Glycoconjugate Journal

, Volume 36, Issue 1, pp 39–55 | Cite as

Structure and biological activities of a hexosamine-rich cell wall polysaccharide isolated from the probiotic Lactobacillus farciminis

  • Emmanuel Maes
  • Irina Sadovskaya
  • Mathilde Lévêque
  • Elisabeth Elass-Rochard
  • Bruno Payré
  • Thierry Grard
  • Vassilia Théodorou
  • Yann Guérardel
  • Muriel Mercier-BoninEmail author
Original Article


Lactobacillus farciminis CIP 103136 is a bacterial strain with recognized probiotic properties. However, the mechanisms underlying such properties have only been partially elucidated. In this study, we isolated and purified a cell-wall associated polysaccharide (CWPS), and evaluated its biological role in vitro. The structure of CWPS and responses from stimulation of (i) human macrophage-like THP-1 cells, (ii) human embryonal kidney (HEK293) cells stably transfected with Toll-like receptors (TLR2 or TLR4) and (iii) human colonocyte-like T84 intestinal epithelial cells, upon exposure to CWPS were studied. The structure of the purified CWPS from L. farciminis CIP 103136 was analyzed by nuclear magnetic resonance (NMR), MALDI-TOF-TOF MS, and methylation analyses in its native form and following Smith degradation. It was shown to be a novel branched polysaccharide, composed of linear backbone of trisaccharide repeating units of: [→6αGlcpNAc1 → 4βManpNAc1 → 4βGlcpNAc1→] highly substituted with single residues of αGlcp, αGalp and αGlcpNAc. Subsequently, the lack of pro- or anti-inflammatory properties of CWPS was established on macrophage-like THP-1 cells. In addition, CWPS failed to modulate cell signaling pathways dependent of TLR2 and TLR4 in transfected HEK-cells. Finally, in T84 cells, CWPS neither influenced intestinal barrier integrity under basal conditions nor prevented TNF-α/IFN-γ cytokine-mediated epithelium impairment.


Lactobacillus farciminis Probiotic Cell wall polysaccharide Structure Immunomodulation Intestinal barrier 



The authors wish to acknowledge Lallemand SA (France) and Lallemand-Institut Rosell (Canada) for providing the L. farciminis strain.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. 1.
    Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L., Canani, R.B., Flint, H.J., Salminen, S., Calder, P.C., Sanders, M.E.: Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506–514 (2014)CrossRefGoogle Scholar
  2. 2.
    McFarland, L.V.: From yaks to yogurt: the history, development, and current use of probiotics. Clin. Infect. Dis. 60, S85–S90 (2015)CrossRefGoogle Scholar
  3. 3.
    Donato, K.A., Gareau, M.G., Wang, Y.J., Sherman, P.M.: Lactobacillus rhamnosus GG attenuates interferon-gamma and tumour necrosis factor-alpha-induced barrier dysfunction and pro-inflammatory signalling. Microbiology. 156, 3288–3297 (2010)CrossRefGoogle Scholar
  4. 4.
    Wells, J.M.: Immunomodulatory mechanisms of lactobacilli. Microb. Cell Factories. 10, S17 (2011)CrossRefGoogle Scholar
  5. 5.
    Lee, I.C., Tomita, S., Kleerebezem, M., Bron, P.A.: The quest for probiotic effector molecules--unraveling strain specificity at the molecular level. Pharmacol. Res. 69, 61–742013 (2013)CrossRefGoogle Scholar
  6. 6.
    Smits, H.H., Engering, A., van der Kleij, D., de Jong, E.C., Schipper, K., van Capel, T.M., Zaat, B.A., Yazdanbakhsh, M., Wierenga, E.A., van Kooyk, Y., Kapsenberg, M.L.: Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J. Allergy Clin. Immunol. 115, 1260–1267 (2005)CrossRefGoogle Scholar
  7. 7.
    Sengupta, R., Altermann, E., Anderson, R.C., McNabb, W.C., Moughan, P.J., Roy, N.C.: The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediat. Inflamm. 2013, 237921 (2013)CrossRefGoogle Scholar
  8. 8.
    Yasuda, E., Serata, M., Sako, T.: Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl. Environ. Microbiol. 74, 4746–4755 (2008)CrossRefGoogle Scholar
  9. 9.
    Górska, S., Schwarzer, M., Jachymek, W., Srutkova, D., Brzozowska, E., Kozakova, H., Gamian, A.: Distinct immunomodulation of bone marrow-derived dendritic cell responses to Lactobacillus plantarum WCFS1 by two different polysaccharides isolated from Lactobacillus rhamnosus LOCK 0900. Appl. Environ. Microbiol. 80, 6506–6516 (2014)CrossRefGoogle Scholar
  10. 10.
    Górska, S., Hermanova, P., Ciekot, J., Schwarzer, M., Srutkova, D., Brzozowska, E., Kozakova, H., Gamian, A.: Chemical characterization and immunomodulatory properties of polysaccharides isolated from probiotic Lactobacillus casei LOCK 0919. Glycobiology. 26, 1014–1024 (2016)CrossRefGoogle Scholar
  11. 11.
    Balzaretti, S., Taverniti, V., Guglielmetti, S., Fiore, W., Minuzzo, M., Ngo, H.N., Ngere, J.B., Sadiq, S., Humphreys, P.N., Laws, A.P.: A novel rhamnose-rich hetero-exopolysaccharide isolated from Lactobacillus paracasei DG activates THP-1 human monocytic cells. Appl. Environ. Microbiol. 83, pii: e02702–pii: e02716 (2017)CrossRefGoogle Scholar
  12. 12.
    Mazmanian, S.K., Kasper, D.L.: The love-hate relationship between bacterial polysaccharides and the host immune system. Nat. Rev. Immunol. 6, 849–858 (2006)CrossRefGoogle Scholar
  13. 13.
    Mazmanian, S.K.: Capsular polysaccharides of symbiotic bacteria modulate immune responses during experimental colitis. J. Pediatr. Gastroenterol. Nutr. 46, E11–E12 (2008)CrossRefGoogle Scholar
  14. 14.
    Mazmanian, S.K., Round, J.L., Kasper, D.L.: A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 453, 620–625 (2008)CrossRefGoogle Scholar
  15. 15.
    Lamine, F., Eutamène, H., Fioramonti, J., Buéno, L., Théodorou, V.: Colonic responses to Lactobacillus farciminis treatment in trinitrobenzene sulphonic acid-induced colitis in rats. Scand. J. Gastroenterol. 39, 1250–1258 (2004a)CrossRefGoogle Scholar
  16. 16.
    Lamine, F., Fioramonti, J., Bueno, L., Nepveu, F., Cauquil, E., Lobysheva, I., Eutamène, H., Théodorou, V.: Nitric oxide released by Lactobacillus farciminis improves TNBS-induced colitis in rats. Scand. J. Gastroenterol. 39, 37–45 (2004b)CrossRefGoogle Scholar
  17. 17.
    Ait-Belgnaoui, A., Han, W., Lamine, F., Eutamène, H., Fioramonti, J., Bueno, L., Théodorou, V.: Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction. Gut. 55, 1090–1094 (2006)CrossRefGoogle Scholar
  18. 18.
    Da Silva, S., Robbe-Masselot, C., Ait Belgnaoui, A., Mancuso, A., Mercade-Loubière, M., Cartier, C., Gillet, M., Ferrier, L., Loubière, P., Dague, E., Théodorou, V., Mercier-Bonin, M.: Stress disrupts intestinal mucus barrier in rats via mucin O-glycosylation shift: prevention by a probiotic treatment. Am. J. Physiol. Gastrointest. Liver Physiol. 307, G420–G429 (2014)CrossRefGoogle Scholar
  19. 19.
    Tareb, R., Bernardeau, M., Horvath, P., Vernoux, J.P.: Rough and smooth morphotypes isolated from Lactobacillus farciminis CNCM I-3699 are two closely-related variants. Int. J. Food Microbiol. 193, 82–90 (2015)CrossRefGoogle Scholar
  20. 20.
    Altman, E., Brisson, J.R., Perry, M.B.: Structure of the O-antigenpolysaccharide of Haemophilus pleuropneumoniae serotype 3 (ATCC 27090) lipopolysaccharide. Carbohydr. Res. 179, 245–258 (1988)CrossRefGoogle Scholar
  21. 21.
    Gerwig, G.J., Kamerling, J.P., Vliegenthart, J.F.: Determination of the absolute configuration of mono-saccharides in complex carbohydrates by capillary G.L.C. Carbohydr. Res. 77, 10–17 (1979)CrossRefGoogle Scholar
  22. 22.
    Ciucanu, I., Kerek, F.: A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 131, 209–217 (1984)CrossRefGoogle Scholar
  23. 23.
    Read, S.M., Currie, G., Bacic, A.: Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr. Res. 281, 187–201 (1996)CrossRefGoogle Scholar
  24. 24.
    Dubois, M., Gilles, K.A., Hamilton, J.F., Rebers, P.A., Smyth, F.: Colorimetric methods for determination of sugars and related substances. Anal. Biochem. 28, 350–356 (1956)Google Scholar
  25. 25.
    Gatt, R., Berman, E.R.: A rapid procedure for the estimation of amino sugars on a micro scale. Anal. Biochem. 15, 167–171 (1966)CrossRefGoogle Scholar
  26. 26.
    Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., Tada, K.: Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer. 26, 171–176 (1980)CrossRefGoogle Scholar
  27. 27.
    Daigneault, M., Preston, J.A., Marriott, H.M., Whyte, M.K.B., Dockrell, D.H.: The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One. 5, e8668 (2010)CrossRefGoogle Scholar
  28. 28.
    Rodriguez, P., Heyman, M., Candalh, C., Blaton, M.A., Bouchaud, C.: Tumour necrosis factor-α induced morphological and functional alterations of intestinal HT29 cl.19A cell monolayers. Cytokine. 7, 441–448 (1995)CrossRefGoogle Scholar
  29. 29.
    Moreau, M., Richards, J.C., Fournier, J.M., Byrd, R.A., Karakawa, W.W., Vann, W.F. Structure of the type 5 capsular polysaccharide of Staphylococcus aureus. Carbohydr. Res. 201, 285–297 (1990).Google Scholar
  30. 30.
    Prakobphol, A., Linzer, R., Genco, R.J.: Purification and characterization of a rhamnose-containing cell wall antigen of Streptococcus mutans B13 (serotype d). Infect. Immun. 27, 150–157 (1980).Google Scholar
  31. 31.
    Sadovskaya, I., Vinogradov, E., Courtin, P., Armalyte, J., Meyrand, M., Giaouris, E., Palussière, S., Furlan, S., Péchoux, C., Ainsworth, S., Mahony, J., van Sinderen, D., Kulakauskas, S., Guérardel, Y., Chapot-Chartier, M.P.: Another brick in the wall: a rhamnan polysaccharide trapped inside peptidoglycan of Lactococcus lactis. MBio. 8, pii: e01303–pii: e01317 (2017)CrossRefGoogle Scholar
  32. 32.
    Goldstein, I.J., Hay, G.W., Lewis, B.A., Smith, F.: Methods Carbohydr. Chem. 5, 361–370 (1965)Google Scholar
  33. 33.
    Koerner, T.A., Prestegard, J.H., Yu, R.K. Oligosaccharide structure by two-dimensional proton nuclear magnetic resonance spectroscopy. Methods Enzymol. 138, 38–59 (1987).Google Scholar
  34. 34.
    Aliprantis, A.O., Yang, R.B., Mark, M.R., Suggett, S., Devaux, B., Radolf, J.D., Klimpel, G.R., Godowski, P., Zychlinsky, A.: Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science. 285, 736–739 (1999)CrossRefGoogle Scholar
  35. 35.
    Angulo, S., Llopis, M., Antolín, M., Gironella, M., Sans, M., Malagelada, J.R., Piqué, J.M., Guarner, F., Panés, J.: Lactobacillus casei prevents the upregulation of ICAM-1 expression and leukocyte recruitment in experimental colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G1155–1162 (2006).Google Scholar
  36. 36.
    Elass-Rochard, E., Rombouts, Y., Coddeville, B., Maes, E., Blervaque, R., Hot, D., Kremer, L., Guérardel, Y.: Structural determination and Toll-like receptor 2-dependent proinflammatory activity of dimycolyl-diarabino-glycerol from Mycobacterium marinum. J. Biol. Chem. 287, 34432-34444 (2012)Google Scholar
  37. 37.
    Prieto, J., Eklund, A., Patarroyo, M.: Regulated expression of integrins and other adhesion molecules during differentiation of monocytes into macrophages. Cell. Immunol. 156, 191–211 (1994)CrossRefGoogle Scholar
  38. 38.
    Lebedeva, T., Dustin, M.L, Sykulev, Y.: ICAM-1 co-stimulates target cells to facilitate antigen presentation. Curr. Opin. Immunol. 17, 251–258 (2005).Google Scholar
  39. 39.
    Ryan, P.M., Ross, R.P., Fitzgerald, G.F., Caplice, N.M., Stanton, C.: Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications. Food Funct. 6, 679–693 (2015).Google Scholar
  40. 40.
    Choudhury, B., Leoff, C., Saile, E., Wilkins, P., Quinn, C.P., Kannenberg, E.L., Carlson, R.W. The structure of the major cell wall polysaccharide of Bacillus anthracis is species-specific. J. Biol. Chem. 281, 27932-27941 (2006)Google Scholar
  41. 41.
    Candela, T., Maes, E., Garenaux, E., Rombouts, Y., Krzewinski, F., Gohar, M., Guerardel, Y.: Environmental and biofilm-dependent changes in a Bacillus cereus secondary cell wall polysaccharide. J. Biol. Chem. 286, 31250-31262 (2011)Google Scholar
  42. 42.
    Forsberg, L.S., Choudhury, B., Leoff, C., Marston, C.K., Hoffmaster, A.R., Saile, E., Quinn, C.P., Kannenberg, E.L., Carlson, R.W.: Secondary cell wall polysaccharides from Bacillus cereus strains G9241, 03BB87 and 03BB102 causing fatal pneumonia share similar glycosyl structures with the polysaccharides from Bacillus anthracis. Glycobiology. 21, 934–948 (2011).Google Scholar
  43. 43.
    Nagaoka, M., Muto, M., Nomoto, K., Matuzaki, T., Watanabe, T., Yokokura, T.: Structure of polysaccharide-peptidoglycan complex from the cell wall of Lactobacillus casei YIT9018. J. Biochem. 108, 568–571 (1990).Google Scholar
  44. 44.
    Vinogradov, E., Sadovskaya, I., Grard, T., Chapot-Chartier, M.P.: Structural studies of the rhamnose-rich cell wall polysaccharide of Lactobacillus casei BL23. Carbohydr Res. 435, 156–161 (2016).Google Scholar
  45. 45.
    Vinogradov, E., Valence, F., Maes, E., Jebava, I., Chuat, V., Lortal, S., Grard, T., Guerardel, Y., Sadovskaya, I.: Structural studies of the cell wall polysaccharides from three strains of Lactobacillus helveticus with different autolytic properties: DPC4571, BROI, and LH1, Carbohydr. Res. 379, 7–12 (2013).Google Scholar
  46. 46.
    Ciszek-Lenda, M., Nowak, B., Srottek, M., Gamian, A., Marcinkiewicz, J.: Immunoregulatory potential of exopolysaccharide from Lactobacillus rhamnosus KL37: effects on the production of inflammatory mediators by mouse macrophages. Int. J. Exp. Pathol. 92, 382–391 (2011)CrossRefGoogle Scholar
  47. 47.
    Gao, K., Wang, C., Liu, L., Dou, X., Liu, J., Yuan, L., Zhang, W., Wang, H.: Immunomodulation and signaling mechanism of Lactobacillus rhamnosus GG and its components on porcine intestinal epithelial cells stimulated by lipopolysaccharide. J. Microbiol. Immunol. Infect. 50, 700–713 (2017).Google Scholar
  48. 48.
    Liu, C.F., Tseng, K.C., Chiang, S.S., Lee, B.H., Hsu, W.H., Pan, T.M.: Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. J. Sci. Food Agric. 91, 2284–2291 (2011)Google Scholar
  49. 49.
    Patten, D.A., Leivers, S., Chadha, M.J., Maqsood, M., Humphreys, P.N., Laws, A.P., Collett, A.: The structure and immunomodulatory activity on intestinal epithelial cells of the EPSs isolated from Lactobacillus helveticus sp. rosyjski and Lactobacillus acidophilus sp. 5e2. Carbohydr. Res. 384, 119–127 (2014)CrossRefGoogle Scholar
  50. 50.
    Patten, D.A., Laws, A.P.: Lactobacillus-produced exopolysaccharides and their potential health benefits: a review. Benef. Microbes. 6, 457–471 (2015)CrossRefGoogle Scholar
  51. 51.
    Shao, L., Wu, Z., Zhang, H., Chen, W., Ai, L., Guo, B.: Partial characterization and immunostimulatory activity of exopolysaccharides from Lactobacillus rhamnosus KF5. Carbohyd. Polym. 107, 51–56 (2014)CrossRefGoogle Scholar
  52. 52.
    Vinderola, G., Perdigon, G., Duarte, J., Farnworth, E., Matar, C.: Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine. 36, 254–260 (2006)CrossRefGoogle Scholar
  53. 53.
    Chanput, W., Mes, J.J., Wichers, H.J.: THP-1 cell line: An in vitro cell model for immune modulation approach. Int. Immunopharmacol. 23, 37–45 (2014)CrossRefGoogle Scholar
  54. 54.
    Lebeer, S., Claes, I.J., Verhoeven, T.L., Vanderleyden, J., De Keersmaecker, S.C.: Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb. Biotechnol. 4, 368–374 (2011)CrossRefGoogle Scholar
  55. 55.
    Chabot, S., Yu, H.-L., Léséleuc, L.D., Cloutier, D., Van Calsteren, M.-R., Lessard, M., Roy, D., Lacroix, M., Oth, D.: Exopolysaccharides from Lactobacillus rhamnosus RW-9595 M stimulate TNF. Lait. 81, 683–697 (2001)CrossRefGoogle Scholar
  56. 56.
    Górska, S., Sandstrőm, C., Wojas-Turek, J., Rossowska, J., Pajtasz-Piasecka, E., Brzozowska, E., Gamian, A.: Structural and immunomodulatory differences among lactobacilli exopolysaccharides isolated from intestines of mice with experimentally induced inflammatory bowel disease. Sci. Rep. 6, 37,613 (2016)CrossRefGoogle Scholar
  57. 57.
    Matsumoto, S., Hara, T., Nagaoka, M., Mike, A., Mitsuyama, K., Sako, T., Yamamoto, M., Kado, S., Takada, T.: A component of polysaccharide peptidoglycan complex on Lactobacillus induced an improvement of murine model of inflammatory bowel disease and colitis-associated cancer. Immunology. 128, e170–80 (2009).Google Scholar
  58. 58.
    Kishimoto, M., Nomoto, R., Mizuno, M., Osawa, R.: An in vitro investigation of immunomodulatory properties of Lactobacillus plantarum and L. delbrueckii cells and their extracellular polysaccharides. Biosci. Microbiota Food Health. 36, 101–110 (2017)CrossRefGoogle Scholar
  59. 59.
    Lebeer, S., Verhoeven, T.L.A., Francius, G., Schoofs, G., Lambrichts, I., Dufrêne, Y., Vanderleyden, J., De Keersmaecker, S.C.J.: Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl. Environ. Microbiol. 75, 3554–3563 (2009)CrossRefGoogle Scholar
  60. 60.
    Górska-Frączek, S., Sandstrom, C., Kenne, L., Rybka, J., Strus, M., Heczko, P., Gamian, A.: Structural studies of the exopolysaccharide consisting of a nonasaccharide repeating unit isolated from Lactobacillus rhamnosus KL37B. Carbohydr. Res. 346, 2926–2932 (2011)CrossRefGoogle Scholar
  61. 61.
    Nikolic, M., López, P., Strahinic, I., Suárez, A., Kojic, M., Fernández-García, M., Topisirovic, L., Golic, N., Ruas-Madiedo, P.: Characterisation of the exopolysaccharide (EPS)-producing Lactobacillus paraplantarum BGCG11 and its non-EPS producing derivative strains as potential probiotics. Int. J. Food Microbiol. 158, 155–162 (2012).Google Scholar
  62. 62.
    Polak-Berecka, M., Waśko, A., Paduch, R., Skrzypek, T., Sroka-Bartnicka, A.: The effect of cell surface components on adhesion ability of Lactobacillus rhamnosus. Antonie Van Leeuwenhoek. 106, 751–762 (2014).Google Scholar
  63. 63.
    Wachi, S., Kanmani, P., Tomosada, Y., Kobayashi, H., Yuri, T., Egusa, S., Shimazu, T., Suda, Y., Aso, H., Sugawara, M., Saito, T., Mishima, T., Villena, J., Kitazawa, H.: Lactobacillus delbrueckii TUA4408L and its extracellular polysaccharides attenuate enterotoxigenic Escherichia coli-induced inflammatory response in porcine intestinal epitheliocytes via Toll-like receptor-2 and 4. Mol. Nutr. Food Res. 58, 2080–2093 (2014)CrossRefGoogle Scholar
  64. 64.
    Devriese, S., Van den Bossche, L., Van Welden, S., Holvoet, T., Pinheiro, I., Hindryckx, P., De Vos, M., Laukens, D.: T84 monolayers are superior to Caco-2 as a model system of colonocytes. Histochem. Cell Biol. 148, 85–93 (2017).Google Scholar
  65. 65.
    Wang, F., Graham, W.V., Wang, Y., Witkowski, E.D., Schwarz, B.T., Turner J.R.: Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am. J. Pathol. 166, 409–419 (2005).Google Scholar
  66. 66.
    Contreras, T. C., Ricciardi, E., Cremonini, E., Oteiza, P.I.: (-)-Epicatechin in the prevention of tumor necrosis alpha-induced loss of Caco-2 cell barrier integrity. Arch. Biochem. Biophys. 573, 84–91 (2015).Google Scholar
  67. 67.
    Cui, W., Li, L.X., Sun, C.M., Wen, Y., Zhou, Y., Dong, Y.L., Liu, P.: Tumor necrosis factor alpha increases epithelial barrier permeability by disrupting tight junctions in Caco-2 cells. J. Med. Biol. Res. 43, 330–337 (2010).Google Scholar
  68. 68.
    Hsieh, C.Y., Osaka, T., Moriyama, E., Date, Y., Kikuchi, J., Tsuneda, S.: Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum. Physiol. Rep. 3, 12,327 (2015)CrossRefGoogle Scholar
  69. 69.
    Kawaguchi, H., Akazawa, Y., Watanabe, Y., Takakura, Y.: Permeability modulation of human intestinal Caco-2 cell monolayers by interferons. Eur. J. Pharm. Biopharm. 59, 45–50 (2005)CrossRefGoogle Scholar
  70. 70.
    Zivkovic, M., Hidalgo-Cantabrana, C., Kojic, M., Gueimonde, M., Golic, N., Ruas-Madiedo, P.: Capability of exopolysaccharide-producing Lactobacillus paraplantarum BGCG11 and its non-producing isogenic strain NB1, to counteract the effect of enteropathogens upon the epithelial cell line HT29-MTX. Food Res. Int. 74, 199–207 (2015).Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Emmanuel Maes
    • 1
  • Irina Sadovskaya
    • 2
  • Mathilde Lévêque
    • 3
  • Elisabeth Elass-Rochard
    • 1
  • Bruno Payré
    • 4
  • Thierry Grard
    • 2
  • Vassilia Théodorou
    • 3
  • Yann Guérardel
    • 1
  • Muriel Mercier-Bonin
    • 3
    Email author
  1. 1.CNRS UMR 8576, UGSF-Unité de Glycobiologie Structurale et FonctionnelleUniv LilleLilleFrance
  2. 2.Equipe Biochimie des Produits Aquatiques BPA, Institut Régional Charles Violette EA 7394, USC Anses-ULCOUniversité du Littoral-Côte d’OpaleBoulogne-sur-mer cedexFrance
  3. 3.Toxalim (Research Centre in Food Toxicology), INRA, ENVT, INP-Purpan, UPSUniversité de ToulouseToulouseFrance
  4. 4.Faculté de Médecine RangueilCentre de Microscopie Electronique Appliquée à la Biologie (CMEAB)Toulouse CedexFrance

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