Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 7261619, 14 pages
https://doi.org/10.1155/2018/7261619
Research Article

Modulation of the Gut Microbiota in Rats by Hugan Qingzhi Tablets during the Treatment of High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease

1Department of Pharmacy, Zhujiang Hospital, Southern Medical University, Guangdong, Guangzhou 510282, China
2School of Traditional Chinese Medicine, Southern Medical University, Guangzhou 510515, China
3Department of Pharmacy, Shantou Central Hospital, Affiliated Shantou Hospital of Sun Yat-sen University, Shantou, 515041 Guangdong, China
4Department of Pharmacy, The Seventh Affiliated Hospital of Sun Yat-sen University, Shenzhen, 518107 Guangdong, China

Correspondence should be addressed to Benjie Zhou; moc.361@361jbuohz and Qiang Liu; nc.ude.ums@gnaiquil

Received 15 July 2018; Revised 12 October 2018; Accepted 25 October 2018; Published 23 December 2018

Guest Editor: Mohamed M. Abdel-Daim

Copyright © 2018 Waijiao Tang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Bashiardes, H. Shapiro, S. Rozin, O. Shibolet, and E. Elinav, “Non-alcoholic fatty liver and the gut microbiota,” Molecular Metabolism, vol. 5, no. 9, pp. 782–794, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Zhou, R. A. Hlady, M. J. Schafer et al., “High fat diet and exercise lead to a disrupted and pathogenic DNA methylome in mouse liver,” Epigenetics, vol. 12, no. 1, pp. 55–69, 2017. View at Publisher · View at Google Scholar · View at Scopus
  3. N. G. C. UK, Non-Alcoholic Fatty Liver Disease: Assessment and Management, National Institute for health and care excellence (UK), London, UK, 2016.
  4. B. Hoefert, “Über die bakterienbefunde im duodenalsaft von gesunden und kranken,” Zeitschrift für klinische Medizin, vol. 92, pp. 221–235, 1921. View at Google Scholar
  5. M. Mouzaki, E. M. Comelli, B. M. Arendt et al., “Intestinal microbiota in patients with nonalcoholic fatty liver disease,” Hepatology, vol. 58, no. 1, pp. 120–127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. J. C. Marshall, “The gut as a potential trigger of exercise-induced inflammatory responses,” Canadian Journal of Physiology and Pharmacology, vol. 76, no. 5, pp. 479–484, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. A. J. Wigg, I. C. Roberts-Thomson, R. B. Dymock, P. McCarthy, R. H. Grose, and A. G. Cummins, “The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor α in the pathogenesis of non-alcoholic steatohepatitis,” Gut, vol. 48, no. 2, pp. 206–211, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Miele, V. Valenza, G. La Torre et al., “Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease,” Hepatology, vol. 49, no. 6, pp. 1877–1887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Bai, Y. Zhu, and Y. Dong, “Response of gut microbiota and inflammatory status to bitter melon (Momordica charantia L.) in high fat diet induced obese rats,” Journal of Ethnopharmacology, vol. 194, pp. 717–726, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. S. S. Zhou, J. Xu, H. Zhu et al., “Gut microbiota-involved mechanisms in enhancing systemic exposure of ginsenosides by coexisting polysaccharides in ginseng decoction,” Scientific Reports, vol. 6, no. 1, article 22474, 2016. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Xu, H. B. Chen, and S. L. Li, “Understanding the molecular mechanisms of the interplay between herbal medicines and gut microbiota,” Medicinal Research Reviews, vol. 37, no. 5, pp. 1140–1185, 2017. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. H. M. Al-Tamimi, R. J. Palframan, J. M. Cooper, G. R. Gibson, and R. A. Rastall, “In vitro fermentation of sugar beet arabinan and arabino-oligosaccharides by the human gut microflora,” Journal of Applied Microbiology, vol. 100, no. 2, pp. 407–414, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Wolf, “Gut microbiota: a factor in energy regulation,” Nutrition Reviews, vol. 64, no. 1, pp. 47–50, 2006. View at Publisher · View at Google Scholar
  14. X. Zhang, Y. Zhao, J. Xu et al., “Modulation of gut microbiota by berberine and metformin during the treatment of high-fat diet-induced obesity in rats,” Scientific Reports, vol. 5, no. 1, article 14405, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. P. E. de Resende, S. G. Verza, S. Kaiser, L. F. Gomes, L. C. Kucharski, and G. G. Ortega, “The activity of mate saponins (Ilex paraguariensis) in intra-abdominal and epididymal fat, and glucose oxidation in male Wistar rats,” Journal of Ethnopharmacology, vol. 144, no. 3, pp. 735–740, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. Z. Liu, Z. Chen, H. Guo et al., “The modulatory effect of infusions of green tea, oolong tea, and black tea on gut microbiota in high-fat-induced obese mice,” Food & Function, vol. 7, no. 12, pp. 4869–4879, 2016. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Yin, Y. Q. Luo, H. L. Deng et al., “Hugan Qingzhi medication ameliorates hepatic steatosis by activating AMPK and PPARα pathways in L02 cells and HepG2 cells,” Journal of Ethnopharmacology, vol. 154, no. 1, pp. 229–239, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. W. Tang, L. Zeng, J. J. Yin et al., “Hugan Qingzhi exerts anti-inflammatory effects in a rat model of nonalcoholic fatty liver disease,” Evidence-based Complementary and Alternative Medicine, vol. 2015, Article ID 810369, 13 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. X. Yao, F. Xia, W. Tang, C. Xiao, M. Yang, and B. Zhou, “Isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomics for the investigation of the effect of Hugan Qingzhi on non-alcoholic fatty liver disease in rats,” Journal of Ethnopharmacology, vol. 212, pp. 208–215, 2018. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Wen, X. Guo, R. H. Liu, L. You, A. M. Abbasi, and X. Fu, “Phenolic contents and cellular antioxidant activity of Chinese hawthorn "Crataegus pinnatifida",” Food Chemistry, vol. 186, pp. 54–62, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. W. Tao, N. Yang, J. A. Duan et al., “Simultaneous determination of eleven major flavonoids in the pollen of Typha angustifolia by HPLC-PDA-MS,” Phytochemical Analysis, vol. 22, no. 5, pp. 455–461, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Schneider and M. Blaut, “Anaerobic degradation of flavonoids by Eubacterium ramulus,” Archives of Microbiology, vol. 173, no. 1, pp. 71–75, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. B. J. Zhou, Y. M. Yan, S. X. Huang, Y. F. Yao, and S. Y. Zhang, “The quality standard study on Hugan qingzhi tablets,” Zhong Yao Cai, vol. 35, no. 4, pp. 644–647, 2012. View at Google Scholar
  24. D. E. Kleiner, E. M. Brunt, M. van Natta et al., “Design and validation of a histological scoring system for nonalcoholic fatty liver disease,” Hepatology, vol. 41, no. 6, pp. 1313–1321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Xu, G. Tan, H. Wang, and X. Gai, “Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure,” European Journal of Soil Biology, vol. 74, pp. 1–8, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. P. D. Schloss, D. Gevers, and S. L. Westcott, “Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies,” PLoS One, vol. 6, no. 12, article e27310, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. X. T. Jiang, X. Peng, G. H. Deng et al., “Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland,” Microbial Ecology, vol. 66, no. 1, pp. 96–104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Segata, J. Izard, L. Waldron et al., “Metagenomic biomarker discovery and explanation,” Genome Biology, vol. 12, no. 6, p. R60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. M. G. I. Langille, J. Zaneveld, J. G. Caporaso et al., “Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences,” Nature Biotechnology, vol. 31, no. 9, pp. 814–821, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. D. H. Parks and R. G. Beiko, “Identifying biologically relevant differences between metagenomic communities,” Bioinformatics, vol. 26, no. 6, pp. 715–721, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. P. C. H. Hollman, M. N. C. P. Bijsman, Y. van Gameren, E. P. J. Cnossen, J. H. M. de Vries, and M. B. Katan, “The sugar moiety is a major determinant of the absorption of dietary flavonoid glycosides in man,” Free Radical Research, vol. 31, no. 6, pp. 569–573, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. N. K. Lee, S. H. Choi, S. H. Park, E. K. Park, and D. H. Kim, “Antiallergic activity of hesperidin is activated by intestinal microflora,” Pharmacology, vol. 71, no. 4, pp. 174–180, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. F. Backhed, H. Ding, T. Wang et al., “The gut microbiota as an environmental factor that regulates fat storage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15718–15723, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. P. J. Turnbaugh, R. E. Ley, M. A. Mahowald, V. Magrini, E. R. Mardis, and J. I. Gordon, “An obesity-associated gut microbiome with increased capacity for energy harvest,” Nature, vol. 444, no. 7122, pp. 1027–1031, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Zhou, Q. Pan, F. Z. Xin et al., “Sodium butyrate attenuates high-fat diet-induced steatohepatitis in mice by improving gut microbiota and gastrointestinal barrier,” World Journal of Gastroenterology, vol. 23, no. 1, pp. 60–75, 2017. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Louis, K. P. Scott, S. H. Duncan, and H. J. Flint, “Understanding the effects of diet on bacterial metabolism in the large intestine,” Journal of Applied Microbiology, vol. 102, no. 5, pp. 1197–1208, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. A. L. Kau, P. P. Ahern, N. W. Griffin, A. L. Goodman, and J. I. Gordon, “Human nutrition, the gut microbiome and the immune system,” Nature, vol. 474, no. 7351, pp. 327–336, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Endo, M. Niioka, N. Kobayashi, M. Tanaka, and T. Watanabe, “Butyrate-producing probiotics reduce nonalcoholic fatty liver disease progression in rats: new insight into the probiotics for the gut-liver axis,” PLoS One, vol. 8, no. 5, article e63388, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Beutler and E. T. Rietschel, “Innate immune sensing and its roots: the story of endotoxin,” Nature Reviews. Immunology, vol. 3, no. 2, pp. 169–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. P. D. Cani, J. Amar, M. A. Iglesias et al., “Metabolic endotoxemia initiates obesity and insulin resistance,” Diabetes, vol. 56, no. 7, pp. 1761–1772, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. A. A. Lindberg, A. Weintraub, U. Zahringer, and E. T. Rietschel, “Structure-activity relationships in lipopolysaccharides of Bacteroides fragilis,” Reviews of Infectious Diseases, vol. 12, Supplement_2, pp. S133–S141, 1990. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Nobili, L. Putignani, A. Mosca et al., “Bifidobacteria and lactobacilli in the gut microbiome of children with non-alcoholic fatty liver disease: which strains act as health players?” Archives of Medical Science, vol. 14, no. 1, pp. 81–87, 2018. View at Publisher · View at Google Scholar · View at Scopus
  43. E. A. Griffiths, L. C. Duffy, F. L. Schanbacher et al., “In vivo effects of Bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice,” Digestive Diseases and Sciences, vol. 49, no. 4, pp. 579–589, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. Wang, G. Xiao, Y. Yao, S. Guo, K. Lu, and Z. Sheng, “The role of Bifidobacteria in gut barrier function after thermal injury in rats,” The Journal of Trauma, vol. 61, no. 3, pp. 650–657, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Zhu, S. S. Baker, C. Gill et al., “Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH,” Hepatology, vol. 57, no. 2, pp. 601–609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. S. F. Clarke, E. F. Murphy, O. O’Sullivan et al., “Targeting the microbiota to address diet-induced obesity: a time dependent challenge,” PLoS One, vol. 8, no. 6, article e65790, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Prorok-Hamon, M. K. Friswell, A. Alswied et al., “Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer,” Gut, vol. 63, no. 5, pp. 761–770, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Al-Jashamy, A. Murad, M. Zeehaida, M. Rohaini, and J. Hasnan, “Prevalence of colorectal cancer associated with Streptococcus bovis among inflammatory bowel and chronic gastrointestinal tract disease patients,” Asian Pacific Journal of Cancer Prevention, vol. 11, no. 6, pp. 1765–1768, 2010. View at Google Scholar
  49. L. K. Brahe, E. Le Chatelier, E. Prifti et al., “Specific gut microbiota features and metabolic markers in postmenopausal women with obesity,” Nutrition & Diabetes, vol. 5, no. 6, article e159, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. L. M. Cox, S. Yamanishi, J. Sohn et al., “Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences,” Cell, vol. 158, no. 4, pp. 705–721, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Goffredo, K. Mass, E. J. Parks et al., “Role of gut microbiota and short chain fatty acids in modulating energy harvest and fat partitioning in youth,” The Journal of Clinical Endocrinology and Metabolism, vol. 101, no. 11, pp. 4367–4376, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. M. A. Hildebrandt, C. Hoffmann, S. A. Sherrill–Mix et al., “High-fat diet determines the composition of the murine gut microbiome independently of obesity,” Gastroenterology, vol. 137, no. 5, pp. 1716–1724.e2, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. P. J. Turnbaugh, V. K. Ridaura, J. J. Faith, F. E. Rey, R. Knight, and J. I. Gordon, “The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice,” Science Translational Medicine, vol. 1, no. 6, article 6ra14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. K. B. M. S. Islam, S. Fukiya, M. Hagio et al., “Bile acid is a host factor that regulates the composition of the cecal microbiota in rats,” Gastroenterology, vol. 141, no. 5, pp. 1773–1781, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. G. Kakiyama, W. M. Pandak, P. M. Gillevet et al., “Modulation of the fecal bile acid profile by gut microbiota in cirrhosis,” Journal of Hepatology, vol. 58, no. 5, pp. 949–955, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Degirolamo, S. Modica, G. Palasciano, and A. Moschetta, “Bile acids and colon cancer: solving the puzzle with nuclear receptors,” Trends in Molecular Medicine, vol. 17, no. 10, pp. 564–572, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. D. J. Parks, S. G. Blanchard, R. K. Bledsoe et al., “Bile acids: natural ligands for an orphan nuclear receptor,” Science, vol. 284, no. 5418, pp. 1365–1368, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Baptissart, A. Vega, S. Maqdasy et al., “Bile acids: from digestion to cancers,” Biochimie, vol. 95, no. 3, pp. 504–517, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. J. I. Barrasa, N. Olmo, M. A. Lizarbe, and J. Turnay, “Bile acids in the colon, from healthy to cytotoxic molecules,” Toxicology In Vitro, vol. 27, no. 2, pp. 964–977, 2013. View at Publisher · View at Google Scholar · View at Scopus