Skip to main content

Advertisement

SpringerLink
Log in

Anti-Inflammatory and Anti-Oxidant Impacts of Lentinan Combined with Probiotics in Ulcerative Colitis

  • Original Paper
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

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.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the present study are available from the corresponding author on reasonable request.

References

  1. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. Hanauer, S. B. (2006). Inflammatory bowel disease: Epidemiology, pathogenesis, and therapeutic opportunities. Inflammatory Bowel Diseases, 12(Suppl 1), S3-9.

    Article  PubMed  Google Scholar 

  4. 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.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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.

    Article  PubMed  Google Scholar 

  8. Eisenstein, M. (2000). Ulcerative colitis: towards remission. Nature, 563(7730), 33.

    Article  Google Scholar 

  9. Mattila, P., Suonpää, K., & Piironen, V. (2000). Functional properties of edible mushrooms. Nutrition, 16(7–8), 694–696.

    Article  CAS  PubMed  Google Scholar 

  10. 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.

    Article  CAS  PubMed  Google Scholar 

  11. 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.

    Article  CAS  PubMed  Google Scholar 

  12. 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.

    Article  CAS  PubMed  Google Scholar 

  13. Zheng, R., Jie, S., Hanchuan, D., & Moucheng, W. (2005). Characterization and immunomodulating activities of polysaccharide from Lentinus edodes. International Immunopharmacology, 5(5), 811–820.

    Article  PubMed  Google Scholar 

  14. 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.

    CAS  PubMed  Google Scholar 

  15. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. 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.

    Article  CAS  PubMed  Google Scholar 

  19. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  PubMed  Google Scholar 

  26. 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.

    Article  PubMed  Google Scholar 

  27. 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.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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.

    Article  CAS  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ungaro, R., Mehandru, S., Allen, P. B., Peyrin-Biroulet, L., & Colombel, J. F. (2017). Ulcerative colitis. Lancet, 389(10080), 1756–1770.

    Article  PubMed  Google Scholar 

  35. Chinese consensus on diagnosis and treatment in inflammatory bowel disease (2018, Beijing). J Dig Dis. 2021;22(6):298–317.

  36. Itzkowitz, S. (2003). Colon carcinogenesis in inflammatory bowel disease: applying molecular genetics to clinical practice. Journal of Clinical Gastroenterology, 36, S70–S74.

    Article  CAS  PubMed  Google Scholar 

  37. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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.

    Article  CAS  PubMed  Google Scholar 

  39. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  41. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  43. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

The Science and Technology Development of Shaanxi Province, China (No. 2020SF-334). The Science and Technology Development of Shaanxi Province, China (No. 2021SF-008).

Author information

Authors and Affiliations

  1. Department of Pharmacy, The First Affiliated Hospital of Xi’an Jiaotong University, No. 277 Yanta West Road, Xi’an City, 710061, Shaanxi Province, China

    CuiYu You, JinYao Sun, Di Zhang, Yan Yan & YaLin Dong

  2. School of Pharmacy, Xi’an Jiaotong University, Xi’an City, 710061, Shaanxi Province, China

    JianFeng Xing

Authors
  1. CuiYu You
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. JianFeng Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. JinYao Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Di Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yan Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. YaLin Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to YaLin Dong.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

All animal care and treatment were carried out following the “Guidelines for the Care and Use of Laboratory Animals” issued by the National Institutes of Health and were approved by the Animal Ethics Committee of The First Affiliated Hospital of Xi'an Jiaotong University.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PNG 171 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12033-023-00878-w

Keywords

Search

Navigation