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Differential response of human basophils and mast cells to recombinant chemokines

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Abstract

Chemokines are proinflammatory peptides regulating the functions of various hematopoietic cells. We have analyzed the effects of seven recombinant human (rh) chemokines (MCAF, RANTES, MIP-1α, MIP-1β, IL-8, GRO, and IP-10) on the growth and function of human basophils and mast cells. We found that MCAF, but not RANTES, MlP-la, MIP-1β, IL-8, GRO, or IP-10, causes direct and dose-dependent histamine release from basophils (MCAF, 5 μg/ml: 26.9 ± 3.4%; other chemokines: < 5% of total histamine). An increased (2.1 to 3.5-fold) response to MCAF was obtained when basophils were preincubated with rh interleukin-3 (100 units/ml). Moreover, IL-3-primed basophils became responsive to physiologic concentrations (< 1 μg/ml) of MCAF, IL-8, and RANTES. None of the chemokines tested was able to induce histamine secretion in mast cells obtained from lung (n=2), skin (n=1), uterus (n=3), or tonsils (n=3), even when cells had been preincubated with the mast cell agonist SCF. The chemokines also failed to modulate the expression of activation antigens (CD11b/C3biR, CD25/IL-2Rβ, CD63, IL-3Rα, CD117/c-kit) on the mast cell line HMC-1 or the basophil cell line KU-812 and were unable to induce differentiation of basophils or mast cells in culture. Together, our results show that basophils respond to rhIL-8, rhMCAF, and rhRANTES and that, unlike human basophils, human mast cells are unresponsive to recombinant chemokines.

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References

  1. Alam R, Forsythe PA, Stafford S, Lett-Brown MA, Grant JA (1992) Macrophage inflammatory protein-1α activates basophils and mast cells. J Exp Med 176:781–786

    PubMed  Google Scholar 

  2. Alam R, Lett-Brown MA, Forsythe PA, Anderson-Walters DJ, Kenamore C, Kormos C, Grant JA (1992) Monocyte chemotactic and activating factor is a potent histamine-releasing factor for basophils. J Clin Invest 89:723–728

    PubMed  Google Scholar 

  3. Alam R, Stafford S, Forsythe P, Harrison R, Faubion D, Lett-Brown MA, Grant JA (1993) RANTES is a chemotactic and activating factor for human eosinophils. J Immunol 150:3442–3448

    PubMed  Google Scholar 

  4. Alam R, Kumar D, Anderson-Walters D, Forsythe PA (1994) Macrophage inflammatory protein-1 alpha and monocyte chemoattractant peptide-1 elicit immediate and late cutaneous reactions and activate murine mast cells in vivo. J Immunol 152:1298–1303

    PubMed  Google Scholar 

  5. Baggiolini M, Walz A, Kunkel SL (1989) Neutrophil-activating peptide 1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest 84:1045–1049

    PubMed  Google Scholar 

  6. Benyon RC, Lowman MA, Church MK (1987) Human skin mast cells: their dispersion, purification, and secretory characterization. J Immunol 138:861–867

    PubMed  Google Scholar 

  7. Bischoff SC, Dahinden CA (1992) c-kit ligand: a unique potentiator of mediator release from human lung mast cells. J Exp Med 175:237–244

    PubMed  Google Scholar 

  8. Bischoff SC, Dahinden CA (1992) Effect of nerve growth factor on the release of inflammatory mediators by mature basophils. Blood 79:2662–2669

    PubMed  Google Scholar 

  9. Bischoff SC, Krieger M, Brunner T, Dahinden CA (1992) Monocyte chemotactic protein 1 is a potent activator of human basophils. J Exp Med 175:1271–1275

    PubMed  Google Scholar 

  10. Bischoff SC, Krieger M, Brunner T, Rot A, von Tscharner V, Baggiolini M, Dahinden CA (1993) RANTES and related chemokines activate human basophil granulocytes through different G protein-coupled receptors. Eur J Immunol 23:761–767

    PubMed  Google Scholar 

  11. Bochner BS, Sterbinsky SA (1991) Altered expression of CD11 and Leu 8 during human basophil degranulation. J Immunol 146:2367–2373

    PubMed  Google Scholar 

  12. Bochner BS, McKelvey AA, Sterbinsky SA, Hildreth JEK, Derse CP, Klunk DA, Lichtenstein LM, Schleimer RP (1990) Interleukin-3 augments adhesiveness for endothelium and CD 11b expression in human basophils but not neutrophils. J Immunol 145:1832–1837

    PubMed  Google Scholar 

  13. Broxmeyer HE, Sherry B, Cooper S, Lu L, Maze R, Beckman MP, Cerami A, Ralph P (1993) Comparative analysis of the human macrophage inflammatory protein family of cytokines (chemokines) on proliferation of human myeloid progenitor cells. Interacting effects involving suppression, synergistic suppression, and blocking of suppression. J Immunol 150:3448–3458

    PubMed  Google Scholar 

  14. Butterfield JH, Weiler D, Dewald G, Gleich GJ (1988) Establishment of an immature mast cell line from a patient with mast cell leukemia. Leuk Res 12:345–355

    PubMed  Google Scholar 

  15. Church MK, Mageed RAK, Holgate ST (1983) Human tonsillar mast cells: characteristics of histamine secretion and methods of dispersion. Int Arch Allergy Appl Immunol 72:188–190

    PubMed  Google Scholar 

  16. Columbo M, Horowitz EM, Botana LM, McGlashan DW, Bochner BS, Gillis S, Zsebo KM, Galli SJ, Lichtenstein LM (1992) The human recombinant c-kit receptor ligand, rhSCF, induces mediator release from human cutaneous mast cells and enhances IgE-dependent mediator release from both skin mast cells and peripheral blood basophils. J Immunol 149:599–608

    PubMed  Google Scholar 

  17. Dahinden CA, Kurimoto Y, de Weck AL, Lindley B, Dewald B, Baggiolini M (1989) The neutrophil activating peptide NAF/NAP-1 induces histamine and leukotriene release by interleukin-3 primed basophils. J Exp Med 170:1787–1792

    PubMed  Google Scholar 

  18. Füreder W, Agis H, Sperr WR, Lechner K, Valent P (1994) The surface membrane antigen phenotype of human blood basophils. Allergy 49:861–865

    PubMed  Google Scholar 

  19. Galli SJ (1990) Biology of disease: New insights into the ‘riddle of the mast cells’: microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab Invest 62:5–33

    PubMed  Google Scholar 

  20. Hirai K, Morita YM, Misaki Y, Ohta K, Takaishi T, Suzuki S, Motoyoshi K, Miyamoto T (1988) Modulation of human basophil histamine release by hemopoietic growth factors. J Immunol 141:3958–3964

    PubMed  Google Scholar 

  21. Hirai K, Yamaguchi M, Misaki Y, Takaishi T, Ohta K, Morita Y, Ito K, Miyamoto T (1990) Enhancement of human basophil histamine release by interleukin 5. J Exp Med 172:1525–1528

    PubMed  Google Scholar 

  22. Kelvin DJ, Michiel DF, Johnston JA, Lloyd AR, Sprenger H, Oppenheim JJ, Wang JM (1993) Chemokines and serpentines: the molecular biology of chemokine receptors. J Leukoc Biol 54:604–612

    PubMed  Google Scholar 

  23. Kishi K (1986) A new leukemic cell line with Philadelphia chromosome characterized as basophil precursors. Leuk Res 9:381–390

    Google Scholar 

  24. Knol EF, Mul FPJ, Jansen H, Calafat J, Roos D (1991) Monitoring human basophil activation via CD63 monoclonal antibody 435. J Allergy Clin Immunol 88:328–338

    PubMed  Google Scholar 

  25. Krieger M, Brunner T, Bischoff SC, vTscharner V, Walz A, Moser B, Baggiolini M, Dahinden CA (1992) Activation of human basophils through the IL-8 receptor. J Immunol 149:2662–2667

    PubMed  Google Scholar 

  26. Kuna P, Reddigari SR, Rucinski D, Oppenheim JJ, Kaplan P (1992) Monocyte chemotactic and activating factor is a potent histamine-releasing factor for human basophils. J Exp Med 175:489–493

    PubMed  Google Scholar 

  27. Kuna P, Reddigari SR, Schall TJ, Rucinski D, Viksman MY, Kaplan AP (1992) RANTES, a monocyte and T lymphocyte chemotactic cytokine, releases histamine from human basophils. J Immunol 149:636–642

    PubMed  Google Scholar 

  28. Kuna P, Reddigari SR, Schall TJ, Rucinski D, Sadick M, Kaplan AP (1993) Characterization of human basophil response to cytokines, growth factors, and histamine-releasing fators of the intercrine/chemokine family. J Immunol 150: 1932–1943

    PubMed  Google Scholar 

  29. Lawrence ID, Warner JA, Cohan VL, Hubbard WC, Kagey-Sobotka A, Lichtenstein LM (1987) Purification and characterization of human skin mast cells. J Immunol 139:3062–3069

    PubMed  Google Scholar 

  30. Massey WA, Guo CB, Dvorak AM, Hrubbard WC, Bhagavan BS, Cohan VL, Warner JA, Sobotka AK, Lichtenstein LM (1991) Human uterine mast cells: purification, characterization, ultrastructure and pharmacology. J Immunol 147:1621–1627

    PubMed  Google Scholar 

  31. Miller MD, Krangel MS (1992) Biology and biochemistry of the chemokines. Crit Rev Immunol 12:17–46

    PubMed  Google Scholar 

  32. Mitsui H, Furitsu T, Dvorak AM, Irani AMA, Schwartz LB, Inagaki N, Takei M, Ishizaka K, Zsebo KM, Gillis S, Ishizaka T (1993) Development of human mast cells from umbilical cord blood cells by recombinant human and murine c-kit ligand. Proc Natl Acad Sci USA 90:735–740

    PubMed  Google Scholar 

  33. Moller A, Lippert U, Lessmann D, Kolde G, Hamann K, Welker P, Schadendorf D, Rosenbach T, Luger T, Czarnetzki BM (1993) Human mast cells produce IL-8. J Immunol 151:3261–3266

    PubMed  Google Scholar 

  34. Saito H, Hatake K, Dvorak AM, Leiferman KM, Donnenberg AD, Arai N, Ishizaka K, Ishizaka T (1988) Selective differentiation and proliferation of hematopoietic cells induced by recombinant human interleukins. Proc Natl Acad Sci USA 85:2288–2292

    PubMed  Google Scholar 

  35. Schall TJ, Bacon T, Toy KJ, Goeddel DV (1990) Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347:669–671

    PubMed  Google Scholar 

  36. Schall TJ, Bacon K, Camp RDR, Kaspari JW, Goeddel DV (1993) Human macrophage inflammatory proteinα (MIP-1α) and MIP1β chemokines attract distinct populations of lymphocytes. J Exp Med 177:1821–1826

    PubMed  Google Scholar 

  37. Schulman ES, Mac Glashan DW, Peters SP, Schleimer RP, Newball HH, Lichtenstein LM (1982) Lung mast cells: purification and characterization. J Immunol 129:2662–2667

    PubMed  Google Scholar 

  38. Schwartz LB, Huff TF (1991) Mast cells. In: Crystal RG, West JB et al. (eds) The lung. Raven Press, New York, pp 601–616

    Google Scholar 

  39. Selvan RS, Butterfield JH, Krangel MS (1994) Expression of multiple chemokine genes by a human mast cell leukemia. J Biol Chem 269:13893–13898

    PubMed  Google Scholar 

  40. Serafin WE, Austen KF (1987) Mediators of immediate hypersensitivity reactions. N Engl J Med 317:30–34

    PubMed  Google Scholar 

  41. Sperr WR, Czerwenka K, Mundigler G, Müller MR, Semper H, Klappacher G, Glogar HD, Lechner K, Valent P (1993) Specific activation of human mast cells by the ligand for c-kit: comparison between lung, uterus and heart mast cells. Int Arch Allergy Appl Immunol 102:170–175

    Google Scholar 

  42. Valent P, Bettelheim P (1992) Cell surface structures on human basophils and mast cells: biochemical and functional characterization. Adv Immunol 52:333–423

    PubMed  Google Scholar 

  43. Valent P, Ashman LK, Hinterberger W, Eckersberger F, Majdic O, Lechner K, Bettelheim P (1989) Mast cell typing: demonstration of a distinct hemopoietic cell type and evidence for immunophenotypic relationship to mononuclear phagocytes. Blood 73:1778–1785

    PubMed  Google Scholar 

  44. Valent P, Schmidt G, Besemer J, Mayer P, Zenke G, Liehl E, Hinterberger W, Lechner K, Bettelheim P (1989) Interleukin-3 is a differentiation factor for human basophils. Blood 73: 1763–1769

    PubMed  Google Scholar 

  45. Valent P, Besemer J, Muhm M, Majdic O, Lechner K, Bettelheim P (1989) Interleukin-3 activates human blood basophils via high-affinity binding sites. Proc Natl Acad Sci USA 86:5542–5546

    PubMed  Google Scholar 

  46. Valent P, Spanblöchl E, Sperr W, Sillaber C, Agis H, Strobl H, Zsebo KM, Geissler K, Bettelheim P, Lechner K (1992) Induction of differentiation of human mast cells from bone marrow and peripheral blood mononuclear cells by recombinant human stem cell factor (SCF)/kit ligand (KL) in long-term culture. Blood 80:2237–2245

    PubMed  Google Scholar 

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This work was supported by FWF Austria, grant P-9359, and by Sandoz, Vienna

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Füreder, W., Agis, H., Semper, H. et al. Differential response of human basophils and mast cells to recombinant chemokines. Ann Hematol 70, 251–258 (1995). https://doi.org/10.1007/BF01784044

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