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. 2015 Jul 1;7(7):5327-46.
doi: 10.3390/nu7075223.

Dietary Fiber Intake is Associated with Increased Colonic Mucosal GPR43+ Polymorphonuclear Infiltration in Active Crohn's Disease

Mingli Zhao  1   2 , Weiming Zhu  3 , Jianfeng Gong  4 , Lugen Zuo  5 , Jie Zhao  6 , Jing Sun  7 , Ning Li  8 , Jieshou Li  9
Affiliations

Dietary Fiber Intake is Associated with Increased Colonic Mucosal GPR43+ Polymorphonuclear Infiltration in Active Crohn's Disease

Mingli Zhao et al. Nutrients. .

Abstract

G protein-coupled receptor 43/free fatty acid receptor 2 (GPR43/FFAR2) is essential for polymorphonuclear (PMN) recruitment. We investigated the expression of GPR43/FFAR2 in the colon from Crohn's disease patients and whether dietary fiber in enteral nutrition increases GPR43+ polymorphonuclear infiltration in mucosa. Segments of ascending colon and white blood cells from peripheral blood were obtained from 46 Crohn's disease patients and 10 colon cancer patients. The Crohn's disease patients were grouped by the activity of disease (active or remission) and enteral nutrition with or without dietary fiber. Histological feature, expression and location of GPR43/FFAR2 and level of tumor necrosis factor-α (TNF-α), interleukine-6 (IL-6) and myeloperoxidase were assessed. The results of hematoxylin-eosin and immunohistochemistry staining revealed that the infiltration of immune cells, including GPR43+ PMN, was more severe in active Crohn's disease patients who consumed normal food or enteral nutrition with dietary fiber than in remission patients and colon cancer patients. This finding was supported by the results of GPR43 and myeloperoxidase expression. Active Crohn's disease (CD) patients who consumed enteral nutrition without dietary fiber exhibited severe immune cell infiltration similar to the other active CD patients, but GPR43+ PMNs were rarely observed. The level of TNF-α mRNA in active Crohn's disease patients was higher than those of the other patients. In conclusion, the use of dietary fiber in enteral nutrition by active Crohn's disease patients might increase GPR43+ PMNs infiltration in colon mucosa. This effect was not observed in Crohn's disease patients in remission.

Keywords: Crohn’s disease; GPR43/FFAR2; dietary fibre; polymorphonuclear.

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Figures

Figure 1
Figure 1
Colon mucosae from different patients. These pictures showed the morphological changes (feature of epithelial and crypt, infiltration of immune cells, and thickness of mucosa) of each group. The most severe morphological damage existed in ac-food group. This damage in re-DF was less severe than that in ac-EN, ac-DF, and re-EN (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 2
Figure 2
Eosinophils (green arrows) and neutrophils (red arrows) in the mucosae. Mucosae from active Crohn’s disease patients (ac-food, ac-EN and ac-DF) had more immune cells than the others did. Neutrophils could be found in mucosae from active Crohn’s disease patients who had dietary fiber in their food or enteral nutrition (ac-food and ac-DF) (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 3
Figure 3
The mRNA of tumor necrosis factor-α (TNF-α) (A) (can. 2.40 ± 1.15, ac-food 15.56 ± 5.60, ac-EN 9.83 ± 3.34, ac-DF 9.87 ± 3.87, re-EN 4.25 ± 1.86, and re-DF 4.84 ± 2.12) and IL-6 (B) (can. 0.94 ± 0.42, ac-food 6.22 ± 1.59, ac-EN 3.19 ± 0.91, ac-DF 3.83 ± 0.89, re-EN 1.76 ± 0.82, and re-DF 1.71 ± 0.61) in mucosae from different groups. Columns with different letters are significantly different (p < 0.05). TNF-α in active Crohn’s patients (ac-food, ac-EN and ac-DF) was higher than that of the Crohn’s disease patients in remission (re-EN and re-DF) and colon cancer patients (can.). The IL-6 of the severe Crohn’s disease patients (ac-food) was higher than in the other patients(can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 4
Figure 4
the amount of zonula occludens-1 (ZO-1), G protein-coupled receptor 43 (GPR43) and Peptide-YY in the mucosa and the amount of GPR43 in the White blood cells (WBC). The expression of ZO-1 (can. 1.25 ± 0.27, ac-food 0.50 ± 0.29, ac-EN 0.83 ± 0.30, ac-DF 1.12 ± 0.22, re-EN 0.99 ± 0.21, and re-DF 1.22 ± 0.22), GPR43 (can. 0.77 ± 0.31, ac-food 1.60 ± 0.42, ac-EN 1.00 ± 0.24, ac-DF 1.53 ± 0.38, re-EN 0.93 ± 0.16, and re-DF 1.11 ± 0.18) and peptide-YY (can. 0.29 ± 0.09, ac-food 0.19 ± 0.07, ac-EN 0.23 ± 0.06, ac-DF 0.24 ± 0.05, re-EN 0.33 ± 0.10, and re-DF 0.33 ± 0.09) in colonic mucosae from different groups. Columns with different letters are significantly different (B, D) (p < 0.05). ZO-1 in ac-food was significantly lower than in the others. GPR-43 in ac-food and ac-DF was significantly higher than that in the others. No significant difference of peptide-YY was found among these groups (C). (ZO-1: zonula occludens-1; GPR-43: G-protein coupled receptor 43. See notes of Table 1 for the definition of each group; can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 5
Figure 5
The expression of G-protein coupled receptor 43 (GPR43) in white blood cells from peripheral blood (can. 0.69 ± 0.08, ac-food 1.81 ± 0.40, ac-EN 1.24 ± 0.18, ac-DF 1.16 ± 0.20, re-EN 1.06 ± 0.28, and re-DF 1.09 ± 0.27). Columns with different letters are significantly different (a vs. c p < 0.05, b vs. a and c p < 0.01). GPR43 from white blood cell (WBC) of ac-food is much higher than that in the other groups, (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 6
Figure 6
Immunohistochemistry showed the expression of G-protein coupled receptor 43 (GPR43) in crypt and lamina propria. For all these groups, GPR43 high expressing epithelial cells could be found in the crypt. GPR43 high expressing cells could be found in lamina propria in ac-food and ac-DF. These GPR43 high expressing cells in lamina propria had small granules in the cytoplasm and segmented nucleus, which illustrated that they might be PMNs (polymorphonuclears). (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 7
Figure 7
Expression of peptide-YY in crypt and lamina propria. For all these groups, peptide-YY high expressing cells could be found in the crypt. Peptide-YY+ cells could not be found in lamina proprial cells in any groups, (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
Figure 8
Figure 8
The expression of myeloperoxidase (MPO) in colon mucosae from different groups (pg/mg tissue) (can. 0.94 ± 0.38, ac-food 5.34 ± 2.00, ac-EN 2.16 ± 0.64, ac-DF 4.43 ± 0.95, re-EN 1.44 ± 0.35, and re-DF 1.76 ± 0.51). Columns with different letters are significantly different (p < 0.01). MPO in colon mucosa from ac-food and ac-DF was significantly higher than that in the other groups, (can.: colon cancer patients; ac-food: active Crohn’s disease patients comsuming normal food before operation; ac-EN: active Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; ac-DF: active Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation; re-EN: remission Crohn’s disease patients comsuming enteral nutrition without dietary fiber before operation; re-DF: remission Crohn’s disease patients comsuming enteral nutrition with dietary fiber before operation.).
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