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The Lactobacillus plantarum Eno A1 Enolase Is Involved in Immunostimulation of Caco-2 Cells and in Biofilm Development

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Advances in Microbiology, Infectious Diseases and Public Health

Abstract

The role of probiotics in prevention and treatment of a variety of diseases is now well assessed. The presence of adhesive molecules on the cell surface of probiotics has been related to the ability to confer health benefit to the host. We have previously shown that the enolase EnoA1 of Lactobacillus plantarum, one of the most predominant species in the gut microbiota of healthy individuals, is cell surface-expressed and is involved in binding with human fibronectin and plasminogen. By means of comparative analysis between L. plantarum LM3 (wild type) and its isogenic LM3-CC1 (ΔenoA1) mutant strain, here we show that EnoA1 affects the ability of this bacterium to modulate immune response as determined by analysis of expression of immune system molecules in Caco-2 cells. Indeed, we observed induction of TLR2 expression in cells exposed to L. plantarum LM3, while no induction was detectable in cells exposed to LM3-CC1. This difference was much less consistent when expression of TLR4 was determined in cells exposed to the two strains. Pro-inflammatory (IL-6) and anti-inflammatory cytokines (IL-10, TGF-β), and the antimicrobial peptide HBD-2 were induced in Caco-2 cells exposed to L. plantarum LM3, while lower levels of induction were detected in cells exposed to LM3-CC1. We also analyzed the ability to develop biofilm of the two strains, and observed a decrease of about 65 % in the development of mature biofilm in LM3-CC1 compared to the wild type.

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References

  • Abreu MT, Thomas LS, Arnold ET, Lukasek K, Michelsen KS, Arditi M (2003) TLR signaling at the intestinal epithelial interface. J Endotoxin Res 9:322–330

    Article  CAS  PubMed  Google Scholar 

  • Abreu MT, Fukata M, Arditi M (2005) TLR signaling in the gut in health and disease. J Immunol 174:4453–4456

    Article  CAS  PubMed  Google Scholar 

  • Adams CA (2010) The probiotic paradox: live and dead cells are biological response modifiers. Nutr Res Rev 23:37–46

    Article  CAS  PubMed  Google Scholar 

  • Adrian PV, Bogaert D, Oprins M, Rapola S, Lahdenkari M, Kilpi T, de Groot R, Kayhty H, Hermans PW (2015) Development of antibodies against pneumococcal proteins alpha-enolase, immunoglobulin A1 protease, streptococcal lipoprotein rotamase A, and putative proteinase maturation protein A in relation to pneumococcal carriage and Otitis Media. Vaccine 22:2737–2742

    Article  Google Scholar 

  • Ahrne S, Hagslatt ML (2011) Effect of lactobacilli on paracellular permeability in the gut. Nutrients 3:104–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bermudez-Brito MB, Munoz-Quezada SM, Gomez-Llorente CG, Matencio E, Bernal MJ, Romero F, Gil A (2012) Human intestinal dendritic cells decrease cytokine release against Salmonella infection in the presence of Lactobacillus paracasei upon TLR activation. Plose one 8:e43197

    Article  Google Scholar 

  • Boirivant M, Strober W (2007) The mechanism of action of probiotics. Curr Opin Gastroenterol 23:679–692

    Article  PubMed  Google Scholar 

  • Cario E, Podolsky DK (2000) Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68:7010–7017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castaldo C, Vastano V, Siciliano RA, Candela M, Vici M, Muscariello L, Marasco R, Sacco M (2009) Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb Cell Fact 8:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Darab G, Mohamed H, Patrisio NN, Michael DV, Arnold G, Samweul IS, Sabah TA, Abd El-Al A, Abdel K, Knut JH, Jurgen S (2011) Suppression subtractive hybridization identifies bacterial genomic regions that are possibly involved in hBD-2 regulation by enterocytes. Mol Nutr Food Res 55:1533–1542

    Article  Google Scholar 

  • Dinis M, Tavares D, Veiga-Malta I (2009) Oral therapeutic vaccination with Streptococcus sobrinus recombinant enolase confers protection against dental caries in rats. J Infect Dis 199:116–123

    Article  PubMed  Google Scholar 

  • Faure E, Thomas L, Xu H, Medvedev AE, Equils O, Arditi M (2001) Bacterial lipopolysaccharide and IFN-γ induce toll-like receptor 2 and toll-like receptor 4 expression in human endothelial cells: role of NF-kB activation. J Immunol 166:2018–2024

    Article  CAS  PubMed  Google Scholar 

  • Gareau MG, Sherman PM, Walker WA (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7:503–514

    Article  PubMed  PubMed Central  Google Scholar 

  • Grimbaldeston MA, Nakae S, Kalesnikoff J, Tsai M, Galli SJ (2007) Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol 8:1095–1104

    Article  CAS  PubMed  Google Scholar 

  • Hamon MA, Lazazzera B (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42:1199–1209

    Article  CAS  PubMed  Google Scholar 

  • Henderson B, Martin A (2013) Bacterial moonlighting proteins and bacterial virulence. Curr Top Microbiol Immunol 358:155–213

    CAS  PubMed  Google Scholar 

  • Himanshu K, Taro K, Shizuo A (2001) Pathogen recognition by the innate immune system. Int Rev Immunol 30:16–34

    Google Scholar 

  • Hugo AA, De Antoni GL, Pérez PF (2010) Lactobacillus delbrueckii subsp lactis (strain CIDCA 133) resists the antimicrobial activity triggered by molecules derived from enterocyte-like Caco-2 cells. Lett Appl Microbiol 50:335–340

    Article  CAS  PubMed  Google Scholar 

  • Jones SE, Bersalivic J (2009) Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 9:35–43

    Article  PubMed  PubMed Central  Google Scholar 

  • Kainulanen V, Korhonen TK (2014) Dancing to another tune-adhesive moonlighting proteins in bacteria. Biology 3:178–204

    Article  Google Scholar 

  • Kaushik JK, Kumar A, Duary RK, Mohanty AK, Grover S (2009) Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PLoS One 4:8099

    Article  Google Scholar 

  • Kelly D, Conway S (2005) Bacterial modulation of mucosal innate immunity. Mol Immunol 42:895–901

    Article  CAS  PubMed  Google Scholar 

  • Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA (2006) Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24:99–146

    Article  CAS  PubMed  Google Scholar 

  • Lonnermark E, Friman V, Lappas G, Sandberg T, Berggren A, Adlerberth I (2010) Intake of Lactobacillus plantarum reduces certain gastrointestinal symptoms during treatment with antibiotics. J Clin Gastroenterol 44:106–112

    Article  PubMed  Google Scholar 

  • Macfarlane S (2008) Microbial biofilm communities in the gastrointestinal tract. J Clin Gastroenterol 42:142–143

    Article  Google Scholar 

  • Marian CA, Colin LN, Jack S (2009) Dysregulation of human β-defensin-2 protein in inflammatory bowel disease. PLoS One 4(7):e6285

    Article  Google Scholar 

  • Melmed G, Thomas LS, Lee N, Tesfay SY, Lukasek K, Michelsen KS, Zhou Y, Hu B, Arditi M, Abreu MT (2003) Human intestinal epithelial cells are broadly unresponsive to toll-like receptor 2-dependent bacterial ligands: implication for host-microbial interaction in the gut. J Immunol 170:1406–1415

    Article  CAS  PubMed  Google Scholar 

  • Muscariello L, Marino C, Capri U, Vastano V, Marasco R, Sacco M (2013) CcpA and three newly identified proteins are involved in biofilm development in Lactobacillus plantarum. J Basic Microbiol 53:62–71

    Article  CAS  PubMed  Google Scholar 

  • Naik S, Kelly EJ, Meijer L, Pettersson S, Sanderson IR (2001) Absence of toll-like receptor 4 explains endotoxin hyporesponsiveness in human intestinal epithelium. J Pediatr Gastroenterol Nutr 32:449–453

    Article  CAS  PubMed  Google Scholar 

  • Otte JM, Cario E, Podolsky DK (2004) Mechanisms of cross hyporesponsiveness to toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126:1054–1070

    Article  CAS  PubMed  Google Scholar 

  • Pancholi V (2001) Multifuncional α-enolase: its role in diseases. Cell Mol Life Sci 58:902–920

    Article  CAS  PubMed  Google Scholar 

  • Peyrin-Biroulet L, Vignal C, Dessein R, Simonet M, Desreumaux P, Chamaillard M (2006) NODs in defence: from vulnerable antimicrobial peptides to chronic inflammation. Trends Microbiol 14:432–438

    Article  CAS  PubMed  Google Scholar 

  • Ruiz PA, Hoffmann M, Szcesny S, Blaut M, Haller D (2005) Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats. Immunology 115:441–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlee M, Wehkamp J, Altenhoefer A, Oelschlaeger T, Stange E, Fellermann K (2007) Induction of human beta-Defensin 2 by the probiotic Escherichia coli NISSLE 1917 is mediated through flagellin. Infect Immun 75:2399–2407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlee M, Harder J, Köten B, Stange EF, Wehkamp J, Fellermann K (2008) Probiotic lactobacilli and VSL#3 induce enterocyte beta-defensin 2. Clin Exp Immunol 151:528–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sieling PA, Modlin RL (2002) Toll-like receptors: mammalian taste receptors for a smorgasbord of microbial invaders. Curr Opin Microbiol 5:70–75

    Article  CAS  PubMed  Google Scholar 

  • Ukena SN, Westendorf AM, Hansen W, Rohde M, Geffers R, Coldewey S, Suerbaum S, Buer J, Gunzer F (2005) The host response to the probiotic Escherichia coli strain Nissle 1917: specific up-regulation of the proinflammatory chemokine MCP-1. BMC Med Genet 6:43–67

    Article  PubMed  PubMed Central  Google Scholar 

  • Valaesk MA, Repa JJ (2005) The power of real-time PCR. Adv Physiol Educ 29:151–159

    Article  Google Scholar 

  • van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, de Groot PJ, Hooiveld GJ, Brummer RJ, Kleerebezem M (2009) Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci 106:2371–2376

    Article  PubMed  PubMed Central  Google Scholar 

  • Vastano V, Capri U, Candela M, Siciliano RA, Russo L, Renda M, Sacco M (2013) Identification of binding sites of Lactobacillus plantarum enolase involved in the interaction with human plasminogen. Microbiol Res 168:65–72

    Article  CAS  PubMed  Google Scholar 

  • Veiga-Malta I, Duarte M, Dinis M, Tavares D, Videira A, Ferreira P (2004) Enolase from Streptococcus sobrinus is an immunosuppressive protein. Cell Microbiol 6:79–88

    Article  CAS  PubMed  Google Scholar 

  • Villena J, Kitazava H (2014) Modulation of intestinal TLR4-inflammatory signaling pathways by probiotic microorganisms: lessons learned from Lactobacillus jensenii TL2937. Frontiers in Immunol 4:512

    Article  Google Scholar 

  • Vinderola G, Matar C, Perdigon G (2005) Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of toll-like receptors. Clin Diagn Lab Immunol 12:1075–1084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vora P, Youdim A, Thomas LS, Fukata M, Tesfay SY, Lukasek K, Michelsen LS, Wada A, Hirayama T, Arditi M, Abreu MT (2004) Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 173:5398–5405

    Article  CAS  PubMed  Google Scholar 

  • Vuotto C, Longo F, Donelli G (2014) Probiotics to counteract biofilm-associated infections: promising and conflicting data. Int J Oral Sci 6:189–194

    Article  PubMed  Google Scholar 

  • Wehkamp J, Harder J, Wehkamp K, Wehkamp-von Meissner B, Schlee M, Enders C, Sonnenborn U, Nuding S, Bengmark S, Fellermann K, Schröder JM, Stange EF (2004) NF-kappaB- and AP-1- mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect Immun 72:5750–5758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Giovanna Donnarumma .

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Vastano, V., Pagano, A., Fusco, A., Merola, G., Sacco, M., Donnarumma, G. (2015). The Lactobacillus plantarum Eno A1 Enolase Is Involved in Immunostimulation of Caco-2 Cells and in Biofilm Development. In: Donelli, G. (eds) Advances in Microbiology, Infectious Diseases and Public Health. Advances in Experimental Medicine and Biology(), vol 897. Springer, Cham. https://doi.org/10.1007/5584_2015_5009

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