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Food Science and Biotechnology

, Volume 28, Issue 6, pp 1871–1879 | Cite as

Anti-inflammatory, anti-oxidative stress effect of Phascolosoma esculenta oligosaccharides on Escherichia coli-induced sepsis mice

  • Zhihao Yang
  • Ying Pan
  • Jiong Chen
  • Hao Zhang
  • Hua Wei
  • Zufang Wu
  • Lianliang LiuEmail author
Article

Abstract

Bacterial infection is the most common cause of sepsis. In this study, Phascolosoma esculenta oligosaccharides (PEOs) were prepared to evaluate their resistance against E. coli-induced sepsis. HPLC–MS and FT-IR indicated that PEOs were composed of d-glucosyl, d-galactosyl, with small amount of d-mannosyl, d-arabinosyl and residues with α- and β-type linkage. Different dosage administrations of PEOs for 30 days significantly improved ICR mice survival rate and bacterial clearance ability (P < 0.01) after as E. coli injection. Moreover, PEOs significantly reduced the secretion of IL-1β and TNF-α and enhanced that of IL-10 in sepsis mice, enhanced the antioxidant enzyme activities and total antioxidant capacity, decreased MDA level in the serum, and upregulated mRNA expression of Nrf2 (P < 0.01). All these results indicate that PEOs could improve the resistance of ICR mice against E. coli-induced sepsis that attributed to anti-inflammatory and anti-oxidative stress.

Keywords

Phascolosoma esculenta oligosaccharides Sepsis Oxidative stress Inflammation 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31601476), Zhejiang Provincial Natural Science Foundation of China (LQ15C200002), and sponsored by K. C. Wong Magna Fund in Ningbo University.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Asci A, Surmeli-Onay O, Erkekoglu P, Yigit S, Yurdakik M, Kocer-Gumusel B. Oxidant and antioxidant status in neonatal proven and clinical sepsis in relation to selenium status. Pediatr. Int. 57(6): 1131–1137 (2015)CrossRefGoogle Scholar
  2. Auddy B, Ferreira M, Blasina F, Lafon L, Arredondo F, Dajas F, Tripathi PC, Seal T. Screening of antioxidant activity of three Indian medicinal plants, traditionally used for the management of neurodegenerative diseases. J. Ethnopharmacol. 84:131–138 (2003)CrossRefGoogle Scholar
  3. Bar-Or D, Carrick MM, Mains CW, Rael LT, Slone D, Brody EN. Sepsis, oxidative stress, and hypoxia: Are there clues to better treatment? Redox Rep. 20(5):193–197 (2015)CrossRefGoogle Scholar
  4. Bian J, Peng F, Peng XP, Xu F, Sun RC, Kennedy JF. Isolation of hemicelluloses from sugarcane bagasse at different temperatures: structure and properties. Carbohydr. Polym. 88:638–645 (2012)CrossRefGoogle Scholar
  5. Cao W, Liu XQ, Liu L, Wang M, Fan HT, Li C, Lv Z, Wang X, Mei Q. Structural analysis of water-soluble glucans from the root of Angelica sinensis (Oliv.) Carbohydr. Res. 341:1870–1877 (2006)CrossRefGoogle Scholar
  6. Catalá A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem. Phys. Lipids. 157: 1–11 (2009)CrossRefGoogle Scholar
  7. Chapple SJ, Siow RCM, Mann GE. Crosstalk between Nrf2 and the proteasome: Therapeutic potential of Nrf2 inducers in vascular disease and aging. Int. J. Biochem. Cell B. 44(8): 1315–1320 (2012)CrossRefGoogle Scholar
  8. Chen L, Lan Z. Polydatin attenuates potassium oxonate-induced hyperuricemia and kidney inflammation by inhibiting NF-κB/NLRP3 inflammasome activation via the AMPK/SIRT1 pathway. Food Funct. 8(5): 1785–1792 (2017)CrossRefGoogle Scholar
  9. Eichacker PQ, Parent C, Kalil A, Esposito C, Cui X, Banks SM, Gerstenberger EP, Fitz Y, Danner RL, Natanson C. Risk and the efficacy of antiinflammatory agents: retrospective and confirmatory studies of sepsis. Am. J. Resp. Crit. Care. 166:1197–1205 (2002)CrossRefGoogle Scholar
  10. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr. Res. Rev. 17:259–275 (2004)CrossRefGoogle Scholar
  11. Hatherill M, Tibby SM, Turner C, Ratnavel N, Murdoch IA, Procalcitonin and cytokine levels: relationship to organ failure and mortality in pediatric septic shock. Crit. Care Med. 28 2591–2594 (2000)CrossRefGoogle Scholar
  12. He YQ, Chen J, Lu XJ, Shi YH. Characterization of P2X7R and its function in the macrophages of ayu, Plecoglossus altivelis. Plos ONE. 8: e57505 (2013)CrossRefGoogle Scholar
  13. Kang DR, Yoon GY, Cho J, Lee SJ, Lee SJ, Park HJ, Kang TH, Han HD, Park WS, Yoon YK, Park YM, Jung ID. Neoagarooligosaccharides prevent septic shock by modulating A20-and cyclooxygenase-2-mediated interleukin-10 secretion in a septic-shock mouse model. Biochem. Bioph. Res. Co. 486: 998–1004 (2017)CrossRefGoogle Scholar
  14. Karapetsa M, Pitsika M, Goutzourelas N, Stagos D, Becker AT, Zakynthinos E. Oxidative status in ICU patients with septic shock. Food Chem. Toxicol. 61(4): 106–111 (2013)CrossRefGoogle Scholar
  15. Kim GY, Roh SI, Park SK, Ahn SC, Oh YH, Lee JD, Park YM. Alleviation of experimental septic shock in mice by acidic polysaccharide isolated from the medicinal mushroom Phellinus linteus. Biol. Pharm. Bull. 26(10): 1418–1423 (2003)CrossRefGoogle Scholar
  16. King EG, Bauzá GJ, Mella JR, Remic DG. Pathophysiologic mechanisms in septic shock. Lab. Invest. 94:4–12 (2014)CrossRefGoogle Scholar
  17. LaRosa SP, Opal SM. Sepsis strategies in development. Clin. Chest. Med. 29: 735–747 (2008)CrossRefGoogle Scholar
  18. Li W, Zhang R, Guo J, Shao H, Yang X. Protective effect of R. glutinosa oligosaccharides against high L-carnitine diet-induced endothelial dysfunction and hepatic injury in mice. Int. J. Biol. Macromol. 85:285–293 (2016)CrossRefGoogle Scholar
  19. Liu L, Cao J, Chen J, Zhang X, Wu Z, Xiang H. Effects of peptides from Phascolosoma esculenta on spatial learning and memory via anti-oxidative character in mice. Neurosci. Lett. 631: 30–35 (2016)CrossRefGoogle Scholar
  20. Lowes DA, Thottakam BM, Webster NR, Murphy MP, Galley HF. The mitochondria-targeted antioxidant MitoQ protects against organ damage in a lipopolysaccharide-peptidoglycan model of sepsis. Free Radical Biol. Med. 45:1559–1565 (2008)CrossRefGoogle Scholar
  21. Lu XJ, Chen J, Huang ZA, Shi YH, Lv JN. Identification and characterization of a novel cathelicidin from ayu, Plecoglossus altivelis. Fish Shellfish Immun. 31: 52–57 (2011)CrossRefGoogle Scholar
  22. Lu XJ, Chen J, Yu CH, Shi YH, He YQ, Zhang RC, Huang ZA, Lv JN, Zhang S, Xu L. LECT2 protects mice against bacterial sepsis by activating macrophages via the CD209a receptor. J. Exp. Med. 210:5–13 (2013)CrossRefGoogle Scholar
  23. Martin GS. Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes. Expert Rev. Anti-Infe. 10: 701–706 (2012)CrossRefGoogle Scholar
  24. Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, Coopersmith CM, Hotchkiss RS. Characterization and modulation of the immunosuppressive phase of sepsis. Infect. Immun. 78(4): 1582–1592 (2010)CrossRefGoogle Scholar
  25. Qiao Y, Bai XF, Du YG. Chitosan oligosaccharides protect mice from LPS challenge by attenuation of inflammation and oxidative stress. Int. Immunopharmacol. 11: 121–127 (2011)CrossRefGoogle Scholar
  26. Ramachandran G. Gram-positive and gram-negative bacterial toxins in sepsis: a brief review. Virulence 5(1): 196–201 (2014)CrossRefGoogle Scholar
  27. Riedemann NC, Guo RF, Ward PA. The enigma of sepsis. J. Clin. Invest. 112:460–467 (2003)CrossRefGoogle Scholar
  28. Santos MI, Araujo-Andrade C, Tymczyszyn EE, Gómez-Zavaglia A. Determination of amorphous/rubbery states in freeze-dried prebiotic sugars using a combined approach of near-infrared spectroscopy and multivariate analysis. Food Res. Int. 64: 514–519 (2014)CrossRefGoogle Scholar
  29. Sun HQ, Song WW, Zhang LJ, Yang XY, Zhu ZY, Ma RC, Wang DY. Structural characterization and inhibition on α-glucosidase of a novel oligosaccharide from barley malt. J. Cereal Sci. 82: 82–93 (2018)CrossRefGoogle Scholar
  30. Underwood MA, Gaerlan S, Leoz M, Dimapasoc L, Kalanetra KM, Lemay DG, German JB, Mills DA, Lebrilla CB. Human milk oligosaccharides in premature infants: absorption, excretion, and influence on the intestinal microbiota. Pediatr. Res. 78: 670–677 (2015)CrossRefGoogle Scholar
  31. Urso ML, Clarkson PM. Oxidative stress, exercise, and antioxidant supplementation. Toxicol. 189:41–54 (2003)CrossRefGoogle Scholar
  32. Vincent JL, Sun Q, Dubois MJ. Clinical trials of immunomodulatory therapies in severe sepsis and septic shock. Clin. Infect. Dis. 34:1084–1093 (2002)CrossRefGoogle Scholar
  33. Xue WL, Bai XY, Zhang L. rhTNFR: Fc increases Nrf2 expression via miR-27a mediation to protect myocardium against sepsis injury. Biochem. Bioph. Res. Co. 464:855–861 (2015)CrossRefGoogle Scholar
  34. Yamamoto Y, Nunome T, Yamauchi R, Kato K, Sone Y. Structure of an exocellular polysaccharide of Lactobacillus helveticus TN-4, a spontaneous mutant strain of Lactobacillus helveticus TY1-2. Carbohydr. Res. 275:319–332 (1995)CrossRefGoogle Scholar
  35. Yang D, He Y, Muñoz-Planillo R, Liu Q, Núñez G. Caspase-11 requires the pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity 43(5): 923–932 (2015)CrossRefGoogle Scholar
  36. Yu Z, Li HY, Qian Y, Yan L. Effect of Lentinus edodes polysaccharide on oxidative stress, immunity activity and oral ulceration of rats stimulated by phenol. Carbohydr. Polym. 75:115–118 (2009)CrossRefGoogle Scholar
  37. Zhang H, Wang J, Liu Y, Sun B. Wheat bran feruloyl oligosaccharides modulate the phase II detoxifying/antioxidant enzymes via Nrf2 signaling. Int. J. Biol. Macromol. 74:150–154 (2015)CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology 2019

Authors and Affiliations

  • Zhihao Yang
    • 1
  • Ying Pan
    • 2
  • Jiong Chen
    • 3
  • Hao Zhang
    • 3
  • Hua Wei
    • 4
  • Zufang Wu
    • 1
  • Lianliang Liu
    • 1
    Email author
  1. 1.College of Food and Pharmaceutical Sciences, Deep Processing Technology Key Laboratory of Zhejiang Province Animal Protein FoodNingbo UniversityNingboPeople’s Republic of China
  2. 2.Nanjing Pukou HospitalNanjingPeople’s Republic of China
  3. 3.School of Marine SciencesNingbo UniversityNingboPeople’s Republic of China
  4. 4.Ningbo College of Health SciencesNingboPeople’s Republic of China

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