Extracellular molecular effectors mediating probiotic attributes

FEMS Microbiology Letters

Volumn 359, Issue 1, 2014, Pages 1-11

  Ruiz, Lorena ^a   Hevia, Arancha ^b   Bernardo, David ^c   Margolles, Abelardo ^b   Sánchez, Borja ^d  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF VIGO   (Spain)

Author keywords

Bioactive compounds; Extracellular molecules; Gut bacteria; Probiotics

Indexed keywords

ACETIC ACID; BACTERIOCIN; CONJUGATED LINOLEIC ACID; EXOPOLYSACCHARIDE; FLAGELLIN; LACTIC ACID; LACTOCEPIN; LIPOTEICHOIC ACID; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; PEPTIDE; PEPTIDOGLYCAN POLYSACCHARIDE; POLYSACCHARIDE A; PROBIOTIC AGENT; PROTEIN P40; PROTEIN P75; PROTEIN SLPA; SERINE PROTEINASE INHIBITOR; TEICHOIC ACID; THURICIN; UNCLASSIFIED DRUG; VSL3; BIOLOGICAL PRODUCT;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; BACTERIAL CELL WALL; BACTERIOSTASIS; BIFIDOBACTERIUM LONGUM; CITROBACTER RODENTIUM; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; COLON INJURY; CROHN DISEASE; DENDRITIC CELL; DRUG EFFECT; ENTEROBACTERIACEAE INFECTION; FIMBRIA; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS AMYLOVORUS; LACTOBACILLUS BREVIS; LACTOBACILLUS CRISPATUS; LACTOBACILLUS GASSERI; LACTOBACILLUS HELVETICUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS KEFIR; LACTOBACILLUS MUCOSAE; LACTOBACILLUS PARAKEFIR; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SOBRIUS; LISTERIOSIS; NONHUMAN; PROTEIN SECRETION; SHORT SURVEY; BACTERIUM; DIET THERAPY; INFLAMMATION; ISOLATION AND PURIFICATION; METABOLISM;

BACTERIA; BIOLOGICAL PRODUCTS; HUMANS; INFLAMMATION; PROBIOTICS;

EID: 84907960845     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12576     Document Type: Short Survey

References (82)

1. Al-Hassi HO, Mann ER, Sánchez B et al. (2013) Altered human gut dendritic cell properties in ulcerative colitis are reversed by Lactobacillus plantarum extracellular encrypted peptide STp. Mol Nutr Food Res 58: 1132-1143.
2. Bassaganya-Riera J, Viladomiu M, Pedragosa M et al. (2012) Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR c to suppress colitis. PLoS One 7: e31238.
3. Bäuerl C, Pérez-Martínez G, Yan F, Polk DB&Monedero V (2010) Functional analysis of the p40 and p75 proteins from Lactobacillus casei BL23. J Mol Microbiol Biotechnol 19:231-241.
4. Bello FD, Walter J, Hertel C&Hammes WP (2001) In vitro study of prebiotic properties of levan-type exopolysaccharides from Lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst Appl Microbiol 24: 232-237.
5. Bermudez-Brito M, Muñoz-Quezada S, Gomez-Llorente C, Matencio E, Bernal MJ, Romero F&Gil A (2012a) Human intestinal dendritic cells decrease cytokine release against Salmonella infection in the presence of Lactobacillus paracasei upon TLR activation. PLoS One 7: e43197.
6. Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C&Gil A (2012b) Probiotic mechanisms of action. Ann Nutr Metab 61: 160-174.
7. Bernardo D, Garrote JA, Nadal I, León AJ, Calvo C, Fernández-Salazar L, Blanco-Quirós A, Sanz Y&Arranz E (2009) Is it true that coeliacs do not digest gliadin? Degradation pattern of gliadin in coeliac disease small intestinal mucosa. Gut 58: 886-887.
8. Bernardo D, Sánchez B, Al-Hassi HO, Mann ER, Urdaci MC, Knight SC&Margolles A (2012) Microbiota/host crosstalk biomarkers: regulatory response of human intestinal dendritic cells exposed to Lactobacillus extracellular encrypted peptide. PLoS One 7: e36262.
9. Carlsson AH, Yakymenko O, Olivier I, Hàkansson F, Postma E, Keita AV&Söderholm JD (2013) Faecalibacterium prausnitzii supernatant improves intestinal barrier function in mice DSS colitis. Scand J Gastroenterol 48: 1136-1144.
10. Ciszek-Lenda M, Nowak B, Sróttek M, Gamian A & Marcinkiewicz J (2011) 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.
11. Claes IJ, Lebeer S, Shen C et al. (2010) Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clin Exp Immunol 162: 306-314.
12. Coakley M, Banni S, Johnson MC, Mills S, Devery R, Fitzgerald G, Paul Ross R&Stanton C (2009) Inhibitory effect of conjugated alpha-linolenic acid from bifidobacteria of intestinal origin on SW480 cancer cells. Lipids 44: 249-256.
13. Corr SC, Li Y, Riedel CU, O'Toole PW, Hill C&Gahan CG (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. P Natl Acad Sci USA 104: 7617-7621.
14. De Vuyst L&Leroy F (2011) Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifidobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol 149:73-80.
15. Dobson A, Cotter PD, Ross RP&Hill C (2012) Bacteriocin production: a probiotic trait? Appl Environ Microbiol 78:1-6.
16. Duncker SC, Wang L, Hols P&Bienenstock J (2008) The D-alanine content of lipoteichoic acid is crucial for Lactobacillus plantarum-mediated protection from visceral pain perception in a rat colorectal distension model. Neurogastroenterol Motil 20: 843-850.
17. Ewaschuk JB, Walker JW, Diaz H&Madsen KL (2006) Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice. J Nutr 136:1483-1487.
18. Fanning S, Hall LJ, Cronin M et al. (2012) Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. P Natl Acad Sci USA 109: 2108-2113.
19. Fukuda S, Toh H, Hase K et al. (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469: 543-547.
20. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, Pot B, Hartung T, Hols P&Mercenier A (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. P Natl Acad Sci USA 102: 10321-10326.
21. Hernandez-Mendoza A, Guzman-de-Peña D&Garcia HS (2009) Key role of teichoic acids on aflatoxin B binding by probiotic bacteria. J Appl Microbiol 107:395-403.
22. Hevia A, Martínez N, Ladero V, Alvarez MA, Margolles A & Sánchez B (2013) An extracellular Serine/Threonine-rich protein from Lactobacillus plantarum NCIMB 8826 is a novel aggregation-promoting factor with affinity to mucin. Appl Environ Microbiol 79: 6059-6066.
23. Hidalgo-Cantabrana C, Sánchez B, Moine D, Berger B, de Los Reyes-Gavilán CG, Gueimonde M, Margolles A & Ruas-Madiedo P (2013) Insights into the ropy phenotype of the exopolysaccharide-producing strain Bifidobacterium animalis subsp. lactis A1dOxR. Appl Environ Microbiol 79:3870-3874.
24. Hooper LV, Littman DR&Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336: 1268-1273.
25. Hosono A, Lee J, Ametani A, Natsume M, Hirayama M, Adachi T&Kaminogawa S (1997) Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101-4. Biosci Biotechnol Biochem 61: 312-316.
26. Hynönen U&Palva A (2013) Lactobacillus surface layer proteins: structure, function and applications. Appl Microbiol Biotechnol 97: 5225-5243.
27. Ismail B&Nampoothiri KM (2010) Production, purification and structural characterization of an exopolysaccharide produced by a probiotic Lactobacillus plantarum MTCC 9510. Arch Microbiol 192: 1049-1057.
28. Ivanov D, Emonet C, Foata F, Affolter M, Delley M, Fisseha M, Blum-Sperisen S, Kochhar S&Arigoni F (2006) A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. J Biol Chem 281: 17246-17252.
29. Kaji R, Kiyoshima-Shibata J, Nagaoka M, Nanno M&Shida KJ (2010) Bacterial teichoic acids reverse predominant IL-12 production induced by certain Lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J Immunol 184: 3505-3513.
30. Kamada N, Seo SU, Chen GY&Núñez G (2013) Role of gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13: 321-335.
31. Kamiya T, Wang L, Forsythe P, Goettsche G, Mao Y, Wang Y, Tougas G&Bienenstock J (2006) Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55: 191-196.
32. Kang CS, Ban M, Choi EJ et al. (2013) Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS One 8: e76520.
33. Kankainen M, Paulin L, Tynkkynen S et al. (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. P Natl Acad Sci USA 106: 17193-17198.
34. Kim Y, Oh S&Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379: 324-329.
35. Kodali VP&Sen R (2008) Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol J 3: 245-251.
36. Konstantinov SR, Smidt H, de Vos WM et al. (2008) S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. P Natl Acad Sci USA 105: 19474-19479.
37. Lebeer S, Vanderleyden J&De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72: 728-764.
38. 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.
39. Lebeer S, Claes IJ, Verhoeven TL, Vanderleyden J&De Keersmaecker SC (2011) Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 4:368-374.
40. Lebeer S, Claes I, Tytgat HL et al. (2012a) Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol 78: 185-193.
41. Lebeer S, Claes IJ&Vanderleyden J (2012b) Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol 20: 5-10.
42. Leivers S, Hidalgo-Cantabrana C, Robinson G, Margolles A, Ruas-Madiedo P&Laws AP (2011) Structure of the high molecular weight exopolysaccharide produced by Bifidobacterium animalis subsp. lactis IPLA-R1 and sequence analysis of its putative eps cluster. Carbohydr Res 346:2710-2717.
43. Littman DR&Pamer EG (2013) Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 10: 311-323.
44. Loscher CE, Draper E, Leavy O, Kelleher D, Mills KH & Roche HM (2005) Conjugated linoleic acid suppresses NF-kappa B activation and IL-12 production in dendritic cells through ERK-mediated IL-10 induction. J Immunol 175: 4990-4998.
45. Mann ER, Bernardo D, Al-Hassi HO et al. (2012) Human gut-specific homeostatic dendritic cells are generated from blood precursors by the gut microenvironment. Inflamm Bowel Dis 18: 1275-1286.
46. Martin R, Miquel S, Ulmer J, Kechanou N, Langella P & Bermudez-Humaran LG (2013) Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb Cell Fact 12: 71.
47. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T&Yoshikai Y (2003) Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor alpha-inducing activities in macrophages through Toll-like receptor 2. Clin Diagn Lab Immunol 10: 259-266.
48. Matsuki T, Pédron T, Regnault B, Mulet C, Hara T & Sansonetti PJ (2013) Epithelial cell proliferation arrest induced by lactate and acetate from Lactobacillus casei and Bifidobacterium breve. PLoS One 8: e63053.
49. Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, Suzuki A&Sata M (2005) Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin Exp Immunol 140: 417-426.
50. Mazmanian SK, Round JL&Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453: 620-625.
51. Mohamadzadeh M, Pfeiler EA, Brown JB et al. (2011) Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. P Natl Acad Sci USA 108(suppl 1): 4623-4630.
52. Mozzi F, Gerbino E, Font de Valdez G&Torino MI (2009) Functionality of exopolysaccharides produced by lactic acid bacteria in an in vitro gastric system. J Appl Microbiol 107:56-64.
53. Nagai T, Makino S, Ikegami S, Itoh H&Yamada H (2011) Effects of oral administration of yogurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 and its exopolysaccharides against influenza virus infection in mice. Int Immunopharmacol 11: 2246-2250.
54. O'Connell Motherway M, Zomer A, Leahy SC et al. (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. P Natl Acad Sci USA 108: 11217-11222.
55. Rea MC, Sit CS, Clayton E, O'Connor PM, Whittal RM, Zheng J, Vederas JC, Ross RP&Hill C (2010) Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. P Natl Acad Sci USA 107: 9352-9357.
56. Reynolds CM, Draper E, Keogh B, Rahman A, Moloney AP, Mills KH, Loscher CE&Roche HM (2009) A conjugated linoleic acid-enriched beef diet attenuates lipopolysaccharide-induced inflammation in mice in part through PPARgamma-mediated suppression of toll-like receptor 4. J Nutr 139: 2351-2357.
57. Rosberg-Cody E, Stanton C, O'Mahony L, Wall R, Shanahan F, Quigley EM, Fitzgerald GF&Ross RP (2011) Recombinant lactobacilli expressing linoleic acid isomerase can modulate the fatty acid composition of host adipose tissue in mice. Microbiology 157: 609-615.
58. Ruas-Madiedo P&de los Reyes-Gavilán CG (2005) Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci 88: 843-856.
59. Ruas-Madiedo P, Medrano M, Salazar N, De Los Reyes-Gavilán CG, Pérez PF&Abraham AG (2010) Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J Appl Microbiol 109:2079-2086.
60. Saier MH (2006) Protein secretion systems in Gram-negative bacteria. Microbe 1: 414-419.
61. Salazar N, Ruas-Madiedo P, Kolida S, Collins M, Rastall R, Gibson G&de Los Reyes-Gavilán CG (2009) Exopolysaccharides produced by Bifidobacterium longum IPLA E44 and Bifidobacterium animalis subsp. lactis IPLA R1 modify the composition and metabolic activity of human faecal microbiota in pH-controlled batch cultures. Int J Food Microbiol 135: 260-267.
62. Sanchez CJ, Shivshankar P, Stol K, Trakhtenbroit S, Sullam PM, Sauer K, Hermans PW&Orihuela CJ (2010) The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesion that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog 6: e1001044.
63. Sánchez B, Arias S, Chaignepain S, Denayrolles M, Schmitter JM, Bressollier P&Urdaci MC (2009) Identification of surface proteins involved in the adhesion of a probiotic Bacillus cereus strain to mucin and fibronectin. Microbiology 155: 1708-1716.
64. Sánchez B, Urdaci MC&Margolles A (2010) Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology 156: 3232-3242.
65. Sánchez B, González-Tejedo C, Ruas-Madiedo P, Urdaci MC & Margolles A (2011) Lactobacillus plantarum extracellular chitin binding protein and its role in the interaction between chitin, Caco-2 cells and mucin. Appl Environ Microbiol 77: 1123-1126.
66. Schlee M, Wehkamp J, Altenhoefer A, Oelschlaeger TA, Stange EF&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.
67. Schneewind O&Missiakas DM (2012) Protein secretion and surface display in Gram-positive bacteria. Philos Trans R Soc Lond B Biol Sci 367: 1123-1139.
68. Seth A, Yan F, Polk DB&Rao RK (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAO kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294: G1060-G1069.
69. Siboo IR, Chambers HF&Sullam PM (2005) Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 73: 2273-2280.
70. Steck N, Hoffmann M, Sava IG et al. (2011) Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology 141:959-971.
71. Troge A, Scheppach W, Schroeder BO, Rund SA, Heuner K, Wehkamp J, Stange EF&Oelschlaeger TA (2012) More than a marine propeller-the flagellum of the probiotic Escherichia coli strain Nissle 1917 is the major adhesin mediating binding to human mucus. Int J Med Microbiol 302: 304-314.
72. Tsilingiri K&Rescigno M (2013) Postbiotics: what else? Benef Microbes 4: 101-107.
73. Turroni F, Serafini F, Foroni E et al. (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. P Natl Acad Sci USA 110: 11151-11156.
74. von Schillde MA, Hörmannsperger G, Weiher M et al. (2012) Lactocepin secreted by Lactobacillus exerts antiinflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe 11: 387-396.
75. Whelan K&Quigley EM (2013) Probiotics in the management of irritable bowel syndrome and inflammatory bowel disease. Curr Opin Gastroenterol 29:184-189.
76. Wu MH, Pan TM, Wu YJ, Chang SJ, Chang MS&Hu CY (2010) Exopolysaccharide activities from probiotic Bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol 144: 104-110.
77. Xu R, Shang N&Li P (2011) In vitro and in vivo antioxidant activity of exopolysaccharide fractions from Bifidobacterium animalis RH. Anaerobe 17: 226-231.
78. Yan F, Cao H, Cover TL, Whitehead R, Washington MK & Polk DB (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575.
79. Yan F, Cao H, Cover TL, Washington MK, Shi Y, Liu L, Chaturvedi R, Peek RM Jr, Wilson KT&Polk DB (2011) Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J Clin Invest 121: 2242-2253.
80. Yasuda E, Serata M&Sako T (2008) 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.
81. You GE, Jung BJ, Kim HR, Kim HG, Kim TR&Chung DK (2013) Lactobacillus sakei lipoteichoic acid inhibits MMP-1 induced by UVA in normal dermal fibroblasts of human. J Microbiol Biotechnol 23: 1357-1364.
82. Zhang L, Liu C, Li D, Zhao Y, Zhang X, Zeng X, Yang Z & Li S (2013) Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int J Biol Macromol 54: 270-275.