Search
Close this search box.

Insight into antioxidant and anti-inflammatory effects of marine bacterial natural exopolysaccharide (EPSSM) using carrageenan-induced paw edema in rats – Scientific Reports

  • Colegate, S. M. & Molyneux, R. J. Bioactive Natural Products: Detection, Isolation, and Structural Determination (CRC Press, 2007).

    Book 

    Google Scholar
     

  • Jenab, A., Roghanian, R. & Emtiazi, G. Bacterial natural compounds with anti-inflammatory and immunomodulatory properties (mini review). Drug Design Dev. Ther. 14, 3787–3801 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Chi, Z. & Fang, Y. Exopolysaccharides from marine bacteria. J. Ocean Univ. China 4, 67–74 (2005).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Nichols, C. M., Guezennec, J. & Bowman, J. Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: A review. Mar. Biotechnol. 7, 253–271 (2005).

    Article 
    CAS 

    Google Scholar
     

  • Mohamed, S. S., Ibrahim, G. S., Ghoneim, M. A. & Hassan, A. I. Evaluating the role of polysaccharide extracted from Pleurotus columbinus on cisplatin-induced oxidative renal injury. Sci. Rep. 13(1), 835 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Banerjee, A. et al. Optimization and characterization of a novel exopolysaccharide from Bacillus haynesii CamB6 for food applications. Biomolecules 12(6), 834 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dal Bello, F., Walter, J., Hertel, C. & Hammes, W. P. In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst. Appl. Microbiol. 24(2), 232–237 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hongpattarakere, T., Cherntong, N., Wichienchot, S., Kolida, S. & Rastall, R. A. In vitro prebiotic evaluation of exopolysaccharides produced by marine isolated lactic acid bacteria. Carbohydr. Polym. 87(1), 846–852 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chaves-López, C. et al. Potential of Borojoa patinoi Cuatrecasas water extract to inhibit nosocomial antibiotic resistant bacteria and cancer cell proliferation in vitro. Food Funct. 9(5), 2725–2734 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Wojdasiewicz, P., Poniatowski, ŁA. & Szukiewicz, D. The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediat. Inflamm. 2014, 561459 (2014).

    Article 

    Google Scholar
     

  • Xiao, X., Wu, Z.-C. & Chou, K.-C. A multi-label classifier for predicting the subcellular localization of gram-negative bacterial proteins with both single and multiple sites. PLoS One 6(6), e20592 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hayakawa, M. & Nonomura, H. Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J. Ferment. Technol. 65(5), 501–509 (1987).

    Article 
    CAS 

    Google Scholar
     

  • Bragadeeswaran, S. et al. Exopolysaccharide production by Bacillus cereus GU812900, a fouling marine bacterium. Afr. J. Microbiol. Res. 5(24), 4124–4132 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Selim, M. S. et al. Production and characterization of exopolysaccharide from marine Bacillus sp. MSHN2016 with studying its effect on isoniazid/rifampicin-induced hepatic and renal toxicities in rats. J. Appl. Pharm. Sci. 8(8), 001–011 (2018).

    CAS 

    Google Scholar
     

  • Yadav, M. P., Moreau, R. A., Hotchkiss, A. T. & Hicks, K. B. A new corn fiber gum polysaccharide isolation process that preserves functional components. Carbohydr. Polym. 87(2), 1169–1175 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Sneath, P. H., Mair, N. S., Sharpe, M. E. & Holt, J. G. Bergey’s Manual of Systematic Bacteriology Vol. 2 (Williams & Wilkins, 1986).


    Google Scholar
     

  • Li, J.-w, Ding, S.-d & Ding, X.-l. Optimization of the ultrasonically assisted extraction of polysaccharides from Zizyphus jujuba cv. jinsixiaozao. J. Food Eng. 80(1), 176–183 (2007).

    Article 
    CAS 

    Google Scholar
     

  • DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. T. & Smith, F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28(3), 350–356 (1956).

    Article 
    CAS 

    Google Scholar
     

  • Filisetti-Cozzi, T. M. & Carpita, N. C. Measurement of uronic acids without interference from neutral sugars. Anal. Biochem. 197(1), 157–162 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dodgson, K. & Price, R. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem. J. 84(1), 106 (1962).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sudhamani, S., Tharanathan, R. & Prasad, M. Isolation and characterization of an extracellular polysaccharide from Pseudomonas caryophylli CFR 1705. Carbohydr. Polym. 56(4), 423–427 (2004).

    Article 
    CAS 

    Google Scholar
     

  • Jun, H.-I., Lee, C.-H., Song, G.-S. & Kim, Y.-S. Characterization of the pectic polysaccharides from pumpkin peel. LWT-Food Sci. Technol. 39(5), 554–561 (2006).

    Article 
    CAS 

    Google Scholar
     

  • You, L. et al. Structural characterisation of polysaccharides from Tricholoma matsutake and their antioxidant and antitumour activities. Food Chem. 138(4), 2242–2249 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ray, B. Polysaccharides from Enteromorpha compressa: Isolation, purification and structural features. Carbohydr. Polym. 66(3), 408–416 (2006).

    Article 
    CAS 

    Google Scholar
     

  • Brand-Williams, W., Cuvelier, M.-E. & Berset, C. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol. 28(1), 25–30 (1995).

    Article 
    CAS 

    Google Scholar
     

  • Oyaizu, M. Studies on products of browning reaction. Jpn. J. Nutr. Diet. 44, 307–315 (1986).

    Article 
    CAS 

    Google Scholar
     

  • Winter, C. A., Risley, E. A. & Nuss, G. W. Carrageenin-induced edema in hind paw of the rat as an assay for antiinflammatory drugs. Proc. Soc. Exp. Biol. Med. 111(3), 544–547 (1962).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bilici, D., Akpinar, E. & Kiziltunc, A. Protective effect of melatonin in carrageenan-induced acute local inflammation. Pharmacol. Res. 46(2), 133–139 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ohkawa, H., Ohishi, N. & Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95(2), 351–358 (1979).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vrablic, A. S., Albright, C. D., Craciunescu, C. N., Salganik, R. I. & Zeisel, S. H. Altered mitochondrial function and overgeneration of reactive oxygen species precede the induction of apoptosis by 1-O-octadecyl-2-methyl-rac-glycero-3-phosphocholine in p53-defective hepatocytes. Faseb J. 15(10), 1739–1744 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, C.-C., Huang, Y.-J., Chen, L.-G., Lee, L.-T. & Yang, L.-L. Inducible nitric oxide synthase inhibitors of Chinese herbs III. Rheum palmatum. Planta Med. 68(10), 869–874 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Beutler, E., Duron, O. & Kelly, B. M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61, 882–888 (1963).

    CAS 
    PubMed 

    Google Scholar
     

  • Masayasu, M. & Hiroshi, Y. A simplified assay method of superoxide dismutase activity for clinical use. Clin. Chim. Acta 92(3), 337–342 (1979).

    Article 

    Google Scholar
     

  • Osumi, T. & Hashimoto, T. Enhancement of fatty acyl-CoA oxidizing activity in rat liver peroxisomes by di-(2-ethylhexyl) phthalate. J. Biochem. 83(5), 1361–1365 (1978).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Willis, L. G., Winston, M. L. & Honda, B. M. Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol. Phylogenet. Evol. 1(3), 169–178 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Guo, S. et al. Structural characteristics and antioxidant activities of the extracellular polysaccharides produced by marine bacterium Edwardsiella tarda. Bioresour. Technol. 101(12), 4729–4732 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Smiderle, F. et al. A 3-O-methylated mannogalactan from Pleurotus pulmonarius: Structure and antinociceptive effect. Phytochemistry 69(15), 2731–2736 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Silveira, M. L. et al. Exopolysaccharide produced by Pleurotus sajor-caju: Its chemical structure and anti-inflammatory activity. Int. J. Biol. Macromol. 75, 90–96 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Salama, Y. et al. Characterization, structure, and function of extracellular polymeric substances (EPS) of microbial biofilm in biological wastewater treatment systems: A review. Desalin. Water Treat. 57(35), 16220–16237 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Poli, A., Anzelmo, G. & Nicolaus, B. Bacterial exopolysaccharides from extreme marine habitats: Production, characterization and biological activities. Mar. Drugs 8(6), 1779–1802 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, L., Wang, X., Wu, H. & Liu, R. Overview on biological activities and molecular characteristics of sulfated polysaccharides from marine green algae in recent years. Mar. Drugs 12(9), 4984–5020 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Caruso, C. et al. Production and biotechnological potential of extracellular polymeric substances from sponge-associated Antarctic bacteria. Appl. Environ. Microbiol. 84(4), e01624-17 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Almutairi, M. H. & Helal, M. M. Biological and microbiological activities of isolated Enterobacter sp. ACD2 exopolysaccharides from Tabuk region of Saudi Arabia. J. King Saud Univ.-Sci. 33(2), 101328 (2021).

    Article 

    Google Scholar
     

  • Xu, Y. et al. Novel insights into the sulfated glucuronic acid-based anti-SARS-CoV-2 mechanism of exopolysaccharides from halophilic archaeon Haloarcula hispanica. Front. Chem. 10, 871509 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kacurakova, M., Capek, P., Sasinkova, V., Wellner, N. & Ebringerova, A. FT-IR study of plant cell wall model compounds: Pectic polysaccharides and hemicelluloses. Carbohydr. Polym. 43(2), 195–203 (2000).

    Article 
    CAS 

    Google Scholar
     

  • Marchessault, R. & Liang, C. Infrared spectra of crystalline polysaccharides. III. Mercerized cellulose. J. Polym. Sci. 43(141), 71–84 (1960).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Hong, T., Yin, J.-Y., Nie, S.-P. & Xie, M.-Y. Applications of infrared spectroscopy in polysaccharide structural analysis: Progress, challenge and perspective. Food Chem.: X 12, 100168 (2021).

    CAS 
    PubMed 

    Google Scholar
     

  • Nikonenko, N. A., Buslov, D. K., Sushko, N. I. & Zhbankov, R. G. Investigation of stretching vibrations of glycosidic linkages in disaccharides and polysaccarides with use of IR spectra deconvolution. Biopolym. Orig. Res. Biomol. 57(4), 257–262 (2000).

    CAS 

    Google Scholar
     

  • Peng, L., Liu, S., Ji, Z., Chen, S. & Mao, J. Structure characterisation of polysaccharide isolated from Huangjiu and its anti-inflammatory activity through MAPK signalling. Int. J. Food Sci. Technol. 54(5), 1874–1883 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Tang, W. et al. Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus SRFM-1. Carbohydr. Polym. 173, 654–664 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Huang-Lin, E., Sánchez-León, E., Amils, R. & Abrusci, C. potential applications of an exopolysaccharide produced by Bacillus xiamenensis RT6 isolated from an acidic environment. Polymers 14(18), 3918 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, M. et al. Structure characterization, antioxidant capacity, rheological characteristics and expression of biosynthetic genes of exopolysaccharides produced by Lactococcus lactis subsp. lactis IMAU11823. Food Chem. 384, 132566 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, W. et al. Structural elucidation and antioxidant activities of exopolysaccharides from Lactobacillus helveticus MB2-1. Carbohydr. Polym. 102, 351–359 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun, C., Wang, J.-W., Fang, L., Gao, X.-D. & Tan, R.-X. Free radical scavenging and antioxidant activities of EPS2, an exopolysaccharide produced by a marine filamentous fungus Keissleriella sp. YS 4108. Life Sci. 75(9), 1063–1073 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun, C., Shan, C., Gao, X. & Tan, R. Protection of PC12 cells from hydrogen peroxide-induced injury by EPS2, an exopolysaccharide from a marine filamentous fungus Keissleriella sp. YS4108. J. Biotechnol. 115(2), 137–144 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Coura, C. O. et al. Mechanisms involved in the anti-inflammatory action of a polysulfated fraction from Gracilaria cornea in rats. PLoS ONE 10(3), e0119319 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carvalho, J. T. et al. Preliminary studies of analgesic and anti-inflammatory properties of Caesalpinia ferrea crude extract. J. Ethnopharmacol. 53(3), 175–178 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hajare, S. W. et al. Anti-inflammatory activity of Dalbergia sissoo leaves. Fitoterapia 72(2), 131–139 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Srinivasan, K. et al. Evaluation of anti-inflammatory activity of Pongamia pinnata leaves in rats. J. Ethnopharmacol. 78(2–3), 151–157 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Iwalewa, E. O., McGaw, L., Naidoo, V., Eloff, J. Inflammation: the foundation of diseases and disorders. A review of phytomedicines of South African origin used to treat pain and inflammatory conditions. Afr. J. Biotechnol. 6(25) (2007).

  • Mueller, M., Hobiger, S. & Jungbauer, A. Anti-inflammatory activity of extracts from fruits, herbs and spices. Food Chem. 122(4), 987–996 (2010).

    Article 
    CAS 

    Google Scholar
     

  • Gangalla, R., Macha, B., Kasarla, S., Eerla, R. & Thampu, R. Anti-inflammatory activity of the exopolysaccharides (EPS) produced from polluted soil. Int. J. Pharm. Biol. Sci. 8, 623–631 (2018).

    CAS 

    Google Scholar
     

  • Murofushi, Y. et al. The toll-like receptor family protein RP105/MD1 complex is involved in the immunoregulatory effect of exopolysaccharides from Lactobacillus plantarum N14. Mol. Immunol. 64(1), 63–75 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kwon, M. et al. Exopolysaccharide isolated from Lactobacillus plantarum L-14 has anti-inflammatory effects via the Toll-like receptor 4 pathway in LPS-induced RAW 264.7 cells. Int. J. Mol. Sci. 21(23), 9283 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Handy, R. L. C. & Moore, P. K. A comparison of the effects of L-NAME, 7-NI and L-NIL on carrageenan-induced hindpaw oedema and NOS activity. Br. J. Pharmacol. 123(6), 1119–1126 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zha, X.-Q. et al. Structural identification and immunostimulating activity of a Laminaria japonica polysaccharide. Int. J. Biol. Macromol. 78, 429–438 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Du, B., Yang, Y., Bian, Z. & Xu, B. Characterization and anti-inflammatory potential of an exopolysaccharide from submerged mycelial culture of Schizophyllum commune. Front. Pharmacol. 8, 252 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ialenti, A., Ianaro, A., Moncada, S. & Di Rosa, M. Modulation of acute inflammation by endogenous nitric oxide. Eur. J. Pharmacol. 211(2), 177–182 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar