Haochen Hui, Zhuoya Wang, Xuerong Zhao, Lina Xu, Lianhong Yin, Feifei Wang, Liping Qu, Jinyong Peng. Gut microbiome-based thiamine metabolism contributes to the protective effect of one acidic polysaccharide from Selaginella uncinata (Desv.) Spring against inflammatory bowel disease[J]. Journal of Pharmaceutical Analysis, 2024, 14(2): 177-195. doi: 10.1016/j.jpha.2023.08.003
Citation: Haochen Hui, Zhuoya Wang, Xuerong Zhao, Lina Xu, Lianhong Yin, Feifei Wang, Liping Qu, Jinyong Peng. Gut microbiome-based thiamine metabolism contributes to the protective effect of one acidic polysaccharide from Selaginella uncinata (Desv.) Spring against inflammatory bowel disease[J]. Journal of Pharmaceutical Analysis, 2024, 14(2): 177-195. doi: 10.1016/j.jpha.2023.08.003

Gut microbiome-based thiamine metabolism contributes to the protective effect of one acidic polysaccharide from Selaginella uncinata (Desv.) Spring against inflammatory bowel disease

doi: 10.1016/j.jpha.2023.08.003
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The authors gratefully acknowledge the funding from the Spring City Plan of the High-Level Talent Promotion and Training Project of Kunming, China (Grant No.: 2022SCP008) and the Independent Research Fund of Yunnan Characteristic Plant Extraction Laboratory, China (Grant No.: 2022YKZY001).

  • Received Date: Apr. 16, 2023
  • Accepted Date: Aug. 07, 2023
  • Rev Recd Date: Jul. 28, 2023
  • Available Online: Mar. 08, 2024
  • Publish Date: Feb. 29, 2024
  • Inflammatory bowel disease (IBD) is a serious disorder, and exploration of active compounds to treat it is necessary. An acidic polysaccharide named SUSP-4 was purified from Selaginella uncinata (Desv.) Spring, which contained galacturonic acid, galactose, xylose, arabinose, and rhamnose with the main chain structure of →4)-α-d-GalAp-(1→ and →6)-β-d-Galp-(1→ and the branched structure of →5)-α-l-Araf-(1→ . Animal experiments showed that compared with Model group, SUSP-4 significantly improved body weight status, disease activity index (DAI), colonic shortening, and histopathological damage, and elevated occludin and zonula occludens protein 1 (ZO-1) expression in mice induced by dextran sulfate sodium salt (DSS). 16S ribosomal RNA (rRNA) sequencing indicated that SUSP-4 markedly downregulated the level of Akkermansia and Alistipes. Metabolomics results confirmed that SUSP-4 obviously elevated thiamine levels compared with Model mice by adjusting thiamine metabolism, which was further confirmed by a targeted metabolism study. Fecal transplantation experiments showed that SUSP-4 exerted an anti-IBD effect by altering the intestinal flora in mice. A mechanistic study showed that SUSP-4 markedly inhibited macrophage activation by decreasing the levels of phospho-nuclear factor kappa-B (p-NF-κB) and cyclooxygenase-2 (COX-2) and elevating NF-E2-related factor 2 (Nrf2) levels compared with Model group. In conclusion, SUSP-4 affected thiamine metabolism by regulating Akkermania and inhibited macrophage activation to adjust NF-κB/Nrf2/COX-2-mediated inflammation and oxidative stress against IBD. This is the first time that plant polysaccharides have been shown to affect thiamine metabolism against IBD, showing great potential for in-depth research and development applications.
  • [1]
    G.G. Kaplan, The global burden of IBD: from 2015 to 2025, Nat. Rev. Gastroenterol. Hepatol. 12 (2015) 720-727.
    [2]
    G.P. Ramos, K.A. Papadakis, Mechanisms of disease: inflammatory bowel diseases, Mayo Clin. Proc. 94 (2019) 155-165.
    [3]
    J. Ni, G.D. Wu, L. Albenberg, et al., Gut microbiota and IBD: causation or correlation? Nat. Rev. Gastroenterol. Hepatol. 14 (2017) 573-584.
    [4]
    B. Al-Bawardy, R. Shivashankar, D.D. Proctor, Novel and emerging therapies for inflammatory bowel disease, Front. Pharmacol. 12 (2021), 651415.
    [5]
    E.K. Wright, N.S. Ding, O. Niewiadomski, Management of inflammatory bowel disease, MJA (Med. J. Aust.). 209 (2018) 318-323.
    [6]
    M.R. Kudelka, S.R. Stowell, R.D. Cummings, et al., Intestinal epithelial glycosylation in homeostasis and gut microbiota interactions in IBD, Nat. Rev. Gastroenterol. Hepatol. 17 (2020) 597-617.
    [7]
    J.R. Marchesi, D.H. Adams, F. Fava, et al., The gut microbiota and host health: a new clinical frontier, Gut. 65 (2016) 330-339.
    [8]
    J.K. Nicholson, E. Holmes, J. Kinross, et al., Host-gut microbiota metabolic interactions, Science. 336 (2012) 1262-1267.
    [9]
    G. Ye, J. Li, J. Zhang, et al., Structural characterization and antitumor activity of a polysaccharide from Dendrobium wardianum, Carbohydr. Polym. 269 (2021), 118253.
    [10]
    S. Zhou, G. Huang, G. Chen, Extraction, structural analysis, derivatization and antioxidant activity of polysaccharide from Chinese yam, Food Chem. 361 (2021), 130089.
    [11]
    Y. Liu, Y. Ye, X. Hu, et al., Structural characterization and anti-inflammatory activity of a polysaccharide from the lignified okra, Carbohydr. Polym. 265 (2021), 118081.
    [12]
    T. Xia, C.-S. Liu, Y.-N. Hu, et al., Coix seed polysaccharides alleviate type 2 diabetes mellitus via gut microbiota-derived short-chain fatty acids activation of IGF1/PI3K/AKT signaling, Food Res. Int. 150 (2021), 110717.
    [13]
    G. Ma, Q. Xu, H. Du, et al., Characterization of polysaccharide from Pleurotus eryngii during simulated gastrointestinal digestion and fermentation, Food Chem. 370 (2022), 131303.
    [14]
    L. Cui, X. Guan, W. Ding, et al., Scutellaria baicalensis Georgi polysaccharide ameliorates DSS-induced ulcerative colitis by improving intestinal barrier function and modulating gut microbiota, Int. J. Biol. Macromol. 166 (2021) 1035-1045.
    [15]
    C. Guo, D. Guo, L. Fang, et al., Ganoderma lucidum polysaccharide modulates gut microbiota and immune cell function to inhibit inflammation and tumorigenesis in colon, Carbohydr. Polym. 267 (2021), 118231.
    [16]
    C. Guo, Y. Wang, S. Zhang, et al., Crataegus pinnatifida polysaccharide alleviates colitis via modulation of gut microbiota and SCFAs metabolism, Int. J. Biol. Macromol. 181 (2021) 357-368.
    [17]
    C. Liu, B. Hu, Y. Cheng, et al., In-depth analysis of the mechanisms of aloe polysaccharides on mitigating subacute colitis in mice via microbiota informatics, Carbohydr. Polym. 265 (2021), 118041.
    [18]
    X.-N. Wu, Y. Yang, H.-H. Zhang, et al., Robustaflavone-4′-dimethyl ether from Selaginella uncinata attenuated lipopolysaccharide-induced acute lung injury via inhibiting FLT3-mediated neutrophil activation, Int. Immunopharm. 82 (2020), 106338.
    [19]
    J. Xu, L. Yang, R. Wang, et al., The biflavonoids as protein tyrosine phosphatase 1B inhibitors from Selaginella uncinata and their antihyperglycemic action, Fitoterapia. 137 (2019), 104255.
    [20]
    J. Zheng, Y. Zheng, H. Zhi, et al., Two new steroidal saponins from Selaginella uncinata (Desv.) Spring and their protective effect against anoxia, Fitoterapia. 88 (2013) 25-30.
    [21]
    H. Hui, M. Gao, X. Zhao, et al., Three water soluble polysaccharides with anti-inflammatory activities from Selaginella uncinata (Desv.) Spring, Int. J. Biol. Macromol. 222 (2022) 1983-1995.
    [22]
    Z. Wu, S. Huang, T. Li, et al., Gut microbiota from green tea polyphenol-dosed mice improves intestinal epithelial homeostasis and ameliorates experimental colitis, Microbiome. 9(1) (2021) 184-184.
    [23]
    E.J. Want, I.D. Wilson, H. Gika, et al., Global metabolic profiling procedures for urine using UPLC-MS, Nat. Protoc. 5 (2010) 1005-1018.
    [24]
    W.B. Dunn, D. Broadhurst, P. Begley, et al., Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry, Nat. Protoc. 6 (2011) 1060-1083.
    [25]
    T. Kind, G. Wohlgemuth, D.Y. Lee, et al., FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry, Anal. Chem. 81 (2009) 10038-10048.
    [26]
    J. Wang, T. Zhang, X. Shen, et al., Serum metabolomics for early diagnosis of esophageal squamous cell carcinoma by UHPLC-QTOF/MS, Metabolomics. 12 (2016), 116.
    [27]
    S. Wang, L. Ni, X. Fu, et al., A sulfated polysaccharide from saccharina japonica suppresses LPS-induced inflammation both in a macrophage cell model via blocking MAPK/NF-κB signal pathways in vitro and a zebrafish model of embryos and larvae in vivo, Mar. Drugs 18 (2020), 593.
    [28]
    Li T, Bai J, Du Y, Tan P, et al., Thiamine pretreatment improves endotoxemia-related liver injury and cholestatic complications by regulating galactose metabolism and inhibiting macrophage activation, Int. Immunopharm. 108 (2022), 108892.
    [29]
    S.F. Barbieri, S. da Costa Amaral, E. Mazepa, et al., Isolation, NMR characterization and bioactivity of a (4-O-methyl-α-D-glucurono)-β-D-xylan from Campomanesia xanthocarpa Berg fruits, Int. J. Biol. Macromol. 207 (2022) 893-904.
    [30]
    T. Komatsu, J. Kikuchi, Comprehensive signal assignment of 13C-labeled lignocellulose using multidimensional solution NMR and 13C chemical shift comparison with solid-state NMR, Anal. Chem. 85 (2013) 8857-8865.
    [31]
    Z. Sheng, L. Wen, B. Yang, Structure identification of a polysaccharide in mushroom Lingzhi spore and its immunomodulatory activity, Carbohydr. Polym. 278 (2022), 118939.
    [32]
    K. Zhao, B. Li, D. He, et al., Chemical characteristic and bioactivity of hemicellulose-based polysaccharides isolated from Salvia miltiorrhiza, Int. J. Biol. Macromol. 165 (2020) 2475-2483.
    [33]
    A.A.S. de Sousa, N.M.B. Benevides, A. de Freitas Pires, et al., A report of a galactan from marine alga Gelidium crinale with in vivo anti-inflammatory and antinociceptive effects, Fund. Clin. Pharmacol. 27 (2013) 173-180.
    [34]
    M. Zou, X. Hu, Y. Wang, et al., Structural characterization and anti-inflammatory activity of a pectin polysaccharide HBHP-3 from Houttuynia cordata, Int. J. Biol. Macromol. 210 (2022) 161-171.
    [35]
    M. Argollo, D. Gilardi, C. Peyrin-Biroulet, et al., Comorbidities in inflammatory bowel disease: a call for action, Lancet Gastroenterol. Hepatol. 4 (2019) 643-654.
    [36]
    B. Chami, N.J.J. Martin, J.M. Dennis, et al., Myeloperoxidase in the inflamed colon: a novel target for treating inflammatory bowel disease, Arch. Biochem. Biophys. 645 (2018) 61-71.
    [37]
    A. dos Santos Ramos, G.C.S. Viana, M. de Macedo Brigido, et al., Neutrophil extracellular traps in inflammatory bowel diseases: implications in pathogenesis and therapeutic targets, Pharmacol. Res. 171 (2021), 105779.
    [38]
    K. Matsuoka, T. Kanai, The gut microbiota and inflammatory bowel disease, Semin. Immunopathol. 37(1) (2015) 47-55.
    [39]
    P.D. Cani, C. Depommier, M. Derrien, et al., Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms, Nat. Rev. Gastroenterol. Hepatol. 19 (2022) 625-637.
    [40]
    C. Belzer, L.W. Chia, S. Aalvink, et al., Microbial metabolic networks at the Mucus Layer lead to diet-independent butyrate and vitamin B(12) production by intestinal symbionts, mBio. 8 (2017), e00770.
    [41]
    R. Caesar, V. Tremaroli, P. Kovatcheva-Datchary, et al., Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling, Cell Metabol. 22 (2015) 658-668.
    [42]
    Y. Zhao, H. Chen, W. Li, et al., Selenium-containing tea polysaccharides ameliorate DSS-induced ulcerative colitis via enhancing the intestinal barrier and regulating the gut microbiota, Int. J. Biol. Macromol. 209 (2022) 356-366.
    [43]
    Y. Ren, Y. Geng, Y. Du, et al., Polysaccharide of Hericium erinaceus attenuates colitis in C57BL/6 mice via regulation of oxidative stress, inflammation-related signaling pathways and modulating the composition of the gut microbiota, J. Nutr. Biochem. 57 (2018) 67-76.
    [44]
    M.M. Rinschen, J. Ivanisevic, M. Giera, et al., Identification of bioactive metabolites using activity metabolomics, Nat. Rev. Mol. Cell Biol. 20 (2019) 353-367.
    [45]
    L. Su, C. Mao, X. Wang, et al., The anti-colitis effect of Schisandra chinensis polysaccharide is associated with the regulation of the composition and metabolism of gut microbiota, Front. Cell. Infect. Microbiol. 10 (2020), 519479.
    [46]
    Y. Sun, L. Fan, W. Mian, et al., Modified apple polysaccharide influences MUC-1 expression to prevent ICR mice from colitis-associated carcinogenesis, Int. J. Biol. Macromol. 120 (2018) 1387-1395.
    [47]
    Y. Wang, N. Zhang, J. Kan, et al., Structural characterization of water-soluble polysaccharide from Arctium lappa and its effects on colitis mice, Carbohydr. Polym. 213 (2019) 89-99.
    [48]
    B. Dalile, L. Van Oudenhove, B. Vervliet, et al., The role of short-chain fatty acids in microbiota-gut-brain communication, Nat. Rev. Gastroenterol. Hepatol. 16 (2019) 461-478.
    [49]
    D. Parada Venegas, M.K. De la Fuente, G. Landskron, et al., Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases, Front. Immunol. 10 (2019), 277.
    [50]
    K.L. Ford, D.J. Jorgenson, E.J.L. Landry, et al., Vitamin and mineral supplement use in medically complex, community-living, older adults, Appl. Physiol. Nutr. Metabol. 44 (2019) 450-453.
    [51]
    L. Chavez-Galan, M.L. Olleros, D. Vesin, et al., Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages, Front. Immunol. 6 (2015), 263.
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