Mast cell heterogeneity: derivation and function, with emphasis on the intestine

Bienenstock, John; Befus, A D; Pearce, F. L.; Denburg, JA; Goodacre, R.L.

doi:10.1016/0091-6749(82)90001-x

Cited by 138 publications

(65 citation statements)

References 38 publications

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“…Moreover, peritoneal mast cells are typical connective tissue mast cells, whereas mast ceil-like cells in the suspension culture are considered to resemble mucosal mast cells (47). Biochemical, functional, and immunological characterization revealed the difference between connective tissue mast cells and mucosal mast cells (47,48). There is a possibility that the peritoneal mast cell with proliferative potentiality may have characteristics similar to mast cell-like cells that developed in vitro.…”

Section: Discussionmentioning

confidence: 99%

Proliferation of peritoneal mast cells in the skin of W/Wv mice that genetically lack mast cells.

Sonoda¹,

Kanayama²,

Hara³

et al. 1984

The Journal of Experimental Medicine

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Presence of mast cell precursors in the mouse peritoneal cavity was demonstrated, and the precursors were characterized. When a cell suspension, containing mast cell precursor(s), was directly injected into the skin of genetically mast cell-deficient WBB6F1 (WB X C57BL/6)-W/Wv mice, a cluster composed of approximately 2,000 mast cells appeared at the injection site. By determining the proportion of injection sites at which the mast cell cluster appeared, the concentration of mast cell precursors can be calculated by limiting dilution analysis. The concentration in the peritoneal cavity was about five times as great as the concentration in the bone marrow. Although peritoneal mast cell precursors were shown to originate from the bone marrow, physical characterization revealed that the peritoneal precursors differed from the marrow precursors. The peritoneal precursors were less susceptible to irradiation than the marrow precursors; the former were heavier than the latter. When a 95% pure mast cell suspension was prepared from the peritoneal cells by the removal of phagocytes and the density gradient centrifugation, 1 out of 16 cells had the potentiality to make a mast cell cluster in the skin of the W/Wv mice. Moreover, when a single mast cell was identified under the phase contrast microscope and picked up with the micromanipulator, 1 out of 17 mast cells made the cluster. This indicated that some peritoneal mast cells kept extensive proliferative potentiality even after morphological differentiation. In other words, some peritoneal mast cells themselves may function as the committed precursors.

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Section: Discussionmentioning

confidence: 99%

Proliferation of peritoneal mast cells in the skin of W/Wv mice that genetically lack mast cells.

Sonoda¹,

Kanayama²,

Hara³

et al. 1984

The Journal of Experimental Medicine

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“…With this aim, we have measured both the resting output of acetylcholine and histamine, and their release resulting from stimulation of the vagus nerve of isolated, vagally innerved guinea-pig auricles, or from the field stimulation of parasympathetic nerve endings of isolated ileal segments of the rat. We have selected these preparations from different animal species containing connective tissue mast cells and mucosal mast cells, in consideration of mast cell heterogeneity in response to the same stimulus (Bienenstock, Befus, Pearce, Denburg & Goodacre, 1982). A preliminary report of some of the results was communicated at the European Histamine Research Society Meetings (Blandina, Barattini, Fantozzi, Masini & Mannaioni, 1983;Blandina, Barattini, Fantozzi, Masini, Brunelleschi & Mannaioni, 1984).…”

Section: Introductionmentioning

confidence: 99%

The release of histamine by parasympathetic stimulation in guinea‐pig auricle and rat ileum.

Bani-Sacchi¹,

Barattini²,

Bianchi³

et al. 1986

The Journal of Physiology

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SUMMARY1. Two preparations, a segment of rat ileum and the vagally innerved guinea-pig auricles, have been used in an analysis of the responses to vagal or to electrical field stimulation.2. The responses to parasympathetic stimulation were depressed by atropine and by tetrodotoxin, and potentiated by eserine.3. Supramaximal stimulation (10-20 Hz) resulted in increased release of acetylcholine and histamine, both in rat ileum and guinea-pig auricles.4. The release of histamine after parasympathetic stimulation did not exhibit tachyphylaxis, and it was not reproduced by non-parasympathetic stimuli.5. In both preparations, atropine produced a significant, dose-related reduction of histamine measured in the bath fluid after stimulation, while eserine increased histamine output.6. A significant diminution of mast cell granules metachromasia was observed in guinea-pig auricles and in rat intestine after parasympathetic stimulation.7. The possibility is discussed that acetylcholine released by parasympathetic stimulation would in turn evoke the secretion of histamine from tissue mast cells.

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“…Major functional differences have been shown between mast cells obtained from the peritoneal cavity (PMCs) and intestinal mucosal mast cells (IMMCs) isolated from the normal lamina propria as well as from rats infected with the nematode Nippostrongylus brasiliensis, which promotes intestinal mast cell hyperplasia (3,4). Many secretagogues that affect PMCs have no effect on IMMCs, and similar differential effects are seen with many anti-allergic compounds (5). Indeed, previous reports (J.B. and coworkers, refs.…”

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confidence: 99%

Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves.

Stead¹,

Tomioka²,

Quinonez³

et al. 1987

Proc. Natl. Acad. Sci. U.S.A.

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Inflammatory or allergic conditions, as well as situations where healing and repair processes occur, are characterized by the presence of increased numbers of mast cells. Previous work on the effect of neuropeptides on mast cell mediator release showed that only substance P caused such release from intestinal mucosal mast cells [Shanahan, F., Denburg, J. A., Fox, J., Bienenstock, J. & Befus, A. D. (1985) J. Immunol. 135, 1331Immunol. 135, -1337. Accordingly, we investigated the microanatomical relationship between mast cells and enteric nerves in normal rat intestine and parasite-infected rat intestine, in which mucosal mast cell hyperplasia occurs. Combined immunohistochemistry for neuron-specific enolase and staining with alcian blue at pH 0.5 was employed on paraffinembedded sections of normal and Nippostrongylus brasiliensisinfected rat jejunum. Sixty-seven percent of intestinal mucosal mast cells were touching subepithelial nerves, and an additional 20% were within 2 ,im of nerves. Assessment of the proportion of the lamina propria occupied by mast cells (12.5%), the average mast cell area (121 ± 28 MAm2), and the density of enteric nerves (one per 788 ± 151 ,um2) suggested that the association was 5 times greater than would be expected by chance alone (P < 0.0001). In consecutive sections, the nerves in contact with mast cells were also shown to contain substance P and/or calcitonin-gene-related peptide. Electron microscopy confirmed this association: 8% of the mast cells in infected rats exhibited membrane-membrane contact with unmyelinated axons containing 70-to 170-nm dense-core vesicles, and an additional 31% were situated less than 250 nm from nerves. Other mast cells appeared to embrace nerve bundles through the projection of lamellopodia. These data provide systematic quantitative evidence that a structural foundation for communication between the immune and nervous systems exists in the rat gastrointestinal tract.The histochemical and functional heterogeneity of mast cells is well described and accepted, especially in the rat (1, 2). Major functional differences have been shown between mast cells obtained from the peritoneal cavity (PMCs) and intestinal mucosal mast cells (IMMCs) isolated from the normal lamina propria as well as from rats infected with the nematode Nippostrongylus brasiliensis, which promotes intestinal mast cell hyperplasia (3, 4). Many secretagogues that affect PMCs have no effect on IMMCs, and similar differential effects are seen with many anti-allergic compounds (5). Indeed, previous reports (J.B. and coworkers, refs. 6 and 7) showed that whereas both endorphins and neuropeptides caused degranulation of PMCs in vitro, only substance P promoted histamine release from IMMCs (6, 7).These in vitro observations are in keeping with in vivo experiments that strongly suggest that mast cells and nerves may communicate directly, presumably through soluble mediators. Kiernan (8) and Lembeck and Holzer (9) suggested that mast cells may be involved in the axon reflex responsible...

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Mast cell heterogeneity: derivation and function, with emphasis on the intestine

Cited by 138 publications

References 38 publications

Proliferation of peritoneal mast cells in the skin of W/Wv mice that genetically lack mast cells.

Proliferation of peritoneal mast cells in the skin of W/Wv mice that genetically lack mast cells.

The release of histamine by parasympathetic stimulation in guinea‐pig auricle and rat ileum.

Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves.

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