S-Layer protein mediates the stimulatory effect of Lactobacillus helveticus MIMLH5 on innate immunity

Applied and Environmental Microbiology

Volumn 79, Issue 4, 2013, Pages 1221-1231

  Taverniti, Valentina ^a   Stuknyte, Milda ^a   Minuzzo, Mario ^a   Arioli, Stefania ^a   De Noni, Ivano ^a   Scabiosi, Christian ^a   Cordova, Zuzet Martinez ^b   Junttila, Ilkka ^b,c   Hämäläinen, Sanna ^b   Turpeinen, Hannu ^b   Mora, Diego ^a   Karp, Matti ^b   Pesu, Marko ^b,c   Guglielmetti, Simone ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c FIMLAB LABORATORIES   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; ANTI-INFLAMMATORY EFFECTS; BACTERIAL CELLS; BACTERIAL STRAINS; CYTOKINES; EPITHELIAL CACO-2 CELLS; EX-VIVO; HUMAN MACROPHAGES; IMMUNE CELLS; IMMUNE RESPONSE; IMMUNOMODULATORY EFFECTS; IN-VITRO; INNATE IMMUNE SYSTEMS; INNATE IMMUNITY; INTERLEUKIN-10; LACTOBACILLUS HELVETICUS; MOUSE BONES; PERITONEAL CAVITY; PROBIOTIC POTENTIALS; PROINFLAMMATORY; S-LAYER PROTEINS; STIMULATORY EFFECTS; TOLL-LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA;

CELL CULTURE; DISEASE CONTROL; MACROPHAGES; PROTEINS;

IMMUNE SYSTEM;

BACTERIAL DNA; BACTERIAL PROTEIN; IMMUNOLOGIC FACTOR; PROBIOTIC AGENT; SURFACE LAYER PROTEIN A, BACTERIA;

BACTERIUM; IMMUNE RESPONSE; IMMUNE SYSTEM; PROTEIN; TUMOR;

ARTICLE; CELL LINE; CHEMISTRY; DNA SEQUENCE; EPITHELIUM CELL; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LACTOBACILLUS HELVETICUS; MICROBIOLOGY; MOLECULAR GENETICS; MONOCYTE; NUCLEOTIDE SEQUENCE;

BACTERIAL PROTEINS; CELL LINE; DNA, BACTERIAL; EPITHELIAL CELLS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; LACTOBACILLUS HELVETICUS; MOLECULAR SEQUENCE DATA; MONOCYTES; PROBIOTICS; SEQUENCE ANALYSIS, DNA;

EID: 84874733256     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03056-12     Document Type: Article

References (76)

1. Hammes WP, Hertel C. 2006. The genera Lactobacillus and Carnobacterium, p 320-403. In Dworkin M, Falkow S (ed), The prokaryotes: a handbook on the biology of bacteria. Springer-Verlag, New York, NY.
2. Ringel-Kulka T, Palsson OS, Maier D, Carroll I, Galanko JA, Leyer G, Ringel Y. 2011. Probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium lactis Bi-07 versus placebo for the symptoms of bloating in patients with functional bowel disorders: a double-blind study. J. Clin. Gastroenterol. 45:518-525.
3. Szajewska H, Wanke M, Patro B. 2011. Meta-analysis: the effects of Lactobacillus rhamnosus GG supplementation for the prevention of healthcare-associated diarrhoea in children. Aliment. Pharmacol. Ther. 34:1079-1087.
4. FAO/WHO. 2002. Report of a joint FAO/WHO expert consultation on guidelines for the evaluation of probiotics in food. World Health Organization and Food and Agriculture Organization of the United Nations, London Ontario, Canada.
5. Won TJ, Kim B, Lee Y, Bang JS, Oh ES, Yoo JS, Hyung KE, Yoon J, Hwang S, Park ES, Park SY, Hwang KW. 2012. Therapeutic potential of Lactobacillus plantarum CJLP133 for house-dust mite-induced dermatitis in NC/Nga mice. Cell. Immunol. 277:49-57.
6. Guglielmetti S, Taverniti V, Minuzzo M, Arioli S, Zanoni I, Stuknyte M, Granucci F, Karp M, Mora D. 2010. A dairy bacterium displays in vitro probiotic properties for the pharyngeal mucosa by antagonizing group A streptococci and modulating the immune response. Infect. Immun. 78:4734-4743.
7. Stuknyte M, De Noni I, Guglielmetti S, Minuzzo M, Mora D. 2011. Potential immunomodulatory activity of bovine casein hydrolysates produced after digestion with proteinases of lactic acid bacteria. Int. Dairy J. 21:763-769.
8. Taverniti V, Minuzzo M, Arioli S, Junttila I, Hämäläinen S, Turpeinen H, Mora D, Karp M, Pesu M, Guglielmetti S. 2012. In vitro functional and immunomodulatory properties of the Lactobacillus helveticus MIMLh5-Streptococcus salivarius ST3 association that are relevant to the development of a pharyngeal probiotic product. Appl. Environ. Microbiol. 78:4209-4216.
9. Adams CA. 2010. The probiotic paradox: live and dead cells are biological response modifiers. Nutr. Res. Rev. 23:37-46.
10. Taverniti V, Guglielmetti S. 2011. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 6:261-274.
11. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, Nieuwenhuijs VB, Bollen TL, van Ramshorst B, Witteman BJ, Rosman C, Ploeg RJ, Brink MA, Schaapherder AF, Dejong CH, Wahab PJ, van Laarhoven CJ, van der Harst E, van Eijck CH, Cuesta MA, Akkermans LM, Gooszen HG. 2008. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, doubleblind, placebo-controlled trial. Dutch Acute Pancreatitis Study Group. Lancet 371:651-659.
12. Callanan M, Kaleta P, O'Callaghan J, O'Sullivan O, Jordan K, McAuliffe O, Sangrador-Vegas A, Slattery L, Fitzgerald GF, Beresford T, Ross RP. 2008. Genome sequence of Lactobacillus helveticus, an organism distinguished by selective gene loss and insertion sequence element expansion. J. Bacteriol. 190:727-735.
13. Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, Molle D, Lortal S, Altermann E, Klaenhammer TR, van Kooyk Y. 2008. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl. Acad. Sci. U. S. A. 105:19474-19479.
14. Weiss G, Rasmussen S, Zeuthen LH, Nielsen BN, Jarmer H, Jespersen L, Frøkiaer H. 2010. Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll-like receptor-2-dependent mechanism. Immunology 131:268-281.
15. Maroof H, Hassan ZM, Mobarez AM, Mohamadabadi MA. 19 June 2012. Lactobacillus acidophilus could modulate the immune response against breast cancer in murine model. J. Clin. Immunol. [Epub ahead of print.]
16. Taverniti V, Guglielmetti S. 2012. Health-promoting properties of Lactobacillus helveticus. Front. Microbiol. 3:392.
17. Lortal S, Vanheijenoort J, Gruber K, Sleytr UB. 1992. S-layer of Lactobacillus helveticus ATCC 12046: isolation, chemical characterization and re-formation after extraction with lithium chloride. J. Gen. Microbiol. 138:611-618.
18. Smit E, Oling F, Demel R, Martinez B, Pouwels PH. 2001. The S-layer protein of Lactobacillus acidophilus ATCC 4356: identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J. Mol. Biol. 305:245-257.
19. Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM. 2007. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell. Microbiol. 9:356-367.
20. Agave Biosystems. 2012. S-layer catalog. Agave Biosystems, Ithaca, NY. Accessed 26 August 2012.
21. Guglielmetti S, Taverniti V, Minuzzo M, Arioli S, Stuknyte M, Karp M, Mora D. 2010. Oral bacteria as potential probiotics for the pharyngeal mucosa. Appl. Environ. Microbiol. 76:3948-3958.
22. Sundstrom C, Nilsson K. 1976. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int. J. Cancer 17:565-577.
23. Harris P, Ralph P. 1985. Human leukemic models of myelomonocytic development: a review of the HL-60 and U937 cell lines. J. Leukoc. Biol. 37:407-422.
24. Radzun HJ, Parwaresch MR, Sundstrom C, Nilsson K, Eissner M. 1983. Monocytic origin of the human hematopoietic cell line U-937 and its convertibility to macrophages evidenced by isoenzyme mapping. Int. J. Cancer 31:181-186.
25. Jones BW, Heldwein KA, Means TK, Saukkonen JJ, Fenton MJ. 2001. Differential roles of Toll-like receptors in the elicitation of proinflammatory responses by macrophages. Ann. Rheum. Dis. 60:iii6-iii12.
26. Flo TH, Ryan L, Latz E, Takeuchi O, Monks BG, Lien E, Halaas Ø, Akira S, Skjåk-Braek G, Golenbock DT, Espevik T. 2002. Involvement of Toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 277:35489-35495.
27. Mozes N, Lortal S. 1995. X-ray photoelectron spectroscopy and biochemical analysis of the surface of Lactobacillus helveticus ATCC 12046. Microbiology 141:11-19.
28. Guglielmetti S, De Noni I, Caracciolo F, Molinari F, Parini C, Mora D. 2008. Bacterial cinnamoyl esterase activity screening for the production of a novel functional food product. Appl. Environ. Microbiol. 74:1284-1288.
29. Gardana C, Barbieri A, Simonetti P, Guglielmetti S. 2012. Biotransformation strategy to reduce allergens in propolis. Appl. Environ. Microbiol. 78:4654-4658.
30. Galdeano CM, de Moreno de LeBlanc A, Vinderola G, Bonet ME, Perdigón G. 2007. Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clin. Vaccine Immunol. 14:485-492.
31. Baldwin AS, Jr. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-683.
32. Yamamoto Y, Gaynor RB. 2001. Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer. J. Clin. Invest. 107:135-142.
33. Åvall-Jääskeläinen S, Palva A. 2005. Lactobacillus surface layers and their applications. FEMS Microbiol. Rev. 29:511-529.
34. Messner P, Allmaier G, Schäffer C, Wugeditsch T, Lortal S, König H, Niemetz R, Dorner M. 1997. Biochemistry of S-layers. FEMS Microbiol. Rev. 20:25-46.
35. Beveridge TJ, Pouwels PH, Sára M, Kotiranta A, Lounatmaa K, Kari K, Kerosuo E, Haapasalo M, Egelseer EM, Schocher I, Sleytr UB, Morelli L, Callegari ML, Nomellini JF, Bingle WH, Smit J, Leibovitz E, Lemaire M, Miras I, Salamitou S, Béguin P, Ohayon H, Gounon P, Matuschek M, Koval SF. 1997. Functions of S-layers. FEMS Microbiol. Rev. 20:99-149.
36. Horie M, Ishiyama A, Fujihira-Ueki Y, Sillanpää J, Korhonen TK, Toba T. 2002. Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing an S-layer. J. Appl. Microbiol. 92:396-403.
37. Smit E, Jager D, Martinez B, Tielen FJ, Pouwels PH. 2002. Structural and functional analysis of the S-layer protein crystallisation domain of Lactobacillus acidophilus ATCC 4356: evidence for protein-protein interaction of two subdomains. J. Mol. Biol. 324:953-964.
38. Frece J, Kos B, Svetec IK, Zgaga Z, Mrsa V, Susković J. 2005. Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J. Appl. Microbiol. 98:285-292.
39. Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić S. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94:981-987.
40. Buck BL, Altermann E, Svingerud T, Klaenhammer TR. 2005. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 71:8344-8351.
41. Li P, Yin Y, Yu Q, Yang Q. 2011. Lactobacillus acidophilus S-layer protein-mediated inhibition of Salmonella-induced apoptosis in Caco-2 cells. Biochem. Biophys. Res. Commun. 409:142-147.
42. Beganović J, Frece J, Kos B, Leboš Pavunc A, Habjanič K, Šušković J. 2011. Functionality of the S-layer protein from the probiotic strain Lactobacillus helveticus M92. Antonie Van Leeuwenhoek 100:43-53.
43. Aderem A, Underhill DM. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17:593-623.
44. Benoit M, Desnues B, Mege JL. 2008. Macrophage polarization in bacterial infections. J. Immunol. 181:3733-3739.
45. Belardelli F. 1995. Role of interferons and other cytokines in the regulation of the immune response. APMIS 103:161-179.
46. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147:3815-3822.
47. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G. 1993. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 178:1041-1048.
48. Williams CS, Mann M, DuBois RN. 1999. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18:7908-7916.
49. Morteau O, Morham SG, Sellon R, Dieleman LA, Langenbach R, Smithies O, Sartor RB. 2000. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J. Clin. Invest. 105:469-478.
50. Christensen HR, Frokiaer H, Pestka JJ. 2002. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 168:171-178.
51. Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, Mizumachi K, Kurisaki J. 2002. Cytokine production by the murine macrophage cell line J774.1 after exposure to lactobacilli. Biosci. Biotechnol. Biochem. 66:1963-1966.
52. Perdigón G, Maldonado GC, Valdez JC, Medici M. 2002. Interaction of lactic acid bacteria with the gut immune system. Eur. J. Clin. Nutr. 56:S21-S26.
53. Ongol MP, Iguchi T, Tanaka M, Sone T, Ikeda H, Asano K, Nishimura T. 2008. Potential of selected strains of lactic acid bacteria to induce a Th1 immune profile. Biosci. Biotechnol. Biochem. 72:2847-2857.
54. Kwon B, Kim BS, Cho HR, Park JE, Kwon BS. 2003. Involvement of tumor necrosis factor receptor superfamily (TNFRSF) members in the pathogenesis of inflammatory diseases. Exp. Mol. Med. 35:8-16.
55. Yasutake N, Matsuzaki T, Kimura K, Hashimoto S, Yokokura T, Yoshikai Y. 1999. The role of tumor necrosis factor (TNF)-alpha in the antitumor effect of intrapleural injection of Lactobacillus casei strain Shirota in mice. Med. Microbiol. Immunol. 188:9-14.
56. Wajant H, Pfizenmaier K, Scheurich P. 2003. Tumor necrosis factor signaling. Cell. Death Differ. 10:45-65.
57. Dinarello CA. 2003. Anti-cytokine therapeutics and infections. Vaccine 21:S24-S34.
58. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2010. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8:171-184.
59. Otte JM, Mahjurian-Namari R, Brand S, Werner I, Schmidt WE, Schmitz F. 2009. Probiotics regulate the expression of COX-2 in intestinal epithelial cells. Nutr. Cancer 61:103-113.
60. Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B. 2010. Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 299:G1118-G1127.
61. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, Sahoo A, Nam JH, Rhee JH, Hwang KC, Im SH. 2010. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. U. S. A. 107:2159-2164.
62. Wallace JL. 2006. COX-2: a pivotal enzyme in mucosal protection and resolution of inflammation. ScientificWorldJournal 6:577-588.
63. Newberry RD, Stenson WF, Lorenz RG. 1999. Cyclooxygenase-2-dependent arachidonic acid metabolites are essential modulators of the intestinal immune response to dietary antigen. Nat. Med. 5:900-906.
64. Tan XD, Chen YH, Liu QP, Gonzalez-Crussi F, Liu XL. 2000. Prostanoids mediate the protective effect of trefoil factor 3 in oxidant-induced intestinal epithelial cell injury: role of cyclooxygenase-2. J. Cell Sci. 113: 2149-2155.
65. de Ambrosini VM, Gonzalez S, Perdigon G, de Ruiz Holgado AP, Oliver G. 1996. Chemical composition of the cell wall of lactic acid bacteria and related species. Chem. Pharm. Bull. 44:2263-2267.
66. Tejada-Simon MV, Pestka JJ. 1999. Proinflammatory cytokine and nitric oxide induction in murine macrophages by cell wall and cytoplasmic extracts of lactic acid bacteria. J. Food Prot. 62:1435-1444.
67. Vinderola CG, Medici M, Perdigón G. 2004. Relationship between interaction sites in the gut, hydrophobicity, mucosal immunomodulating capacities and cell wall protein profiles in indigenous and exogenous bacteria. J. Appl. Microbiol. 96:230-243.
68. Arribas B, Rodríguez-Cabezas ME, Camuesco D, Comalada M, Bailón E, Utrilla P, Nieto A, Concha A, Zarzuelo A, Gálvez J. 2009. A probiotic strain of Escherichia coli, Nissle 1917, given orally exerts local and systemic anti-inflammatory effects in lipopolysaccharide-induced sepsis in mice. Br. J. Pharmacol. 157:1024-1033.
69. Arribas B, Rodríguez-Cabezas ME, Comalada M, Bailón E, Camuesco D, Olivares M, Xaus J, Zarzuelo A, Gálvez J. 2009. Evaluation of the preventative effects exerted by Lactobacillus fermentum in an experimental model of septic shock induced in mice. Br. J. Nutr. 101:51-58.
70. Habil N, Al-Murrani W, Beal J, Foey AD. 2011. Probiotic bacterial strains differentially modulate macrophage cytokine production in a strain-dependent and cell subset-specific manner. Benef. Microbes 2:283-293.
71. Marcinkiewicz J, Ciszek M, Bobek M, Strus M, Heczko PB, Kurnyta M, Biedroń R, Chmielarczyk A. 2007. Differential inflammatory mediator response in vitro from murine macrophages to lactobacilli and pathogenic intestinal bacteria. Int. J. Exp. Pathol. 88:155-164.
72. Vizoso Pinto MG, Rodriguez Gómez M, Seifert S, Watzl B, Holzapfel WH, Franz CM. 2009. Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int. J. Food Microbiol. 133:86-93.
73. Zeuthen LH, Fink LN, Frøkiaer H. 2008. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology 124:489-502.
74. Sleytr UB, Gyorvary E, Pum D. 2003. Crystallization of S-layer protein lattices on surfaces and interfaces. Prog. Org. Coat. 47:279-287.
75. Sleytr UB, Egelseer EM, Ilk N, Pum D, Schuster B. 2007. S-layers as a basic building block in a molecular construction kit. FEBS J. 274:323-334.
76. Pum D, Sleytr UB. 1999. The application of bacterial S-layers in molecular nanotechnology. Trends Biotechnol. 17:8-12.