Extracted yam bean (Pachyrhizus erosus (L.) Urb.) fiber counteracts adiposity, insulin resistance, and inflammation while modulating gut microbiota composition in mice fed with a high-fat diet

Putra Santoso , Rita Maliza, Resti Rahayu, Yunita Astrina, Firman Syukri, Septalian Maharani

Abstract


Background and purpose: Yam bean (Pachyrhizus erosus) is a potent medicinal plant exerting therapeutical effects against diseases. However, investigations on the health benefits of its fiber remain limited. This study aimed to investigate the potential of yam bean fiber (YBF) against a high-fat diet (HFD)-induced metabolic diseases, inflammation, and gut dysbiosis.

Experimental approach: Adult male mice were assigned to four groups (8 each), namely a normal diet-fed group (ND), HFD-fed group, and HFD supplemented with YBF groups (HFD + YBF) at a dose of 2.5% and 10%, respectively. Treatments were implemented for ten weeks. Thereafter, indicators of metabolic diseases, oxidative stress, inflammation, and gut microbiota composition were determined.

Findings / Results: A dosage of 10% YBF significantly inhibited excessive body weight gain (2.3 times lower than HFD group) and white adipose tissue (WAT) mass (2.2 times lower than HFD group) while sustaining brown adipose tissue mass. YBF prevented malondialdehyde elevation, catalase activity reduction, and expression of the interleukin-6 increment (2.7 times lower than the HFD group) within the WAT. Furthermore, YBF sustained normoglycaemia, glucose tolerance, and insulin sensitivity while precluding hyperinsulinemia. YBF modulated the gut microbiota community by increasing health-promoting microbiota including Lactobacillus reuteri, L. johnsonii, and inhibiting a pathogenic Mucispirillum sp. YBF prevented histopathology and inflammation of the colon.

Conclusion and implications: YBF at the dose of 10% is proved to be useful in the prevention of diet-induced metabolic diseases, microbiota dysbiosis, and inflammation. Hence, YBF is recommended as a potential natural-based remedy to diminish the detrimental effects of high-fat foods. 


Keywords


Hyperinsulinemia; Inflammation; Interleukin-6; Metabolic diseases; Mucispirillum sp.; White adipose tissue.

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References


Yang XF, Qiu YQ, Wang L, Gao KG, Jiang ZY. A high-fat diet increases body fat mass and up-regulates expression of genes related to adipogenesis and inflammation in a genetically lean pig. J Zhejiang Univ Sci B. 2018;19(11):884-894. DOI: 10.1631/jzus.B1700507.

Gao M, Ma Y, Liu D. High-fat diet-induced adiposity, adipose inflammation, hepatic steatosis and hyperinsulinemia in outbred CD-1 mice. PLoS One. 2015;10(3):e0119784,1-15. DOI: 10.1371/journal.pone.0119784.

Martinez KB, Leone V, Chang EB. Western diets, gut dysbiosis, and metabolic diseases: are they linked? Gut Microbes. 2017;8(2):130-142. DOI: 10.1080/19490976.2016.1270811.

Saklayen MG. The global epidemic of the metabolic syndrome. Curr Hypertens Rep. 2018;20(2):12,1-8. DOI: 10.1007/s11906-018-0812-z.

Aiswal V, Chauhan S, Lee H-J. The bioactivity and phytochemicals of Pachyrhizus erosus (L.). urb: a multifunctional underutilized crop plant. Antioxidants. 2022;11(1):58,1-23. DOI: 10.3390/antiox11010058.

Park CJ, Han J-S. Hypoglycemic effect of jicama (Pachyrhizus erosus) extract on streptozotocin-induced diabetic mice. Prev Nutr Food Sci. 2015;20(2):88-93. DOI: 10.3746/pnf.2015.20.2.88.

Park CJ, Lee H-A, Han JS. Jicama (Pachyrhizus erosus) extract increases insulin sensitivity and regulates hepatic glucose in C57BL/Ksj-db/db mice. J Clin Biochem Nutr. 2016;58(1):56-63. DOI: 10.3164/jcbn.15-59.

Thaptimthong T, Kasemsuk T, Sibmooh N, Unchern S. Platelet inhibitory effects of juices from Pachyrhizus erosus L. root and Psidium guajava L. fruit: a randomized controlled trial in healthy volunteers. BMC Complement Altern Med. 2016;16:269,1-12. DOI: 10.1186/s12906-016-1255-1.

Kumalasari ID, Nishi K, Harmayani E, Raharjo S, Sugahara T. Immunomodulatory activity of bengkoang (Pachyrhizus erosus) fiber extract in vitro and in vivo. Cytotechnology. 2014;66(1):75-85. DOI: 10.1007/s10616-013-9539-5.

Santoso P, Amelia A, Rahayu R. Jicama (Pachyrhizus erosus) fiber prevents excessive blood glucose and body weight increase without affecting food intake in mice fed with high-sugar diet. J Adv Vet Anim Res. 2019;6(2):222-230. DOI: 10.5455/javar.2019.f336.

Wang ZQ, Yu Y, Zhang XH, Floyd ZE, Boudreau A, Lian K, et al. Comparing the effects of nano-sized sugarcane fiber with cellulose and psyllium on hepatic cellular signaling in mice. Int J Nanomedicine. 2012;7:2999-3012. DOI: 10.2147/IJN.S30887.

Li X, Guo J, Ji K, Zhang P. Bamboo shoot fiber prevents obesity in mice by modulating the gut microbiota. Sci Rep. 2016;6:32953,1-11. DOI: 10.1038/srep32953.

Sunarti, Rini SLS, Sinorita H, Ariani D. Effect of fiber-rich snacks on C-reactive protein and atherogenic index in type 2 diabetes patients. Rom J Diabet Nutr Metab Dis. 2018;25(4):357-362. DOI:rjdnmd.org/index.php/RJDNMD/article/view/531.

Ding S, Jiang J, Yu P, Zhang G, Zhang G, Liu X. Green tea polyphenol treatment attenuates atherosclerosis in high-fat diet-fed apolipoprotein E-knockout mice via alleviating dyslipidemia and up-regulating autophagy. PLoS One. 2017;12(8):e0181666,1-18. DOI: 10.1371/journal.pone.0181666.

Yao L, Wei J, Shi S, Guo K, Wang X, Wang Q, et al. Modified lingguizhugan decoction incorporated with dietary restriction and exercise ameliorates hyperglycemia, hyperlipidemia and hypertension in a rat model of the metabolic syndrome. BMC Complement Altern Med. 2017;17(1):132,1-12. DOI: 10.1186/s12906-017-1557-y.

Keinicke H, Sun G, Mentzel CMJ, Fredholm M, John LM, Andersen B, et al. FGF21 regulates hepatic metabolic pathways to improve steatosis and inflammation. Endocr Connect. 2020;9(8):755-768. DOI: 10.1530/EC-20-0152.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods.2001;25(4):402-408. DOI: 10.1006/meth.2001.1262.

Li J, Wu H, Liu Y, Yang L. High fat diet induced obesity model using four strains of mice: kunming, C57BL/6, BALB/c and ICR. Exp Anim. 2020;69(3):326-335. DOI: 10.1538/expanim.19-0148.

Wang B, Kong Q, Li X, Zhao J, Zhang H, Chen W, et al. A high-fat diet increases gut microbiota biodiversity and energy expenditure due to nutrient difference. Nutrients. 2020;12(10):3197,1-20. DOI: 10.3390/nu12103197.

Feng R, Sun G, Zhang Y, Sun Q, Ju L, Sun C, et al. Short-term high-fat diet exacerbates insulin resistance and glycolipid metabolism disorders in young obese men with hyperlipidemia, as determined by metabolomics analysis using ultra-HPLC-quadrupole time-of-flight mass spectrometry. J Diabetes. 2019;11(2):148-160. DOI: 10.1111/1753-0407.12828.

Ruhee RT, Suzuki K. Dietary fiber and its effect on obesity, Adv Med Res. 2018;1:1,1-14. DOI: 10.12715/amr.2018.1.2

Engin A. Adipose tissue hypoxia in obesity and its impact on preadipocytes and macrophages: hypoxia hypothesis. Adv Exp Med Biol.2017;960:305-326. DOI: 10.1007/978-3-319-48382-5_13.

Trayhurn P. Hypoxia and adipose tissue function and dysfunction in obesity. Physiol Rev. 2013;93(1):1-21. DOI:10.1152/physrev.00017.2012.

Revelo XS, Luck H, Winer S, Winer DA. Morphological and inflammatory changes in visceral adipose tissue during obesity. Endocr Pathol. 2014;25(1):93-101. DOI: 10.1007/s12022-013-9288-1.

Netzer N, Gatterer H, Faulhaber M, Burtscher M, Pramsohler S, Pesta D. Hypoxia, oxidative stress and fat. Biomolecules. 2015;5(2):1143-1150. DOI: 10.3390/biom5021143.

Ogata M, Van Hung T, Tari H, Arakawa T, Suzuki T. Dietary psyllium fiber increases intestinal heat shock protein 25 expression in mice. Nutr Res. 2017;39:25-33. DOI: 10.1016/j.nutres.2017.02.002.

Segain JP, de la Bletiere DR, Bourreille A, Leray V, Gervois N, Rosales C et al. Butyrate inhibits inflammatory responses through NF kappa B inhibition: implications for Crohn’s disease. Gut. 2000;47(3):397-403. DOI: 10.1136/gut.47.3.397.

Filippone A, Lanza M, Campolo M, Casili G, Paterniti I, Cuzzocrea S, et al. The anti-inflammatory and antioxidant effects of sodium propionate. Int J Mol Sci. 2020; 21(8):3026,1-17. DOI: 10.3390/ijms21083026.

González-Bosch C, Boorman E, Zunszain PA, Mann GE. Short-chain fatty acids as modulators of redox signaling in health and disease. Redox Biol. 2021;47:102165,1-11.

DOI:10.1016/j.redox.2021.102165.

Ratajczak W, Rył A, Mizerski A, Walczakiewicz K, Sipak O, Laszczyńska M. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim Pol. 2019;66(1):1-12. DOI:10.18388/abp.2018_2648.

Rasouli N. Adipose tissue hypoxia and insulin resistance. J Investig Med. 2016;64(4):830-832. DOI: 10.1136/jim-2016-000106.

Lawler HM, Underkofler CM, Kern PA, Erickson C, Bredbeck B, Rasouli N. Adipose tissue hypoxia, inflammation, and fibrosis in obese insulin-sensitive and obese insulin-resistant subjects. J Clin Endocrinol Metab. 2016;101(4):1422-1428. DOI: 10.1210/jc.2015-4125.

Santoso P, Maliza R, Insani SJ, Fadhila Q, Rahayu R. Preventive effect of jicama (Pachyrhizus erosus) fiber against diabetes development in mice fed with high-fat diet. J Appl Pharm Sci. 2021;11(1):137-143. DOI: 10.7324/JAPS.2021.110116.

Zhai X, Lin D, Zhao Y, Li W, Yang X. Effects of dietary fiber supplementation on fatty acid metabolism and intestinal microbiota diversity in C57BL/6J mice fed with a high-fat diet. J Agric Food Chem. 2018;66(48):12706-12718. DOI: 10.1021/acs.jafc.8b05036.

Makki K, Deehan EC, Walter J, Bäckhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe. 2018;23(6):705-715. DOI: 10.1016/j.chom.2018.05.012.

Holscher HD, Bauer LL, Gourineni V, Pelkman CL, Fahey Jr GC, Swanson KS. Agave inulin supplementation affects the fecal microbiota of healthy adults participating in a randomized, double-blind, placebo-controlled, crossover trial. J Nutr. 2015;145(9):2025-2032. DOI: 10.3945/jn.115.217331.

Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55-60. DOI: 10.1038/nature11450.

Abhisingha M, Dumnil J, Pitaksutheepong C. Selection of potential probiotic Lactobacillus with inhibitory activity against Salmonella and fecal coliform bacteria. Probiotics Antimicrob Proteins. 2018;10(2):218-227. DOI: 10.1007/s12602-017-9304-8.

Wang P, Li Y, Xiao H, Shi Y, Le G-W, Sun J. Isolation of Lactobacillus reuteri from Peyer's patches and their effects on sIgA production and gut microbiota diversity. Mol Nutr Food Res. 2016;60(9):2020-2030. DOI: 10.1002/mnfr.201501065.

Xin J, Zeng D, Wang H, Sun N, Zhao Y, Dan Y, et al. Probiotic Lactobacillus johnsonii BS15 promotes growth performance, intestinal immunity, and gut microbiota in piglets. Prob Antimicrob Prot. 2020;12(1):184-193. DOI: 10.1007/s12602-018-9511-y.

Yang G, Hong E, Oh S, Kim E. Non- viable Lactobacillus johnsonii JNU3402 protects against diet-induced obesity. Foods. 2020;9(10):1494,1-11. DOI: 10.3390/foods9101494.

Herp S, Durai Raj AC, Salvado Silva M, Woelfel S, Stecher B. The human symbiont Mucispirillum schaedleri: causality in health and disease. Med Microbiol Immunol. 2021;210(4):173-179. DOI: 10.1007/s00430-021-00702-9.

Ussar S, Griffin NW, Bezy O, Fujisaka S, Vienberg S, Softic S, et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and netabolic syndrome. Cell Metab. 2015;22(3):516-530. DOI: 10.1016/j.cmet.2015.07.007.

Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16(3):255-261. DOI:10.1016/j.mib.2013.06.003.

Deehan EC, Duar RM, Armet AM, Perez-Muñoz ME, Jin M, Walter J. Modulation of the gastrointestinal microbiome with nondigestible fermentable carbohydrates to improve human health. Microbiol Spectr. 2017;5(5):1-24. DOI: 10.1128/microbiolspec.BAD-0019-2017.


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