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Aqueous Extract of Lysimachia christinae Hance Prevents Cholesterol Gallstone in Mice by Affecting the Intestinal Microflora

  • Liu, Shijia (First Clinical College, Chongqing Medical University) ;
  • Luorong, Quji (College of Traditional Chinese Medicine, Chongqing Medical University) ;
  • Hu, Kaizhi (Chongqing Institute of Pharmaceutical Plant) ;
  • Cao, Weiguo (College of Traditional Chinese Medicine, Chongqing Medical University) ;
  • Tao, Wei (College of Traditional Chinese Medicine, Chongqing Medical University) ;
  • Liu, Handeng (Laboratory of Tissue and Cell Biology, Experimental Teaching Center, Chongqing Medical University) ;
  • Zhang, Dan (College of Traditional Chinese Medicine, Chongqing Medical University)
  • Received : 2021.06.15
  • Accepted : 2021.07.13
  • Published : 2021.09.28

Abstract

With changes in human dietary patterns, the proportion of high-fat and high-cholesterol foods in the daily diet has increased. As a result, the incidence rate of cholelithiasis is increasing rapidly. Many studies have reported on the crucial role that the intestinal microflora plays in the progression of gallstones. Although the whole herb of Lysimachia christinae, a traditional Chinese medicine, has long been extensively used as a remedy for cholelithiasis in China, its effects on the intestinal microflora remain unknown. Hence, in this study, we investigated the ability of the aqueous extract of L. christinae (LAE) to prevent cholesterol gallstones (CGSs) in model animals by affecting the intestinal microflora. The effects of LAE on body weight, serum lipid profile, visceral organ indexes, and histomorphology were studied in male C57BL/6J mice, which were induced by a lithogenic diet. After the 8-week study, CGSs formation was greatly reduced after LAE treatment. LAE also reduced body weight gain and hyperlipidemia and restored the histomorphological changes. Moreover, the intestinal microflora exhibited significant variation. In the model group fed the lithogenic diet, the abundances of the genera unclassified Porphyromonadaceae, Lactobacillus and Alloprevotella decreased, but in contrast, Akkermansia dramatically increased compared with the control check group, which was fed a normal diet; the administration of LAE reversed these changes. These results imply that L. christinae can be considered an efficient therapy for eliminating CGSs induced by a high-fat and high-cholesterol diet, which may be achieved by influencing the intestinal microflora.

Keywords

Acknowledgement

This research is funded by the Chongqing Technology Innovation and Application Demonstration Project (Grant No. cstc2017shmsA130014, cstc2018jscx-mszd0007 and cstc2019jscx-gksbX0010) and the Important Science and Technology Research Projects for Forestry of Chongqing (Grant No. 2018-3).

References

  1. Hu FL, Chen HT, Guo FF, Yang M, Jiang X, Yu JH, et al. 2021. Biliary microbiota and mucin 4 impact the calcification of cholesterol gallstones. Hepatobiliary Pancreat. Dis. Int. 20: 61-66. https://doi.org/10.1016/j.hbpd.2020.12.002
  2. Deng J, Ren ML, Dai XQ, Qu DH, Yang MX, Zhang T, et al. 2015. Lysimachia christinae Hance regresses preestablished cholesterol gallstone in mice. J. Ethnopharmacol. 166: 102-108. https://doi.org/10.1016/j.jep.2015.03.031
  3. van Dooren I, Faouzi ME, Foubert K, Theunis M, Pieters L, Cherrah Y, et al. 2015. Cholesterol lowering effect in the gall bladder of dogs by a standardized infusion of Herniaria hirsuta L. J. Ethnopharmacol. 169: 69-75. https://doi.org/10.1016/j.jep.2015.03.081
  4. Verpoorte R, Houghton PJ, Heinrich M, Mukherjee PK, Hirschmann GS, van Staden J, et al. 2006. Editorial. J. Ethnopharmacol. 103: 309-310. https://doi.org/10.1016/j.jep.2005.12.008
  5. Reshetnyak VI. 2012. Concept of the pathogenesis and treatment of cholelithiasis. World J. Hepatol. 4: 18-34. https://doi.org/10.4254/wjh.v4.i2.18
  6. Blottiere HM, Dore J. 2016. Impact of newly developed metagenomic tools on our knowledge of the gut microbiota and its role in human health: diagnostic and therapeutic issues. Med. Sci. 32: 944-951.
  7. Conlon MA, Bird AR. 2015. The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7: 17-44. https://doi.org/10.3390/nu7010017
  8. Gao Y, Liu C, Li J, Zhai Y, Lin M, Wu Q, et al. 2020. Efficacy of Lidan Tang on high-fat-diet induced gallstone in mice and possible mechanism. J. Tradit. Chin. Med. 40: 584-592.
  9. Li Y, Gao X-X, Qin X-M. 2020. Advances in research of traditional Chinese medicine for promoting bile secretion and excretion. Zhongguo zhong. Yao Za Zhi 45: 1287-1296.
  10. Chen QL, Zhang YY, Li SA, Chen SJ, Lin XJ, Li CD, et al. 2019. Mechanisms underlying the prevention and treatment of cholelithiasis using traditional chinese medicine. Evid. Based Complement. Alternat. Med. 2019: 2536452.
  11. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998. https://doi.org/10.1038/nmeth.2604
  12. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41: D590-D596.
  13. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73: 5261-5267. https://doi.org/10.1128/AEM.00062-07
  14. vanBerge-Henegouwen GP, Venneman NG, Portincasa P, Kosters A, van Erpecum KJ, Groen AK. 2004. Relevance of hereditary defects in lipid transport proteins for the pathogenesis of cholesterol gallstone disease. Scand. J. Gastroenterol. 241: 60-69.
  15. Jayachandran M, Chen JL, Chung SSM, Xu BJ. 2018. A critical review on the impacts of beta-glucans on gut microbiota and human health. J. Nutr. Biochem. 61: 101-110. https://doi.org/10.1016/j.jnutbio.2018.06.010
  16. Kanmani P, Suganya K, Kim H. 2020. The gut microbiota: how does it influence the development and progression of liver diseases. Biomedicines 8: 501. https://doi.org/10.3390/biomedicines8110501
  17. Kelly D, Conway S, Aminov R. 2005. Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol. 26: 326-333. https://doi.org/10.1016/j.it.2005.04.008
  18. Olmo BGM, Butler MJ, Barrientos RM. 2021. Evolution of the human diet and its impact on gut microbiota, immune responses, and brain health. Nutrients 13: 16.
  19. Zhang N, Ju ZJ, Zuo T. 2018. Time for food: The impact of diet on gut microbiota and human health. Nutrition 51-52: 80-85. https://doi.org/10.1016/j.nut.2017.12.005
  20. Oyri SF, Muzes G, Sipos F. 2015. Dysbiotic gut microbiome: a key element of Crohn's disease. Comp. Immunol. Microbiol. Infect. Dis. 43: 36-49. https://doi.org/10.1016/j.cimid.2015.10.005
  21. Leung JSM. 2020. Circulating intestinal bacteria as a biological marker for colonic cancer. Hong Kong Med. J. 26: 353-353. https://doi.org/10.12809/hkmj198299
  22. Chen XP, Devaraj S. 2018. Gut microbiome in obesity, metabolic syndrome, and diabetes. Curr. Diab. Rep. 18: 129. https://doi.org/10.1007/s11892-018-1104-3
  23. Kolodziejczyk AA, Zheng D, Shibolet O, Elinav E. 2019. The role of the microbiome in NAFLD and NASH. EMBO Mol. Med. 11: e9302. https://doi.org/10.15252/emmm.201809302
  24. Tomasello G, Bellavia M, Palumbo VD, Gioviale MC, Damiani P, Lo Monte AI. 2011. From gut microflora imbalance to mycobacteria infection: is there a relationship with chronic intestinal inflammatory diseases? Ann. Ital. Chir. 82: 361-368.
  25. Clemente JC, Ursell LK, Parfrey LW, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270. https://doi.org/10.1016/j.cell.2012.01.035
  26. Gerard P, Lepercq P, Leclerc M, Gavini F, Raibaud P, Juste C. 2007. Bacteroides sp. strain D8, the first cholesterol-reducing bacterium isolated from human feces. Appl. Environ. Microbiol. 73: 5742-5749. https://doi.org/10.1128/AEM.02806-06
  27. Gutierrez-Diaz I, Molinero N, Cabrera A, Rodriguez JI, Margolles A, Delgado S, et al. 2018. Diet: cause or consequence of the microbial profile of cholelithiasis disease? Nutrients 10: 13. https://doi.org/10.3390/nu10010013
  28. Wang L, Guo M-J, Gao Q, Yang J-F, Yang L, Pang X-L, et al. 2018. The effects of probiotics on total cholesterol A meta-analysis of randomized controlled trials. Medicine 97: e9679. https://doi.org/10.1097/MD.0000000000009679
  29. Pereira DIA, Gibson GR. 2002. Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl. Environ. Microbiol. 68: 4689-4693. https://doi.org/10.1128/AEM.68.9.4689-4693.2002
  30. Wang QH, Jiao L, He CQ, Sun HD, Cai Q, Han TQ, et al. 2017. Alteration of gut microbiota in association with cholesterol gallstone formation in mice. BMC Gastroenterol. 17: 74. https://doi.org/10.1186/s12876-017-0629-2
  31. Zhang Z, Li D. 2018. Thermal processing of food reduces gut microbiota diversity of the host and triggers adaptation of the microbiota: evidence from two vertebrates. Microbiome 6: 99 https://doi.org/10.1186/s40168-018-0471-y
  32. Ghetti FdF, Oliveira DG, de Oliveira JM, Vieira de Castro Ferreira LEV, Cesar DE, Boroni Moreira AP. 2018. Influence of gut microbiota on the development and progression of nonalcoholic steatohepatitis. Eur. J. Nutr. 57: 861-876. https://doi.org/10.1007/s00394-017-1524-x
  33. Wang Q, Hao C, Yao W, Zhu D, Lu H, Li L, et al. 2020. Intestinal flora imbalance affects bile acid metabolism and is associated with gallstone formation. BMC Gastroenterol. 20: 59. https://doi.org/10.1186/s12876-020-01195-1
  34. Donovan SM. 2017. Introduction to the special focus issue on the impact of diet on gut microbiota composition and function and future opportunities for nutritional modulation of the gut microbiome to improve human health. Gut Microbes 8: 75-81. https://doi.org/10.1080/19490976.2017.1299309