Dextran sodium sulfate-induced inflammation alters the expression of proteins by intestinal Escherichia coli strains in a gnotobiotic mouse model

Applied and Environmental Microbiology

Volumn 78, Issue 5, 2012, Pages 1513-1522

  Schumann, Sara ^a   Alpert, Carl ^a   Engst, Wolfram ^a   Loh, Gunnar ^a   Blaut, Michael ^a  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY EFFECTS; BACTERIAL FERMENTATIONS; DOWN-REGULATION; E. COLI; ENERGY GENERATIONS; GEL ELECTROPHORESIS; IN-CONTROL; IN-VITRO; INTESTINAL INFLAMMATION; INTRACELLULAR LEVELS; MOUSE MODELS; PROBIOTICS; REACTIVE OXYGEN SPECIES; REPAIR PROTEINS; REPORTER GENE ASSAYS; TRYPTOPHANASE; ULCERATIVE COLITIS;

AMINO ACIDS; CARBOHYDRATES; DEXTRAN; ELECTROPHORESIS; GENES; MAMMALS; PATHOLOGY; PROTEINS; STRAIN;

ESCHERICHIA COLI;

DEXTRAN SULFATE; ESCHERICHIA COLI PROTEIN;

CARBOHYDRATE; COLIFORM BACTERIUM; ELECTROKINESIS; ENZYME ACTIVITY; FERMENTATION; PROTEIN; RODENT; SODIUM; SULFATE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CECUM; CHEMICALLY INDUCED DISORDER; CHEMISTRY; COMPARATIVE STUDY; ENTERITIS; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENETICS; GERMFREE ANIMAL; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CECUM; DEXTRAN SULFATE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENTERITIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; GERM-FREE LIFE; MICE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MUS;

EID: 84857088288     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07340-11     Document Type: Article

References (50)

1. Angelini S, et al. 2008. NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. J. Biol. Chem. 283:14084-14091.
2. Bansal T, Alaniz RC, Wood TK, Jayaraman A. 2010. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc. Natl. Acad. Sci. U. S. A. 107:228-233.
3. Bansal T, et al. 2007. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect. Immun. 75:4597-4607.
4. Bartolomé B, Jubete Y, Martinez é, de la Cruz F. 1991. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102:75-78.
5. Baumgart M, et al. 2007. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 1:403-418.
6. Birgens HS. 1985. Lactoferrin in plasma measured by an ELISA technique: evidence that plasma lactoferrin is an indicator of neutrophil turnover and bone marrow activity in acute leukaemia. Scand. J. Haematol. 34:326-331.
7. Burich A, et al. 2001. Helicobacter-induced inflammatory bowel disease in IL-10- and T cell-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281:G764-G778.
8. 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.
9. Cukrowska B, et al. 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.
10. Darfeuille-Michaud A, et al. 1998. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115:1405-1413.
11. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
12. Flint DH, Tuminello JF, Emptage MH. 1993. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 268:22369-22376.
13. Ganz T, Weiss J. 1997. Antimicrobial peptides of phagocytes and epithelia. Semin. Hematol. 34:343-354.
14. Grabig A, 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.
15. Grozdanov L, et al. 2004. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J. Bacteriol. 186: 5432-5441.
16. Guzy C, et al. 2008. The probiotic Escherichia coli strain Nissle 1917 induces γδ T cell apoptosis via caspase- and FasL-dependent pathways. Int. Immunol. 20:829-840.
17. Hagiwara D, et al. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J. Bacteriol. 185:5735-5746.
18. Heimesaat MM, et al. 2007. Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS One 2:e662.
19. Jang S, Imlay JA. 2007. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282:929-937.
20. Keyer K, Imlay JA. 1997. Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J. Biol. Chem. 272:27652-27659.
21. Kim CJ, et al. 2010. L-Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis. J. Nutr. Biochem. 21:468-475.
22. Kim SC, et al. 2005. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128:891-906.
23. Kim SY, et al. 2005. The gene yggE functions in restoring physiological defects of Escherichia coli cultivated under oxidative stress conditions. Appl. Environ. Microbiol. 71:2762-2765.
24. Kotlowski R, Bernstein CN, Sepehri S, Krause DO. 2007. High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669-675.
25. Krishnaiah D, et al. 2007. Physiological responses of Escherichia coli cells cultivated under a sublethal oxidative stress condition. Malaysian J. Microbiol. 3:14-18.
26. Kruis W, 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.
27. Kruis W, et al. 1997. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther. 11:853-858.
28. Kuo CF, Mashino T, Fridovich I. 1987. α,β-Dihydroxyisovalerate dehydratase. A superoxide-sensitive enzyme. J. Biol. Chem. 262:4724-4727.
29. Lai YC, Peng HL, Chang HY. 2001. Identification of genes induced in vivo during Klebsiella pneumoniae CG43 infection. Infect. Immun. 69: 7140-7145.
30. Le Borgne S, Palmeros B, Bolivar F, Gosset G. 2001. Improvement of the pBRINT-Ts plasmid family to obtain marker-free chromosomal insertion of cloned DNA in E. coli. Biotechniques 30:252-254, 256.
31. Lennox ES. 1955. Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1:190-206.
32. Mattivi F, Vrhovsek U, Versini G. 1999. Determination of indole-3-acetic acid, tryptophan and other indoles in must and wine by highperformance liquid chromatography with fluorescence detection. J. Chromatogr. A 855:227-235.
33. Ojima Y, Kawase D, Nishioka M, Taya M. 2009. Functionally undefined gene, yggE, alleviates oxidative stress generated by monoamine oxidase in recombinant Escherichia coli. Biotechnol. Lett. 31:139-145.
34. 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.
35. Pavlick KP, et al. 2002. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic. Biol. Med. 33:311-322.
36. Rabilloud T, Strub JM, Luche S, van Dorsselaer A, Lunardi J. 2001. A comparison between Sypro Ruby and ruthenium II tris (bathophenanthroline disulfonate) as fluorescent stains for protein detection in gels. Proteomics 1:699-704.
37. Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, Axon AT. 1999. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 354:635-639.
38. Rolhion N, Darfeuille-Michaud A. 2007. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm. Bowel Dis. 13:1277-1283.
39. Sartor RB. 2006. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3:390-407.
40. Schlee M, et al. 2007. Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect. Immun. 75:2399-2407.
41. Schultz M, et al. 2004. Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin. Diagn. Lab. Immunol. 11:372-378.
42. Schuppler M, Lotzsch K, Waidmann M, Autenrieth IB. 2004. An abundance of Escherichia coli is harbored by the mucosa-associated bacterial flora of interleukin-2-deficient mice. Infect. Immun. 72:1983-1990.
43. Sepehri S, Kotlowski R, Bernstein CN, Krause DO. 2007. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm. Bowel Dis. 13:675-683.
44. Swidsinski A, et al. 2002. Mucosal flora in inflammatory bowel disease. Gastroenterology 122:44-54.
45. Ukena SN, et al. 2007. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS One 2:e1308.
46. Vogel-Scheel J, Alpert C, Engst W, Loh G, Blaut M. 2010. Escherichia coli must synthesize purines and pyrimidines to establish in the mouse intestine. Appl. Environ. Microbiol. 76:5181-5187.
47. Waidmann M, et al. 2003. Bacteroides vulgatus protects against Escherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice. Gastroenterology 125:162-177.
48. Watanabe T, Snell EE. 1972. Reversibility of the tryptophanase reaction: synthesis of tryptophan from indole, pyruvate, and ammonia. Proc. Natl. Acad. Sci. U. S. A. 69:1086-1090.
49. Wohlgemuth S, Haller D, Blaut M, Loh G. 2009. Reduced microbial diversity and high numbers of one single Escherichia coli strain in the intestine of colitic mice. Environ. Microbiol. 11:1562-1571.
50. Zyrek AA, et al. 2007. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKC redistribution resulting in tight junction and epithelial barrier repair. Cell. Microbiol. 9:804-816.