The combined impact of sauerkraut with Leuconostoc mesenteroides to enhance immunomodulatory activity in Escherichia coli-infected mice

Abstract

This study investigated the combined impact of sauerkraut and Leuconostoc mesenteroides culture on immunomodulatory activity in experimental animal. The in vivo immunomodulatory activity of Escherichia coli-infected Balb-C mice was ascertained in fermented sauerkrauts [test vs. control]. Both sauerkrauts enhanced the adaptive immune response [evidenced by an increase in CD4+ CD8+ IFN-γ, TNFα] and innate immune response [represented by a decrease of CD68-IL-6]. Nevertheless, the in vivo immunomodulatory activity of sauerkraut combined with L. mesenteroides was higher than that shown in sauerkraut control solely.

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References

  1. 1.

    Spelman K, Burns J, Nichols D, Winters N, Ottersberg S, Tenborg M (2006) Modulation of cytokine expression by traditional medicines: a review of herbal immunomodulator. Altern Med Rev 11(2):128–150

    PubMed  PubMed Central  Google Scholar 

  2. 2.

    Abbas AK, Lichtman AH, Pillai S (2007) Cellular and molecular immunology, 6th edn. Elsevier, Philadelphia

    Google Scholar 

  3. 3.

    Penas E, Martinez-Villaluenga C, Frias J, Sanchez-Martines MJ, Perez-Corona MT, Madrid Y, Camara C, Vidal-Valverde C (2012) Se improves indole glucosinolate hydrolysis product content, Se-methylselenocysteine content, antioxidant capacity and potential anti-inflammatory properties of sauerkraut. Food Chem 132(2):907–914

    CAS  Article  Google Scholar 

  4. 4.

    Vaughn RH (1985) In: Wood BJB (ed) Microbiology of vegetable fermented foods. Elsevier, London

    Google Scholar 

  5. 5.

    Lu Z, Breidt F, Plengvidhya V, Fleming HP (2003) Bacteriophage ecology in commercial sauerkraut fermentations. Appl Environ Microbiol 69:3192–3202

    CAS  Article  PubMed Central  Google Scholar 

  6. 6.

    Plengvidhya V, Breidt F, Lu Z, Fleming HP (2007) DNA fingerprinting of latic acid bacteria in sauerkraut fermentations. Appl Environ Microbiol 73:7697–7702

    CAS  Article  PubMed Central  Google Scholar 

  7. 7.

    Wiander B, Ryhänen EL (2005) Laboratory and large-scale fermentation of white cabbage into sauerkraut and sauerkraut juice by using starters in combination with mineral salt with a low NaCl content. Euro Food Res Technol 220:191–195

    CAS  Article  Google Scholar 

  8. 8.

    Yang X, Hu W, Jiang A, Xiu Z, Ji Y, Guan Y, Sarengaowa, Yang X (2019) Effect of salt concentration on quality of Chinese Northeast sauerkraut fermented by Leuconostoc mesenteroides and Lactobacillus plantarum. Food Biosci 30:100421. https://doi.org/10.1016/j.fbio.2019.100421

    CAS  Article  Google Scholar 

  9. 9.

    Penas E, Frias J, Sidro B, Vidal-Valverde C (2010) Chemical evaluation and sensory quality of sauerkraut obtained by natural and induced fermentations at different NaCl levels from Brassica oleracea var. capitata cv. Bronco grown in Eastern Spain. Effect of storage. J Agric Food Chem 58:3549–3557

    CAS  Article  PubMed Central  Google Scholar 

  10. 10.

    Shahidi F, Ho CT (2005) In: Shahidi F, Ho CT (eds) Phenolics Compounds in food and natural health products. American Chemical Society, Washington DC

    Google Scholar 

  11. 11.

    Murray RK, Granner DK, Mayes PA, Rodwell VW (2003) Harper’s Illustrated Biochemistry, 26th edn. McGraw-Hill Medical, New York

    Google Scholar 

  12. 12.

    Romeo L, Iori R, Rollin P, Bramanti P, Mazzon E (2018) Isothiocyanates: an overview of their antimicrobial activity against human infections. Molecules 23(3):624. https://doi.org/10.3390/molecules23030624

    CAS  Article  Google Scholar 

  13. 13.

    Ranggana S (1977) Handbook of analysis and quality control for fruit & vegetable products. McGraw-Hill Publishing Company, New Delhi

    Google Scholar 

  14. 14.

    Yang J, Paulino R, Janke-Stedronsky S, Abawi F (2007) Free radical scavenging activity and total phenol of noni (Morinda citrifolia L.) juice and powder in processing and storage. Food Chem 102(1):302–308

    CAS  Article  Google Scholar 

  15. 15.

    Kim HJ, Lee MJ, Jeong MH, Kim JE (2017) Identification and quantification of glucosinolates in kimchi by liquid chromatography-electrospray tandem mass spectrometry. Int J Anal Chem 2017:6753481. https://doi.org/10.1155/2017/6753481

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Hosseinzadeh H, Bazzaz BSF, Haghi MM (2007) Antibacterial activity of total extracts and essential oil of Nigella sativa L. seeds in mice. Pharmacologyonline 2:429–435

    Google Scholar 

  17. 17.

    Tolonen M, Rajaniemi S, Pihlava JM, Korhonen H, Ryhanen EL (2004) Formation of nisin, plant derived biomolecules and antimicrobial activity in starter culture fermentations of sauerkraut. Food Microbiol 20:391–395

    Google Scholar 

  18. 18.

    Essawet NA, Cvetkovic D, Velicanski A, Canadanovic-Brunet J, Vulic J, Maksimovic V, Markov S (2015) Polyphenols and antioxidant activities of Kombucha beverage enriched with coffeeberry extract. Chem Ind Chem Eng Q 21(3):399–409

    CAS  Article  Google Scholar 

  19. 19.

    Lee NK, Jeong JH, Oh J, Kim Y, Ha YS, Jeong Y (2015) Conversion of flavonols, kaempferol and quarcetin in mulberry (Morus alba L.) leaf using plant-fermenting Lactobacillus plantarum. J Food Biochem 39:765–770

    CAS  Article  Google Scholar 

  20. 20.

    Castillo NA, Perdigon G, de Moreno de LeBlanc A (2011) Oral administration of a probiotic Lactobacillus modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar typhimurium infection in mice. BMC Microbiol 11:177. https://doi.org/10.1186/1471-2180-11-177

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Lestari LA, Soesatyo M, Iravati S, Harmayani E (2012) Enhancement of phagocytic activity and nitric oxide production of peritoneal macrophage of spague Dawley rats fed with Lactobacillus plantarum Mut7 and sweet potato fiber. J Gizi Klinik Indones 9(2):64–72

    Article  Google Scholar 

  22. 22.

    Martinez-Villaluenga C, Penas E, Sidro B, Ullate M, Frias J, Vidal-Valverde C (2012) White cabbage fermentation improves ascorbigen content, antioxidant and nitric oxide production inhibitory activity in LPS-induced macrophages. LWT Food Sci Technol 46(1):77–83

    CAS  Article  Google Scholar 

  23. 23.

    Hayes J, Kelleher M, Eggleston I (2008) The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur J Nutr 47(Suppl. 2):73–88

    CAS  Article  PubMed Central  Google Scholar 

  24. 24.

    Aires A, Mota VR, Saavedra MJ, Rosa EA, Bennett RN (2009) The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J Appl Microbiol 106:2086–2095

    CAS  Article  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported through Professor Research Grant, Brawijaya University, with contract number of 2571/UN10.F10/PN/2019.

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Correspondence to Elok Zubaidah.

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Zubaidah, E., Susanti, I., Yuwono, S.S. et al. The combined impact of sauerkraut with Leuconostoc mesenteroides to enhance immunomodulatory activity in Escherichia coli-infected mice. Eur Food Res Technol (2020). https://doi.org/10.1007/s00217-020-03540-w

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Keywords

  • Immunomodulatory activity
  • Sauerkraut
  • Leuconostoc mesenteroides
  • Mice