Integration of network pharmacology and intestinal flora to investigate the mechanism of action of Chinese herbal Cichorium intybus formula in attenuating adenine and ethambutol hydrochloride-induced hyperuricemic nephropathy in rats

References

• Abdel-Gadir A, Stephen-Victor E, Gerber GK, Noval Rivas M, Wang S, Harb H, Wang L, Li N, Crestani E, Spielman S, et al. 2019. Microbiota therapy acts via a regulatory T cell MyD88/RORgammat pathway to suppress food allergy. Nat Med. 25(7):1164–1174.
   PubMed Web of Science ®Google Scholar
• Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, et al. 2011. Navigating the multiple meanings of beta diversity: a roadmap for the practicing ecologist. Ecol Lett. 14(1):19–28.
   PubMed Web of Science ®Google Scholar
• Barton BE. 1997. IL-6: insights into novel biological activities. Clin Immunol Immunopathol. 85(1):16–20.
   PubMedGoogle Scholar
• Bian M, Lin Z, Wang Y, Zhang B, Li G, Wang H. 2018. Bioinformatic and metabolomic analysis reveal intervention effects of chicory in a quail model of hyperuricemia. Evid Based Complement Alternat Med. 2018:5730385.
   PubMed Web of Science ®Google Scholar
• Bian M, Wang J, Wang Y, Nie A, Zhu C, Sun Z, Zhou Z, Zhang B. 2020. Chicory ameliorates hyperuricemia via modulating gut microbiota and alleviating LPS/TLR4 axis in quail. Biomed Pharmacother. 131:110719.
   PubMed Web of Science ®Google Scholar
• Bitencourt-Ferreira G, Pintro VO, de Azevedo WF. Jr. 2019. Docking with AutoDock4. Methods Mol Biol. 2053:125–148.,
   PubMedGoogle Scholar
• Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA. 108(38):16050–16055.
   PubMed Web of Science ®Google Scholar
• Chan EW, Lye PY, Wong SK. 2016. Phytochemistry, pharmacology, and clinical trials of Morus alba. Chin J Nat Med. 14(1):17–30.
   PubMed Web of Science ®Google Scholar
• Chen C, Lu JM, Yao Q. 2016. Hyperuricemia-related diseases and xanthine oxidoreductase (XOR) inhibitors: an overview. Med Sci Monit. 22:2501–2512.
   PubMed Web of Science ®Google Scholar
• Chen X, Ge H-Z, Lei S-S, Jiang Z-T, Su J, He X, Zheng X, Wang H-Y, Yu Q-X, Li B, et al. 2020. Dendrobium officinalis six nostrum ameliorates urate under-excretion and protects renal dysfunction in lipid emulsion-induced hyperuricemic rats. Biomed Pharmacother. 132:110765.
   PubMed Web of Science ®Google Scholar
• Chou YC, Kuan JC, Yang T, Chou WY, Hsieh PC, Bai CH, You SL, Chen CH, Wei CY, Sun CA. 2015. Elevated uric acid level as a significant predictor of chronic kidney disease: a cohort study with repeated measurements. J Nephrol. 28(4):457–462.
   PubMed Web of Science ®Google Scholar
• Coussement PA. 1999. Inulin and oligofructose: safe intakes and legal status. J Nutr. 129(7 Suppl):1412S–1417S.
   PubMed Web of Science ®Google Scholar
• Crișan TO, Cleophas MCP, Oosting M, Lemmers H, Toenhake-Dijkstra H, Netea MG, Jansen TL, Joosten LAB. 2016. Soluble uric acid primes TLR-induced proinflammatory cytokine production by human primary cells via inhibition of IL-1Ra. Ann Rheum Dis. 75(4):755–762.
   PubMed Web of Science ®Google Scholar
• de Oliveira EP, Burini RC. 2012. High plasma uric acid concentration: causes and consequences. Diabetol Metab Syndr. 4:12–18.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26(19):2460–2461.
   PubMed Web of Science ®Google Scholar
• Evenepoel P, Poesen R, Meijers B. 2017. The gut-kidney axis. Pediatr Nephrol. 32(11):2005–2014.
   PubMed Web of Science ®Google Scholar
• Fathallah-Shaykh SA, Cramer MT. 2014. Uric acid and the kidney. Pediatr Nephrol. 29(6):999–1008.
   PubMed Web of Science ®Google Scholar
• Feng Y, Sun F, Gao Y, Yang J, Wu G, Lin S, Hu J. 2017. Taurine decreased uric acid levels in hyperuricemic rats and alleviated kidney injury. Biochem Biophys Res Commun. 489(3):312–318.
   PubMed Web of Science ®Google Scholar
• Gaya P, Arqués JL, Medina M, Álvarez I, Landet JM. 2016. A new HPLC-PAD/HPLC-ESI-MS method for the analysis of phytoestrogens produced by bacterial metabolism. Food Ana. Methods. 9(2):537–547.
   Web of Science ®Google Scholar
• Guo Z, Zhang J, Wang Z, Ang KY, Huang S, Hou Q, Su X, Qiao J, Zheng Y, Wang L, et al. 2016. Intestinal microbiota distinguish gout patients from healthy humans. Sci Rep. 6:20602.
   PubMed Web of Science ®Google Scholar
• Hsin KY, Ghosh S, Kitano H. 2013. Combining machine learning systems and multiple docking simulation packages to improve docking prediction reliability for network pharmacology. PLoS One. 8(12):e83922.
   PubMed Web of Science ®Google Scholar
• Hu QH, Zhang X, Wang X, Jiao RQ, Kong LD. 2012. Quercetin regulates organic ion transporter and uromodulin expression and improves renal function in hyperuricemic mice. Eur J Nutr. 51(5):593–606.
   PubMed Web of Science ®Google Scholar
• Hu QH, Zhu JX, Ji J, Wei LL, Miao MX, Ji H. 2013. Fructus Gardenia extract ameliorates oxonate-induced hyperuricemia with renal dysfunction in mice by regulating organic ion transporters and mOIT3. Molecules. 18(8):8976–8993.
   PubMed Web of Science ®Google Scholar
• Hu X, Zhang X, Jin G, Shi Z, Sun W, Chen F. 2017. Geniposide reduces development of streptozotocin-induced diabetic nephropathy via regulating nuclear factor-kappa B signaling pathways. Fundam Clin Pharmacol. 31(1):54–63.
   PubMed Web of Science ®Google Scholar
• Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. 2015. Role of the normal gut microbiota. World J Gastroenterol. 21(29):8787–8803.
   PubMed Web of Science ®Google Scholar
• Jin YN, Lin ZJ, Zhang B, Bai YF. 2018. Effects of chicory on serum uric acid, renal function, and GLUT9 expression in hyperuricaemic rats with renal injury and in vitro verification with cells. Evid Based Complement Alternat Med. 2018:1764212.
   PubMed Web of Science ®Google Scholar
• Johnson RJ, Nakagawa T, Jalal D, Sanchez-Lozada LG, Kang DH, Ritz E. 2013. Uric acid and chronic kidney disease: which is chasing which? Nephrol Dial Transplant. 28(9):2221–2228.
   PubMed Web of Science ®Google Scholar
• Kaneko K, Aoyagi Y, Fukuuchi T, Inazawa K, Yamaoka N. 2014. Total purine and purine base content of common foodstuffs for facilitating nutritional therapy for gout and hyperuricemia. Biol Pharm Bull. 37(5):709–721.
   PubMed Web of Science ®Google Scholar
• Kang L, Miao JX, Cao LH, Miao YY, Miao MS, Liu HJ, Xiang LL, Song YG. 2020. Total glucosides of herbaceous peony (Paeonia lactiflora Pall.) flower attenuate adenine- and ethambutol-induced hyperuricaemia in rats. J Ethnopharmacol. 261:113054.
   PubMed Web of Science ®Google Scholar
• Lee EJ, Hong JK, Whang WK. 2014. Simultaneous determination of bioactive marker compounds from Gardeniae fructus by high performance liquid chromatography. Arch Pharm Res. 37(8):992–1000.
   PubMed Web of Science ®Google Scholar
• Lee H, Lee Y, Kim J, An J, Lee S, Kong H, Song Y, Lee CK, Kim K. 2018. Modulation of the gut microbiota by metformin improves metabolic profiles in aged obese mice. Gut Microbes. 9(2):155–165.
   PubMed Web of Science ®Google Scholar
• Li H, Yang H, Xue X, Liu XF, Poh YH, Cai H, Lee YH, Yu H, Yu H, et al. 2016. A metabolomics approach to study the dual modulation by characterization of chemical alteration during processing of Gardeniae Fructus using UPLC-ESI-QTOF. Anal Methods. 2016:3629–3635.
   Google Scholar
• Li S, Zhang B. 2013. Traditional Chinese medicine network pharmacology: theory, methodology and application. Chin. J Nat Med. 11(2):110–120.
   Web of Science ®Google Scholar
• Li F, Chen Y, Li Y, Huang M, Zhao W. 2020. Geniposide alleviates diabetic nephropathy of mice through AMPK/SIRT1/NF-kappaB pathway. Eur J Pharmacol. 886:173449.
   PubMed Web of Science ®Google Scholar
• Li X, Meng X, Timofeeva M, Tzoulaki I, Tsilidis KK, Ioannidis JP, Campbell H, Theodoratou E. 2017. Serum uric acid levels and multiple health outcomes: umbrella review of evidence from observational studies, randomised controlled trials, and Mendelian randomisation studies. BMJ. 357:j2376.
   PubMed Web of Science ®Google Scholar
• Liang G, Nie Y, Chang Y, Zeng S, Liang C, Zheng X, Xiao D, Zhan S, Zheng Q. 2019. Protective effects of Rhizoma Smilacis glabrae extracts on potassium oxonate- and monosodium urate-induced hyperuricemia and gout in mice. Phytomedicine. 59:152772.
   PubMed Web of Science ®Google Scholar
• Liang X, Wang Q, Jiang Z, Li Z, Zhang M, Yang P, Wang X, Wang Y, Qin Y, Li T, et al. 2020. Clinical research linking Traditional Chinese Medicine constitution types with diseases: a literature review of 1639 observational studies. J Tradit Chin Med. 40(4):690–702.
   PubMed Web of Science ®Google Scholar
• Liu LM, Cheng SF, Shieh PC, Lee JC, Chen JJ, Ho CT, Kuo SC, Kuo DH, Huang LJ, Way TD. 2014. The methanol extract of Euonymus laxiflorus, Rubia lanceolata and Gardenia jasminoides inhibits xanthine oxidase and reduce serum uric acid level in rats. Food Chem Toxicol. 70:179–184.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhai T, Ma R, Luo C, Wang H, Liu L. 2018. Effects of uric acid-lowering therapy on the progression of chronic kidney disease: a systematic review and meta-analysis. Ren Fail. 40(1):289–297.
   PubMed Web of Science ®Google Scholar
• Luecha P, Umehara K, Miyase T, Noguchi H. 2009. Antiestrogenic constituents of the Thai medicinal plants Capparis flavicans and Vitex glabrata. J Nat Prod. 72(11):1954–1959.
   PubMed Web of Science ®Google Scholar
• Luo TT, Lu Y, Yan SK, Xiao X, Rong XL, Guo J. 2020. Network pharmacology in research of Chinese medicine formula: methodology, application and prospective. Chin J Integr Med. 26(1):72–80.
   PubMed Web of Science ®Google Scholar
• Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R. 2020. The Firmicutes/Bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. 12(5):1474–1490.
   PubMed Web of Science ®Google Scholar
• Mariat D, Firmesse O, Levenez F, Guimarăes V, Sokol H, Doré J, Corthier G, Furet J-P. 2009. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9:123–128.
   PubMed Web of Science ®Google Scholar
• Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem. 30(16):2785–2791.
   PubMed Web of Science ®Google Scholar
• Olivier M, Hollstein M, Hainaut P. 2010. TP53 mutations in human cancers: origins, consequences, and clinical use. Cold Spring Harb Perspect Biol. 2(1):a001008.
   PubMed Web of Science ®Google Scholar
• Opal SM, DePalo VA. 2000. Anti-inflammatory cytokines. Chest. 117(4):1162–1172.
   PubMed Web of Science ®Google Scholar
• Perovic J, Tumbas Saponjac V, Kojic J, Krulj J, Moreno DA, Garcia-Viguera C, Bodroza-Solarov M, Ilic N. 2021. Chicory (Cichorium intybus L.) as a food ingredient - Nutritional composition, bioactivity, safety, and health claims: a review. Food Chem. 336:127676.
   PubMed Web of Science ®Google Scholar
• Postlethwaite AE, Kelley WN. 1972. Studies on the mechanism of ethambutol-induced hyperuricemia. Arthritis Rheum. 15(4):403–409.
   PubMedGoogle Scholar
• Pundir CS, Jakhar S, Narwal V. 2019. Determination of urea with special emphasis on biosensors: A review. Biosens Bioelectron. 123:36–50.
   PubMed Web of Science ®Google Scholar
• Ren Q, Tao S, Guo F, Wang B, Yang L, Ma L, Fu P. 2021. Natural flavonol fisetin attenuated hyperuricemic nephropathy via inhibiting IL-6/JAK2/STAT3 and TGF-beta/SMAD3 signaling. Phytomedicine. 87:153552.
   PubMed Web of Science ®Google Scholar
• Rolnik A, Olas B. 2021. The plants of the Asteraceae family as agents in the protection of human health. IJMS. 22(6):3009–3018.
   Google Scholar
• Roman YM. 2019. The Daniel K. Inouye College of Pharmacy scripts: perspectives on the epidemiology of gout and hyperuricemia. Hawaii J Med Public Health. 78:71–76.
   PubMedGoogle Scholar
• Ru J, Li P, Wang J, Zhou W, Li B, Huang C, Li P, Guo Z, Tao W, Yang Y, et al. 2014. TCMSP: a database of systems pharmacology for drug discovery from herbal medicines. J Cheminform. 6:13–18.
   PubMed Web of Science ®Google Scholar
• Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau MC, Roberfroid M, Rowland I. 1998. Functional food science and gastrointestinal physiology and function. Br J Nutr. 80 Suppl 1: s 147–171.
   Web of Science ®Google Scholar
• Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12(6):R60.
   PubMed Web of Science ®Google Scholar
• Sharaf El Din UAA, Salem MM, Abdulazim DO. 2017. Uric acid in the pathogenesis of metabolic, renal, and cardiovascular diseases: a review. J Adv Res. 8(5):537–548.
   PubMed Web of Science ®Google Scholar
• Shi Y, Williamson G. 2016. Quercetin lowers plasma uric acid in pre-hyperuricaemic males: a randomised, double-blinded, placebo-controlled, cross-over trial. Br J Nutr. 115(5):800–806.
   PubMed Web of Science ®Google Scholar
• Sun X, Gao RL, Xiong YK, Huang QC, Xu M. 2014. Antitumor and immunomodulatory effects of a water-soluble polysaccharide from Lilii Bulbus in mice. Carbohydr Polym. 102:543–549.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Milaneschi Y, Zhang Y, Becker KG, Zukley L, Ferrucci L. 2017. A double blind placebo controlled randomized trial of the effect of acute uric acid changes on inflammatory markers in humans: a pilot study. PLoS One. 12(8):e0181100.
   PubMed Web of Science ®Google Scholar
• Tang L, Xu Y, Wei Y, He X. 2017. Uric acid induces the expression of TNF alpha via the ROSMAPKNFkappaB signaling pathway in rat vascular smooth muscle cells. Mol Med Rep. 16(5):6928–6933.
   PubMed Web of Science ®Google Scholar
• The UniProt C. 2017. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 45(D1):D158–D169.
   PubMed Web of Science ®Google Scholar
• Tian D, Yang Y, Yu M, Han Z, Wei M, Zhang H, Jia H, Zou Z. 2020. Anti-inflammatory chemical constituents of Flos Chrysanthemi Indici determined by UPLC-MS/MS integrated with network pharmacology. Food Funct. 11(7):6340–6351.
   PubMed Web of Science ®Google Scholar
• Tian J, Qin S, Han J, Meng J, Liang A. 2022. A review of the ethnopharmacology, phytochemistry, pharmacology and toxicology of Fructus Gardeniae (Zhi-zi). J Ethnopharmacol. 289:114984.
   PubMed Web of Science ®Google Scholar
• Wan L, Chen G, Jian S, Yin XJ, Zhu H. 2018. Antioxidant and xanthine oxidase inhibitory properties and LC-MS/MS identification of compounds of ethanolic extract from mulberry leaves. Acta Sci Pol Technol Aliment. 17(4):313–319.
   PubMed Web of Science ®Google Scholar
• Wang C, Li W, Wang H, Ma Y, Zhao X, Zhang X, Yang H, Qian J, Li J. 2019. Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-alpha and IL-6 levels and functions and by rebalancing intestinal microbiota. BMC Microbiol. 19(1):246–257.
   PubMed Web of Science ®Google Scholar
• Wang X, Zhang Y, Zhang M, Kong H, Wang S, Cheng J, Qu H, Zhao Y. 2019. Novel carbon dots derived from Puerariae lobatae radix and their anti-gout effects. Molecules. 24(22):4152–4163.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wen J, Zheng W, Zhao L, Fu X, Wang Z, Xiong Z, Li F, Xiao W. 2015. Simultaneous determination of neochlorogenic acid, chlorogenic acid, cryptochlorogenic acid and geniposide in rat plasma by UPLC-MS/MS and its application to a pharmacokinetic study after administration of Reduning injection. Biomed Chromatogr. 29(1):68–74.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yin Y, Chen X, Zhao Y, Wu Y, Li Y, Wang X, Chen H, Xiang C. 2019. Induction of intestinal Th17 cells by flagellins from segmented filamentous bacteria. Front Immunol. 10:2750.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang G, Pan J, Gong D. 2015. Novel insights into the inhibitory mechanism of kaempferol on xanthine oxidase. J Agric Food Chem. 63(2):526–534.
   PubMed Web of Science ®Google Scholar
• Wu Y, Wang X, Fan E. 2012. Optimisation of ultrasound-assisted extraction of puerarin and total isoflavones from Puerariae Lobatae Radix (Pueraria lobata (Wild.) Ohwi) with response surface methodology. Phytochem Anal. 23(5):513–519.
   PubMed Web of Science ®Google Scholar
• Xu S, Cao X. 2010. Interleukin-17 and its expanding biological functions. Cell Mol Immunol. 7(3):164–174.
   PubMed Web of Science ®Google Scholar
• Xu ZJ, Shu S, Li ZJ, Liu YM, Zhang RY, Zhang Y. 2017. Liuwei Dihuang pill treats diabetic nephropathy in rats by inhibiting of TGF-beta/SMADS, MAPK, and NF-kB and upregulating expression of cytoglobin in renal tissues. Medicine (Baltimore). 96(3):e5879.
   PubMed Web of Science ®Google Scholar
• Xuan-Qing CHEN, Xiang-Yu LV, Shi-Jia LIU. 2021. Baitouweng decoction alleviates dextran sulfate sodium-induced ulcerative colitis by regulating intestinal microbiota and the IL-6/STAT3 signaling pathway. J Ethnopharmacol. 265:113357.
   PubMed Web of Science ®Google Scholar
• Yan D, Tu Y, Jiang F, Wang J, Zhang R, Sun X, Wang T, Wang S, Bao Y, Hu C, et al. 2015. Uric acid is independently associated with diabetic kidney disease: a cross-sectional study in a Chinese population. PLoS One. 10(6):e0129797.
   PubMed Web of Science ®Google Scholar
• Yan J, Zhang G, Hu Y, Ma Y. 2013. Effect of luteolin on xanthine oxidase: inhibition kinetics and interaction mechanism merging with docking simulation. Food Chem. 141(4):3766–3773.
   PubMed Web of Science ®Google Scholar
• Yao F, Zhang R, Fu R, He W. 2011. Preventive and therapeutic effects of quercetin on hyperuricemia and renal injury in rats. Wei Sheng Yan Jiu. 40(2):175–177.
   PubMedGoogle Scholar
• Yu L, Gao F, Yang L, Xu L, Wang Z, Ye H. 2012. Biotransformation of puerarin into puerarin-6″-O-phosphate by Bacillus cereus. J Ind Microbiol Biotechnol. 39(2):299–305.
   PubMed Web of Science ®Google Scholar
• Yu S, Hong Q, Wang Y, Hou K, Wang L, Zhang Y, Fu B, Zhou Y, Zheng W, Chen X, et al. 2015. High concentrations of uric acid inhibit angiogenesis via regulation of the Kruppel-like factor 2-vascular endothelial growth factor-A axis by miR-92a. Circ J. 79(11):2487–2498.
   PubMed Web of Science ®Google Scholar
• Yuan H, Ma Q, Cui H, Liu G, Zhao X, Li W, Piao G. 2017. How can synergism of traditional medicines benefit from network pharmacology? Molecules. 22(7):1135–1153.
   PubMed Web of Science ®Google Scholar
• Zhang D, Gao YL, Jiang S, Chen Y, Zhang Y, Pan Z. 2018. The similarity and variability of the iridoid glycoside profile and antioxidant capacity of aerial and underground parts of Lamiophlomis rotata according to UPLC-TOF-MS and multivariate analyses. RSC Adv. 8(5):2459–2468.
   PubMed Web of Science ®Google Scholar
• Zhang T, Qiu F. 2020. Icariin protects mouse insulinoma min6 cell function by activating the PI3K/AKT pathway. Med Sci Monit. 26:e924453.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Pan R, Xu Y, Zhao Y. 2020. Treatment of refractory gout with TNF-alpha antagonist etanercept combined with febuxostat. Ann Palliat Med. 9(6):4332–4338.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Lam TN, Zuo Z. 2013. Radix Puerariae: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol. 53(8):787–811.
   PubMed Web of Science ®Google Scholar
• Zhou X, Zhang B, Zhao X, Lin Y, Wang J, Wang X, Hu N, Wang S. 2021. Chlorogenic acid supplementation ameliorates hyperuricemia, relieves renal inflammation, and modulates intestinal homeostasis. Food Funct. 12(12):5637–5649.
   PubMed Web of Science ®Google Scholar