Bacteriocinogeny in experimental pigs treated with indomethacin and Escherichia coli Nissle

. 2011 Feb 07 ; 17 (5) : 609-17.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21350709

AIM: To evaluate bacteriocinogeny in short-term high-dose indomethacin administration with or without probiotic Escherichia coli Nissle 1917 (EcN) in experimental pigs. METHODS: Twenty-four pigs entered the study: Group A (controls), Group B (probiotics alone), Group C (indomethacin alone) and Group D (probiotics and indomethacin). EcN (3.5×10(10) bacteria/d for 14 d) and/or indomethacin (15 mg/kg per day for 10 d) were administrated orally. Anal smears before and smears from the small and large intestine were taken from all animals. Bacteriocin production was determined with 6 different indicator strains; all strains were polymerase chain reaction tested for the presence of 29 individual bacteriocin-encoding determinants. RESULTS: The general microbiota profile was rather uniform in all animals but there was a broad diversity in coliform bacteria (parallel genotypes A, B1, B2 and D found). In total, 637 bacterial strains were tested, mostly Escherichia coli (E. coli). There was a higher incidence of non-E. coli strains among samples taken from the jejunum and ileum compared to that of the colon and rectum indicating predominance of E. coli strains in the large intestine. Bacteriocinogeny was found in 24/77 (31%) before and in 155/560 (28%) isolated bacteria at the end of the study. Altogether, 13 individual bacteriocin types (out of 29 tested) were identified among investigated strains. Incidence of four E. coli genotypes was equally distributed in all groups of E. coli strains, with majority of genotype A (ranging from 81% to 88%). The following types of bacteriocins were most commonly revealed: colicins Ia/Ib (44%), microcin V (18%), colicin E1 (16%) and microcin H47 (6%). There was a difference in bacteriocinogeny between control group A (52/149, 35%) and groups with treatment at the end of the study: B: 31/122 (25%, P=0.120); C: 43/155 (28%, P=0.222); D: 29/134 (22%, P=0.020). There was a significantly lower prevalence of colicin Ib, microcins H47 and V (probiotics group, P<0.001), colicin E1 and microcin H47 (indomethacin group, P<0.001) and microcins H47 and V (probiotics and indomethacin group, P=0.025) compared to controls. Escherichia fergusonii (E. fergusonii) was identified in 6 animals (6/11 isolates from the rectum). One strain was non-colicinogenic, while all other strains of E. fergusonii solely produced colicin E1. All animals started and remained methanogenic despite the fact that EcN is a substantial hydrogen producer. There was an increase in breath methane (after the treatment) in 5/6 pigs from the indomethacin group (C). CONCLUSION: EcN did not exert long-term liveability in the porcine intestine. All experimental pigs remained methanogenic. Indomethacin and EcN administered together might produce the worst impact on bacteriocinogeny.

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Hawkey CJ. NSAIDs, coxibs, and the intestine. J Cardiovasc Pharmacol. 2006;47 Suppl 1:S72–S75. PubMed

Fortun PJ, Hawkey CJ. Nonsteroidal antiinflammatory drugs and the small intestine. Curr Opin Gastroenterol. 2007;23:134–141. PubMed

Wong Kee Song LM, Marcon NE. NSAIDs: Adverse effects on the distal small bowel and colon. 2010. Available from: URL: http://www.uptodate.com/patients/content/topic.do?topicKey=~icYPTJgCSGCuc.

Robert A, Asano T. Resistance of germfree rats to indomethacin-induced intestinal lesions. Prostaglandins. 1977;14:333–341. PubMed

Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. October 2001. Available from: http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf.

Ohland CL, Macnaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298:G807–G819. PubMed

Arribas B, Rodríguez-Cabezas ME, Camuesco D, Comalada M, Bailón E, Utrilla P, Nieto A, Concha A, Zarzuelo A, Gálvez J. 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. 2009;157:1024–1033. PubMed PMC

Carol M, Borruel N, Antolin M, Llopis M, Casellas F, Guarner F, Malagelada JR. Modulation of apoptosis in intestinal lymphocytes by a probiotic bacteria in Crohn's disease. J Leukoc Biol. 2006;79:917–922. PubMed

Brady LJ, Gallaher DD, Busta FF. The role of probiotic cultures in the prevention of colon cancer. J Nutr. 2000;130:410S–414S. PubMed

Sanders ME. Considerations for use of probiotic bacteria to modulate human health. J Nutr. 2000;130:384S–390S. PubMed

Wollowski I, Rechkemmer G, Pool-Zobel BL. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr. 2001;73:451S–455S. PubMed

Gotteland M, Cruchet S, Verbeke S. Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indometacin in humans. Aliment Pharmacol Ther. 2001;15:11–17. PubMed

Kamil R, Geier MS, Butler RN, Howarth GS. Lactobacillus rhamnosus GG exacerbates intestinal ulceration in a model of indomethacin-induced enteropathy. Dig Dis Sci. 2007;52:1247–1252. PubMed

Watanabe T, Nishio H, Tanigawa T, Yamagami H, Okazaki H, Watanabe K, Tominaga K, Fujiwara Y, Oshitani N, Asahara T, et al. Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid. Am J Physiol Gastrointest Liver Physiol. 2009;297:G506–G513. PubMed

Montalto M, Gallo A, Curigliano V, D'Onofrio F, Santoro L, Covino M, Dalvai S, Gasbarrini A, Gasbarrini G. Clinical trial: the effects of a probiotic mixture on non-steroidal anti-inflammatory drug enteropathy - a randomized, double-blind, cross-over, placebo-controlled study. Aliment Pharmacol Ther. 2010;32:209–214. PubMed

Sturm A, Rilling K, Baumgart DC, Gargas K, Abou-Ghazalé T, Raupach B, Eckert J, Schumann RR, Enders C, Sonnenborn U, et al. Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via toll-like receptor 2 signaling. Infect Immun. 2005;73:1452–1465. PubMed PMC

Grabig A, Paclik D, Guzy C, Dankof A, Baumgart DC, Erckenbrecht J, Raupach B, Sonnenborn U, Eckert J, Schumann RR, et al. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect Immun. 2006;74:4075–4082. PubMed PMC

Hardy KG. Colicinogeny and related phenomena. Bacteriol Rev. 1975;39:464–515. PubMed PMC

Smarda J, Smajs D. Colicins--exocellular lethal proteins of Escherichia coli. Folia Microbiol (Praha) 1998;43:563–582. PubMed

Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 2002;84:357–364. PubMed

Farkas-Himsley H, Cheung R. Bacterial proteinaceous products (bacteriocins) as cytotoxic agents of neoplasia. Cancer Res. 1976;36:3561–3567. PubMed

Smarda J, Keprtová J. Cytotoxic effects of colicins E1-E5 and K on hamster fibroblasts. Folia Microbiol (Praha) 1987;32:133–136. PubMed

Farkas-Himsley H, Hill R, Rosen B, Arab S, Lingwood CA. The bacterial colicin active against tumor cells in vitro and in vivo is verotoxin 1. Proc Natl Acad Sci USA. 1995;92:6996–7000. PubMed PMC

Smarda J, Fialová M, Smarda J Jr. Cytotoxic effects of colicins E1 and E3 on v-myb-transformed chicken monoblasts. Folia Biol (Praha) 2001;47:11–13. PubMed

Chumchalová J, Smarda J. Human tumor cells are selectively inhibited by colicins. Folia Microbiol (Praha) 2003;48:111–115. PubMed

Farkas-Himsley H, Zhang YS, Yuan M, Musclow CE. Partially purified bacteriocin kills malignant cells by apoptosis: programmed cell death. Cell Mol Biol (Noisy-le-grand) 1992;38:643–651. PubMed

Anderluh G, Lakey JH. Disparate proteins use similar architectures to damage membranes. Trends Biochem Sci. 2008;33:482–490. PubMed

Bures J, Horák V, Duben J. Importance of colicinogeny for the course of acute bacillary dysentery. Zentralbl Bakteriol Orig A. 1979;245:469–475. PubMed

Bures J, Horák V, Buresová E, Fixa B, Komárková O, Hartmann M. Colicinogeny in chronic inflammatory bowel disease. Scand J Gastroenterol. 1986;21:819–823. PubMed

Bures J, Horák V, Fixa B, Komárková O, Zaydlar K, Lonský V, Masurka V. Colicinogeny in colorectal cancer. Neoplasma. 1986;33:233–237. PubMed

Gillor O, Etzion A, Riley MA. The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol. 2008;81:591–606. PubMed PMC

Patzer SI, Baquero MR, Bravo D, Moreno F, Hantke K. 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. 2003;149:2557–2570. PubMed

Grozdanov L, Raasch C, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Dobrindt U. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol. 2004;186:5432–5441. PubMed PMC

Vassiliadis G, Destoumieux-Garzón D, Lombard C, Rebuffat S, Peduzzi J. Isolation and characterization of two members of the siderophore-microcin family, microcins M and H47. Antimicrob Agents Chemother. 2010;54:288–297. PubMed PMC

Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos. 1995;16:351–380. PubMed

Bures J, Kopácová M, Kvetina J, Osterreicher J, Sinkorová Z, Svoboda Z, Tachecí I, Filip S, Spelda S, Kunes M, et al. Different solutions used for submucosal injection influenced early healing of gastric endoscopic mucosal resection in a preclinical study in experimental pigs. Surg Endosc. 2009;23:2094–2101. PubMed PMC

Tachecí I, Kvetina J, Bures J, Osterreicher J, Kunes M, Pejchal J, Rejchrt S, Spelda S, Kopácová M. Wireless capsule endoscopy in enteropathy induced by nonsteroidal anti-inflammatory drugs in pigs. Dig Dis Sci. 2010;55:2471–2477. PubMed

Kopácová M, Tachecí I, Kvetina J, Bures J, Kunes M, Spelda S, Tycová V, Svoboda Z, Rejchrt S. Wireless video capsule enteroscopy in preclinical studies: methodical design of its applicability in experimental pigs. Dig Dis Sci. 2010;55:626–630. PubMed PMC

Council of Europe. European convention for the protection of vertebrate animals used for experimental and other scientific purposes. Strasbourg: Council of Europe; 1986.

Smarda J, Obdrzálek V. Incidence of colicinogenic strains among human Escherichia coli. J Basic Microbiol. 2001;41:367–374. PubMed

Smarda J, Smajs D, Horynová S. Incidence of lysogenic, colicinogenic and siderophore-producing strains among human non-pathogenic Escherichia coli. Folia Microbiol (Praha) 2006;51:387–391. PubMed

Rosen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa: Humana Press; 2000. pp. 365–386. PubMed

Gordon DM, O'Brien CL. Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology. 2006;152:3239–3244. PubMed

Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66:4555–4558. PubMed PMC

Oelschlaeger TA. Mechanisms of probiotic actions - A review. Int J Med Microbiol. 2010;300:57–62. PubMed

Dunne C, O'Mahony L, Murphy L, Thornton G, Morrissey D, O'Halloran S, Feeney M, Flynn S, Fitzgerald G, Daly C, et al. In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr. 2001;73:386S–392S. PubMed

Fairbrother JM, Nadeau E, Gyles CL. Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev. 2005;6:17–39. PubMed

Lata J, Juránková J, Doubek J, Příbramská V, Frič P, Dítě P, Kolář M, Scheer P, Kosáková D. Labelling and content evaluation of commercial veterinary probiotics. Acta Vet Brno. 2006;75:139–144.

Setia A, Bhandari SK, House JD, Nyachoti CM, Krause DO. Development and in vitro evaluation of an Escherichia coli probiotic able to inhibit the growth of pathogenic Escherichia coli K88. J Anim Sci. 2009;87:2005–2012. PubMed

Yun JH, Lee KB, Sung YK, Kim EB, Lee HG, Choi YJ. Isolation and characterization of potential probiotic lactobacilli from pig feces. J Basic Microbiol. 2009;49:220–226. PubMed

Duncker SC, Lorentz A, Schroeder B, Breves G, Bischoff SC. Effect of orally administered probiotic E. coli strain Nissle 1917 on intestinal mucosal immune cells of healthy young pigs. Vet Immunol Immunopathol. 2006;111:239–250. PubMed

Kleta S, Steinrück H, Breves G, Duncker S, Laturnus C, Wieler LH, Schierack P. Detection and distribution of probiotic Escherichia coli Nissle 1917 clones in swine herds in Germany. J Appl Microbiol. 2006;101:1357–1366. PubMed

Schroeder B, Duncker S, Barth S, Bauerfeind R, Gruber AD, Deppenmeier S, Breves G. Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Dig Dis Sci. 2006;51:724–731. PubMed

Barth S, Duncker S, Hempe J, Breves G, Baljer G, Bauerfeind R. Escherichia coli Nissle 1917 for probiotic use in piglets: evidence for intestinal colonization. J Appl Microbiol. 2009;107:1697–1710. PubMed

Schultz M, Watzl S, Oelschlaeger TA, Rath HC, Göttl C, Lehn N, Schölmerich J, Linde HJ. Green fluorescent protein for detection of the probiotic microorganism Escherichia coli strain Nissle 1917 (EcN) in vivo. J Microbiol Methods. 2005;61:389–398. PubMed

Schierack P, Walk N, Reiter K, Weyrauch KD, Wieler LH. Composition of intestinal Enterobacteriaceae populations of healthy domestic pigs. Microbiology. 2007;153:3830–3837. PubMed

Unmack MA, Hansen MB, Grondahl ML, Olsen JE, Christensen P, Skadhauge E. Effects of indomethacin on Salmonella typhimurium- and cholera toxin-induced fluid accumulation in the porcine small intestine. J Vet Med A Physiol Pathol Clin Med. 2001;48:153–163. PubMed

Dalby AB, Frank DN, St Amand AL, Bendele AM, Pace NR. Culture-independent analysis of indomethacin-induced alterations in the rat gastrointestinal microbiota. Appl Environ Microbiol. 2006;72:6707–6715. PubMed PMC

Chang-Ying Y, Yi L, Jun-Cheng Z, Dan Z. Inhibitory effect of copper complex of indomethacin on bacteria studied by microcalorimetry. Biol Trace Elem Res. 2008;122:82–88. PubMed

Upreti RK, Kannan A, Pant AB. Experimental impact of aspirin exposure on rat intestinal bacteria, epithelial cells and cell line. Hum Exp Toxicol. 2010;29:833–843. PubMed

Bomba A, Nemcová R, Gancarcíková S, Herich R, Guba P, Mudronová D. Improvement of the probiotic effect of micro-organisms by their combination with maltodextrins, fructo-oligosaccharides and polyunsaturated fatty acids. Br J Nutr. 2002;88 Suppl 1:S95–S99. PubMed

Deng ZY, Zhang JW, Li J, Fan YW, Cao SW, Huang RL, Yin YL, Zhong HY, Li TJ. Effect of polysaccharides of cassiae seeds on the intestinal microflora of piglets. Asia Pac J Clin Nutr. 2007;16 Suppl 1:143–147. PubMed

Dixit SM, Gordon DM, Wu XY, Chapman T, Kailasapathy K, Chin JJ. Diversity analysis of commensal porcine Escherichia coli - associations between genotypes and habitat in the porcine gastrointestinal tract. Microbiology. 2004;150:1735–1740. PubMed

Farmer JJ 3rd, Fanning GR, Davis BR, O'Hara CM, Riddle C, Hickman-Brenner FW, Asbury MA, Lowery VA 3rd, Brenner DJ. Escherichia fergusonii and Enterobacter taylorae, two new species of Enterobacteriaceae isolated from clinical specimens. J Clin Microbiol. 1985;21:77–81. PubMed PMC

Wragg P, La Ragione RM, Best A, Reichel R, Anjum MF, Mafura M, Woodward MJ. Characterisation of Escherichia fergusonii isolates from farm animals using an Escherichia coli virulence gene array and tissue culture adherence assays. Res Vet Sci. 2009;86:27–35. PubMed

Smajs D, Karpathy SE, Smarda J, Weinstock GM. Colicins produced by the Escherichia fergusonii strains closely resemble colicins encoded by Escherichia coli. FEMS Microbiol Lett. 2002;208:259–262. PubMed

Smarda J, Smajs D, Lhotová H. Three recently acknowledged Escherichia species strikingly differ in the incidence of bacteriocinogenic and lysogenic strains. J Basic Microbiol. 2002;42:429–433. PubMed

Christl SU, Murgatroyd PR, Gibson GR, Cummings JH. Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology. 1992;102:1269–1277. PubMed

Hamilton LH. Breath tests and gastroenterology. 2nd ed. Milwaukee: QuinTron Instrument Company; 1998.

Gasbarrini A, Corazza GR, Gasbarrini G, Montalto M, Di Stefano M, Basilisco G, Parodi A, Usai-Satta P, Vernia P, Anania C, et al. Methodology and indications of H2-breath testing in gastrointestinal diseases: the Rome Consensus Conference. Aliment Pharmacol Ther. 2009;29 Suppl 1:1–49. PubMed

Strocchi A, Levitt MD. Factors affecting hydrogen production and consumption by human fecal flora. The critical roles of hydrogen tension and methanogenesis. J Clin Invest. 1992;89:1304–1311. PubMed PMC

Strocchi A, Levitt MD. Maintaining intestinal H2 balance: credit the colonic bacteria. Gastroenterology. 1992;102:1424–1426. PubMed

Strocchi A, Ellis CJ, Levitt MD. Use of metabolic inhibitors to study H2 consumption by human feces: evidence for a pathway other than methanogenesis and sulfate reduction. J Lab Clin Med. 1993;121:320–327. PubMed

Strocchi A, Ellis CJ, Furne JK, Levitt MD. Study of constancy of hydrogen-consuming flora of human colon. Dig Dis Sci. 1994;39:494–497. PubMed

Strocchi A, Furne J, Ellis C, Levitt MD. Methanogens outcompete sulphate reducing bacteria for H2 in the human colon. Gut. 1994;35:1098–1101. PubMed PMC

Koetse HA, Vonk RJ, Pasterkamp S, Pal J, de Bruijn S, Stellaard F. Variations in colonic H2 and CO2 production as a cause of inadequate diagnosis of carbohydrate maldigestion in breath tests. Scand J Gastroenterol. 2000;35:607–611. PubMed

Bures J, Cyrany J, Lesna J, Kopacova M, Vorisek V, Palicka V, Rejchrt S. Hydrogen breath tests: hydrogenic and methanogenic bacteria are common Enterobacteriaceae strains. Gut. 2008;57 Suppl 2:A223.

Cyrany J, Kvetina J, Kunes M, Förstl M, Moravkova M, Lesna J, Bartos V, Kopacova M, Rejchrt S, Bures J. Non-steroidal anti-inflammatory drugs and probiotics influence on porcine colonic bacteria evaluated by hydrogen production in vitro - a pilot study. Gut. 2009;58 Suppl 2:A257–A258.

Bures J, Cyrany J, Kohoutova D, Förstl M, Rejchrt S, Kvetina J, Vorisek V, Kopacova M. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol. 2010;16:2978–2990. PubMed PMC

McKay LF, Holbrook WP, Eastwood MA. Methane and hydrogen production by human intestinal anaerobic bacteria. Acta Pathol Microbiol Immunol Scand B. 1982;90:257–260. PubMed

Forbes BA, Sahm DF, Weissfeld AS. Bailey & Scott's diagnostic microbiology. 12th ed. St. Louis: Mosby Inc; 2007.

Kien CL, Murray RD, Qualman SJ, Marcon M. Lactulose feeding in piglets: a model for persistent diarrhea and colitis induced by severe sugar malabsorption. Dig Dis Sci. 1999;44:1476–1484. PubMed

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