Alterations in the mucosal immune system by a chronic exhausting exercise in Wistar rats

Abstract

Exhausting exercise can disturb immune and gastrointestinal functions. Nevertheless, the impact of it on mucosal-associated lymphoid tissue has not been studied in depth. Here, we aim to establish the effects of an intensive training and exhausting exercise on the mucosal immunity of rats and to approach the mechanisms involved. Rats were submitted to a high-intensity training consisting of running in a treadmill 5 days per week for 5 weeks, involving 2 weekly exhaustion tests. At the end, samples were obtained before (T), immediately after (TE) and 24 h after (TE24) an additional final exhaustion test. The training programme reduced the salivary production of immunoglobulin A, impaired the tight junction proteins' gene expression and modified the mesenteric lymph node lymphocyte composition and function, increasing the ratio between Tαβ+ and B lymphocytes, reducing their proliferation capacity and enhancing their interferon-γ secretion. As a consequence of the final exhaustion test, the caecal IgA content increased, while it impaired the gut zonula occludens expression and enhanced the interleukin-2 and interferon-γ secretion. Our results indicate that intensive training for 5 weeks followed or not by an additional exhaustion disrupts the mucosal-associated lymphoid tissue and the intestinal epithelial barrier integrity in rats.

Figure 1

Body weight (a), chow intake (b), and food efficiency (c) throughout the intensive training period. The sedentary (SED) group is represented by white symbols (○) and the runner group by grey symbols ( ). Data are expressed as mean ± standard error (n = 8 animals for the SED group and n = 24 animals for the runner group in (a); n = 3 cages for the SED group and n = 8 cages for the runner group in b,c). Statistical differences (Student’s t test): *p < 0.05 vs SED group.

Figure 2

Changes in submaxillary salivary gland IgA and IgM concentration compared to the sedentary group. SED sedentary rats, T trained rats, TE T rats immediately after a final exhaustion test, TE24 TE rats 24 h after the final exhaustion test. Data are expressed as mean ± standard error (n = 8). Statistical differences (one-way ANOVA followed by post-hoc Tukey test): *p < 0.05 vs SED group.

Figure 3

Changes in gut wash IgA (a), and caecal content IgA (b) concentration compared to the sedentary group. SED sedentary rats, T trained rats, TE T rats immediately after a final exhaustion test, TE24 TE rats 24 h after the final exhaustion test. Data are expressed as mean ± standard error (n = 8). Statistical differences (Kruskal–Wallis followed by Mann–Whitney U test): ^фp < 0.05 vs. T group.

Figure 4

Changes in gut wash alpha-1-antytripsin (a1AT) concentration compared to the sedentary group. SED sedentary rats, T trained rats, TE T rats immediately after a final exhaustion test, TE24 TE rats 24 h after the final exhaustion test. Data are expressed as mean ± standard error (n = 8).

Figure 5

Changes in the proportion of mesenteric lymph node lymphocytes compared to the sedentary group. Main lymphocyte subsets (a); Tαβ/B lymphocytes ratio (b); main Tαβ subsets (c); Th/Tc ratio (d) and Treg proportion (e). SED sedentary rats, T trained rats, TE T rats with an additional final exhaustion test, TE24 TE rats 24 h after the additional final exhaustion test. Data are expressed as mean ± SEM (n = 8). Statistical differences (one-way ANOVA followed by post-hoc Tukey test for (a,b) and Kruskal–Wallis followed by Mann–Whitney U test for c–e): *p < 0.05 vs SED group; ^фp < 0.05 vs T group; ^λp < 0.05 vs TE group.

Figure 6

Changes in the proliferative response (a) and cytokine concentration released (b–f) by mesenteric lymph node lymphocyte stimulated by concanavalin A (ConA) compared to the sedentary group. SED sedentary rats, T trained rats, TE T rats with a final exhaustion test, TE24 TE rats 24 h after the final exhaustion test. Data are expressed as mean ± standard error (n = 8). Statistical differences (one-way ANOVA followed by post-hoc Tukey test for b,d, and Kruskal–Wallis followed by Mann–Whitney U test for a,c,e): *p < 0.05 vs SED group; ^фp < 0.05 vs T group.

Figure 7

Changes in the IgA (a), IgM (b) and IgG (c) concentration in mesenteric lymph node lymphocyte supernatants compared to the sedentary group. SED sedentary rats, T trained rats, TE T rats with a final exhaustion test, TE24 TE rats 24 h after the final exhaustion test. Data are expressed as mean ± standard error (n = 8). Statistical differences (Kruskal–Wallis followed by Mann–Whitney U test): *p < 0.05 vs SED group.