Skip to main content

Fermented Pueraria Lobata extract ameliorates dextran sulfate sodium-induced colitis by reducing pro-inflammatory cytokines and recovering intestinal barrier function

Abstract

Inflammatory bowel disease is a chronic inflammatory disorder occurring in the gastrointestinal track. However, the efficacy of current therapeutic strategies has been limited and accompanied by side effects. In order to eliminate the limitations, herbal medicines have recently been developed for treatment of IBD. Peuraria Lobata (Peuraria L.) is one of the traditional herbal medicines that have anti-inflammatory effects. Bioavailability of Peuraria L., which is rich in isoflavones, is lower than that of their fermented forms. In this study, we generated fermented Peuraria L. extracts (fPue) and investigated the role of fPue in inflammation and intestinal barrier function in vitro and in vivo. As the mice or intestinal epithelial cells were treated with DSS/fPue, mRNA expression of pro-inflammatory cytokines was reduced and the architecture and expression of tight junction proteins were recovered, compared to the DSS-treated group. In summary, fPue treatment resulted in amelioration of DSS-induced inflammation in the colon, and the disrupted intestinal barrier was recovered as the expression and architecture of tight junction proteins were retrieved. These results suggest that use of fPue could be a new therapeutic strategy for treatment of IBD.

References

  1. 1.

    Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012; 142(1): 46–54.

    Article  Google Scholar 

  2. 2.

    Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet 2007; 369(9573): 1627–1640.

    CAS  Article  Google Scholar 

  3. 3.

    Walker JR, Ediger JP, Graff LA, Greenfeld JM, Clara I, Lix L, Rawsthorne P, Miller N, Rogala L, McPhail CM, Bernstein CN. The Manitoba IBD cohort study: a population-based study of the prevalence of lifetime and 12-month anxiety and mood disorders. Am J Gastroenterol 2008; 103(8): 1989–1997.

    Article  Google Scholar 

  4. 4.

    Goodhand JR, Wahed M, Mawdsley JE, Farmer AD, Aziz Q, Rampton DS. Mood disorders in inflammatory bowel disease: relation to diagnosis, disease activity, perceived stress, and other factors. Inflamm Bowel Dis 2012; 18(12): 2301–2309.

    CAS  Article  Google Scholar 

  5. 5.

    Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004; 287(1): G7–G17.

    CAS  Article  Google Scholar 

  6. 6.

    Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of populationbased cohort studies. Clin Gastroenterol Hepatol 2012; 10(6): 639–645.

    Article  Google Scholar 

  7. 7.

    Reinecker HC, Steffen M, Witthoeft T, Pflueger I, Schreiber S, MacDermott RP, Raedler A. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn’s disease. Clin Exp Immunol 1993; 94(1): 174–181.

    CAS  Article  Google Scholar 

  8. 8.

    Fries W, Renda MC, Lo Presti MA, Raso A, Orlando A, Oliva L, Giofre MR, Maggio A, Mattaliano A, Macaluso A, Cottone M. Intestinal permeability and genetic determinants in patients, firstdegree relatives, and controls in a high-incidence area of Crohn’s disease in Southern Italy. Am J Gastroenterol 2005; 100(12): 2730–2736.

    CAS  Article  Google Scholar 

  9. 9.

    Reuter BK, Pizarro TT. Mechanisms of tight junction dysregulation in the SAMP1/YitFc model of Crohn’s disease-like ileitis. Ann N Y Acad Sci 2009; 1165: 301–307.

    CAS  Article  Google Scholar 

  10. 10.

    Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn’s disease. Gut 2007; 56(1): 61–72.

    CAS  Article  Google Scholar 

  11. 11.

    Bruewer M, Samarin S, Nusrat A. Inflammatory bowel disease and the apical junctional complex. Ann N Y Acad Sci 2006; 1072: 242–252.

    CAS  Article  Google Scholar 

  12. 12.

    Zareie M, Johnson-Henry K, Jury J, Yang PC, Ngan BY, McKay DM, Soderholm JD, Perdue MH, Sherman PM. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 2006; 55(11): 1553–1560.

    CAS  Article  Google Scholar 

  13. 13.

    Fakhoury M, Negrulj R, Mooranian A, Al-Salami H. Inflammatory bowel disease: clinical aspects and treatments. J Inflamm Res 2014; 7: 113–120.

    Article  Google Scholar 

  14. 14.

    Peyrin-Biroulet L, Lemann M. Review article: remission rates achievable by current therapies for inflammatory bowel disease. Aliment Pharmacol Ther 2011; 33(8): 870–879.

    CAS  Article  Google Scholar 

  15. 15.

    Clark M, Colombel JF, Feagan BC, Fedorak RN, Hanauer SB, Kamm MA, Mayer L, Regueiro C, Rutgeerts P, Sandborn WJ, Sands BE, Schreiber S, Targan S, Travis S, Vermeire S. American gastroenterological association consensus development conference on the use of biologics in the treatment of inflammatory bowel disease, June 21–23, 2006. Gastroenterology 2007; 133(1): 312–339.

    Article  Google Scholar 

  16. 16.

    Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol 2014; 14(5): 329–342.

    CAS  Article  Google Scholar 

  17. 17.

    Gisbert JP, Panes J. Loss of response and requirement of infliximab dose intensification in Crohn’s disease: a review. Am J Gastroenterol 2009; 104(3): 760–767.

    CAS  Article  Google Scholar 

  18. 18.

    Billioud V, Sandborn WJ, Peyrin-Biroulet L. Loss of response and need for adalimumab dose intensification in Crohn’s disease: a systematic review. Am J Gastroenterol 2011; 106(4): 674–684.

    CAS  Article  Google Scholar 

  19. 19.

    Langmead L, Rampton DS. Review article: complementary and alternative therapies for inflammatory bowel disease. Aliment Pharmacol Ther 2006; 23(3): 341–349.

    CAS  Article  Google Scholar 

  20. 20.

    Jackson LN, Zhou Y, Qiu S, Wang Q, Evers BM. Alternative medicine products as a novel treatment strategy for inflammatory bowel disease. Am J Chin Med 2008; 36(5): 953–965.

    Article  Google Scholar 

  21. 21.

    Jun M, Hong J, Jeong WS, Ho CT. Suppression of arachidonic acid metabolism and nitric oxide formation by kudzu isoflavones in murine macrophages. Mol Nutr Food Res 2005; 49(12): 1154–1159.

    CAS  Article  Google Scholar 

  22. 22.

    Bebrevska L, Foubert K, Hermans N, Chatterjee S, Van Marck E, De Meyer G, Vlietinck A, Pieters L, Apers S. In vivo antioxidative activity of a quantified Pueraria lobata root extract. J Ethnopharmacol 2010; 127(1): 112–117.

    Article  Google Scholar 

  23. 23.

    Jiang RW, Lau KM, Lam HM, Yam WS, Leung LK, Choi KL, Waye MM, Mak TC, Woo KS, Fung KP. A comparative study on aqueous root extracts of Pueraria thomsonii and Pueraria lobata by antioxidant assay and HPLC fingerprint analysis. J Ethnopharmacol 2005; 96(1–2): 133–138.

    Article  Google Scholar 

  24. 24.

    Izumi T, Piskula MK, Osawa S, Obata A, Tobe K, Saito M, Kataoka S, Kubota Y, Kikuchi M. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr 2000; 130(7): 1695–1699.

    CAS  Article  Google Scholar 

  25. 25.

    Boismenu R, Chen Y. Insights from mouse models of colitis. J Leukoc Biol 2000; 67(3): 267–278.

    CAS  Article  Google Scholar 

  26. 26.

    Nishiyama Y, Kataoka T, Yamato K, Taguchi T, Yamaoka K. Suppression of dextran sulfate sodium-induced colitis in mice by radon inhalation. Mediators Inflamm 2012; 2012: 239617.

    Article  Google Scholar 

  27. 27.

    Stillie R, Stadnyk AW. Role of TNF receptors, TNFR1 and TNFR2, in dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 2009; 15(10): 1515–1525.

    Article  Google Scholar 

  28. 28.

    Stevceva L, Pavli P, Husband AJ, Doe WF. The inflammatory infiltrate in the acute stage of the dextran sulphate sodium induced colitis: B cell response differs depending on the percentage of DSS used to induce it. BMC Clin Pathol 2001; 1(1): 3.

    Article  Google Scholar 

  29. 29.

    Samak G, Chaudhry KK, Gangwar R, Narayanan D, Jaggar JH, Rao R. Calcium/Ask1/MKK7/JNK2/c-Src signalling cascade mediates disruption of intestinal epithelial tight junctions by dextran sulfate sodium. Biochem J 2015; 465(3): 503–515.

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was conducted under the industrial infrastructure program (No. N0000888) for fundamental technologies, which is funded by the Ministry of Trade, Industry, and Energy (MOTIE, Korea), and also supported by High Value-added Food Technology Development Program 114006-04, Ministry of Agriculture, Food and Rural Affairs.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Seung Hyun Oh.

Electronic supplementary material

Rights and permissions

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Choi, S., Woo, J., Jang, Y. et al. Fermented Pueraria Lobata extract ameliorates dextran sulfate sodium-induced colitis by reducing pro-inflammatory cytokines and recovering intestinal barrier function. Lab Anim Res 32, 151–159 (2016). https://doi.org/10.5625/lar.2016.32.3.151

Download citation

Keywords

  • IBD
  • herbal medicines
  • Pueraria Lobata
  • inflammation
  • intestinal barrier