Submucosal mast cells in the gastrointestinal tract are a target of staphylococcal enterotoxin type A

Abstract

Staphylococcal enterotoxin A (SEA) is a leading causative toxin of staphylococcal food poisoning. However, it remains unclear how this toxin induces emesis in humans, primates, and certain experimental animals. To understand the mechanism of SEA-induced emesis, we investigated the behavior of SEA in the gastrointestinal (GI) tract in vivo using the house musk shrew (Suncus murinus). Immunofluorescence of GI sections showed that perorally administered SEA translocated from the lumen to the interior tissues of the GI tract and rapidly accumulated in certain submucosa cells. These SEA-binding cells in the submucosa were both tryptase- and FcεRIα-positive, suggesting these SEA-binding cells were mast cells. These SEA-binding mast cells were 5-hydroxytryptamine (5-HT)-positive, but the intensity of the 5-HT signal decreased over time compared to that of mast cells in the negative control. Furthermore, toluidine blue staining showed the number of metachromatic mast cells was decreased in the duodenal submucosa, suggesting that SEA binding induced degranulation and release of 5-HT from submucosal mast cells. These observations suggest that the target cells of SEA are submucosal mast cells in the GI tract and that 5-HT released from submucosal mast cells plays an important role in SEA-induced emesis.

Identification and Characterization of a Novel Staphylococcal Emetic Toxin

“…The cloning and preparation of recombinant SEA and SET have been described elsewhere (5,17). To construct the recombinant SElY expression plasmid, PCR primers including the BamHI and EcoRI sites were designed to amplify a fragment of the sely gene corresponding to the mature form of SElY ( Table 2).…”

Goblet cells are involved in translocation of staphylococcal enterotoxin A in the intestinal tissue of house musk shrew (Suncus murinus )

“…It has been shown that SEA interacts to the mast cells in the submucosa of the stomach and duodenum (Ono et al . ). However, our result demonstrated that SEA remains in the portion of mucus and does not translocate into the mucosa of the gastric loop.…”

“…).In addition, 5‐HT‐containing mast cells in the submucosa of stomach and duodenum undergo degranulation from 30 to 90 min after PO administration of SEA (Ono et al . ). From these results, it is hypothesized that SEA can translocate across the gastrointestinal mucosal barrier rapidly after PO administration.…”

“…Our previous study demonstrated that sensory stimulus of vomiting caused by SEA is transmitted from the abdominal viscera through the vagus and sympathetic nerve in house musk shrew and that 5hydroxytryptamine (5-HT) released in the small intestine by stimulation with SEA is involved in the emetic response (Hu et al 2007). In addition, 5-HT-containing mast cells in the submucosa of stomach and duodenum undergo degranulation from 30 to 90 min after PO administration of SEA (Ono et al 2012). From these results, it is hypothesized that SEA can translocate across the gastrointestinal mucosal barrier rapidly after PO administration.…”

Serotonin‐induced contractile responses of esophageal smooth muscle in the house musk shrew (Suncus murinus)

“…This is because the suncus has ability to vomit in response to mild shaking or chemicals . In the suncus, moreover, serotonin that is released from submucosal mast cells in the stomach and duodenum stimulated by a bacterial toxin plays an important role in toxin‐induced emesis …”