Abstract
Multi-methods have been developed to control ulcerative colitis. This research targeted to probe that lentinan combined with probiotics suppresses inflammation and oxidative stress responses in a dextran sulfate sodium (DSS)-induced colitis model. A mouse model of colitis was induced through oral administration with 2.5% DSS and treated with lentinan and probiotics independently or in combination. Then, bodyweight and Disease Activity Index (DAI) of mice were determined. Histopathology of colon tissue was analyzed, and apoptosis, inflammation and oxidative stress in the colon tissue of mice were observed. An HT-29 cell model of colitis was established by DSS stimulation and cultured with lentinan and/or probiotics to examine cell proliferation and apoptosis. The data discovered that after DSS induction of colitis, mice developed weight loss, increased DAI score, and shortened the length of colon. Also, severe histopathology of the colon, and increased apoptosis, inflammation and oxidative stress were recognizable. Lentinan could alleviate DSS-induced colitis, and the highest dose was the most significant. Probiotics could also relieve UC in mice, and mixed probiotics had a better therapeutic effect than single probiotics. Lentinan combined with probiotics could further alleviate DSS-induced colitis damage. In addition, lentinan combined with probiotics impaired apoptosis and enhanced proliferation of DSS-treated HT-29 cells. In a word, lentinan combined with probiotics reduces the inflammatory response and oxidative stress of UC.
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The datasets used and/or analyzed during the present study are available from the corresponding author on reasonable request.
References
Chen, Q., Fang, X., Yao, N., Wu, F., Xu, B., & Chen, Z. (2020). Suppression of miR-330-3p alleviates DSS-induced ulcerative colitis and apoptosis by upregulating the endoplasmic reticulum stress components XBP1. Hereditas, 157(1), 18.
Ma, J., Yin, G., Lu, Z., Xie, P., Zhou, H., Liu, J., et al. (2018). Casticin prevents DSS induced ulcerative colitis in mice through inhibitions of NF-κB pathway and ROS signaling. Phytotherapy Research, 32(9), 1770–1783.
Hanauer, S. B. (2006). Inflammatory bowel disease: Epidemiology, pathogenesis, and therapeutic opportunities. Inflammatory Bowel Diseases, 12(Suppl 1), S3-9.
Yu, Y. R., & Rodriguez, J. R. (2017). Clinical presentation of Crohn’s, ulcerative colitis, and indeterminate colitis: Symptoms, extraintestinal manifestations, and disease phenotypes. Seminars in Pediatric Surgery, 26(6), 349–355.
Bamias, G., Corridoni, D., Pizarro, T. T., & Cominelli, F. (2012). New insights into the dichotomous role of innate cytokines in gut homeostasis and inflammation. Cytokine, 59(3), 451–459.
Alexander, K. L., Targan, S. R., & Elson, C. O., 3rd. (2014). Microbiota activation and regulation of innate and adaptive immunity. Immunological Reviews, 260(1), 206–220.
Le Berre, C., Ananthakrishnan, A. N., Danese, S., Singh, S., & Peyrin-Biroulet, L. (2020). Ulcerative colitis and crohn’s disease have similar burden and goals for treatment. Clinical Gastroenterology and Hepatology, 18(1), 14–23.
Eisenstein, M. (2000). Ulcerative colitis: towards remission. Nature, 563(7730), 33.
Mattila, P., Suonpää, K., & Piironen, V. (2000). Functional properties of edible mushrooms. Nutrition, 16(7–8), 694–696.
Liu, Y., Zhao, J., Zhao, Y., Zong, S., Tian, Y., Chen, S., et al. (2019). Therapeutic effects of lentinan on inflammatory bowel disease and colitis-associated cancer. Journal of Cellular and Molecular Medicine, 23(2), 750–760.
Xu, W., Zhang, F., Luo, Y., Ma, L., Kou, X., & Huang, K. (2009). Antioxidant activity of a water-soluble polysaccharide purified from Pteridium aquilinum. Carbohydrate Research, 344(2), 217–222.
Xu, X., Yan, H., Tang, J., Chen, J., & Zhang, X. (2014). Polysaccharides in Lentinus edodes: Isolation, structure, immunomodulating activity and future prospective. Critical Reviews in Food Science and Nutrition, 54(4), 474–487.
Zheng, R., Jie, S., Hanchuan, D., & Moucheng, W. (2005). Characterization and immunomodulating activities of polysaccharide from Lentinus edodes. International Immunopharmacology, 5(5), 811–820.
Masterson, C. H., Murphy, E. J., Gonzalez, H., Major, I., McCarthy, S. D., O’Toole, D., et al. (2020). Purified β-glucans from the Shiitake mushroom ameliorates antibiotic-resistant Klebsiella pneumoniae-induced pulmonary sepsis. Letters in Applied Microbiology, 71(4), 405–412.
Li, X., Zhang, W., Li, P., & Lu, G. (2020). The protective effect and mechanism of lentinan on acute kidney injury in septic rats. Ann Transl Med, 8(14), 883.
Ding, C., Han, F., Xiang, H., Wang, Y., Li, Y., Zheng, J., et al. (2019). Probiotics ameliorate renal ischemia-reperfusion injury by modulating the phenotype of macrophages through the IL-10/GSK-3β/PTEN signaling pathway. Pflugers Archiv. European Journal of Physiology, 471(4), 573–581.
Salim, S. Y., Young, P. Y., Lukowski, C. M., Madsen, K. L., Sis, B., Churchill, T. A., et al. (2013). VSL#3 probiotics provide protection against acute intestinal ischaemia/reperfusion injury. Benef Microbes, 4(4), 357–365.
Deng, B., Wu, J., Li, X., Men, X., & Xu, Z. (2017). Probiotics and probiotic metabolic product improved intestinal function and ameliorated LPS-induced injury in rats. Current Microbiology, 74(11), 1306–1315.
Gong, Z. Y., Yuan, Z. Q., Dong, Z. W., & Peng, Y. Z. (2017). Glutamine with probiotics attenuates intestinal inflammation and oxidative stress in a rat burn injury model through altered iNOS gene aberrant methylation. Am J Transl Res, 9(5), 2535–2547.
Li, B., Ding, Y., Cheng, X., Sheng, D., Xu, Z., Rong, Q., et al. (2020). Polyethylene microplastics affect the distribution of gut microbiota and inflammation development in mice. Chemosphere, 244, 125492.
Derikx, L. A., Dieleman, L. A., & Hoentjen, F. (2016). Probiotics and prebiotics in ulcerative colitis. Best Practice and Research Clinical Gastroenterology, 30(1), 55–71.
Guo, J., Zhang, R., Zhao, Y., & Wang, J. (2021). MiRNA-29c-3p promotes intestinal inflammation via targeting leukemia inhibitory factor in ulcerative colitis. Journal of Inflammation Research, 14, 2031–2043.
Wang, Y., Xie, Q., Zhang, Y., Ma, W., Ning, K., Xiang, J. Y., et al. (2020). Combination of probiotics with different functions alleviate DSS-induced colitis by regulating intestinal microbiota, IL-10, and barrier function. Applied Microbiology and Biotechnology, 104(1), 335–349.
Wei, B., Zhang, R., Zhai, J., Zhu, J., Yang, F., Yue, D., et al. (2018). Suppression of Th17 cell response in the alleviation of dextran sulfate sodium-induced colitis by ganoderma lucidum polysaccharides. Journal of Immunology Research, 2018, 2906494.
Zhu, F., Li, H., Liu, Y., Tan, C., Liu, X., Fan, H., et al. (2020). miR-155 antagomir protect against DSS-induced colitis in mice through regulating Th17/Treg cell balance by Jarid2/Wnt/β-catenin. Biomedicine and Pharmacotherapy, 126, 109909.
Zhao, H. M., Liu, Y., Huang, X. Y., Liu, X. K., Chen, F., Zhang, X. Y., et al. (2019). Pharmacological mechanism of Sishen Wan(®) attenuated experimental chronic colitis by inhibiting wnt/β-catenin pathway. Journal of Ethnopharmacology, 240, 111936.
Moniruzzaman, M., Hasan, K. N., & Maitra, S. K. (2016). Melatonin actions on ovaprim (synthetic GnRH and domperidone)-induced oocyte maturation in carp. Reproduction, 151(4), 285–296.
Liu, X. C., Xu, L., Cai, Y. L., Zheng, Z. Y., Dai, E. N., & Sun, S. (2020). MiR-1207-5p/CX3CR1 axis regulates the progression of osteoarthritis via the modulation of the activity of NF-κB pathway. International Journal of Rheumatic Diseases, 23(8), 1057–1065.
Ai, C., Ma, G., Deng, Y., Zheng, Q., Gen, Y., Li, W., et al. (2020). Nm23-H1 inhibits lung cancer bone-specific metastasis by upregulating miR-660-5p targeted SMARCA5. Thorac Cancer, 11(3), 640–650.
Wang, F., Gu, T., Chen, Y., Chen, Y., Xiong, D., & Zhu, Y. (2021). Long non-coding RNA SOX21-AS1 modulates lung cancer progress upon microRNA miR-24-3p/PIM2 axis. Bioengineered, 12(1), 6724–6737.
Liu, F., Yao, Y., Lu, Z., Zhang, Q., Liu, C., Zhu, C., et al. (2021). 5-Hydroxy-4-methoxycanthin-6-one alleviates dextran sodium sulfate-induced colitis in rats via regulation of metabolic profiling and suppression of NF-κB/p65 signaling pathway. Phytomedicine, 82, 153438.
Suzuki, M., Takatsuki, F., Maeda, Y. Y., Hamuro, J., & Chihara, G. (1994). Antitumor and immunological activity of lentinan in comparison with LPS. International Journal of Immunopharmacology, 16(5–6), 463–468.
Rodríguez-Padilla, Á., Morales-Martín, G., Pérez-Quintero, R., Gómez-Salgado, J., & Ruiz-Frutos, C. (2021). Serological biomarkers and diversion colitis: changes after stimulation with probiotics. Biomolecules, 11(5), 684.
Ungaro, R., Mehandru, S., Allen, P. B., Peyrin-Biroulet, L., & Colombel, J. F. (2017). Ulcerative colitis. Lancet, 389(10080), 1756–1770.
Chinese consensus on diagnosis and treatment in inflammatory bowel disease (2018, Beijing). J Dig Dis. 2021;22(6):298–317.
Itzkowitz, S. (2003). Colon carcinogenesis in inflammatory bowel disease: applying molecular genetics to clinical practice. Journal of Clinical Gastroenterology, 36, S70–S74.
Loynes, C. A., Lee, J. A., Robertson, A. L., Steel, M. J., Ellett, F., Feng, Y., et al. (2018). PGE(2) production at sites of tissue injury promotes an anti-inflammatory neutrophil phenotype and determines the outcome of inflammation resolution in vivo. Science Advances, 4(9), eaar8320.
Duan, S., Du, X., Chen, S., Liang, J., Huang, S., Hou, S., et al. (2020). Effect of vitexin on alleviating liver inflammation in a dextran sulfate sodium (DSS)-induced colitis model. Biomedicine and Pharmacotherapy, 121, 109683.
Cho, Y. E., Mezey, E., Hardwick, J. P., Salem, N., Jr., Clemens, D. L., & Song, B. J. (2017). Increased ethanol-inducible cytochrome P450–2E1 and cytochrome P450 isoforms in exosomes of alcohol-exposed rodents and patients with alcoholism through oxidative and endoplasmic reticulum stress. Hepatol Commun, 1(7), 675–690.
Akanda, M. R., Kim, I. S., Ahn, D., Tae, H. J., Nam, H. H., Choo, B. K., et al. (2018). Anti-inflammatory and gastroprotective roles of rabdosia inflexa through downregulation of pro-inflammatory cytokines and MAPK/NF-κB signaling pathways. International Journal of Molecular Sciences, 19(2), 584.
Wu, T., Wang, J., Zhang, Y., Shao, Y., Li, X., Guo, Y., et al. (2021). Lentinan protects against pancreatic β-cell failure in chronic ethanol consumption-induced diabetic mice via enhancing β-cell antioxidant capacity. Journal of Cellular and Molecular Medicine, 25(13), 6161–6173.
Lin, M., Dong, L., Chen, Q., Xu, H., Han, X., Luo, R., et al. (2021). Lentinan-based oral nanoparticle loaded budesonide with macrophage-targeting ability for treatment of ulcerative colitis. Front Bioeng Biotechnol, 9, 702173.
Peng, L., Zhong, Y., Wang, A., & Jiang, Z. (2019). Probiotics combined with aminosalicylic acid affiliates remission of ulcerative colitis: a meta-analysis of randomized controlled trial. Bioscience Reports, 39(1), BSR20180943.
McFarland, L. V., Surawicz, C. M., Greenberg, R. N., Fekety, R., Elmer, G. W., Moyer, K. A., et al. (1994). A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA, 271(24), 1913–1918.
Plaza-Díaz, J., Ruiz-Ojeda, F. J., Vilchez-Padial, L. M., & Gil, A. (2017). Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients, 9(6), 555.
Guo, X., Chen, J., Yang, J., He, Q., Luo, B., Lu, Y., et al. (2021). Seaweed polysaccharide mitigates intestinal barrier dysfunction induced by enterotoxigenic Escherichia coli through NF-κB pathway suppression in porcine intestinal epithelial cells. J Anim Physiol Anim Nutr (Berl), 105(6), 1063–1074.
Yang, J., Qiu, Y., Hu, S., Zhu, C., Wang, L., Wen, X., et al. (2021). Lactobacillus plantarum inhibited the inflammatory response induced by enterotoxigenic Escherichia coli K88 via modulating MAPK and NF-κB signalling in intestinal porcine epithelial cells. Journal of Applied Microbiology, 130(5), 1684–1694.
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The Science and Technology Development of Shaanxi Province, China (No. 2020SF-334). The Science and Technology Development of Shaanxi Province, China (No. 2021SF-008).
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You, C., Xing, J., Sun, J. et al. Anti-Inflammatory and Anti-Oxidant Impacts of Lentinan Combined with Probiotics in Ulcerative Colitis. Mol Biotechnol (2023). https://doi.org/10.1007/s12033-023-00878-w
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DOI: https://doi.org/10.1007/s12033-023-00878-w