Abstract
Although previous studies have characterized some aspects of the immune response of the teleost gut in response to diverse pathogens or stimuli, most studies have focused on the posterior segments exclusively. However, there are still many details of how teleost intestinal immunity is regulated that remain unsolved, including the location of IgM+ and IgT+ B cells along the digestive tract and their role during the course of a local stimulus. Thus, in the current work, we have studied the B cell response in five different segments of the rainbow trout (Oncorhynchus mykiss) digestive tract in both naïve fish and fish orally vaccinated with an alginate-encapsulated DNA vaccine against infectious pancreatic necrosis virus (IPNV). IgM+ and IgT+ cells were identified all along the tract with the exception of the stomach in naïve fish. While IgM+ cells were mostly located in the lamina propria (LP), IgT+ cells were primarily localized as intraepithelial lymphocytes (IELs). Scattered IgM+ IELs were only detected in the pyloric caeca. In response to oral vaccination, the pyloric caeca region was the area of the digestive tract in which a major recruitment of B cells was demonstrated through both real time PCR and immunohistochemistry, observing a significant increase in the number of both IgM+ and IgT+ IELs. Our findings demonstrate that both IgM+ and IgT+ respond to oral stimulation and challenge the paradigm that teleost IELs are exclusively T cells. Unexpectedly, we have also detected B cells in the fat tissue associated to the digestive tract that respond to vaccination, suggesting that these cells surrounded by adipocytes also play a role in mucosal defense.
Highlights
Mucosal immunity in fish has recently become a broadly explored field of research, mainly busted by the need for oral vaccination strategies
In the foregut, a strong specific reactivity to IgM was observed in the apical surface of the enterocytes, most IgM+ cells were present in the loose connective tissue underlying the enterocytes, the lamina propria (LP)
Even in basal conditions most IgT+ cells in the pyloric caeca were found as intraepithelial lymphocytes (IELs), upon vaccination, we observed a significant increase in the number of IgT+ IELs, while still only some IgT+ cells were present in the LP (Fig. 7C, 7D and 7E)
Summary
Mucosal immunity in fish has recently become a broadly explored field of research, mainly busted by the need for oral vaccination strategies. As many of the features of the mucosal immune system present in mammals such as Peyer’s patches or IgA are not found in fish, very few assumptions can be established [1]. The first segment or foregut is where the food protein uptake appears to take place, with enterocytes acting as absorptive cells. This segment includes the esophagus and a defined stomach, present in salmonids and not clearly defined in some other fish species such as cyprinids. Present in species such as salmonids, are an adaptation to increase gut surface area, contributing to a higher macromolecule uptake than that of the rest of the digestive tract. The third segment is the hindgut in which enterocytes are thought to have an osmorregulatory function, and includes an anal region that in certain species can constitute a proper rectum separated by valves
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