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A More Robust Gut Microbiota in Calorie-Restricted Mice Is Associated with Attenuated Intestinal Injury Caused by the Chemotherapy Drug Cyclophosphamide

Liu, Tao, Wu, Yanqiu, Wang, Linghua, Pang, Xiaoyan, Zhao, Liping, Yuan, Huijuan, Zhang, Chenhong·2019·mBio
DOI 10.1128/mbio.02903-18PMC PMC6414708
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Abstract

Improving the gut microbiota via calorie restriction is beneficial for human health. Our findings showed differential responses between calorie-restricted mice and ad libitum -fed mice. Compared with the ad libitum -fed mice, the calorie-restricted mice were less susceptible to cyclophosphamide side effects otherwise observed on the gut integrity and its microbiota. These results show the potential benefits of manipulating the gut microbiota with CR prior to cancer chemotherapy.

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FIG 1 CR reduced the intestinal permeability and protected the epithelium from CTX. (A) Histological section by HE staining. (B) Histological scores of colon epithelium based on inflammation and mucosal damage. For each group, there were five mice (n = 5) every day. (C) BrdU staining of colon slices. Red arrows point to stem cells. (D) Number of ISC per 10 crypts. For each group, n = 5. (E) Concentration of FITC in serum at 2 days CTX injection. (F) Number of bacteria (CFU) in the MLN and spleen. (G) Concentration of lipopolysaccharide-binding protein (LBP) in serum after CTX injection. The data are shown as means ± SEM (error bars). Two-way ANOVA was used to analyze variation at the same time point. Values that are statistically significantly different are indicated by bars and asterisks as follows: *, P < 0.05; **, P < 0.01; ***, P < 0.001.
FIG 1 CR reduced the intestinal permeability and protected the epithelium from CTX. (A) Histological section by HE staining. (B) Histological scores of colon epithelium based on inflammation and mucosal damage. For each group, there were five mice (n = 5) every day. (C) BrdU staining of colon slices. Red arrows point to stem cells. (D) Number of ISC per 10 crypts. For each group, n = 5. (E) Concentration of FITC in serum at 2 days CTX injection. (F) Number of bacteria (CFU) in the MLN and spleen. (G) Concentration of lipopolysaccharide-binding protein (LBP) in serum after CTX injection. The data are shown as means ± SEM (error bars). Two-way ANOVA was used to analyze variation at the same time point. Values that are statistically significantly different are indicated by bars and asterisks as follows: *, P < 0.05; **, P < 0.01; ***, P < 0.001.CC BY · PubMed Central
FIG 2 The microbiota of the mice in the CR group were much more stable than the microbiota of the mice in the ad libitum-fed group treated with CTX. (A and B) Variation of gut microbiota structure of ad libitum group and CR group after CTX injection along PC1 and PC2 of PCoA based on the Bray-Curtis distance. (C) Clustering of gut microbiota based on distances between different groups calculated by multivariate analysis of variance test of the first 35 PCs of Bray-Curtis PCoA data. (D) Bray-Curtis distance between CTX treatment and the NS control and one-way ANOVA test were used. *, P < 0.05; **, P < 0.01; ***, P < 0.001.
FIG 2 The microbiota of the mice in the CR group were much more stable than the microbiota of the mice in the ad libitum-fed group treated with CTX. (A and B) Variation of gut microbiota structure of ad libitum group and CR group after CTX injection along PC1 and PC2 of PCoA based on the Bray-Curtis distance. (C) Clustering of gut microbiota based on distances between different groups calculated by multivariate analysis of variance test of the first 35 PCs of Bray-Curtis PCoA data. (D) Bray-Curtis distance between CTX treatment and the NS control and one-way ANOVA test were used. *, P < 0.05; **, P < 0.01; ***, P < 0.001.CC BY · PubMed Central
FIG 3 RDA-derived key phylotypes of the ad libitum-fed group responding to CR and CTX effects. The heat map colors of the spots in the panel represent the mean relative abundance (log-transformed) values of the OTUs in each group. The values on the color bar are the relative abundance indicated by the corresponding color. OTUs are arrayed by the Spearman correlation cluster. The key comparisons and direction of changes are summarized in three columns to the right of the heat map. A two-sided Mann-Whitney test was used for analysis. The FDR of <0.05 are shown with blue and pink box. The “ad libitum Vs. CR” column compares CR+NS mice to ad libitum+NS mice at 28d. A blue box indicates that the OTU was significantly lower in CR+NS mice, and a pink box indicates that it was significantly higher. The “NS Vs. CTX in ad libitum” column compares ad libitum+CTX mice to the ad libitum+NS mice. A blue box indicates that the OTU was significantly decreased by CTX, and a pink box indicates that the OTU was significantly increased by CTX. The “NS Vs. CTX in CR” column compares CR+CTX mice to the CR+NS mice.
FIG 3 RDA-derived key phylotypes of the ad libitum-fed group responding to CR and CTX effects. The heat map colors of the spots in the panel represent the mean relative abundance (log-transformed) values of the OTUs in each group. The values on the color bar are the relative abundance indicated by the corresponding color. OTUs are arrayed by the Spearman correlation cluster. The key comparisons and direction of changes are summarized in three columns to the right of the heat map. A two-sided Mann-Whitney test was used for analysis. The FDR of <0.05 are shown with blue and pink box. The “ad libitum Vs. CR” column compares CR+NS mice to ad libitum+NS mice at 28d. A blue box indicates that the OTU was significantly lower in CR+NS mice, and a pink box indicates that it was significantly higher. The “NS Vs. CTX in ad libitum” column compares ad libitum+CTX mice to the ad libitum+NS mice. A blue box indicates that the OTU was significantly decreased by CTX, and a pink box indicates that the OTU was significantly increased by CTX. The “NS Vs. CTX in CR” column compares CR+CTX mice to the CR+NS mice.CC BY · PubMed Central
FIG 4 Coabundance groups of all the key OTUs in mice. (A) OTU-level network diagram of 146 key OTUs responding to the effects of CTX and different diet. The size of the node indicates the mean abundance of each OTU. Lines between nodes represent correlations between the nodes they connect, with the line width indicating correlation magnitude and color for correlation (red for a negative correlation, gray for a positive correlation). Only lines corresponding to correlations with a magnitude greater than 0.5 are drawn. OTUs are grouped into 22 CAGs by permutation multivariate analysis of variance (PERMANOVA) when P < 0.05. (B) Heat map of the FDR value for CAGs, indicating the changes induced by diet or CTX stress. The tests of significance were performed using a two-sided Mann-Whitney test, and the calculation of FDR was performed using the procedure originally introduced by Benjamini and Hochberg.
FIG 4 Coabundance groups of all the key OTUs in mice. (A) OTU-level network diagram of 146 key OTUs responding to the effects of CTX and different diet. The size of the node indicates the mean abundance of each OTU. Lines between nodes represent correlations between the nodes they connect, with the line width indicating correlation magnitude and color for correlation (red for a negative correlation, gray for a positive correlation). Only lines corresponding to correlations with a magnitude greater than 0.5 are drawn. OTUs are grouped into 22 CAGs by permutation multivariate analysis of variance (PERMANOVA) when P < 0.05. (B) Heat map of the FDR value for CAGs, indicating the changes induced by diet or CTX stress. The tests of significance were performed using a two-sided Mann-Whitney test, and the calculation of FDR was performed using the procedure originally introduced by Benjamini and Hochberg.CC BY · PubMed Central

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Metadata

Authors
Liu, T., Wu, Y., Wang, L., Pang, X., Zhao, L., Yuan, H., & Zhang, C.
Affiliations
  • State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China
  • Henan Provincial People’s Hospital, Zhengzhou, Henan Province, China
Venue
mBio
Publisher
American Society for Microbiology
Published
2019-04-30
Volume
10
Issue
2
ISSN
  • 2161-2129
  • 2150-7511
DOI
10.1128/mbio.02903-18
PMC
PMC6414708
Cited by
56
References
7
Language
en
Licence
Funders
  • National Natural Science Foundation of China (81871091, 31330005, 81401141)
  • Science and Technology Commission of Shanghai Municipality (14YF1402200)

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