An extra honey polyphenols-rich diet ameliorates the high-fat diet induced chronic kidney disease via modulating gut microbiota in C57BL/6 mice

References

• de Vries APJ, Ruggenenti P, Ruan XZ, et al. Fatty kidney: emerging role of ectopic lipid in obesity-related renal disease. Lancet Diabetes Endocrinol. 2014;2(5):1–15. doi: 10.1016/S2213-8587(14)70065-8.
   PubMed Web of Science ®Google Scholar
• Asghari G, Momenan M, Yuzbashian E, et al. Dietary pattern and incidence of chronic kidney disease among adults: a population-based study. Nutr Metab. 2018;15(1):88. doi: 10.1186/s12986-018-0322-7.
   Google Scholar
• van der Heijden RA, Bijzet J, Meijers WC, et al. Obesity-induced chronic inflammation in high fat diet challenged C57BL/6J mice is associated with acceleration of age-dependent renal amyloidosis. Sci Rep. 2015;5(1):16474. doi: 10.1038/srep16474.
   PubMedGoogle Scholar
• Gai Z, Wang T, Visentin M, et al. Lipid accumulation and chronic kidney disease. Nutrients. 2019;11(4):722. doi: 10.3390/nu11040722.
   PubMed Web of Science ®Google Scholar
• Targher G, Byrne CD. Non-alcoholic fatty liver disease: an emerging driving force in chronic kidney disease. Nat Rev Nephrol. 2017;13(5):297–310. doi: 10.1038/nrneph.2017.16.
   PubMed Web of Science ®Google Scholar
• Nallu A, Sharma S, Ramezani A, et al. Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res. 2017;179:24–37. doi: 10.1016/j.trsl.2016.04.007.
   PubMed Web of Science ®Google Scholar
• Sampaio-Maia B, Simões-Silva L, Pestana M, et al. The role of the gut microbiome on chronic kidney disease. Adv Appl Microbiol. 2016;96:65–94. doi: 10.1016/bs.aambs.2016.06.002.
   PubMed Web of Science ®Google Scholar
• Vaziri ND, Wong J, Pahl M, et al. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013;83(2):308–315. doi: 10.1038/ki.2012.345.
   PubMed Web of Science ®Google Scholar
• Jiang S, Xie S, Lv D, et al. Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep. 2017;7(1):2870. doi: 10.1038/s41598-017-02989-2.
   PubMed Web of Science ®Google Scholar
• Cosola C, Rocchetti MT, Sabatino A, et al. Microbiota ­issue in CKD: how promising are gut-targeted ­approaches? J Nephrol. 2019;32(1):27–37. doi: 10.1007/s40620-018-0516-0.
   PubMed Web of Science ®Google Scholar
• Kalantar-Zadeh K, Fouque D. Nutritional management of chronic kidney disease. N Engl J Med. 2018;378(6):584–585. doi: 10.1056/NEJMc1715765.
   PubMedGoogle Scholar
• Chen S, Wu F, Yang C, et al. Alternative to sugar, honey does not provoke insulin resistance in rats based on lipid profiles, inflammation, and IRS/PI3K/AKT signaling pathways modulation. J Agric Food Chem. 2022;70(33):10194–10208. doi: 10.1021/ACS.JAFC.2C03639.
   PubMed Web of Science ®Google Scholar
• Chen S, Xu Y, Cheng N, et al. Mitigation of DSS-induced colitis potentially via Th1/Th2 cytokine and immunological function balance induced by phenolic-enriched buckwheat (Fagopyrum esculentum Moench) bee pollen extract. Foods. 2022;11(9):1293. doi: 10.3390/FOODS11091293.
   Web of Science ®Google Scholar
• Zhang J, Cao W, Zhao H, et al. Protective mechanism of Fagopyrum esculentum Moench. Bee pollen EtOH ­extract against type II diabetes in a high-fat diet/streptozocin-induced C57BL/6J mice. Front Nutr. 2022;9:925351. doi: 10.3389/FNUT.2022.925351.
   PubMed Web of Science ®Google Scholar
• Rapa SF, Di Iorio BR, Campiglia P, et al. Inflammation and oxidative stress in chronic kidney disease—potential therapeutic role of minerals, vitamins and plant-derived metabolites. Int J Mol Sci. 2019;21(1):263. doi: 10.3390/ijms21010263.
   PubMed Web of Science ®Google Scholar
• Mafra D, Borges N, Alvarenga L, et al. Dietary components that may influence the disturbed gut microbiota in chronic kidney disease. Nutrients. 2019;11(3):496. doi: 10.3390/nu11030496.
   PubMed Web of Science ®Google Scholar
• Bogdanov S, Jurendic T, Sieber R, et al. Honey for nutrition and health: a review. J Am Coll Nutr. 2008;27(6):677–689. doi: 10.1080/07315724.2008.10719745.
   PubMed Web of Science ®Google Scholar
• Meo SA, Al-Asiri SA, Mahesar AL, et al. Role of honey in modern medicine. Saudi J Biol Sci. 2017;24(5):975–978. doi: 10.1016/j.sjbs.2016.12.010.
   PubMed Web of Science ®Google Scholar
• Erejuwa OO, Aja DOJ, Uwaezuoke NI, et al. Effects of honey supplementation on renal dysfunction and metabolic acidosis in rats with high-fat diet-induced chronic kidney disease. J Basic Clin Physiol Pharmacol. 2021;32(1):20190151. doi: 10.1515/jbcpp-2019-0151.
   Google Scholar
• Cianciosi D, Forbes-Hernández TY, Afrin S, et al. Phenolic compounds in honey and their associated health benefits: a review. Molecules. 2018;23(9):2322. doi: 10.3390/molecules23092322.
   PubMed Web of Science ®Google Scholar
• Gil MI, Ferreres F, Ortiz A, et al. Plant phenolic metabolites and floral origin of rosemary honey. J Agric Food Chem. 1995;43(11):2833–2838. doi: 10.1021/jf00059a012.
   Web of Science ®Google Scholar
• Aronne G, Giovanetti M, Sacchi R, et al. From flower to honey bouquet: possible markers for the botanical origin of Robinia honey. The Scientific World Journal. 2014;2014:1–7. doi: 10.1155/2014/547275.
   Google Scholar
• Catalkaya G, Venema K, Lucini L, et al. Interaction of dietary polyphenols and gut microbiota: microbial metabolism of polyphenols, influence on the gut microbiota, and implications on host health. Food Frontiers. 2020;1(2):109–133. doi: 10.1002/fft2.25.
   Google Scholar
• Ozdal T, Sela DA, Ao J, et al. The reciprocal interactions between polyphenols and gut microbiota and effects on bioaccessibility. Nutrients. 2016;8(2):78. doi: 10.3390/nu8020078.
   PubMed Web of Science ®Google Scholar
• Maalej A, Mahmoudi A, Bouallagui Z, et al. Olive phenolic compounds attenuate deltamethrin-induced liver and kidney toxicity through regulating oxidative stress, inflammation and apoptosis. Food Chem Toxicol. 2017;106(Pt A):455–465. doi: 10.1016/j.fct.2017.06.010.
   PubMedGoogle Scholar
• Tzounis X, Rodriguez-Mateos A, Vulevic J, et al. Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am J Clin Nutr. 2011;93(1):62–72. doi: 10.3945/ajcn.110.000075.
   PubMed Web of Science ®Google Scholar
• Massot-Cladera M, Pérez-Berezo T, Franch A, et al. Cocoa modulatory effect on rat faecal microbiota and colonic crosstalk. Arch Biochem Biophys. 2012;527(2):105–112. doi: 10.1016/j.abb.2012.05.015.
   PubMed Web of Science ®Google Scholar
• Bialonska D, Ramnani P, Kasimsetty SG, et al. The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. Int J Food Microbiol. 2010;140(2–3):175–182. doi: 10.1016/j.ijfoodmicro.2010.03.038.
   PubMed Web of Science ®Google Scholar
• Shackelford C, Long G, Wolf J, et al. Qualitative and quantitative analysis of nonneoplastic lesions in toxicology studies. Toxicol Pathol. 2002;30(1):93–96. doi: 10.1080/01926230252824761.
   PubMed Web of Science ®Google Scholar
• Zhao H, Cheng N, Zhou W, et al. Honey polyphenols ameliorate DSS‐ulcerative colitis via modulating gut microbiota in rats. Mol Nutr Food Res. 2019;63(23):e1900638. doi: 10.1002/mnfr.201900638.
   PubMed Web of Science ®Google Scholar
• Miller DN, Bryant JE, Madsen EL, et al. Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol. 1999;65(11):4715–4724. doi: 10.1128/AEM.65.11.4715-4724.1999.
   PubMed Web of Science ®Google Scholar
• Tucker PS, Scanlan AT, Dalbo VJ. Chronic kidney disease influences multiple systems: describing the relationship between oxidative stress, inflammation, kidney damage, and concomitant disease. Oxid Med Cell Longev. 2015;2015:806358–806358. doi: 10.1155/2015/806358.
   PubMed Web of Science ®Google Scholar
• Kurts C, Panzer U, Anders HJ, et al. The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol. 2013;13(10):738–753. doi: 10.1038/nri3523.
   PubMed Web of Science ®Google Scholar
• Chang CL, Marra G, Chauhan DP, et al. Oxidative stress inactivates the human DNA mismatch repair system. Am J Physiol Cell Physiol. 2002;283(1):C148–C154. doi: 10.1152/ajpcell.00422.2001.
   PubMed Web of Science ®Google Scholar
• Djudjaj S, Boor P. Cellular and molecular mechanisms of kidney fibrosis. Mol Aspects Med. 2019;65:16–36. doi: 10.1016/j.mam.2018.06.002.
   PubMed Web of Science ®Google Scholar
• Zoccali C, Vanholder R, Massy ZA, European Renal and Cardiovascular Medicine (EURECA-m) Working Group of the European Renal Association–European Dialysis Transplantation Association (ERA-EDTA), et al. The systemic nature of CKD. Nat Rev Nephrol. 2017;13(6):344–358. doi: 10.1038/nrneph.2017.52.
   PubMed Web of Science ®Google Scholar
• Zhao H, Cheng N, He L, et al. Antioxidant and hepatoprotective effects of A. cerana honey against acute alcohol-induced liver damage in mice. Food Res Int. 2017;101:35–44. doi: 10.1016/j.foodres.2017.08.014.
   PubMed Web of Science ®Google Scholar
• Zhao H, Cheng N, Wang Q, et al. Effects of honey-extracted polyphenols on serum antioxidant capacity and metabolic phenotype in rats. Food Funct. 2019;10(5):2347–2358. doi: 10.1039/c8fo02138d.
   PubMed Web of Science ®Google Scholar
• Abrass CK. Cellular lipid metabolism and the role of lipids in progressive renal disease. Am J Nephrol. 2004;24(1):46–53. doi: 10.1159/000075925.
   PubMed Web of Science ®Google Scholar
• Moorhead JF, El-Nahas M, Chan MK, et al. Lipid nephrotoxicity in chronic progressive glomerular and tubulo-interstitial disease. Lancet. 1982;2(8311):1309–1311. doi: 10.1016/s0140-6736(82)91513-6.
   PubMed Web of Science ®Google Scholar
• Panov A, Mayorov VI, Dikalov S. Metabolic syndrome and β-oxidation of long-chain fatty acids in the brain, heart, and kidney mitochondria. Int J Mol Sci. 2022;23(7):4047. doi: 10.3390/ijms23074047.
   PubMed Web of Science ®Google Scholar
• Juszczak F, Caron N, Mathew AV, et al. Critical role for AMPK in metabolic disease-induced chronic kidney disease. Int J Mol Sci. 2020;21(21):7994. doi: 10.3390/ijms21217994.
   PubMed Web of Science ®Google Scholar
• Declèves A-E, Mathew AV, Cunard R, et al. AMPK mediates the initiation of kidney disease induced by a high-fat diet. J Am Soc Nephrol. 2011;22(10):1846–1855. doi: 10.1681/ASN.2011010026.
   PubMed Web of Science ®Google Scholar
• Juszczak F, Vlassembrouck M, Botton O, et al. Delayed exercise training improves obesity-induced chronic kidney disease by activating AMPK pathway in high-fat diet-fed mice. Int J Mol Sci. 2020;22(1):350. doi: 10.3390/ijms22010350.
   PubMed Web of Science ®Google Scholar
• Ahmed S, Sulaiman SA, Baig AA, et al. Honey as a potential natural antioxidant medicine: an insight into its molecular mechanisms of action. Oxid Med Cell Longev. 2018;2018:8367846–8367819. doi: 10.1155/2018/8367846.
   PubMed Web of Science ®Google Scholar
• Susla O, Shin HS, Jung YS, et al. Nutrition, inflammation and oxidative stress – CKD 1-5. Nephrol Dial Transplant. 2012;27(suppl 2):ii405–ii413. doi: 10.1093/ndt/gfs238.
   Google Scholar
• Colgan SM, Hashimi AA, Austin RC. Endoplasmic reticulum stress and lipid dysregulation. Expert Rev Mol Med. 2011;13:e4. doi: 10.1017/S1462399410001742.
   PubMed Web of Science ®Google Scholar
• Arany I, Hall S, Reed DK, et al. Nicotine enhances high-fat diet-induced oxidative stress in the kidney. Nicotine Tob Res. 2016;18(7):1628–1634. doi: 10.1093/ntr/ntw029.
   PubMed Web of Science ®Google Scholar
• Qiu M, Li S, Jin L, et al. Combination of chymostatin and aliskiren attenuates ER stress induced by lipid overload in kidney tubular cells. Lipids Health Dis. 2018;17(1):183. doi: 10.1186/s12944-018-0818-1.
   PubMedGoogle Scholar
• Pasupuleti VR, Arigela CS, Gan SH, et al. A review on oxidative stress, diabetic complications, and the roles of honey polyphenols. Oxid Med Cell Longev. 2020;2020:8878172–8878116. doi: 10.1155/2020/8878172.
   PubMed Web of Science ®Google Scholar
• Le Chatelier E, Nielsen T, Qin J, MetaHIT Consortium, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–546. doi: 10.1038/nature12506.
   PubMed Web of Science ®Google Scholar
• Dalby MJ, Aviello G, Ross AW, et al. Diet induced obesity is independent of metabolic endotoxemia and TLR4 signalling, but markedly increases hypothalamic expression of the acute phase protein, SerpinA3N. Sci Rep. 2018;8(1):15648. doi: 10.1038/s41598-018-33928-4.
   PubMedGoogle Scholar
• Ley RE, Turnbaugh PJ, Klein S, et al. Human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023. doi: 10.1038/4441022a.
   PubMed Web of Science ®Google Scholar
• Yan H, Fei N, Wu G, et al. Regulated inflammation and lipid metabolism in colon mRNA expressions of obese germfree mice responding to Enterobacter cloacae B29 combined with the high fat diet. Front Microbiol. 2016;7:1786. doi: 10.3389/fmicb.2016.01786.
   PubMed Web of Science ®Google Scholar
• Duda-Chodak A, Tarko T, Satora P, et al. Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review. Eur J Nutr. 2015;54(3):325–341. doi: 10.1007/s00394-015-0852-y.
   PubMed Web of Science ®Google Scholar
• Foley KP, Zlitni S, Denou E, et al. Long term but not short term exposure to obesity related microbiota promotes host insulin resistance. Nat Commun. 2018;9(1):4681. doi: 10.1038/s41467-018-07146-5.
   PubMedGoogle Scholar
• Ding T, Wang S, Zhang X, et al. Kidney protection effects of dihydroquercetin on diabetic nephropathy through suppressing ROS and NLRP3 inflammasome. Phytomedicine. 2018;41:45–53. doi: 10.1016/j.phymed.2018.01.026.
   PubMed Web of Science ®Google Scholar
• Firrman J, Liu L, Zhang L, et al. The effect of quercetin on genetic expression of the commensal gut microbes Bifidobacterium catenulatum, Enterococcus caccae and Ruminococcus gauvreauii. Anaerobe. 2016;42:130–141. doi: 10.1016/j.anaerobe.2016.10.004.
   PubMed Web of Science ®Google Scholar
• Li Q, Van de Wiele T. Gut microbiota as a driver of the interindividual variability of cardiometabolic effects from tea polyphenols. Crit Rev Food Sci Nutr. 2023;63(11):1500–1526. doi: 10.1080/10408398.2021.1965536.
   PubMed Web of Science ®Google Scholar
• Tzounis X, Vulevic J, Kuhnle GG, et al. Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr. 2008;99(4):782–792. doi: 10.1017/S0007114507853384.
   PubMed Web of Science ®Google Scholar
• Li L, Ma L, Fu P. Gut microbiota–derived short-chain ­fatty acids and kidney diseases. Drug Des Devel Ther. 2017;11:3531–3542. doi: 10.2147/DDDT.S150825.
   PubMed Web of Science ®Google Scholar
• Mythri RB, Bharath MS. Omics and epigenetics of polyphenol-mediated neuroprotection: the curcumin perspective. In: Farooqui T, Farooqui AA, editors. Curcumin for neurological and ­psychiatric disorders. Academic Press; 2019. p. 169–189. doi: 10.1016/B978-0-12-815461-8.00009-8.
   Google Scholar
• Zhou M, Wang S, Zhao A, et al. Transcriptomic and metabonomic profiling reveal synergistic effects of quercetin and resveratrol supplementation in high fat diet fed mice. J Proteome Res. 2012;11(10):4961–4971. doi: 10.1021/pr3004826.
   PubMed Web of Science ®Google Scholar
• van der Beek CM, Dejong CH, Troost FJ, et al. Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing. Nutr Rev. 2017;75(4):286–305. doi: 10.1093/nutrit/nuw067.
   PubMed Web of Science ®Google Scholar