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. 2022 Sep 14:13:952892.
doi: 10.3389/fmicb.2022.952892. eCollection 2022.

Excessive fructose intake inhibits skeletal development in adolescent rats via gut microbiota and energy metabolism

Tianlin Gao  1   2 , Chunyan Tian  1 , Ge Tian  1 , Li Ma  3 , Lili Xu  4 , Wendong Liu  5 , Jing Cai  1   2 , Feng Zhong  1   2 , Huaqi Zhang  1 , Aiguo Ma  1   2
Affiliations

Excessive fructose intake inhibits skeletal development in adolescent rats via gut microbiota and energy metabolism

Tianlin Gao et al. Front Microbiol. .

Abstract

Excessive fructose intake from desserts and beverages may influence bone development among adolescents. The gut microbiota (GM) and energy metabolism play important roles in bone development. In this study, 40 female adolescent rats were randomly assigned to the control group, the fructose group with two concentrations, and the glucose group as the positive control group. After 10 weeks, serum glucose and lipids were detected by means of an automatic analyzer, and the bone microstructure was analyzed by Micro-CT. Then, the GM was determined via 16S rRNA sequencing analysis, and energy metabolism was detected by measuring serum carbohydrate metabolites. At last, bone metabolism markers were measured via ELISA kits. The results showed that excessive fructose intake could increase body weight and influence the glucolipid metabolism of female adolescent rats. Meanwhile, the bone microstructures were impaired with excessive fructose intake. Mechanistically, excessive fructose intake shifted the GM of rats with the decrease of Lachnospiraceae, Ruminococcaceae, and increase of Allobaculum, Lachnospiraceae. Energy metabolism analysis suggested that most metabolites of fructose did not enter the tricarboxylic acid cycle to provide energy for the body's development. Furthermore, serum bone metabolism markers showed that excessive fructose intake could decrease both bone formation and resorption. Our results suggested that excessive fructose intake could inhibit skeletal development in adolescents. One potential mechanism might be that it affected the intestinal microbiota homeostasis in the juvenile body, thus changing the energy metabolism level, and ultimately affecting the bone metabolic balance.

Keywords: adolescent; bone development; energy metabolism; fructose; gut microbiota.

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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

Scheme 1
Scheme 1
Graphical abstract of excessive fructose intake inhibiting the skeletal development of adolescent rats via gut microbiota and energy metabolism.
FIGURE 1
FIGURE 1
Effects of excessive fructose intake on the physical and physiological parameters of rats: (A) body weight, (B) blood glucose, and (C) blood fructose after 10 weeks. The values were presented as mean ± SD (n = 10); a means p < 0.05 compared with the CON group; b means p < 0.05 compared with the 10% GLU group; and c means p < 0.05 compared with the 10% FRU group.
FIGURE 2
FIGURE 2
3D reconstruction images and bone microstructure parameters of the metaphysis of distal femur in different groups: (A) 3D reconstruction of the metaphyseal of the distal femur and (B–I) microstructure parameters of distal femur metaphyseal bone. The values were presented as mean ± SD (n = 4); a means p < 0.05 compared with the CON group; b means p < 0.05 compared with the 10% GLU group; and c means p < 0.05 compared with the 10% FRU group.
FIGURE 3
FIGURE 3
Responses of the diversity, richness, and structure of the gut microbiota to fructose treatment in rats: (A) goods-coverage diversity index, (B) observed species diversity index, (C) Chao1 index, (D) Shannon index, (E) principal component analysis (PCA) score plot based on weights, and (F) unweighted UniFrac distance. Values were presented as mean ± SEM (n = 5). Ma or red color represented the CON group, Mb or green color represented the 10% FRU group, Mc or blue color represented the 20% FRU group, and Md or purple color represented the 10% GLU group.
FIGURE 4
FIGURE 4
Relative abundances of the gut microbiota at the phylum level (A), genus level (B) and some different bacterial taxa (Allobaculum, Bacteroides, Clostridium, Lachnospiraceae, Lactobacillales, and Ruminococcaceae) obtained in fecal microbiota from the LefSe results (C). Values were presented as mean ± SEM (n = 5). Red color represented the CON group, green color represented the 10% FRU group, blue color represented the 20% FRU group, and purple color represented the 10% GLU group.
FIGURE 5
FIGURE 5
Effects of excessive fructose intake on the metabolites of central carbon metabolism in rats: (A) glyceraldehyde-3-phosphate, (B) fructose-1,6-diphosphate, (C) dihydroxyacetone phosphate, (D) citric acid, (E) isocitrate, and (F) ureide propionic acid. The values were presented as mean ± SD (n = 7); a means p < 0.05 compared with the CON group and b means p < 0.05 compared with the 10% GLU group.
FIGURE 6
FIGURE 6
Analysis of serum markers of bone formation and resorption: (A) BALP, (B) OCN, (C) P1NP, and (D) TRACP. The values were presented as mean ± SD (n = 7); a means p < 0.05 compared with the CON group and b means p < 0.05 compared with the 10% GLU group.
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