Sulfated Polysaccharides from Sea Cucumber Cooking Liquid Prevents Obesity by Modulating Gut Microbiome, Transcriptome, and Metabolite Profiles in Mice Fed a High-Fat Diet

Overview

Journal Foods

Specialty Biotechnology

Date 2024 Jul 13

PMID 38998524

Authors

Xue Sang

Xin Guan

Yao Tong

Fuyi Wang

Boqian Zhou

Ying Li

Qiancheng Zhao

Affiliations

Soon will be listed here.

Abstract

We aimed to explore the anti-obesity mechanism from the microbiome, metabolome, and transcriptome viewpoints, focusing on the sulfated polysaccharides found in the cooking liquid of (CLSP) to explore the potential mediators of the anti-obesity effects in mice fed a high-fat diet (HFD). The mice treated with CLSP showed a decrease in obesity and blood lipid levels. Gut microbiome dysbiosis caused by the HFD was reversed after CLSP supplementation, along with increased levels of indole-3-ethanol, N-2-succinyl-L-glutamic acid 5-semialdehyde, and urocanic acid. These increases were positively related to the increased , , , and . Transcriptome analysis showed that B cell receptor signaling and cytochrome P450 xenobiotic metabolism were the main contributors to the improvement in obesity. Metabolome-transcriptome analysis revealed that CLSP reversal of obesity was mainly due to amino acid metabolism. These findings suggest that CLSP could be a valuable prebiotic preparation for preventing obesity-related diseases.

References

Bousova I, Kostakova S, Matouskova P, Bartikova H, Szotakova B, Skalova L . Monosodium glutamate-induced obesity changed the expression and activity of glutathione S-transferases in mouse heart and kidney. Pharmazie. 2018; 72(5):257-259. DOI: 10.1691/ph.2017.6886. View

Leth M, Ejby M, Workman C, Ewald D, Pedersen S, Sternberg C . Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. Nat Microbiol. 2018; 3(5):570-580. DOI: 10.1038/s41564-018-0132-8. View

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

Cani P, Depommier C, Derrien M, Everard A, de Vos W . Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol. 2022; 19(10):625-637. DOI: 10.1038/s41575-022-00631-9. View

Ejtahed H, Angoorani P, Soroush A, Hasani-Ranjbar S, Siadat S, Larijani B . Gut microbiota-derived metabolites in obesity: a systematic review. Biosci Microbiota Food Health. 2020; 39(3):65-76. PMC: 7392910. DOI: 10.12938/bmfh.2019-026. View

Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y . Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017; 23(7):859-868. DOI: 10.1038/nm.4358. View

Amor A, Perea V . Dyslipidemia in nonalcoholic fatty liver disease. Curr Opin Endocrinol Diabetes Obes. 2019; 26(2):103-108. DOI: 10.1097/MED.0000000000000464. View

Xie B, Zu X, Wang Z, Xu X, Liu G, Liu R . Ginsenoside Rc ameliorated atherosclerosis regulating gut microbiota and fecal metabolites. Front Pharmacol. 2022; 13:990476. PMC: 9520581. DOI: 10.3389/fphar.2022.990476. View

Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P . The Firmicutes/Bacteroidetes Ratio: A Relevant Marker of Gut Dysbiosis in Obese Patients?. Nutrients. 2020; 12(5). PMC: 7285218. DOI: 10.3390/nu12051474. View

10.

Ding Z, Ericksen R, Escande-Beillard N, Lee Q, Loh A, Denil S . Metabolic pathway analyses identify proline biosynthesis pathway as a promoter of liver tumorigenesis. J Hepatol. 2019; 72(4):725-735. DOI: 10.1016/j.jhep.2019.10.026. View

11.

Bernini L, Simao A, Alfieri D, Lozovoy M, Mari N, de Souza C . Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: A randomized trial. Effects of probiotics on metabolic syndrome. Nutrition. 2016; 32(6):716-9. DOI: 10.1016/j.nut.2015.11.001. View

12.

Tkachenko A, Kupcova K, Havranek O . B-Cell Receptor Signaling and Beyond: The Role of Igα (CD79a)/Igβ (CD79b) in Normal and Malignant B Cells. Int J Mol Sci. 2024; 25(1). PMC: 10779339. DOI: 10.3390/ijms25010010. View

13.

Carpita N . Measurement of uronic acids without interference from neutral sugars. Anal Biochem. 1991; 197(1):157-62. DOI: 10.1016/0003-2697(91)90372-z. View

14.

Lukic I, Getselter D, Ziv O, Oron O, Reuveni E, Koren O . Antidepressants affect gut microbiota and Ruminococcus flavefaciens is able to abolish their effects on depressive-like behavior. Transl Psychiatry. 2019; 9(1):133. PMC: 6456569. DOI: 10.1038/s41398-019-0466-x. View

15.

Takeuchi T, Kameyama K, Miyauchi E, Nakanishi Y, Kanaya T, Fujii T . Fatty acid overproduction by gut commensal microbiota exacerbates obesity. Cell Metab. 2023; 35(2):361-375.e9. DOI: 10.1016/j.cmet.2022.12.013. View

16.

Liu J, Yue S, Yang Z, Feng W, Meng X, Wang A . Oral hydroxysafflor yellow A reduces obesity in mice by modulating the gut microbiota and serum metabolism. Pharmacol Res. 2018; 134:40-50. DOI: 10.1016/j.phrs.2018.05.012. View

17.

Ogata Y, Suda W, Ikeyama N, Hattori M, Ohkuma M, Sakamoto M . Complete Genome Sequence of Phascolarctobacterium faecium JCM 30894, a Succinate-Utilizing Bacterium Isolated from Human Feces. Microbiol Resour Announc. 2019; 8(3). PMC: 6346166. DOI: 10.1128/MRA.01487-18. View

18.

Wu F, Guo X, Zhang J, Zhang M, Ou Z, Peng Y . abundant colonization in human gastrointestinal tract. Exp Ther Med. 2017; 14(4):3122-3126. PMC: 5585883. DOI: 10.3892/etm.2017.4878. View

19.

Ma N, Ma X . Dietary Amino Acids and the Gut-Microbiome-Immune Axis: Physiological Metabolism and Therapeutic Prospects. Compr Rev Food Sci Food Saf. 2020; 18(1):221-242. DOI: 10.1111/1541-4337.12401. View

20.

Zhang J, Wen C, Duan Y, Zhang H, Ma H . Advance in Cordyceps militaris (Linn) Link polysaccharides: Isolation, structure, and bioactivities: A review. Int J Biol Macromol. 2019; 132:906-914. DOI: 10.1016/j.ijbiomac.2019.04.020. View