Probiotics: Properties, examples, and specific applications

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 3, 2013, Pages

  Behnsen, Judith ^a   Deriu, Elisa ^a   Sassone Corsi, Martina ^a   Raffatellu, Manuela ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOLOGIC FACTOR; PROBIOTIC AGENT;

DRUG DESIGN; ENTEROPATHY; GASTROINTESTINAL TRACT; HUMAN; METABOLIC ENGINEERING; METAGENOME; MICROBIOLOGY; PHYSIOLOGY; REVIEW;

CYTOKINES; DRUG DESIGN; GASTROINTESTINAL TRACT; HUMANS; IMMUNOLOGIC FACTORS; INTESTINAL DISEASES; METABOLIC ENGINEERING; METAGENOME; PROBIOTICS;

EID: 84874690210     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a010074     Document Type: Article

References (135)

1. Altenhoefer A, Oswald S, Sonnenborn U, Enders C, Schulze J, Hacker J, Oelschlaeger TA. 2004. The probiotic Escherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroin vasive bacterial pathogens. FEMS Immunol Med Microbiol 40: 223-229.
2. Andrews NC, Schmidt PJ. 2007. Iron homeostasis. Annu Rev Physiol 69: 69-85.
3. Anukam KC, Reid G. 2008. Probiotics: 100 years (1907-2007) after Elie Metchnikoff 's observations. In Communicating current research and educational topics and trends in applied microbiology, 2007 ed. (ed. Anukam KC, Reid G), pp. 466-474. Formatex.org, Spain.
4. Artis D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8: 411-420.
5. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.
6. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, et al. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341.
7. Aureli P, Capurso L, Castellazzi AM, Clerici M, Giovannini M, Morelli L, Poli A, Pregliasco F, Salvini F, Zuccotti GV. 2011. Probiotics and health: An evidencebased review. Pharmacol Res 63: 366-376.
8. Baquero F, Moreno F. 2006. The microcins. FEMS Microbiol Lett 23: 117-124.
9. Bäumler AJ, Norris TL, Lasco T, Voight W, Reissbrodt R, Rabsch W, Heffron F. 1998. IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol 180: 1446-1453.
10. Bevins CL, Salzman NH. 2011. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9: 356-368.
11. Blum G, Marre R, Hacker J. 1995. Properties of Escherichia coli strains of serotype O6. Infection 23: 234-236.
12. Boudeau J, Glasser AL, Julien S, Colombel JF, Darfeuille-Michaud A. 2003. Inhibitory effect of probiotic Escherichia coli strain Nissle 1917 on adhesion to and invasion of intestinal epithelial cells by adherent-invasive E. coli strains isolated from patients with Crohn's disease. Aliment Pharmacol Ther 18: 45-56.
13. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L. 2006. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 4: 754-759.
14. Burns SM, Hull SI. 1998. Comparison of loss of serum resistance by defined lipopolysaccharide mutants and an acapsular mutant of uropathogenic Escherichia coli O75:K5. Infect Immun 66: 4244-4253.
15. Caluwaerts S, Vandenbroucke K, Steidler L, Neirynck S, Vanhoenacker P, Corveleyn S, Watkins B, Sonis S, Coulie B, Rottiers P. 2010. AG013, a mouth rinse formulation of Lactococcus lactis secreting human Trefoil Factor 1, provides a safe and efficacious therapeutic tool for treating oral mucositis. Oral Oncol 46: 564-570.
16. 2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65: 857-875.
17. Choi HJ, Ahn JH, Park SH, Do KH, Kim J, Moon Y. 2012. Enhanced wound healing by recombinant Escherichia coli Nissle 1917 via human epidermal growth factor receptor in human intestinal epithelial cells: Therapeutic implication using recombinant probiotics. Infect Immun 80: 1079-1087.
18. Cobb BA, Wang Q, Tzianabos AO, Kasper DL. 2004. Polysaccharide processing and presentation by the MHCII pathway. Cell 117: 677-687.
19. Colombel JF, Rutgeerts P, Malchow H, Jacyna M, Nielsen OH, Rask-Madsen J, Van Deventer S, Ferguson A, Desreumaux P, Forbes A, et al. 2001. Interleukin 10 (Tenovil) in the prevention of postoperative recurrence of Crohn's disease. Gut 49: 42-46.
20. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: Developing innate immunity for food. Nat Rev Microbiol 3: 777-788.
21. Coyne MJ, Reinap B, Lee MM, Comstock LE. 2005. Human symbionts use a host-like pathway for surface fucosylation. Science 307: 1778-1781.
22. Crosa JH, Mey AR, Payne SM. 2004. Iron transport in bacteria. ASM Press, Washington, DC.
23. Cross ML, Ganner A, Teilab D, Fray LM. 2004. Patterns of cytokine induction by gram-positive and gram-negative probiotic bacteria. FEMS Immunol Med Microbiol 42: 173-180.
24. Cukrowska B, Lodinova-Zadnikova R, Enders C, Sonnenborn U, Schulze J, Tlaskalova-Hogenova H. 2002. Specific proliferative and antibody responses of premature infants to intestinal colonization with nonpathogenic probiotic E. coli strain Nissle 1917. Scand J Immunol 55: 204-209.
25. Depaolo RW, Tang F, Kim I, Han M, Levin N, Ciletti N, Lin A, Anderson D, Schneewind O, Jabri B. 2008. Tolllike receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4: 350-361.
26. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, Rittmann BE. 2008. Gut microbiota and its possible relationship with obesity. Mayo Clin Proc 83: 460-469.
27. Duquesne S, Destoumieux-Garzon D, Peduzzi J, Rebuffat S. 2007. Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat Prod Rep 24: 708-734.
28. FAO/WHO. 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Cordoba, Argentina, October 1-4.
29. Fava F, Danese S. 2011. Intestinal microbiota in inflammatory bowel disease: Friend of foe? World J Gastroenterol 17: 557-566.
30. Fellermann K, Stange EF. 2001. Defensins-Innate immunity at the epithelial frontier. Eur J Gastroenterol Hepatol 13: 771-776.
31. Feng T, Wang L, Schoeb TR, Elson CO, Cong Y. 2010. Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med 207: 1321-1332.
32. Fischbach MA, Lin H, Zhou L, Yu Y, Abergel RJ, Liu DR, Raymond KN, Wanner BL, Strong RK, Walsh CT, et al. 2006. The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2. Proc Natl Acad Sci 103: 16502-16507.
33. Floch MH, Walker WA, Madsen K, Sanders ME, Macfarlane GT, Flint HJ, Dieleman LA, Ringel Y, Guandalini S, Kelly CP, et al. 2011. Recommendations for probiotic use-2011 update. J Clin Gastroenterol 45 (Suppl): S168-S171.
34. Foligne B, Dessein R, Marceau M, Poiret S, Chamaillard M, Pot B, Simonet M, Daniel C. 2007. Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein. Gastroenterology 133: 862-874.
35. Ganz T. 2003. Defensins: Antimicrobial peptides of innate immunity. Nat Rev Immunol 3: 710-720.
36. Garcia EC, Brumbaugh AR, Mobley HL. 2011. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun 79: 1225-1235.
37. Gophna U, Sommerfeld K, Gophna S, Doolittle WF, Veldhuyzen van Zanten SJ. 2006. Differences between tissueassociated intestinal microfloras of patients with Crohn's disease and ulcerative colitis. J Clin Microbiol 44: 4136-4141.
38. Grabig A, Paclik D, Guzy C, Dankof A, Baumgart DC, Erckenbrecht J, Raupach B, Sonnenborn U, Eckert J, Schumann RR, et al. 2006. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via Toll-like receptor 2-and Toll-like receptor 4-dependent pathways. Infect Immun 74: 4075-4082.
39. Grosse C, Scherer J, Koch D, Otto M, Taudte N, Grass G. 2006. A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62: 120-131.
40. Grozdanov L, Zahringer U, Blum-Oehler G, Brade L, Henne A, Knirel YA, Schombel U, Schulze J, Sonnenborn U, Gottschalk G, et al. 2002. A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. J Bacteriol 184: 5912-5925.
41. Grozdanov L, Raasch C, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Dobrindt U. 2004. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186: 5432-5441.
42. Gunzer F, Hennig-Pauka I, Waldmann KH, Sandhoff R, Grone HJ, Kreipe HH, Matussek A, Mengel M. 2002. Gnotobiotic piglets develop thrombotic microangiopathy after oral infection with enterohemorrhagic Escherichia coli. Am J Clin Pathol 118: 364-375.
43. Guzy C, Paclik D, Schirbel A, Sonnenborn U, Wiedenmann B, Sturm A. 2008. The probiotic Escherichia coli strain Nissle 1917 induces γδ T cell apoptosis via caspaseand FasL-dependent pathways. Int Immunol 20: 829-840.
44. Hacker J, Carniel E. 2001. Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2: 376-381.
45. Hacker J, Kaper JB. 2000. Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
46. Hafez M, Hayes K, Goldrick M, Warhurst G, Grencis R, Roberts IS. 2009. The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infect Immun 77: 2995-3003.
47. Hafez M, Hayes K, Goldrick M, Grencis RK, Roberts IS. 2010. The K5 capsule of Escherichia coli strain Nissle 1917 is important in stimulating expression of Toll-like receptor 5, CD14, MyD88, and TRIF together with the induction of interleukin-8 expression via the mitogenactivated protein kinase pathway in epithelial cells. Infect Immun 78: 2153-2162.
48. Hancock V, Vejborg RM, Klemm P. 2010. Functional genomics of probiotic Escherichia coli Nissle 1917 and 83972, and UPEC strain CFT073: Comparison of transcriptomes, growth and biofilm formation. Mol Genet Genomics 284: 437-454.
49. Hantke K, Nicholson G, Rabsch W, Winkelmann G. 2003. Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci 100: 3677-3682.
50. Hayashi H, Takahashi R, Nishi T, Sakamoto M, Benno Y. 2005. Molecular analysis of jejunal, ileal, caecal and rectosigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol 54 (Pt 11): 1093-1101.
51. Henker J, Laass M, Blokhin BM, Bolbot YK, Maydannik VG, Elze M, Wolff C, Schulze J. 2007. The probiotic Escherichia coli strain Nissle 1917 (EcN) stops acute diarrhoea in infants and toddlers. Eur J Pediatr 166: 311-318.
52. Hentschel U, Hacker J. 2001. Pathogenicity islands: The tip of the iceberg. Microbes Infect 3: 545-548.
53. Herias MV, Midtvedt T, Hanson LA, Wold AE. 1997. Escherichia coli K5 capsule expression enhances colonization of the large intestine in the gnotobiotic rat. Infect Immun 65: 531-536.
54. Hockertz S. 1991. Immunomodulating effect of killed, apathogenic Escherichia coli, strain Nissle 1917, on the macrophage system. Arzneimittelforschung 41: 1108-1112.
55. Hockertz S. 1997. Augmentation of host defence against bacterial and fungal infections of mice pretreated with the non-pathogenic Escherichia coli strain Nissle 1917. Arzneimittelforschung 47: 793-796.
56. Hogenauer C, Hammer HF, Krejs GJ, Reisinger EC. 1998. Mechanisms and management of antibiotic-associated diarrhea. Clin Infect Dis 27: 702-710.
57. Hooper LV, Gordon JI. 2001. Commensal host-bacterial relationships in the gut. Science 292: 1115-1118.
58. Høverstad T, Midtvedt T. 1986. Short-chain fatty acids in germfree mice and rats. J Nutr 116: 1772-1776.
59. Hughes C, Phillips R, Roberts AP. 1982. Serum resistance among Escherichia coli strains causing urinary tract infection in relation to O type and the carriage of hemolysin, colicin, and antibiotic resistance determinants. Infect Immun 35: 270-275.
60. Huibregtse IL, Zaat SA, Kapsenberg ML, Sartori da Silva MA, Peppelenbosch MP, van Deventer SJ, Braat H. 2011. Genetically modified Lactococcus lactis for delivery of human interleukin-10 to dendritic cells. Gastroenterol Res Pract 2012: 639291.
61. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498.
62. Jervis HR, Biggers DC. 1964. Mucosal enzymes in the cecum of conventional and germfree mice. Anat Rec 148: 591-597.
63. Kaper JB, Hacker J. 1999. Pathogenicity islands and other mobile virulence elements. ASM Press, Washington, DC.
64. Karin M, Lawrence T, Nizet V. 2006. Innate immunity gone awry: Linking microbial infections to chronic inflammation and cancer. Cell 124: 823-835.
65. Kehl-Fie TE, Skaar EP. 2010. Nutritional immunity beyond iron: A role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
66. Kjellev S. 2009. The trefoil factor family-Small peptides with multiple functionalities. Cell Mol Life Sci 66: 1350-1369.
67. Koonin EV, Makarova KS, Aravind L. 2001. Horizontal gene transfer in prokaryotes: Quantification and classification. Annu Rev Microbiol 55: 709-742.
68. Kruis W, Schutz E, Fric P, Fixa B, Judmaier G, Stolte M. 1997. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 11: 853-858.
69. Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, Kascak M, Kamm MA, Weismueller J, Beglinger C, Stolte M, et al. 2004. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53: 1617-1623.
70. Lammers KM, Helwig U, Swennen E, Rizzello F, Venturi A, Caramelli E, Kamm MA, Brigidi P, Gionchetti P, Campieri M. 2002. Effect of probiotic strains on interleukin 8 production by HT29/19A cells. Am J Gastroenterol 97: 1182-1186.
71. Lasaro MA, Salinger N, Zhang J, Wang Y, Zhong Z, Goulian M, Zhu J. 2009. F1C fimbriae play an important role in biofilm formation and intestinal colonization by the Escherichia coli commensal strain Nissle 1917. Appl Environ Microbiol 75: 246-251.
72. Le Loir Y, Azevedo V, Oliveira SC, Freitas DA, Miyoshi A, Bermudez-Humaran LG, Nouaille S, Ribeiro LA, Leclercq S, Gabriel JE, et al. 2005. Protein secretion in Lactococcus lactis: An efficient way to increase the overall heterologous protein production. Microb Cell Fact 4: 2.
73. Léveillé S, Caza M, Johnson JR, Clabots C, Sabri M, Dozois CM. 2006. Iha from an Escherichia coli urinary tract infection outbreak clonal group A strain is expressed in vivo in the mouse urinary tract and functions as a catecholate siderophore receptor. Infect Immun 74: 3427-3436.
74. Liu CH, Lee SM, Vanlare JM, Kasper DL, Mazmanian SK. 2008. Regulation of surface architecture by symbiotic bacteria mediates host colonization. Proc Natl Acad Sci 105: 3951-3956.
75. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, et al. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11: 227-239.
76. Lodinova-Zadnikova R, Sonnenborn U. 1997. Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants. Biol Neonate 71: 224-232.
77. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, Shah N, Wang C, Magrini V, Wilson RK, et al. 2009. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci 106: 5859-5864.
78. Mandel L, Trebichavsky I, Splichal I, Schulze J. 1995. Stimulation of intestinal immune cells by E. coli in gnotobiotic piglets. Adv Exp Med Biol 371A: 463-464.
79. Marco ML, Pavan S, Kleerebezem M. 2006. Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17: 204-210.
80. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, et al. 2009. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-1286.
81. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
82. Mierau I, Kleerebezem M. 2005. 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. Appl Microbiol Biotechnol 68: 705-717.
83. Mollenbrink M, Bruckschen E. 1994. Treatment of chronic constipation with physiologic Escherichia coli bacteria. Results of a clinical study of the effectiveness and tolerance of microbiological therapy with the E. coli Nissle 1917 strain (Mutaflor). Med Klin (Munich) 89: 587-593.
84. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL. 2012. IBD-What role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 9: 219-230.
85. Müller SI, Valdebenito M, Hantke K. 2009. Salmochelin, the long-overlooked catecholate siderophore of Salmonella. Biometals 22: 691-695.
86. Nagalingam NA, Lynch SV. 2012. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 18: 968-984.
87. Nissle A. 1959. Explanations of the significance of colonic dysbacteria & the mechanism of action of E. coli therapy (mutaflor). Medizinische 4: 1017-1022.
88. Nouaille S, Ribeiro LA, Miyoshi A, Pontes D, Le Loir Y, Oliveira SC, Langella P, Azevedo V. 2003. Heterologous protein production and delivery systems for Lactococcus lactis. Genet Mol Res 2: 102-111.
89. 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.
90. Ouwehand AC, Salminen S, Isolauri E. 2002. Probiotics: An overview of beneficial effects. Antonie Van Leeuwenhoek 82: 279-289.
91. Pang Q, Ji Y, Li Y, Bermudez-Humaran LG, Hu G, Zeng Y. 2008. Intragastric administration with recombinant Lactococcus lactis producing heme oxygenase-1 prevents lipopolysaccharide-induced endotoxemia in rats. FEMS Microbiol Lett 283: 62-68.
92. Pang QF, Ji Y, Bermudez-Humaran LG, Zhou QM, Hu G, Zeng Y. 2009. Protective effects of a heme oxygenase-1-secreting Lactococcus lactis on mucosal injury induced by hemorrhagic shock in rats. J Surg Res 153: 39-45.
93. Patzer SI, Baquero MR, Bravo D, Moreno F, Hantke K. 2003. The colicin G, H and X determinants encode microcins M and H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN. Microbiology 149: 2557-2570.
94. Peterbauer C, Maischberger T, Haltrich D. 2011. Food-grade gene expression in lactic acid bacteria. Biotechnol J 6: 1147-1161.
95. Raber-Durlacher JE, Elad S, Barasch A. 2010. Oral mucositis. Oral Oncol 46: 452-456.
96. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA, Butler BP, Chu H, Santos RL, Berger T, et al. 2009. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5: 476-486.
97. Rao S, Hu S, McHugh L, Lueders K, Henry K, Zhao Q, Fekete RA, Kar S, Adhya S, Hamer DH. 2005. Toward a live microbial microbicide for HIV: Commensal bacteria secreting an HIV fusion inhibitor peptide. Proc Natl Acad Sci 102: 11993-11998.
98. Reid G, Howard J, Gan BS. 2001. Can bacterial interference prevent infection? Trends Microbiol 9: 424-428.
99. Sanders ME. 2003. Probiotics: Considerations for human health. Nutr Rev 61: 91-99.
100. Schlee M, Wehkamp J, Altenhoefer A, Oelschlaeger TA, Stange EF, Fellermann K. 2007. Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect Immun 75: 2399-2407.
101. Schotte L, Steidler L, Vandekerckhove J, Remaut E. 2000. Secretion of biologically active murine interleukin-10 by Lactococcus lactis. Enzyme Microb Technol 27: 761-765.
102. Schultz M, Lindstrom AL. 2008. Rationale for probiotic treatment strategies in inflammatory bowel disease. Expert Rev Gastroenterol Hepatol 2: 337-355.
103. Schulze A, Downward J. 2001. Navigating gene expression using microarrays-A technology review. Nat Cell Biol 3: E190-E195.
104. Schutz E. 1989. The treatment of intestinal diseases with Mutaflor. A multicenter retrospective study. Fortschr Med 107: 599-602.
105. Servin AL. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28: 405-440.
106. H 17 cells in the intestine. J Exp Med 209: 251-258.
107. Skaar EP. 2010. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6: e1000949.
108. Smith KD. 2007. Iron metabolism at the host pathogen interface: Lipocalin 2 and the pathogen-associated iroA gene cluster. Int J Biochem Cell Biol 39: 1776-1780.
109. Splichal I, Fagerhol MK, Trebichavsky I, Splichalova A, Schulze J. 2005. The effect of intestinal colonization of germ-free pigs with Escherichia coli on calprotectin levels in plasma, intestinal and bronchoalveolar lavages. Immunobiology 209: 681-687.
110. Spor A, Koren O, Ley R. 2011. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9: 279-290.
111. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E. 2000. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289: 1352-1355.
112. Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermeire A, Goddeeris B, Cox E, Remon JP, Remaut E. 2003. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol 21: 785-789.
113. Steidler L, Rottiers P, Coulie B. 2009. Actobiotics as a novel method for cytokine delivery. Ann NY Acad Sci 1182: 135-145.
114. Stentebjerg-Olesen B, Chakraborty T, Klemm P. 1999. Type 1 fimbriation and phase switching in a natural Escherichia coli fimB null strain, Nissle 1917. J Bacteriol 181: 7470-7478.
115. Sturm A, Rilling K, Baumgart DC, Gargas K, Abou-Ghazale T, Raupach B, Eckert J, Schumann RR, Enders C, Sonnenborn U, et al. 2005. Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via Toll-like receptor 2 signaling. Infect Immun 73: 1452-1465.
116. Tarr PI, Bilge SS, Vary JC Jr, Jelacic S, Habeeb RL, Ward TR, Baylor MR, Besser TE. 2000. Iha: A novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68: 1400-1407.
117. Tilg H, van Montfrans C, van den Ende A, Kaser A, van Deventer SJ, Schreiber S, Gregor M, Ludwiczek O, Rutgeerts P, Gasche C, et al. 2002. Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon γ. Gut 50: 191-195.
118. Tlaskalova-Hogenova H, Stepankova R, Kozakova H, Hudcovic T, Vannucci L, Tuckova L, Rossmann P, Hrncir T, Kverka M, Zakostelska Z, et al. 2011. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: Contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol 8: 110-120.
119. Torres AG, Redford P, Welch RA, Payne SM. 2001. TonBdependent systems of uropathogenic Escherichia coli: Aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 69: 6179-6185.
120. Tran CP, Cook GA, Yeomans ND, Thim L, Giraud AS. 1999. Trefoil peptide TFF2 (spasmolytic polypeptide) potently accelerates healing and reduces inflammation in a rat model of colitis. Gut 44: 636-642.
121. 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.
122. Ukena SN, Singh A, Dringenberg U, Engelhardt R, Seidler U, Hansen W, Bleich A, Bruder D, Franzke A, Rogler G, et al. 2007. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS ONE 2: e1308.
123. Valdebenito M, Crumbliss AL, Winkelmann G, Hantke K. 2006. Environmental factors influence the production of enterobactin, salmochelin, aerobactin, and yersiniabactin in Escherichia coli strain Nissle 1917. Int J Med Microbiol 296: 513-520.
124. Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, Rottiers P, Steidler L. 2004. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 127: 502-513.
125. Vandenbroucke K, de Haard H, Beirnaert E, Dreier T, Lauwereys M, Huyck L, Van Huysse J, Demetter P, Steidler L, Remaut E, et al. 2010. Orally administered L. lactis secreting an anti-TNF Nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol 3: 49-56.
126. van Deventer SJ, Elson CO, Fedorak RN. 1997. Multiple doses of intravenous interleukin 10 in steroid-refractory Crohn's disease. Crohn's Disease Study Group. Gastroenterology 113: 383-389.
127. Vassiliadis G, Destoumieux-Garzon D, Lombard C, Rebuffat S, Peduzzi J. 2010. Isolation and characterization of two members of the siderophore-microcin family, microcins M and H47. Antimicrob Agents Chemother 54: 288-297.
128. Vejborg RM, Friis C, Hancock V, Schembri MA, Klemm P. 2010. Avirulent parent with probiotic progeny: Comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972. Mol Genet Genomics 283: 469-484.
129. Vijayan V, Mueller S, Baumgart-Vogt E, Immenschuh S. 2010. Heme oxygenase-1 as a therapeutic target in inflammatory disorders of the gastrointestinal tract. World J Gastroenterol 16: 3112-3119.
130. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R. 2011. Regulation of inflammation by short chain fatty acids. Nutrients 3: 858-876.
131. Wehkamp J, Harder J, Wehkamp K, Wehkamp-von Meissner B, Schlee M, Enders C, Sonnenborn U, Nuding S, Bengmark S, Fellermann K, et al. 2004. NF-κB-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.
132. Welch RA, Burland V, Plunkett G III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, et al. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci 99: 17020-17024.
133. Westendorf AM, Gunzer F, Deppenmeier S, Tapadar D, Hunger JK, Schmidt MA, Buer J, Bruder D. 2005. Intestinal immunity of Escherichia coli NISSLE 1917: A safe carrier for therapeutic molecules. FEMS Immunol Med Microbiol 43: 373-384.
134. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
135. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. 2007. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCζ redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 9: 804-816.