Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand

doi:10.1084/jem.175.4.1003

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Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand

MF Gurish, N Ghildyal, HP McNeil, KF Austen, S Gillis and RL Stevens
Department of Medicine, Harvard Medical School, Boston, Massachusetts 02115.

It is now established that the subclasses of mast cells (MC) that reside in mucosal and serosal environments can be distinguished from one another in terms of their expression of specific secretory granule- localized proteases and proteoglycans. Further, the hematopoietic- and connective tissue-derived cytokines that regulate expression of the genes that encode these constituents of the granule can now be identified using recently developed gene-specific probes and recombinant cytokines. When bone marrow-derived MC (BMMC) were developed with recombinant interleukin 3 (rIL-3) and maintained with this cytokine in the absence or presence of recombinant c-kit ligand (rKL), they remained safranin-, produced almost no 35S-labeled heparin proteoglycans, and contained greater levels of mouse MC protease (MMCP) -5 mRNA and mast cell carboxypeptidase A (MC-CPA) mRNA than MMCP-6 mRNA. They did not contain MMCP-4 or -2 mRNA, genes expressed late in the differentiation of progenitor cells into serosal and mucosal MCs, respectively. In contrast, BMMC developed with rKL alone or by sequential culture in medium containing rIL-3 followed by rKL expressed high levels of MMCP-4 and -6 mRNA, as well as the transcripts that encode MMCP-5 and MC-CPA. Although rKL-developed BMMC were safranin+ and produced substantial amounts of 35S-labeled heparin proteoglycans, they contained only minimal amounts of histamine and MC-CPA enzymatic activity relative to serosal MC. These are the first studies to characterize the transcriptional granule phenotype of a population of BMMC derived using any recombinant cytokine, to demonstrate a dissociation between histochemical staining and granule maturation, and to demonstrate antagonistic regulation of late expressed protease genes by a cytokine.
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Chen, Y., Garrison, S., Weis, J. J., Weis, J. H. (1998). Identification of Pactolus, an Integrin beta �Subunit-like Cell-surface Protein Preferentially Expressed by Cells of the Bone Marrow. J. Biol. Chem. 273: 8711-8718 [Abstract] [Full Text]
Toru, H., Eguchi, M., Matsumoto, R., Yanagida, M., Yata, J., Nakahata, T. (1998). Interleukin-4 Promotes the Development of Tryptase and Chymase Double-Positive Human Mast Cells Accompanied by Cell Maturation. Blood 91: 187-195 [Abstract] [Full Text]
Morii, E., Jippo, T., Tsujimura, T., Hashimoto, K., Kim, D.-K., Lee, Y.-M., Ogihara, H., Tsujino, K., Kim, H.-M., Kitamura, Y. (1997). Abnormal Expression of Mouse Mast Cell Protease 5�Gene in Cultured Mast Cells Derived From Mutant mi/mi Mice. Blood 90: 3057-3066 [Abstract] [Full Text]
Gurish, M. F., Friend, D. S., Webster, M., Ghildyal, N., Nicodemus, C. F., Stevens, R. L. (1997). Mouse Mast Cells That Possess Segmented/Multi-lobular Nuclei. Blood 90: 382-390 [Abstract] [Full Text]
Ohtsu, H., Kuramasu, A., Suzuki, S., Igarashi, K., Ohuchi, Y., Sato, M., Tanaka, S., Nakagawa, S., Shirato, K., Yamamoto, M., Ichikawa, A., Watanabe, T. (1996). Histidine Decarboxylase Expression in Mouse Mast Cell Line P815 Is Induced by Mouse Peritoneal Cavity Incubation. J. Biol. Chem. 271: 28439-28444 [Abstract] [Full Text]
Xia, Z., Ghildyal, N., Austen, K. F., Stevens, R. L. (1996). Post-transcriptional Regulation of Chymase Expression in Mast Cells. J. Biol. Chem. 271: 8747-8753 [Abstract] [Full Text]
Murakami, M., Austen, K. F., Bingham, C. O. , III, Friend, D. S., Penrose, J. F., Arm, J. P. (1995). Interleukin-3 Regulates Development of the 5-Lipoxygenase/Leukotriene C(4) Synthase Pathway in Mouse Mast Cells. J. Biol. Chem. 270: 22653-22656 [Abstract] [Full Text]
Samet, J. M., Fasano, M. B., Fonteh, A. N., Chilton, F. H. (1995). Selective Induction of Prostaglandin G/H Synthase I by Stem Cell Factor and Dexamethasone in Mast Cells. J. Biol. Chem. 270: 8044-8049 [Abstract] [Full Text]
Murakami, M., Matsumoto, R., Urade, Y., Austen, K. F., Arm, J. P. (1995). c-Kit Ligand Mediates Increased Expression of Cytosolic Phospholipase A(2), Prostaglandin Endoperoxide Synthase-1, and Hematopoietic Prostaglandin D(2) Synthase and Increased IgE-dependent Prostaglandin D(2) Generation in Immature Mouse Mast Cells. J. Biol. Chem. 270: 3239-3246 [Abstract] [Full Text]
Li, L., Macpherson, J. J., Adelstein, S., Bunn, C. L., Atkinson, K., Phadke, K., Krilis, S. A. (1995). Conditioned Media from a Cell Strain Derived from a Patient with Mastocytosis Induces Preferential Development of Cells That Possess High Affinity IgE Receptors and the Granule Protease Phenotype of Mature Cutaneous Mast Cells. J. Biol. Chem. 270: 2258-2263 [Abstract] [Full Text]
Pevny, L, Lin, C., D'Agati, V, Simon, M., Orkin, S., Costantini, F (1995). Development of hematopoietic cells lacking transcription factor GATA-1. Development 121: 163-172 [Abstract]