Possible role of Escherichia coli in propagation and perpetuation of chronic inflammation in ulcerative colitis

BMC Gastroenterology

Magdalena Strus¹  Piotr B Heczko¹  Tomasz Mach³  Malgorzata Zwolinska-Wcislo³  Pawel Adamski²  Anna Tomusiak¹  Tomasz Gosiewski¹  Agnieszka Chmielarczyk¹  Magdalena Pilarczyk-Zurek¹ 

[1] Department of Microbiology, Jagiellonian University Medical College, Czysta 18 Street, Cracow, 31-121, Poland;Polish Academy of Sciences, Institute of Nature Conservation, 33 Mickiewicza Avenue, Cracow, 31-120, Poland;Department of Gastroenterology, Hepatology and Infectious Diseases, Jagiellonian University Medical College, Śniadeckich 5 Street, Cracow, 31-531, Poland

关键词: Iron acquisition;    Escherichia coli;    Ulcerative colitis;   

Others  :  858096
DOI  :  10.1186/1471-230X-13-61

 received in 2012-10-17, accepted in 2013-03-19,  发布年份 2013

【 摘 要 】

Background

This study investigated a possible role of Escherichia coli in propagation and perpetuation of the chronic inflammation in ulcerative colitis (UC). The lesions of UC are located superficially on the rectal and/or colonic mucosa. It is suggested that the commensal bacteria of the digestive tract may play a role in the pathogenesis of UC. Several studies have demonstrated proliferation of E. coli in the gut of UC patients. An increase in the number of E. coli in the inflamed tissue is most probably related to the abundance of iron ions produced by the bacteria.

Methods

Colon mucosal biopsies were collected from 30 patients with acute-phase UC, both from tissues with inflammatory changes (n = 30) and unchanged tissue with no inflammatory changes (n = 30) from the same patient. Biopsies were also taken from 16 patients with irritable bowel syndrome diarrhea who comprised the control group. Quantitative and qualitative analysis of the biopsy specimens was performed using culture methods and real-time polymerase chain reaction (PCR). Genotyping of the E. coli isolates was done using pulsed-field gel electrophoresis. Multiplex PCR was used to compare the E. coli strains for the presence of genes responsible for synthesis of iron acquisition proteins: iroN, iutA, iha, ireA, chuA, and hlyA.

Results

We demonstrated that there was a significant increase in the number of E. coli at the sites of inflammation in patients with UC compared to the control group (P = 0.031). Comparative analysis of the restriction patterns of E. coli isolated from inflammatory and unchanged tissues showed that the local inflammatory changes did not promote specific E. coli strains. There was a significant difference in the frequency of the iroN gene in E. coli isolated from patients with UC as compared to the control group.

Conclusions

The increase in the numbers of E. coli in the inflammatory tissues is related to the presence of chuA and iutA genes, which facilitate iron acquisition during chronic intestinal inflammatory processes.

【 授权许可】

   
2013 Pilarczyk-Zurek et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Mpofu C: Ireland. Inflammatory bowel disease-the disease and it’s diagnosis. Hospital Pharmacist 2006, 13:153-158.
• [2]Sepehri S, Kotlowski R, Bernstein CN, Krause DO: Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm Bowel Dis 2007, 13(6):675-683.
• [3]Dudhgaonkar SP, Tandan SK, Kumar D, Raviprakash V, Kataria M: Influence of simultaneous inhibition of cyclooxygenase-2 and inducible nitric oxide synthase in experimental colitis in rats. Inflammopharmacology 2007, 15(5):188-195.
• [4]Sandborn WJ, Stenson WF, Brynskov J, Lorenz RG, Steidle GM, Robbins JL, Kent JD, Bloom BJ: Safety of celecoxib in patients with ulcerative colitis in remission: a randomized, placebo-controlled, pilot study. Clin Gastroenterol Hepatol 2006, 4(2):203-211.
• [5]Hulten K, El-Zimaity HM, Karttunen TJ, Almashhrawi A, Schwartz MR, Graham DY, El-Zaatari FA: Detection of Mycobacterium avium subspecies paratuberculosis in Crohn’s diseased tissues by in situ hybridization. Am J Gastroenterol 2001, 96(5):1529-1535.
• [6]Strus M, Uhlig H, Powrie F, Hultgren Hornquist E, Bland P, Drzewiecki A, Kochan P, Heczko PB: A role of bacteria in inflammatory bowel disease evoked in animal models. Gastroenterol Pol 2005, 12:15-20.
• [7]Gosiewski T, Strus M, Fyderek K, Kowalska-Duplaga K, Wedrychowicz A, Jedynak-Wasowicz U, Sladek M, Pieczarkowski S, Adamski P, Heczko P: Horizontal Distribution of the Fecal Microbiota in Adolescents With Inflammatory Bowel Disease. J Pediatr Gastroenterol Nutr 2012, 54(1):20-27.
• [8]Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, Berg D, Schukken Y, Scherl E, Simpson KW: 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 2007, 1(5):403-418. Epub 2007 Jul 12
• [9]Kotlowski R, Bernstein CN, Sepehri S, Krause DO: High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 2007, 56(5):669-675.
• [10]Wohlgemuth S, Haller D, Blaut M, Loh G: Reduced microbial diversity and high numbers of one single Escherichia coli strain in the intestine of colitic mice. Environ Microbiol 2009, 11(6):1562-1571.
• [11]Law D, Wilkie KM, Freeman R, Gould FK: The iron uptake mechanisms of enteropathogenic Escherichia coli: the use of haem and haemoglobin during growth in an iron-limited environment. J Med Microbiol 1992, 37(1):15-21.
• [12]Byron CH, Chu BC, Vogel HJ: A structural and functional analysis of type III periplasmic and substrate binding proteins: their role in bacterial siderophore and heme transport. Biol Chem 2011, 392(1–2):39-52.
• [13]Gentschev I, Dietrich G, Goebel W: The E. coli alpha-hemolysin secretion system and its use in vaccine development. Trends Microbiol 2002, 10(1):39-45.
• [14]Masseret E, Boudeau J, Colombel JF, Neut C, Desreumaux P, Joly B, Cortot A, Darfeuille-Michaud A: Genetically related Escherichia coli strains associated with Crohn’s disease. Gut 2001, 48(3):320-325.
• [15]Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF: High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology 2004, 127(2):412-421.
• [16]Simmonds NJ, Rampton DS: Inflammatory bowel disease a radical view. Gut 1993, 34:865-868.
• [17]Geboes K, Riddell R, Ost A, Jensfelt B, Persson T, Löfberg R: A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut 2000, 47(3):404-409.
• [18]Conte MP, Schippa S, Zamboni I, Penta M, Chiarini F, Seganti L, Osborn J, Falconieri P, Borrelli O, Cuchiara S: Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 2006, 55:1760-1767.
• [19]Clark PA, Cotton LN, Martin JH: Selection of bifidobacteria for use as dietary adjuncts in cultured dairy foods. II. Tolerance to simulated pH of human stomachs. Cult Dairy Prod J. 1993, 28:11-14.
• [20]Chiba N, Murayama SY, Morozumi M, Nakayama E, Okada T, Iwata S, Sunakawa K, Ubukata K: Rapid detection of eight causative pathogens for the diagnosis of bacterial meningitis by real-time PCR. J Infect Chemother 2009, 15(2):92-98. Epub 2009 Apr 25
• [21]Lyons SR, Griffen AL, Leys EJ: Quantitative real-time PCR for Porphyromonas gingivalis and total bacteria. J Clin Microbiol 2000, 38(6):2362-2365.
• [22]Online protocol 11. Pulse Net USA, Standardized Laboratory Protocol for Molecular Subtyping of Escherichia coli O157:H7, non-typhoidal Salmonella serotypes, and Shigella sonnei. Pulsed Field Gel Electrophoresis (PFGE); 2002.
• [23]Zhao L, Gao S, Huan H, Xu X, Zhu X, Yang W, Gao Q, Liu X: Comparison of virulence factors and expression of specific genes between uropathogenic Escherichia coli and avian pathogenic E. coli in a murine urinarytract infection model and a chicken challenge model. Microbiology 2009, 155:1634-1644.
• [24]Aranda KR, Fabbricotti SH, Fagundes-Neto U, Scaletsky IC: Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxin-producing Escherichia coli strains in Brazilian children. FEMS Microbiol Lett 2007, 267(2):145-150.
• [25]Strus M, Gosiewski T, Fyderek K, Wedrychowicz A, Kowalska-Duplaga K, Kochan P, Adamski P, Heczko PB: A role of hydrogen peroxide producing commensal bacteria present in colon of adolescents with inflammatory bowel disease in perpetuation of the inflammatory process. J Physiol Pharmacol 2009, 60(Suppl 6):49-54.
• [26]Mylonaki M, Rayment NB, Rampton DS, Hudspith BN, Brostoff J: Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis 2005, 11(5):481-487.
• [27]Kleessen B, Kroesen AJ, Buhr HJ, Blaut M: Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand J Gastroenterol 2002, 37(9):1034-1041.
• [28]Cornelis P, Wei Q, Andrews SC, Vinckx T: Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 2011, 3(6):540-549. Epub 2011 May 13
• [29]Ott SJ, Musfeldt M, Ullmann U, Hampe J, Schreiber S: Quantification of intestinal bacterial populations by real-time PCR with a universal primer set and minor groove binder probes: a global approach to the enteric flora. J Clin Microbiol 2004, 42(6):2566-2572.
• [30]Garénaux A, Caza M, Dozois CM: The Ins and Outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Vet Microbiol 2011, 153(1–2):89-98.
• [31]Thomazini CM, Samegima DA, Rodrigues MA, Victoria CR, Rodrigues J: High prevalence of aggregative adherent Escherichia coli strains in the mucosa-associated microbiota of patients with inflammatory bowel diseases. Int J Med Microbiol 2011, 301(6):475-479.
• [32]Andrews SC, Robinson AK, Rodríguez-Quiñones F: Bacterial iron homeostasis. FEMS Microbiol Rev 2003, 27(2–3):215-237.
• [33]Westendorf AM, Gunzer F, Deppenmeier S, Tapadar D, Hunger JK, Schmidt MA, Buer J, Bruder D: Intestinal immunity of Escherichia coli NISSLE 1917: a safe carrier for therapeutic molecules. FEMS Immunol Med Microbiol 2005, 43(3):373-384.