells , 1991, The Journal of experimental medicine.

[7]  M. Welham,et al.  Modulation of c-kit mRNA and protein by hemopoietic growth factors , 1991, Molecular and cellular biology.

[8]  O. Majdic,et al.  Interleukin 4 promotes expression of mast cell ICAM-1 antigen. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. Leder,et al.  Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the SId mutant , 1991, Cell.

[10]  K. Zsebo,et al.  Recombinant human stem cell factor synergises with GM-CSF, G-CSF, IL-3 and epo to stimulate human progenitor cells of the myeloid and erythroid lineages. , 1991, Experimental hematology.

[11]  T. Mosmann,et al.  Interleukin 10: a novel stimulatory factor for mast cells and their progenitors , 1991, The Journal of experimental medicine.

[12]  L. Ashman,et al.  Monoclonal antibody YB5.B8 identifies the human c-kit protein product. , 1991, Blood.

[13]  O. Majdic,et al.  Failure to detect IL-3-binding sites on human mast cells. , 1990, Journal of immunology.

[14]  P. Leder,et al.  The hematopoietic growth factor KL is encoded by the SI locus and is the ligand of the c-kit receptor, the gene product of the W locus , 1990, Cell.

[15]  C. March,et al.  Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms , 1990, Cell.

[16]  David A. Williams,et al.  Stem cell factor is encoded at the SI locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor , 1990, Cell.

[17]  N. Copeland,et al.  Mast cell growth factor maps near the steel locus on mouse chromosome 10 and is deleted in a number of steel alleles , 1990, Cell.

[18]  C. March,et al.  Identification of a ligand for the c-kit proto-oncogene , 1990, Cell.

[19]  K. Zsebo,et al.  Primary structure and functional expression of rat and human stem cell factor DNAs , 1990, Cell.

[20]  P. Valent,et al.  Recombinant human interleukin-3 expands the pool of circulating hematopoietic progenitor cells in primates--synergism with recombinant human granulocyte/macrophage colony-stimulating factor. , 1990, Blood.

[21]  L. Hültner,et al.  Purification of MEA, a mast cell growth-enhancing activity, to apparent homogeneity and its partial amino acid sequencing. , 1990, Journal of immunology.

[22]  Joseph Schlessinger,et al.  Signal transduction by receptors with tyrosine kinase activity , 1990, Cell.

[23]  R. Stead,et al.  The role of mast cell degranulation products in mast cell hyperplasia. I. Mechanism of action of nerve growth factor. , 1990, Journal of immunology.

[24]  S. Galli,et al.  New insights into "the riddle of the mast cells": microenvironmental regulation of mast cell development and phenotypic heterogeneity. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[25]  A. Dvorak,et al.  Development of human mast cells in vitro. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Metcalfe,et al.  Inhibition of the growth of IL-3-dependent mast cells from murine bone marrow by recombinant granulocyte macrophage-colony-stimulating factor. , 1989, Journal of immunology.

[27]  M. Muhm,et al.  Interleukin 3 activates human blood basophils via high-affinity binding sites. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Valent,et al.  Interleukin-3 is a differentiation factor for human basophils. , 1989, Blood.

[29]  L. Ashman,et al.  Mast cell typing: demonstration of a distinct hematopoietic cell type and evidence for immunophenotypic relationship to mononuclear phagocytes. , 1989, Blood.

[30]  D. Metcalf,et al.  The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells , 1989, Nature.

[31]  S. Dreskin,et al.  IL-3-dependent growth of basophil-like cells and mastlike cells from human bone marrow. , 1989, Journal of immunology.

[32]  L. Schwartz,et al.  Ultrastructural analysis of maturing human T and TC mast cells in situ. , 1989, Laboratory investigation; a journal of technical methods and pathology.

[33]  A. Dvorak,et al.  Preferential differentiation of inflammatory cells by recombinant human interleukins. , 1989, International archives of allergy and applied immunology.

[34]  H. Kronenberg,et al.  Identification and characterization of human hemopoietic mast cell colonies. , 1988, Experimental hematology.

[35]  D. Housman,et al.  The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene , 1988, Cell.

[36]  J. Denburg,et al.  Nerve growth factor promotes human hemopoietic colony growth and differentiation. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A. Donnenberg,et al.  Selective differentiation and proliferation of hematopoietic cells induced by recombinant human interleukins. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[38]  C. Juttner,et al.  Expression of a 150-kD cell surface antigen identified by monoclonal antibody YB5.B8 is associated with poor prognosis in acute non-lymphoblastic leukaemia. , 1988, Leukemia research.

[39]  G. Dewald,et al.  Establishment of an immature mast cell line from a patient with mast cell leukemia. , 1988, Leukemia research.

[40]  A. B. Lyons,et al.  A monoclonal antibody to a human mast cell/myeloid leukaemia-specific antigen binds to normal haemopoietic progenitor cells and inhibits colony formation in vitro. , 1988, Leukemia research.

[41]  U. Jäger,et al.  Human blood basophils display a unique phenotype including activation linked membrane structures. , 1987, Blood.

[42]  J. Sierra,et al.  [Prognosis in acute non-lymphoblastic leukemia]. , 1987, Medicina clinica.

[43]  R. Kamen,et al.  The human hematopoietic colony-stimulating factors. , 1987, Science.

[44]  L. Ashman,et al.  Specificity of a mouse monoclonal antibody raised against acute myeloid leukaemia cells for mast cells in human mucosal and connective tissues , 1987, Immunology and cell biology.

[45]  C. Sieff.  Hematopoietic growth factors. , 1987, The Journal of clinical investigation.

[46]  P. H. Fitzgerald,et al.  A monoclonal antibody reacting with human basophils. , 1987, Blood.

[47]  L. Schwartz,et al.  Quantitation of histamine, tryptase, and chymase in dispersed human T and TC mast cells. , 1987, Journal of immunology.

[48]  L. Schwartz,et al.  Evaluation of human peripheral blood leukocytes for mast cell tryptase. , 1987, Journal of immunology.

[49]  T. Honjo,et al.  Interleukin 4 as an essential factor for in vitro clonal growth of murine connective tissue-type mast cells , 1987, The Journal of experimental medicine.

[50]  K. Austen,et al.  Fibroblasts maintain the phenotype and viability of the rat heparin-containing mast cell in vitro. , 1985, Journal of immunology.

[51]  L. Ashman,et al.  A murine monoclonal antibody specific for a cell-surface antigen expressed by a subgroup of human myeloid leukaemias. , 1985, Leukemia research.

[52]  D. Seldin,et al.  Interleukin 3: A differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. , 1984, Journal of immunology.

[53]  M. Horton,et al.  Characterization of human mast cells in long-term culture. , 1983, Blood.

[54]  J. Ihle,et al.  Biologic properties of homogeneous interleukin 3. I. Demonstration of WEHI-3 growth factor activity, mast cell growth factor activity, p cell-stimulating factor activity, colony-stimulating factor activity, and histamine-producing cell-stimulating factor activity. , 1983, Journal of immunology.

[55]  J. Denburg,et al.  Basophil/Mast Cell Precursors in Human Peripheral Blood , 1983 .

[56]  W. Sterry,et al.  In vitro generation of mast cell-like cells from human peripheral mononuclear phagocytes. , 1983, International archives of allergy and applied immunology.

[57]  J. Bienenstock,et al.  Basophil/mast cell precursors in human peripheral blood. , 1983, Blood.

[58]  Y. Kitamura,et al.  Spleen colony-forming cell as common precursor for tissue mast cells and granulocytes , 1981, Nature.

[59]  O. Garson,et al.  The presence of mast cells in agar cultures. , 1980, Experimental hematology.

[60]  Y. Kitamura,et al.  Decreased production of mast cells in S1/S1d anemic mice. , 1979, Blood.

[61]  Y. Kitamura,et al.  Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. , 1978, Blood.

[62]  D. Lagunoff,et al.  THE IN VITRO DIFFERENTIATION OF MAST CELLS , 1967, The Journal of cell biology.