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The ameliorative and neuroprotective effects of dietary fibre on hyperuricaemia mice: a perspective from microbiome and metabolome

Published online by Cambridge University Press:  03 June 2024

Yu Wang Open the ORCID record for Yu Wang [Opens in a new window] ,
Fengping Miao ,
Jun Wang ,
Maokun Zheng ,
Feng Yu  and
Yuetao Yi
Yu Wang
Affiliation:
Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, People’s Republic of China University of Chinese Academy of Sciences, Beijing, People’s Republic of China
Fengping Miao
Affiliation:
Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, People’s Republic of China
Jun Wang
Affiliation:
Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, People’s Republic of China University of Chinese Academy of Sciences, Beijing, People’s Republic of China
Maokun Zheng
Affiliation:
Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, People’s Republic of China
Feng Yu
Affiliation:
Department of Gastroenterology, Zibo Central Hospital, Zibo, Shandong, People’s Republic of China
Yuetao Yi*
Affiliation:
Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, People’s Republic of China Shandong Saline-Alkali Land Modern Agriculture Company, Dongying, People’s Republic of China
*
*Corresponding author: Yuetao Yi, email [email protected]
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Abstract

The effect of single dietary fibre (DF) on lowering uric acid (UA) level has been reported in the literature. However, the potential protective mechanism of DF against potassium oxybate-induced hyperuricaemia (HUA), as modelled by prophylactic administration, remains unclear. The data demonstrate that DF significantly decreased serum and cerebral tissue UA concentrations, inhibited xanthine oxidase expression and activity in the liver and reduced levels of creatinine and urea nitrogen in the serum. Additionally, it mitigated the deposition of amyloid-β in cerebral tissue. Correlation analysis showed that DF modulated the Toll-like receptor 4/NF-κB signalling pathway, attenuating oxidative stress and inflammatory responses in HUA mice. Additionally, DF helps to maintain the composition of the gut microbiota, reducing harmful Desulfovibrio and enriching beneficial Akkermansia and Ruminococcus populations. The results of the faecal metabolomics analysis indicate that DF facilitates the regulation of metabolic pathways involved in oxidative stress and inflammation. These pathways include pyrimidine metabolism, tryptophan metabolism, nucleotide metabolism and vitamin B6 metabolism. Additionally, the study found that DF has a preventive effect on anxiety-like behaviour induced by HUA. In summary, DF shows promise in mitigating HUA and cognitive deficits, primarily by modulating gut microbiota and metabolites.

Keywords

HyperuricaemiaDietary fibreMicrobiomeMetabolomeAnxiety
Type
Research Article
Information
British Journal of Nutrition , Volume 132 , Issue 3 , 14 August 2024 , pp. 275 - 288
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Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Rai, SK, Fung, TT, Lu, N, et al. (2017) The Dietary Approaches to Stop Hypertension (DASH) diet, Western diet, and risk of gout in men: prospective cohort study. BMJ 357, j1794.Google ScholarPubMed
Kyu, HH, Abate, D, Abate, KH, et al. (2018) Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392, 1859–1922.CrossRefGoogle Scholar
Rakoff-Nahoum, S, Foster, KR & Comstock, LE (2016) The evolution of cooperation within the gut microbiota. Nature 533, 255–259.CrossRefGoogle ScholarPubMed
Lv, Q, Xu, D, Zhang, X, et al. (2020) Association of hyperuricemia with immune disorders and intestinal barrier dysfunction. Front Physiol 11, 524236.CrossRefGoogle ScholarPubMed
Yin, H, Liu, N & Chen, J (2022) The role of the intestine in the development of hyperuricemia. Front Immunol 13, 845684.CrossRefGoogle Scholar
Zhao, F, Zhao, Z, Man, D, et al. (2023) Changes in gut microbiota structure and function in gout patients. Food Biosci 54, 102912.CrossRefGoogle Scholar
Tang, DH, Ye, YS, Wang, CY, et al. (2017) Potassium oxonate induces acute hyperuricemia in the tree shrew (tupaia belangeri chinensis). Exp Anim 66, 209–216.CrossRefGoogle ScholarPubMed
Martínez-Nava, GA, Méndez-Salazar, EO, Vázquez-Mellado, J, et al. (2023) The impact of short-chain fatty acid–producing bacteria of the gut microbiota in hyperuricemia and gout diagnosis. Clin Rheumatol 42, 203–214.CrossRefGoogle ScholarPubMed
Dang, K, Zhang, N, Gao, H, et al. (2023) Influence of intestinal microecology in the development of gout or hyperuricemia and the potential therapeutic targets. Int J Rheum Dis 26, 1911–1922.CrossRefGoogle ScholarPubMed
Ju, YH, Bhalla, M, Hyeon, SJ, et al. (2022) Astrocytic urea cycle detoxifies Aβ-derived ammonia while impairing memory in Alzheimer’s disease. Cell Metab 34, 1104–1120.e1108.CrossRefGoogle Scholar
Khaled, Y, Abdelhamid, AA, Al-Mazroey, H, et al. (2023) Higher serum uric acid is associated with poorer cognitive performance in healthy middle-aged people: a cross-sectional study. Intern Emerg Med 18, 1701–1709.CrossRefGoogle ScholarPubMed
Li, L, Yan, S, Liu, S, et al. (2023) In-depth insight into correlations between gut microbiota and dietary fiber elucidates a dietary causal relationship with host health. Food Res Int 172, 113133.CrossRefGoogle ScholarPubMed
Zarrinpar, A, Chaix, A, Yooseph, S, et al. (2014) Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab 20, 1006–1017.CrossRefGoogle ScholarPubMed
Fu, J, Zheng, Y, Gao, Y, et al. (2022) Dietary fiber intake and gut microbiota in human health. Microorganisms 10, 2507.CrossRefGoogle ScholarPubMed
Tawfick, MM, Xie, H, Zhao, C, et al. (2022) Inulin fructans in diet: role in gut homeostasis, immunity, health outcomes and potential therapeutics. Int J Biol Macromol 208, 948–961.CrossRefGoogle ScholarPubMed
Zhu, Q, Yu, L, Li, Y, et al. (2022) Association between dietary fiber intake and hyperuricemia among Chinese adults: analysis of the China adult chronic disease and nutrition surveillance (2015). Nutrients 14, 1433.CrossRefGoogle ScholarPubMed
Sun, Y, Sun, J, Zhang, P, et al. (2019) Association of dietary fiber intake with hyperuricemia in U.S. adults. Food Funct 10, 4932–4940.CrossRefGoogle Scholar
Guo, Y, Yu, Y, Li, H, et al. (2021) Inulin supplementation ameliorates hyperuricemia and modulates gut microbiota in Uox-knockout mice. Eur J Nutr 60, 2217–2230. 2020/10/27 ed.CrossRefGoogle ScholarPubMed
Khazaie, S, Jafari, M, Heydari, J, et al. (2019) Modulatory effects of vitamin C on biochemical and oxidative changes induced by acute exposure to diazinon in rat various tissues: prophylactic and therapeutic roles. J Anim Physiol Anim Nutr (Berl) 103, 1619–1628.CrossRefGoogle ScholarPubMed
Takashi, K (2021) Modification of dietary habits for prevention of gout in Japanese people: gout and macronutrient Intake. Am J Health Res 9, 128–142.Google Scholar
Handley, RR, Reid, SJ, Brauning, R, et al. (2017) Brain urea increase is an early Huntington’s disease pathogenic event observed in a prodromal transgenic sheep model and HD cases. Proc Natl Acad Sci USA 114, E11293–E11302.CrossRefGoogle Scholar
Mijailovic, NR, Vesic, K & Borovcanin, MM (2022) The influence of serum uric acid on the brain and cognitive dysfunction. Front Psychiatry 13, 828476.CrossRefGoogle ScholarPubMed
Liu, X, Lv, Q, Ren, H, et al. (2020) The altered gut microbiota of high-purine-induced hyperuricemia rats and its correlation with hyperuricemia. PeerJ 8, e8664.CrossRefGoogle Scholar
Sun, Y, Xu, D, Zhang, G, et al. (2024) Wild-type Escherichia coli Nissle 1917 improves hyperuricemia by anaerobically degrading uric acid and maintaining gut microbiota profile of mice. J Funct Foods 112, 105935.CrossRefGoogle Scholar
Wang, H, Shen, Q, Fu, Y, et al. (2023) Effects on diabetic mice of consuming lipid extracted from foxtail millet (Setaria italica): gut microbiota analysis and serum metabolomics. J Agric Food Chem 71, 10075–10086.CrossRefGoogle ScholarPubMed
Yuan, L, Zhao, J, Liu, Y, et al. (2024) Multiomics analysis revealed the mechanism of the anti-diabetic effect of Salecan. Carbohydr Polym 327, 121694.CrossRefGoogle Scholar
Wu, Y, Wang, Y, Hu, A, et al. (2022) Lactobacillus plantarum-derived postbiotics prevent Salmonella-induced neurological dysfunctions by modulating gut-brain axis in mice. Front Nutr 9, 946096.CrossRefGoogle Scholar
Yan, S, Chen, J, Zhu, L, et al. (2022) Oryzanol attenuates high fat and cholesterol diet-induced hyperlipidemia by regulating the gut microbiome and amino acid metabolism. J Agric Food Chem 70, 6429–6443.CrossRefGoogle ScholarPubMed
Kaakoush, NO (2015) Insights into the role of erysipelotrichaceae in the human host. Front Cell Infect Microbiol 5, 84.CrossRefGoogle Scholar
Downes, J, Dewhirst, FE, Tanner, ACR, et al. (2013) Description of Alloprevotella rava gen. nov., sp. nov., isolated from the human oral cavity, and reclassification of Prevotella tannerae Moore et al. 1994 as Alloprevotella tannerae gen. nov., comb. nov. Int J Syst Evol Microbiol 63, 1214–1218.CrossRefGoogle Scholar
Meng, Y, Hu, Y, Wei, M, et al. (2023) Amelioration of hyperuricemia by Lactobacillus acidophilus F02 with uric acid -lowering ability via modulation of NLRP3 inflammasome and gut microbiota homeostasis. J Funct Foods 111, 105903.CrossRefGoogle Scholar
Wang, R, Hu, B, Ye, C, et al. (2022) Stewed rhubarb decoction ameliorates adenine-induced chronic renal failure in mice by regulating gut microbiota dysbiosis. Front Pharmacol 13, 842720.CrossRefGoogle Scholar
Pan, L, Han, P, Ma, S, et al. (2020) Abnormal metabolism of gut microbiota reveals the possible molecular mechanism of nephropathy induced by hyperuricemia. Acta Pharm Sin B 10, 249–261.CrossRefGoogle ScholarPubMed
Zhang, Y, Chen, S, Yuan, M, et al. (2022) Gout and diet: a comprehensive review of mechanisms and management. Nutrients 14, 3525.CrossRefGoogle Scholar
Srivastava, A, Kaze, AD, McMullan, CJ, et al. (2018) Uric acid and the risks of kidney failure and death in individuals with CKD. Am J Kidney Dis 71, 362–370.CrossRefGoogle ScholarPubMed
Chilappa, CS, Aronow, WS, Shapiro, D, et al. (2010) Gout and hyperuricemia. Compr Ther 36, 3–13.Google ScholarPubMed
Leblanc, M, Garred, LJ, Cardinal, J, et al. (1998) Catabolism in critical illness: estimation from urea nitrogen appearance and creatinine production during continuous renal replacement therapy. Am J Kidney Dis 32, 444–453.CrossRefGoogle ScholarPubMed
Chaudhary, P, Janmeda, P, Docea, AO, et al. (2023) Oxidative stress, free radicals and antioxidants: potential crosstalk in the pathophysiology of human diseases. Front Chem 11, 1158198.CrossRefGoogle Scholar
Li, Q, Lin, L, Zhang, C, et al. (2024) The progression of inorganic nanoparticles and natural products for inflammatory bowel disease. J Nanobiotechnol 22, 17.CrossRefGoogle ScholarPubMed
Tomasello, G, Mazzola, M, Leone, A, et al. (2016) Nutrition, oxidative stress and intestinal dysbiosis: influence of diet on gut microbiota in inflammatory bowel diseases. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 160, 461–466.CrossRefGoogle ScholarPubMed
Bian, M, Wang, J, Wang, Y, et al. (2020) Chicory ameliorates hyperuricemia via modulating gut microbiota and alleviating LPS/TLR4 axis in quail. Biomed Pharmacother 131, 110719.CrossRefGoogle ScholarPubMed
Li, X, Chen, Y, Gao, X, et al. (2021) Antihyperuricemic effect of green alga Ulva lactuca ulvan through regulating urate transporters. J Agric Food Chem 69, 11225–11235.CrossRefGoogle ScholarPubMed
Oshima, S, Shiiya, S & Nakamura, Y (2019) Serum uric acid -lowering effects of combined glycine and tryptophan treatments in subjects with mild hyperuricemia: a randomized, double-blind, placebo-controlled, crossover study. Nutrients 11, 564.CrossRefGoogle ScholarPubMed
Zhang, K, Qin, X, Qiu, J, et al. (2023) Desulfovibrio desulfuricans aggravates atherosclerosis by enhancing intestinal permeability and endothelial TLR4/NF-κB pathway in Apoe (-/-) mice. Genes Dis 10, 239–253.CrossRefGoogle ScholarPubMed
Fang, J, Wang, H, Zhou, Y, et al. (2021) Slimy partners: the mucus barrier and gut microbiome in ulcerative colitis. Exp Mol Med 53, 772–787.CrossRefGoogle ScholarPubMed
Murros, KE, Huynh, VA, Takala, TM, et al. (2021) Desulfovibrio bacteria are associated with Parkinson’s disease. Front Cell Infect Microbiol 11, 652617.CrossRefGoogle Scholar
Huynh, VA, Takala, TM, Murros, KE, et al. (2023) Desulfovibrio bacteria enhance α-synuclein aggregation in a Caenorhabditis elegans model of Parkinson’s disease. Front Cell Infect Microbiol 13, 1181315.CrossRefGoogle Scholar
Li, LL, Ma, YH, Bi, YL, et al. (2021) Serum uric acid may aggravate Alzheimer’s disease risk by affecting amyloidosis in cognitively intact older adults: the CABLE study. J Alzheimers Dis 81, 389–401.CrossRefGoogle ScholarPubMed
Xu, Y, Yang, Y, Li, B, et al. (2022) Dietary methionine restriction improves gut microbiota composition and prevents cognitive impairment in D-galactose-induced aging mice. Food Funct 13, 12896–12914.CrossRefGoogle ScholarPubMed
Sun, Y, Koyama, Y & Shimada, S (2022) Inflammation from peripheral organs to the brain: how does systemic inflammation cause neuroinflammation? Front Aging Neurosci 14, 903455.CrossRefGoogle Scholar
Nettleton, JE, Klancic, T, Schick, A, et al. (2021) Prebiotic, probiotic, and synbiotic consumption alter behavioral variables and intestinal permeability and microbiota in BTBR mice. Microorganisms 9, 1833.CrossRefGoogle ScholarPubMed
Hsiao, EY, McBride, SW, Hsien, S, et al. (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451–1463.CrossRefGoogle Scholar
Inoue, R, Sakaue, Y, Kawada, Y, et al. (2019) Dietary supplementation with partially hydrolyzed guar gum helps improve constipation and gut dysbiosis symptoms and behavioral irritability in children with autism spectrum disorder. J Clin Biochem Nutr 64, 217–223.CrossRefGoogle ScholarPubMed
Valdivielso, JM, Eritja, À, Caus, M, et al. (2020) Glutamate-gated NMDA receptors: insights into the function and signaling in the kidney. Biomolecules 10, 1051.CrossRefGoogle Scholar
Wang, R, Halimulati, M, Huang, X, et al. (2023) Sulforaphane-driven reprogramming of gut microbiome and metabolome ameliorates the progression of hyperuricemia. J Adv Res 52, 19–28.CrossRefGoogle ScholarPubMed
Olajide, OJ & Chapman, CA (2021) Amyloid-β (1–42) peptide induces rapid NMDA receptor-dependent alterations at glutamatergic synapses in the entorhinal cortex. Neurobiol Aging 105, 296–309.CrossRefGoogle Scholar
Wu, GM, Du, CP & Xu, Y (2023) Oligomeric Aβ25–35 induces the tyrosine phosphorylation of PSD-95 by SrcPTKs in rat hippocampal CA1 subfield. Int J Neurosci 133, 888–895.CrossRefGoogle ScholarPubMed
Oshima, S, Shiiya, S & Nakamura, Y (2019) Combined supplementation with glycine and tryptophan reduces purine-induced serum uric acid elevation by accelerating urinary uric acid excretion: a randomized, single-blind, placebo-controlled, crossover study. Nutrients 11, 2562.CrossRefGoogle ScholarPubMed
Han, EH, Lim, MK, Lee, SH, et al. (2018) Synergic effect in the reduction of serum uric acid level between ethanol extract of Aster glehni and vitamin B(6). Food Sci Biotechnol 27, 1439–1444.CrossRefGoogle ScholarPubMed
Zhang, Y & Qiu, H (2018) Folate, vitamin B6 and vitamin B12 intake in relation to hyperuricemia. J Clin Med 7, 210.CrossRefGoogle Scholar
Wang, L, Li, X, Montazeri, A, et al. (2023) Phenome-wide association study of genetically predicted B vitamins and homocysteine biomarkers with multiple health and disease outcomes: analysis of the UK Biobank. Am J Clin Nutr 117, 564–575.CrossRefGoogle Scholar
Mesripour, A, Alhimma, F & Hajhashemi, V (2019) The effect of vitamin B6 on dexamethasone-induced depression in mice model of despair. Nutr Neurosci 22, 744–749.CrossRefGoogle ScholarPubMed
Theofylaktopoulou, D, Ulvik, A, Midttun, Ø, et al. (2014) Vitamins B2 and B6 as determinants of kynurenines and related markers of interferon-γ-mediated immune activation in the community-based Hordaland Health Study. Br J Nutr 112, 1065–1072.CrossRefGoogle ScholarPubMed
Wang, J, Chen, Y, Zhong, H, et al. (2022) The gut microbiota as a target to control hyperuricemia pathogenesis: potential mechanisms and therapeutic strategies. Crit Rev Food Sci Nutr 62, 3979–3989.CrossRefGoogle Scholar
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