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Role of Dietary Defatted Rice Bran in the Modulation of Gut Microbiota in AOM/DSS-Induced Colitis-Associated Colorectal Cancer Rat Model

Tajasuwan, Laleewan, Kettawan, Aikkarach, Rungruang, Thanaporn, Wunjuntuk, Kansuda, Prombutara, Pinidphon·2023·Nutrients
DOI 10.3390/nu15061528PMC PMC10052090
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Abstract

Defatted rice bran (DRB) is a by-product of rice bran derived after the oil extraction. DRB contains several bioactive compounds, including dietary fiber and phytochemicals. The supplementation with DRB manifests chemopreventive effects in terms of anti-chronic inflammation, anti-cell proliferation, and anti-tumorigenesis in the azoxymethane (AOM) and dextran sodium sulfate (DSS)-induced colitis-associated colorectal cancer (CRC) model in rats. However, little is known about its effect on gut microbiota. Herein, we investigated the effect of DRB on gut microbiota and short chain fatty acid (SCFA) production, colonic goblet cell loss, and mucus layer thickness in the AOM/DSS-induced colitis-associated CRC rat model. The results suggested that DRB enhanced the production of beneficial bacteria (Alloprevotella, Prevotellaceae UCG-001, Ruminococcus, Roseburia, Butyricicoccus) and lessened the production of harmful bacteria (Turicibacter, Clostridium sensu stricto 1, Escherichia–Shigella, Citrobacter) present in colonic feces, mucosa, and tumors. In addition, DRB also assisted the cecal SCFAs (acetate, propionate, butyrate) production. Furthermore, DRB restored goblet cell loss and improved the thickness of the mucus layer in colonic tissue. These findings suggested that DRB could be used as a prebiotic supplement to modulate gut microbiota dysbiosis, which decreases the risks of CRC, therefore encouraging further research on the utilization of DRB in various nutritional health products to promote the health-beneficial bacteria in the colon.

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Figure 1 (A) Experimental animal design of AOM/DSS-induced colitis-associated CRC model. (B) Representative images of the colonic tissue in each experimental group. Rats induced with AOM/DSS appeared tumors in the colon. Bar represents 2 cm. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 1 (A) Experimental animal design of AOM/DSS-induced colitis-associated CRC model. (B) Representative images of the colonic tissue in each experimental group. Rats induced with AOM/DSS appeared tumors in the colon. Bar represents 2 cm. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 2 (A) Representative images of the goblet cells of colonic tissue sections stained with alcian blue and Periodic acid–Schiff under a light microscope at 100× magnification. The black arrow represents goblet cells which are stained with alcian blue. The red arrow is a colon crypt with goblet cell loss. Scale bars represent 100 µm. (B) The number of goblet cells per crypt in each group; control, DRBL, DRBH, induction, induction + DRBL, and induction + DRBH (n = 5–6/group). Data are expressed as mean ± S.E.M. Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 2 (A) Representative images of the goblet cells of colonic tissue sections stained with alcian blue and Periodic acid–Schiff under a light microscope at 100× magnification. The black arrow represents goblet cells which are stained with alcian blue. The red arrow is a colon crypt with goblet cell loss. Scale bars represent 100 µm. (B) The number of goblet cells per crypt in each group; control, DRBL, DRBH, induction, induction + DRBL, and induction + DRBH (n = 5–6/group). Data are expressed as mean ± S.E.M. Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 3 (A) Representative images of the mucus layer thickness of colonic tissue sections stained with alcian blue and Periodic acid–Schiff under a light microscope at 100× magnification. The black arrow represents the mucus layer. Scale bars represent 100 µm. (B) The muscular layer thickness (µm) in each experimental group: control, DRBL, DRBH, induction, induction + DRBL, and induction + DRBH (n = 5–6/group). Data are expressed as mean ± S.E.M. Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 3 (A) Representative images of the mucus layer thickness of colonic tissue sections stained with alcian blue and Periodic acid–Schiff under a light microscope at 100× magnification. The black arrow represents the mucus layer. Scale bars represent 100 µm. (B) The muscular layer thickness (µm) in each experimental group: control, DRBL, DRBH, induction, induction + DRBL, and induction + DRBH (n = 5–6/group). Data are expressed as mean ± S.E.M. Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 4 Alpha diversity analysis of gut microbiota in feces in each experimental group: control (n = 10), DRBL (n = 10), DRBH (n = 10), induction (n = 12), induction + DRBL (n = 12), and induction + DRBH (n = 12). Diversity within bacterial communities was measured by Pielou’s evenness (A), Faith’s phylogenetic diversity (B), Observed OTUs (C), and Shannon diversity index (D). Bars with asterisks (*) indicate statistically significant results for the control group (p < 0.05). The statistical analysis used the Kruskal–Wallis test. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g; OTUs, operational taxonomic units.
Figure 4 Alpha diversity analysis of gut microbiota in feces in each experimental group: control (n = 10), DRBL (n = 10), DRBH (n = 10), induction (n = 12), induction + DRBL (n = 12), and induction + DRBH (n = 12). Diversity within bacterial communities was measured by Pielou’s evenness (A), Faith’s phylogenetic diversity (B), Observed OTUs (C), and Shannon diversity index (D). Bars with asterisks (*) indicate statistically significant results for the control group (p < 0.05). The statistical analysis used the Kruskal–Wallis test. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g; OTUs, operational taxonomic units.CC BY · PubMed Central
Figure 5 Alpha diversity analysis of gut microbiota in colonic mucosa: control (n = 5), DRBL (n = 5), DRBH (n = 5), induction (n = 6), induction + DRBL (n = 6), and induction + DRBH (n = 6) and in colonic tumor; induction (n = 5), induction + DRBL (n = 6), and induction + DRBH (n = 6). Diversity within bacterial communities was measured by Pielou’s evenness (A), Faith’s phylogenetic diversity (B), Observed OTUs (C), and Shannon diversity index (D). Bars with asterisks (*) and double asterisks (**) indicate statistically significant results for the control and induction groups in mucosa, respectively (p < 0.05). The statistical analysis used the Kruskal–Wallis test. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g; OTUs, operational taxonomic units.
Figure 5 Alpha diversity analysis of gut microbiota in colonic mucosa: control (n = 5), DRBL (n = 5), DRBH (n = 5), induction (n = 6), induction + DRBL (n = 6), and induction + DRBH (n = 6) and in colonic tumor; induction (n = 5), induction + DRBL (n = 6), and induction + DRBH (n = 6). Diversity within bacterial communities was measured by Pielou’s evenness (A), Faith’s phylogenetic diversity (B), Observed OTUs (C), and Shannon diversity index (D). Bars with asterisks (*) and double asterisks (**) indicate statistically significant results for the control and induction groups in mucosa, respectively (p < 0.05). The statistical analysis used the Kruskal–Wallis test. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g; OTUs, operational taxonomic units.CC BY · PubMed Central
Figure 6 The principal coordinate analysis of beta diversity in feces based on Bray–Curtis dissimilarity (A), Jaccard index (B), and weighted (C) and un-weighted UniFac distance (D) in each experiment group: control (n = 10), DRBL (n = 10), DRBH (n = 10), induction (n = 12), induction + DRBL (n = 12), and induction + DRBH (n = 12). The differences in beta diversity were tested by Permutational multivariate analysis of variance. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 6 The principal coordinate analysis of beta diversity in feces based on Bray–Curtis dissimilarity (A), Jaccard index (B), and weighted (C) and un-weighted UniFac distance (D) in each experiment group: control (n = 10), DRBL (n = 10), DRBH (n = 10), induction (n = 12), induction + DRBL (n = 12), and induction + DRBH (n = 12). The differences in beta diversity were tested by Permutational multivariate analysis of variance. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 7 The principal coordinate analysis of beta diversity in colonic mucosa: control (n = 5), DRBL (n = 5), DRBH (n = 5), induction (n = 6), induction + DRBL (n = 6), and induction + DRBH (n = 6) and in colonic tumor; induction (n = 5), induction + DRBL (n = 6), and induction + DRBH (n = 6) based on Bray–Curtis dissimilarity (A), Jaccard index (B), and weighted (C) and unweighted UniFac distance (D) in each experiment group. The differences in beta diversity were tested by Permutational multivariate analysis of variance. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 7 The principal coordinate analysis of beta diversity in colonic mucosa: control (n = 5), DRBL (n = 5), DRBH (n = 5), induction (n = 6), induction + DRBL (n = 6), and induction + DRBH (n = 6) and in colonic tumor; induction (n = 5), induction + DRBL (n = 6), and induction + DRBH (n = 6) based on Bray–Curtis dissimilarity (A), Jaccard index (B), and weighted (C) and unweighted UniFac distance (D) in each experiment group. The differences in beta diversity were tested by Permutational multivariate analysis of variance. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 8 The relative abundance of bacterial taxonomic profile in feces at the phylum (A), family (B), and genus levels (C) in each experimental group (n = 10–12/group) and in colonic mucosa and tumor at the phylum (D), family (E), and genus levels (F) in each experimental group (n = 5–6/group). DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 8 The relative abundance of bacterial taxonomic profile in feces at the phylum (A), family (B), and genus levels (C) in each experimental group (n = 10–12/group) and in colonic mucosa and tumor at the phylum (D), family (E), and genus levels (F) in each experimental group (n = 5–6/group). DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 9 Histogram of biomarker bacterial genus in feces (n = 10–12/group) (A) and colonic mucosa and tumor (n = 5–6/group) (B) with significant difference among groups were detected by Linear discriminant analysis (LDA) effect size (LEfSe) analysis with LDA score ≥3. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 9 Histogram of biomarker bacterial genus in feces (n = 10–12/group) (A) and colonic mucosa and tumor (n = 5–6/group) (B) with significant difference among groups were detected by Linear discriminant analysis (LDA) effect size (LEfSe) analysis with LDA score ≥3. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central
Figure 10 Cecal short-chain fatty acid contents (mmol/kg wet sample) in rats: (A) acetic acid, (B) propionic acid, and (C) butyric acid contents. Data are expressed as means ± S.E.M (n = 5–6/group). Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.
Figure 10 Cecal short-chain fatty acid contents (mmol/kg wet sample) in rats: (A) acetic acid, (B) propionic acid, and (C) butyric acid contents. Data are expressed as means ± S.E.M (n = 5–6/group). Data from all experimental groups are compared using one-way ANOVA followed by Tukey’s HSD post hoc test. Mean with an asterisk (*) and number signs (#) superscript in each bar is significantly different (p < 0.05) when compared to the control and induction groups, respectively. DRBL, defatted rice bran 3 g; DRBH, defatted rice bran 6 g.CC BY · PubMed Central

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Metadata

Authors
Tajasuwan, L., Kettawan, A., Rungruang, T., Wunjuntuk, K., & Prombutara, P.
Venue
Nutrients
Publisher
MDPI AG
Published
2023-03-22
Volume
15
Issue
6
Pages
1528
ISSN
2072-6643
DOI
10.3390/nu15061528
PMC
PMC10052090
Cited by
49
References
6
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Thailand Research Fund (TRF) and the Researchers for Industries (RRI) Scheme (PHD62I0006, PRP6405030310)
  • Thai Ruam Jai Vegetable Oil Co., Ltd. (Phra Nakhon Si Ayutthaya, Thailand) (PHD62I0006, PRP6405030310)
  • Agricultural Research Development Agency (Public Organization) or “ARDA” (PHD62I0006, PRP6405030310)

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Tajasuwan, L., Kettawan, A., Rungruang, T., Wunjuntuk, K., & Prombutara, P. (2023). Role of Dietary Defatted Rice Bran in the Modulation of Gut Microbiota in AOM/DSS-Induced Colitis-Associated Colorectal Cancer Rat Model. Nutrients. https://doi.org/10.3390/nu15061528