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. 2022 Sep 20:9:992102.
doi: 10.3389/fnut.2022.992102. eCollection 2022.

Benefits of neutral polysaccharide from rhizomes of Polygonatum sibiricum to intestinal function of aged mice

Li-Xia Li  1 , Xin Feng  1 , Meng-Ting Tao  1 , Berit Smestad Paulsen  2 , Chao Huang  3 , Bin Feng  4 , Wei Liu  5 , Zhong-Qiong Yin  1 , Xu Song  1 , Xinghong Zhao  1 , Xiao-Xia Liang  1 , Li-Zi Yin  1 , Hua-Qiao Tang  6 , Yuan-Feng Zou  1
Affiliations

Benefits of neutral polysaccharide from rhizomes of Polygonatum sibiricum to intestinal function of aged mice

Li-Xia Li et al. Front Nutr. .

Abstract

One purified neutral polysaccharide fraction was obtained from the rhizome of Polygonatum sibiricum by DEAE ion exchange and gel chromatography. Structure elucidation was performed by methanolysis, methylation, FT-IR, and NMR. The results indicated that PSP-NP was composed of 1,4-β-D-Gal,1, 4, 6-β-D-Gal, T-α-D-Man,1, 4-α-D-Glc, and T-α-D-Glc with a molecular weight of 43.0 kDa. We supplied this polysaccharide to aged mice and found it is of benefits to intestinal functions, as indicated by better tissue integrity and motility, improved oxidative stress and inflammation, reduced intestinal permeability and serum LPS level, as well as balanced gut microbial composition and short-chain fatty acids production. These results display a novel Polygonatum sibiricum polysaccharide to improve the intestinal function of aged mice, which provides pieces of evidence for its further development and utilization.

Keywords: Polygonatum sibiricum; anti-aging; colon; heteropolysaccharide; jejunum.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Technical roadmap for extraction and purification of Polygonatum Polysaccharide from different varieties and elution profiles of polysaccharides in gel column. (A) PSP-NP, (B) PCP-NP, (C) PKP-NP, (D) PSP- AP, (E) PCP-AP, (F) PKP-AP.
FIGURE 2
FIGURE 2
Comparison of polysaccharide fractions from different species of Polygonati Rhizoma. Influence of purified polysaccharides on cell gene expression of SOD1 in vitro. (A) PSP-NP; (B) PSP-AP; (C) PCP-AP; (D) PCP-NP. *Indicated significant difference compared with a control group, P < 0.05; ** indicated significantly.
FIGURE 3
FIGURE 3
Structure elucidation of PSP-NP. (A) FT-IR spectrum. (B) 1H NMR spectrum. (C) 13C NMR spectrum.
FIGURE 4
FIGURE 4
PSP-NP improves intestinal integrity of aged mice. (A–D) HE stain of jejunum in the control, high, medium and low dose groups, respectively. Arrows indicated the gaps between villi and epithelial cells. It showed that severe shedding of intestinal villi epithelium and gaps at the top of the villi were improved after drug administration. Bar: 200 μm; (E–H) HE stain of colon in the control, high, medium and low dose groups, respectively. Arrows indicated the epithelium and intestinal glands. It showed that epithelium dysplastic and intestinal glands were improved after drug administration. Bar: 200 μm; (I) The degree of microscopic injury was evaluated by mucosal and inflammatory conditions from a previously published and wildly used scoring system. The jejunum and colon scores decreased as the concentrations of PSP-NP increased and showed remarkable changes in the high group. (J) The length of villi and the depth of crypt in HE stain slice were analyzed by Image-Pro Plus, and the ratios were compared. PSP-NP increased the villi length and suppressed the crypt depth, thus heightening the ratio of villus length/crypt depth in jejunum. (K) The number and the length of Colonic glands in HE stain slice were analyzed by Image-ProPlus. PSP-NP increased the length of intestinal glands in colon. There was no significant effect on the number of intestinal glands. (L) Gene expression of VIP measured by qRT-PCR in jejunum and colon was significantly reduced in all three doses of PSP-NP. Control indicated control group administrated with saline; and High, Medium and Low indicated high, medium and low dose groups administrated with 200/100/50 mg/kg PSP-NP, respectively. Error bars indicated SEM. N = 8. All data were analyzed by SPSS with the one-way analysis of variance (ANOVA) by LSD test, *P < 0.05, **P < 0.01, ***P < 0.001, compared with the control group.
FIGURE 5
FIGURE 5
PSP-NP improves intestinal integrity of aged mice. (A) Gene expressions of tight junction protein Occludin in jejunum were up-regulated in jejunum but down-regulated in colon. N = 8. (B) Gene expressions of ZO-1 in jejunum and colon, which were both up-regulated. N = 8. (C) The LPS contents in serum (ng/mL) were analyzed by ELISA, and it was remarkably decreased after administration of PSP-NP, N = 16. (D) The content of carbonylated proteins (ng/mg) in jejunum and colon was determined by ELISA, and it was statistically reduced by PSP-NP in all the three groups of PSP-NP. Control indicated the control group administrated with saline, and High, Medium and Low indicated the high, medium and low dose groups administrated with 200/100/50 mg/kg PSP-NP, respectively. Error bars indicated SEM. N = 16. All data were analyzed by SPSS with the one-way analysis of variance (ANOVA) by LSD test, *P < 0.05, **P < 0.01, ***P < 0.001, compared with the control group.
FIGURE 6
FIGURE 6
PSP-NP enhances the intestinal immunity of aged mice. (A–D) AB-PAS stain of jejunum in the control, high, medium and low dose groups, respectively. Arrows indicated the goblet cells. It showed the goblet cells in jejunum treated with different doses of PSP-NP. Bar: 200 μm. (E–H) AB-PAS stain of colon in the control, high, medium and low dose groups, respectively. Arrows indicated the goblet cells. It showed the goblet cells in colon treated with different doses of PSP-NP. Bar: 200 μm. (I) The goblet cell count of jejunum and colon in the control, high, medium and low dose groups, respectively, it showed the goblet cells increased as the concentrations of PSP-NP increased and showed remarkable changes in the high group. N = 4. (J) The Gene expression of Mucin 2 in jejunum and colon was measured by qRT-PCR. The quantification showed that PSP-NP up-regulated gene expression of Mucin 2 in jejunum, there is no significant effect in the colon. N = 4. (K) The content of sIgA in jejunum and colon was analyzed by ELISA. PSP-NP improved the content of sIgA (μg/mg) in the jejunum and colon in the medium and high dose groups. N = 8. Error bars indicated SEM. All data were analyzed by SPSS with the one-way analysis of variance (ANOVA) by LSD test, *P < 0.05, **P < 0.01, ***P < 0.001, compared with a control group.
FIGURE 7
FIGURE 7
PSP-NP enhances the intestinal immunity of aged mice. (A–I) Gene expressions of IL-12A, IL-23, IL-6, IL-1β, TNF-α, IL-17, IL-4, IL-10, and TGF-β measured by qRT-PCR in jejunum and colon, respectively. PSP-NP significantly down-regulated the gene expressions of pro-inflammatory factors including IL-12A, IL-23, IL-6, IL-1β (No significant effect in colon), TNF-α and IL-17, and up-regulated anti-inflammatory factors involving IL-4, IL-10, and TGF-β. Control indicated the control group administrated with saline, and High, Medium and Low indicated high, medium and low dose groups administrated with 200/100/50 mg/kg PSP-NP, respectively. Error bars indicated SEM. N = 8. All data were analyzed by SPSS with the one-way analysis of variance (ANOVA) by LSD test, *P < 0.05, **P < 0.01, ***P < 0.001, compared with a control group.
FIGURE 8
FIGURE 8
(A) The amount of Escherichia coli in the content of the intestine was calculated after diluted with 10-fold dilutions of saline from 102 to 107 and cultured in EMB agar medium. It was expressed as. It was reduced by PSP-NP, but showed no significance. (B) Bifidobacteria in the content of intestine was cultured in MRS and the amount of Bifidobacteria was calculated and expressed the same as panel (A). It was significantly increased in the high dose group of PSP-NP. (C) Lactobacillus in the content of intestine was cultured in BS and the amount of Lactobacillus was calculated and expressed the same as panel (A). The results showed that PSP-NP improved the amount of Lactobacillus. (D−F) The contents of acetic acid, propionic acid and butyric acid, respectively, were analyzed by GC. They were all remarkably increased, and the middle dose group showed the best activities. Control indicated the control group administrated with saline, and High, Medium, and Low indicated the high, medium and low dose groups administrated with 200/100/50 mg/kg PSP-NP, respectively. Error bars indicated SEM. N = 16. All data were analyzed by SPSS with the one-way analysis of variance (ANOVA) by LSD test, *P < 0.05, **P < 0.01, ***P < 0.001, compared with the control group.
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