DOI QR코드

DOI QR Code

Anti-Inflammatory Effect of Korean Soybean Sauce (Ganjang) on Mice with Induced Colitis

  • Received : 2024.04.15
  • Accepted : 2024.05.24
  • Published : 2024.07.28

Abstract

Inflammatory bowel disease (IBD), characterized by chronic inflammation of the gut, is caused by several factors. Among these factors, microbial factors are correlated with the gut microbiota, which produces short-chain fatty acids (SCFAs) via anaerobic fermentation. Fermented foods are known to regulate the gut microbiota composition. Ganjang (GJ), a traditional fermented Korean soy sauce consumed worldwide, has been shown to exhibit antioxidant, anticancer, anti-colitis, and antihypertensive activities. However, its effects on the gut microbiota remain unknown. In the present study, we aimed to compare the anti-inflammatory effects of GJ manufactured using different methods and investigate its effect on SCFA production in the gut. To evaluate the anti-inflammatory effects of GJ in the gut, we performed animal experiments using a mouse model of dextran sulfate sodium (DSS)-induced colitis. All GJ samples attenuated DSS-induced colitis symptoms, including reduced colonic length, by suppressing the expression of inflammatory cytokines. In addition, GJ administration modulated SCFA production in the DSS-induced colitis model. Overall, GJ exerted anti-inflammatory effects by reducing DSS-induced symptoms via regulation of inflammation and modulation of SCFA levels in a DSS-induced colitis model. Thus, GJ is a promising fermented food with the potential to prevent IBD.

Keywords

Acknowledgement

This research was supported by Functional research of fermented soybean food (safety monitoring) under the Ministry of Agriculture, Food, and Rural Affairs and partly Korea Agro-Fisheries and Food Trade Corporation in 2023.

References

  1. Rubin DC, Shaker A, Levin MS. 2012. Chronic intestinal inflammation: Inflammatory bowel disease and colitis-associated colon cancer. Front. Immunol. 3: 107. 
  2. Zhang YZ, Li YY. 2014. Inflammatory bowel disease: Pathogenesis. World J. Gastroenterol. 20: 91-99. 
  3. Rieder F, Fiocchi C, Rogler G. 2017. Mechanisms, management, and treatment of fibrosis in patients with inflammatory bowel diseases. Gastroenterology 152: 340-350. 
  4. Guan Q. 2019. A comprehensive review and update on the pathogenesis of inflammatory bowel disease. J. Immunol. Res. 2019: 7247238. 
  5. McDaniel DK, Eden K, Ringel VM, Allen IC. 2016. Emerging roles for noncanonical NF-κB signaling in the modulation of inflammatory bowel disease pathobiology. Inflamm. Bowel Dis. 22: 2265-2279. 
  6. Seyedian SS, Nokhostin F, Malamir MD. 2019. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J. Med. Life 12: 113-122. 
  7. Bryant RV, Brain O, Travis SP. 2015. Conventional drug therapy for inflammatory bowel disease. Scand. J. Gastroenterol. 50: 90-112. 
  8. Lewis JD. 2016. The role of diet in inflammatory bowel disease. Gastroenterol. Hepatol. (NY) 12: 51-53. 
  9. Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54: 2325-2340. 
  10. Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J, Chen ZS. 2022. Microbiota in health and diseases. Signal Transduct. Target. Ther. 7: 135. 
  11. Devanthi PVP, Gkatzionis K. 2019. Soy sauce fermentation: Microorganisms, aroma formation, and process modification. Food Res. Int. 120: 364-374. 
  12. Jang CH, Oh J, Lim JS, Kim HJ, Kim JS. 2021. Fermented soy products: Beneficial potential in neurodegenerative diseases. Foods 10: 636. 
  13. Chun BH, Han DM, Kim HM, Park D, Jeong DM, Kang HA, Jeon CO. 2021. Metabolic features of ganjang (a Korean traditional soy sauce) fermentation revealed by genome-centered metatranscriptomics. mSystems 6: e0044121. 
  14. Kim HR, Park IS, Park SB, Yang HJ, Jeong DY, Kim SY. 2022. Comparison of laxative effects of fermented soybeans (Cheonggukjang) containing toxins and biogenic amines against loperamide-induced constipation mouse model. Nutr. Res. Pract. 16: 435-449. 
  15. Lim HJ, Kim HR, Jeong SJ, Yang HJ, Ryu MS, Jeong DY, Kim SY, Jung CH. 2022. Protective effects of fermented soybeans (cheonggukjang) on dextran sodium sulfate (DSS)-induced colitis in a mouse model. Foods 11: 776. 
  16. Lim HJ, Park IS, Jeong SJ, Ha GS, Yang HJ, Jeong DY, Kim SY, Jung CH. 2023. Effects of cheonggukjang (fermented soybean) on the development of colitis-associated colorectal cancer in mice. Foods 12: 383. 
  17. Kolios G, Valatas V, Ward SG. 2004. Nitric oxide in inflammatory bowel disease: A universal messenger in an unsolved puzzle. Immunology 113: 427-437. 
  18. Pandurangan AK, Mohebali N, Esa NM, Looi CY, Ismail S, Saadatdoust Z. 2015. Gallic acid suppresses inflammation in dextran sodium sulfate-induced colitis in mice: Possible mechanisms. Int. Immunopharmacol. 28: 1034-1043. 
  19. Chelakkot C, Ghim J, Ryu SH. 2018. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp. Mol. Med. 50: 1-9. 
  20. Cong J, Zhou P, Zhang R. 2022. Intestinal microbiota-derived short chain fatty acids in host health and disease. Nutrients 14: 1977. 
  21. Zhang Z, Zhang H, Chen T, Shi L, Wang D, Tang D. 2022. Regulatory role of short-chain fatty acids in inflammatory bowel disease. Cell Commun. Signal. 20: 64. 
  22. Alvarez MA, Moreno-Arribas MV. 2014. The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trends Food Sci. Technol. 39: 146-55. 
  23. Mah JH, Park YK, Jin YH, Lee JH, Hwang HJ. 2019. Bacterial production and control of biogenic amines in Asian fermented soybean foods. Foods 8: 85. 
  24. Leeuwendaal NK, Stanton C, O'Toole PW, Beresford TP. 2022. Fermented foods, health and the gut microbiome. Nutrient 14: 1527. 
  25. Song JL, Choi JH, Seo JH, Lim YI, Park KY. 2014. Anti-colitic effects of kanjangs (fermented soy sauce and sesame sauce) in dextran sulfate sodium-induced colitis in mice. J. Med. Food 17: 1027-1035. 
  26. Nguyen PT, Nguyen-Thi TU, Nguyen HT, Pham MN, Nguyen TT. 2024. Halophilic lactic acid bacteria - Play a vital role in the fermented food industry. Folia Microbiol. (Praha) 69: 305-321. 
  27. Schuerwegh AJ, Dombrecht EJ, Stevens WJ, Van Offel JF, Bridts CH, De Clerck LS. 2003. Influence of pro-inflammatory (IL-1 alpha, IL-6, TNF-alpha, IFN-gamma) and anti-inflammatory (IL-4) cytokines on chondrocyte function. Osteoarthr. Cartil. 11: 681-687. 
  28. Chassaing B. Aitken JD, Malleshappa M, Vijay-Kumar M. 2014. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104: 15.25.1-15.25.14. 
  29. Lee YD, Hong YF, Jeon B, Jung BJ, Chung DK, Kim H. 2016. Differential cytokine regulatory effect of three Lactobacillus strains isolated from fermented foods. J. Microbiol. Biotechnol. 26: 1517-1526. 
  30. Azad MAK, Sarker M, Wan D. 2018. Immunomodulatory effects of probiotics on cytokine profiles. Biomed Res. Int. 2018: 8063647. 
  31. Elkholy SE, Maher SA, Abd El-Hamid NR, Elsayed HA, Hassan WA, Abdelmaogood AKK, et al. 2023. The immunomodulatory effects of probiotics and azithromycin in dextran sodium sulfate-induced ulcerative colitis in rats via TLR4-NF-κB and p38-MAPK pathway. Biomed Pharmacother. 165: 115005. 
  32. Suzuki T. 2020. Regulation of the intestinal barrier by nutrients: The role of tight junctions. Anim. Sci. J. 91: e13357. 
  33. Qiu P, Ishimoto T, Fu L, Zhang J. Zhang Z, Liu Y. 2022. The gut microbiota in inflammatory bowel disease. Front. Cell. Infect. Microbiol. 12: 733992. 
  34. Portincasa P, Bonfrate L, Vacca M, De Angelis M, Farella I, Lanza E, et al. 2022. Gut microbiota and short chain fatty acids: Implications in glucose homeostasis. Int. J. Mol. Sci. 23: 1105. 
  35. Parada Venegas D, De la Fuente MK, Landskron G, Gonzalez MJ, Quera R, Dijkstra G, et al. 2019. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front. Immunol. 10: 277. 
  36. Van Zanten GC, Knudsen A, Roytio H, Forssten S, Lawther M, Blennow A, et al. 2012. The effect of selected synbiotics on microbial composition and short-chain fatty acid production in a model system of the human colon. PLoS One 7: e47212. 
  37. Bell V, Ferrao J, Pimentel L, Pintado M, Fernandes T. 2018. One Health, fermented foods, and gut microbiota. Foods 7: 195.