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Fecal microbiota transplantation from young donor mice improves ovarian function in aged mice

Xu, Li, Zhang, Qiankun, Dou, Xiaowei, Wang, Yipeng, Wang, Jianwei, Zhou, Yong, Liu, Xingyin, Li, Jing·2022·Journal of Genetics and Genomics
DOI 10.1016/j.jgg.2022.05.006
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Fig. 1 FMT reshaped the gut microbiota of aged recipient mice. A : Experimental design and sample collection. The whole experiment was divided into three phases. After treatment with antibiotics for two weeks, the mice accepted fecal transplantation three times each week for eight weeks, then fecal collection, ovarian histology, and a fertility test were completed. B : The Shannon index and the observed-OTUs index analysis between the three groups at the genus level. C : Principal coordinate analysis of the microbiota based on the unweighted UniFrac distance metrics for the three groups. R ¼ 0.71348, P ¼ 0.001. D : Heatmap of community composition of the three groups at genus level by cluster analysis. E : Functional analysis of the different gut microbiota compositions between non-FMT and FMT groups. * , P < 0.05 versus the non-FMT group. n ¼ 8.
Fig. 1 FMT reshaped the gut microbiota of aged recipient mice. A : Experimental design and sample collection. The whole experiment was divided into three phases. After treatment with antibiotics for two weeks, the mice accepted fecal transplantation three times each week for eight weeks, then fecal collection, ovarian histology, and a fertility test were completed. B : The Shannon index and the observed-OTUs index analysis between the three groups at the genus level. C : Principal coordinate analysis of the microbiota based on the unweighted UniFrac distance metrics for the three groups. R ¼ 0.71348, P ¼ 0.001. D : Heatmap of community composition of the three groups at genus level by cluster analysis. E : Functional analysis of the different gut microbiota compositions between non-FMT and FMT groups. * , P < 0.05 versus the non-FMT group. n ¼ 8.CC-BY-NC-ND · From the PDF
Fig. 2 Discrepancies of the genera co-occurrence networks based on the 16S rRNA data. A e C : Genera co-occurrence network between non-FMT ( A ), young ( B ), and FMT groups ( C ) based on the Spearman correlation algorithms. Each node presents a bacterial genus. The node size indicates the relative abundance of each genus per group, and the density of the dashed line represents the Spearman coefficient. Red links stand for positive interactions between nodes, and green links stand for negative interactions. D : Discrepancies of nodes in non-FMT, young, and FMT groups co-occurrence network.
Fig. 2 Discrepancies of the genera co-occurrence networks based on the 16S rRNA data. A e C : Genera co-occurrence network between non-FMT ( A ), young ( B ), and FMT groups ( C ) based on the Spearman correlation algorithms. Each node presents a bacterial genus. The node size indicates the relative abundance of each genus per group, and the density of the dashed line represents the Spearman coefficient. Red links stand for positive interactions between nodes, and green links stand for negative interactions. D : Discrepancies of nodes in non-FMT, young, and FMT groups co-occurrence network.CC-BY-NC-ND · From the PDF
Fig. 3 The changes of serum inflammatory cytokines after FMT. A : Levels of serum IL-4. B : Levels of serum IL-6. C : Levels of serum IL-10. D : Levels of serum IL-17. E : Levels of serum IL-23. F : Levels of serum IFNg . H : Spearman correlation analysis between the gut microbiota and inflammatory cytokines. The heatmap color indicates the Spearman correlation coefficients (blue, negative; red, positive). The results are represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. n ¼ 8 e 10. SEM, standard error of the mean.
Fig. 3 The changes of serum inflammatory cytokines after FMT. A : Levels of serum IL-4. B : Levels of serum IL-6. C : Levels of serum IL-10. D : Levels of serum IL-17. E : Levels of serum IL-23. F : Levels of serum IFNg . H : Spearman correlation analysis between the gut microbiota and inflammatory cytokines. The heatmap color indicates the Spearman correlation coefficients (blue, negative; red, positive). The results are represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. n ¼ 8 e 10. SEM, standard error of the mean.CC-BY-NC-ND · From the PDF
Fig. 4 Effects of FMT on fertility. A : Percentage of female pregnancy (%) ( n ¼ 10 for the non-FMT group, n ¼ 7 for the FMT group). B : Number of pups of first litter per female ( n ¼ 4 for the non-FMT group, n ¼ 3 for the FMT group). C : Number of oocytes per female. D : Ovarian morphology by H & E staining. d, e, f are higher magnifications of insets in a, b, c (red asterisk, atretic follicle). E : Percentage of follicles at different stages per ovary ( n ¼ 5 for the young group, n ¼ 8 for the non-FMT group, n ¼ 9 for the FMT group). F : p-rpS6 immunohistochemistry of mouse ovarian sections in different groups. d, e, f are higher magnifications of insets in a, b, c. The results are represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. n ¼ 7 e 10. SEM, standard error of the mean. Scale bars, 200 m m ( D ), 50 m m ( F ).
Fig. 4 Effects of FMT on fertility. A : Percentage of female pregnancy (%) ( n ¼ 10 for the non-FMT group, n ¼ 7 for the FMT group). B : Number of pups of first litter per female ( n ¼ 4 for the non-FMT group, n ¼ 3 for the FMT group). C : Number of oocytes per female. D : Ovarian morphology by H & E staining. d, e, f are higher magnifications of insets in a, b, c (red asterisk, atretic follicle). E : Percentage of follicles at different stages per ovary ( n ¼ 5 for the young group, n ¼ 8 for the non-FMT group, n ¼ 9 for the FMT group). F : p-rpS6 immunohistochemistry of mouse ovarian sections in different groups. d, e, f are higher magnifications of insets in a, b, c. The results are represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. n ¼ 7 e 10. SEM, standard error of the mean. Scale bars, 200 m m ( D ), 50 m m ( F ).CC-BY-NC-ND · From the PDF
Fig. 5 FMT group showed decreased apoptosis and increased cellular proliferation in ovaries. A : Cleaved-caspase-3 immunohistochemistry of mouse ovarian sections in different groups. d, e, f are higher magnifications of insets in a, b, c, respectively (black arrow, the positive expression of Cleaved-caspase-3). B : Number of Cleaved-caspase-3 ( þ ) signals in the maximum section of mouse ovaries ( n ¼ 3 per group). C : TUNEL immunofluorescence of mouse ovarian sections in different groups. d, e, and f are higher magnifications of insets in a, b, and c, respectively (red arrow, the positive expression of TUNEL). D : Number of the apoptosis index of young, non-FMT, and FMT mouse ovarian sections ( n ¼ 3 per group). E : PCNA immunohistochemistry of ovarian sections in different groups. a, b, c are representative secondary follicles; d, e, f are representative antral follicles. F : Immunofluorescence staining of Ki-67 (green). Bule, nucleus. G : Number of Ki-67 ( þ ) signals in the maximum section of mouse ovaries ( n ¼ 3 per group). The results were represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. SEM, standard error of the mean. Scale bars, 25 m m ( E ), 50 m m ( A , C , F ).
Fig. 5 FMT group showed decreased apoptosis and increased cellular proliferation in ovaries. A : Cleaved-caspase-3 immunohistochemistry of mouse ovarian sections in different groups. d, e, f are higher magnifications of insets in a, b, c, respectively (black arrow, the positive expression of Cleaved-caspase-3). B : Number of Cleaved-caspase-3 ( þ ) signals in the maximum section of mouse ovaries ( n ¼ 3 per group). C : TUNEL immunofluorescence of mouse ovarian sections in different groups. d, e, and f are higher magnifications of insets in a, b, and c, respectively (red arrow, the positive expression of TUNEL). D : Number of the apoptosis index of young, non-FMT, and FMT mouse ovarian sections ( n ¼ 3 per group). E : PCNA immunohistochemistry of ovarian sections in different groups. a, b, c are representative secondary follicles; d, e, f are representative antral follicles. F : Immunofluorescence staining of Ki-67 (green). Bule, nucleus. G : Number of Ki-67 ( þ ) signals in the maximum section of mouse ovaries ( n ¼ 3 per group). The results were represented as means ± SEM. * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group and the young group. SEM, standard error of the mean. Scale bars, 25 m m ( E ), 50 m m ( A , C , F ).CC-BY-NC-ND · From the PDF
Fig. 6 Effects of FMT on the immune microenvironment in ovaries. Real-time PCR of inflammatory cytokines in the ovaries of non-FMT and FMT groups. A : Relative expression of IL-4 . B : Relative expression of IL-6 . C : Relative expression of IL-10 . D : Relative expression of IL-23 . E : Relative expression of IFNg . F: Immunofluorescence co-staining of iNOS (red) and F4/ 80 (green). Bule, nucleus. G : Immunofluorescence co-staining of CD206 (red) and F4/80 (green). Bule, nucleus. The results are represented as means ± SEM; * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group. n ¼ 3. H: a -SMA immunohistochemistry of ovaries was visible in a cluster (red box) in the ovarian sections of different groups. d, e, f are higher magnifications of insets in a, b, c, respectively. SEM, standard error of the mean. Scale bar, 50 m m ( F and G ).
Fig. 6 Effects of FMT on the immune microenvironment in ovaries. Real-time PCR of inflammatory cytokines in the ovaries of non-FMT and FMT groups. A : Relative expression of IL-4 . B : Relative expression of IL-6 . C : Relative expression of IL-10 . D : Relative expression of IL-23 . E : Relative expression of IFNg . F: Immunofluorescence co-staining of iNOS (red) and F4/ 80 (green). Bule, nucleus. G : Immunofluorescence co-staining of CD206 (red) and F4/80 (green). Bule, nucleus. The results are represented as means ± SEM; * , P < 0.05; ** , P < 0.01; *** , P < 0.001 versus the non-FMT group. n ¼ 3. H: a -SMA immunohistochemistry of ovaries was visible in a cluster (red box) in the ovarian sections of different groups. d, e, f are higher magnifications of insets in a, b, c, respectively. SEM, standard error of the mean. Scale bar, 50 m m ( F and G ).CC-BY-NC-ND · From the PDF

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Metadata

Authors
Xu, L., Zhang, Q., Dou, X., Wang, Y., Wang, J., Zhou, Y., Liu, X., & Li, J.
ORCID
Venue
Journal of Genetics and Genomics
Publisher
Elsevier BV
Published
2022-11
Volume
49
Issue
11
Pages
1042-1052
ISSN
1673-8527
DOI
10.1016/j.jgg.2022.05.006
Cited by
58
References
7
Language
en
Licence
Funders
  • Ministry of Science and Technology of the People&apos;s Republic of China Department of Science and Technology for Social Development (2018YFC1003703-1)
  • National Key Research and Development Program of China
  • National Natural Science Foundation of China (81871628, 81902027, 82172288)

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Xu, L., Zhang, Q., Dou, X., Wang, Y., Wang, J., Zhou, Y., Liu, X., & Li, J. (2022). Fecal microbiota transplantation from young donor mice improves ovarian function in aged mice. Journal of Genetics and Genomics. https://doi.org/10.1016/j.jgg.2022.05.006