Escherichia coli from biopsies differ in virulence genes between patients with colorectal neoplasia and healthy controls

. 2023 ; 14 () : 1141619. [epub] 20230413

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37125208

INTRODUCTION: Pathogenic strains of Escherichia coli have been clearly identified as the causative agents of extraintestinal and diarrheal infections; however, the etiopathogenic role of E. coli in other conditions, including colorectal cancer, remains unclear. METHODS: This study aimed to characterize mucosal E. coli isolates (n = 246) from 61 neoplasia patients and 20 healthy controls for the presence of 35 genetic determinants encoding known virulence factors. RESULTS: Virulence determinants encoding invasin (ibeA), siderophore receptor (iroN), S-fimbriae (sfa), and genotoxin (usp) were more prevalent among E. coli isolated from patients with neoplasia compared to the control group (p < 0.05). In addition, the prevalence of these virulence determinants was increased in more advanced neoplasia stages (p adj < 0.0125). Compared to patients with advanced colorectal adenoma and carcinoma, the ibeA gene was rarely found in the control group and among patients with non-advanced adenoma (p < 0.05), indicating its potential as the advanced-neoplasia biomarker. Patients with neoplasia frequently had E. coli strains with at least one of the abovementioned virulence factors, whereby specific combinations of these virulence factors were found. DISCUSSION: These findings suggest that E. coli strains isolated from patients with colorectal neoplasia possess several virulence factors, which could contribute to the development of neoplastic processes in the large intestine.

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Arthur J. C., Perez-Chanona E., Mühlbauer M., Tomkovich S., Uronis J. M., Fan T. J., et al. (2012). Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338 120–123. 10.1126/science.1224820 PubMed DOI PMC

Azpiroz M. F., Poey M. E., Laviña M. (2009). Microcins and urovirulence in Escherichia coli. Microb. Pathog. 47 274–280. 10.1016/j.micpath.2009.09.003 PubMed DOI

Beutin L., Martin A. (2012). Outbreak of shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J. Food Prot. 75 408–418. 10.4315/0362-028X.JFP-11-452 PubMed DOI

Bonnet M., Buc E., Sauvanet P., Darcha C., Dubois D., Pereira B., et al. (2014). Colonization of the human gut by E. coli and colorectal cancer risk. Clin. Cancer Res. 20 859–867. 10.1158/1078-0432.CCR-13-1343 PubMed DOI

Bonnington S. N., Rutter M. D. (2016). Surveillance of colonic polyps: are we getting it right? World J. Gastroenterol. 22 1925–1934. 10.3748/wjg.v22.i6.1925 PubMed DOI PMC

Bosák J., Hrala M., Micenková L., Šmajs D. (2021). Non-antibiotic antibacterial peptides and proteins of Escherichia coli: efficacy and potency of bacteriocins. Expert Rev. Anti. Infect. Ther. 19 309–322. 10.1080/14787210.2020.1816824 PubMed DOI

Brennan C. A., Garrett W. S. (2016). Gut microbiota, inflammation, and colorectal cancer. Annu. Rev. Microbiol. 70 395–411. 10.1146/annurev-micro-102215-095513 PubMed DOI PMC

Buc E., Dubois D., Sauvanet P., Raisch J., Delmas J., Darfeuille-Michaud A., et al. (2013). High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One 8:e56964. 10.1371/journal.pone.0056964 PubMed DOI PMC

Chattopadhyay I., Dhar R., Pethusamy K., Seethy A., Srivastava T., Sah R., et al. (2021). Exploring the role of gut microbiome in colon cancer. Appl. Biochem. Biotechnol. 193 1780–1799. 10.1007/s12010-021-03498-9 PubMed DOI

Cieza R. J., Hu J., Ross B. N., Sbrana E., Torres A. G. (2015). The IbeA invasin of adherent-invasive Escherichia coli mediates interaction with intestinal epithelia and macrophages. Infect. Immun. 83 1904–1918. 10.1128/IAI.03003-14 PubMed DOI PMC

Clermont O., Bonacorsi S., Bingen E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66 4555–4558. 10.1128/AEM.66.10.4555-4558.2000 PubMed DOI PMC

Dale A. P., Woodford N. (2015). Extra-intestinal pathogenic Escherichia coli (ExPEC): disease, carriage and clones. J. Infect. 71 615–626. 10.1016/J.JINF.2015.09.009 PubMed DOI

Denamur E., Clermont O., Bonacorsi S., Gordon D. (2021). The population genetics of pathogenic Escherichia coli. Nat. Rev. Microbiol. 19 37–54. 10.1038/s41579-020-0416-x PubMed DOI

Desvaux M., Dalmasso G., Beyrouthy R., Barnich N., Delmas J., Bonnet R. (2020). Pathogenicity factors of genomic islands in intestinal and extraintestinal Escherichia coli. Front. Microbiol. 11:2065. 10.3389/fmicb.2020.02065 PubMed DOI PMC

Dobrindt U., Blum-Oehler G., Hartsch T., Gottschalk G., Ron E. Z., Fünfstück R., et al. (2001). S-fimbria-encoding determinant sfaI is located on pathogenicity island III536 of uropathogenic Escherichia coli strain 536. Infect. Immun. 69 4248–4256. 10.1128/IAI.69.7.4248-4256.2001 PubMed DOI PMC

Dutta S., Guin S., Ghosh S., Pazhani G. P., Rajendran K., Bhattacharya M. K., et al. (2013). Trends in the prevalence of diarrheagenic Escherichia coli among hospitalized diarrheal patients in Kolkata, India. PLoS One 8:e56068. 10.1371/journal.pone.0056068 PubMed DOI PMC

Eppinger M., Cebula T. A. (2015). Future perspectives, applications and challenges of genomic epidemiology studies for food-borne pathogens: a case study of enterohemorrhagic Escherichia coli (EHEC) of the O157:H7 serotype. Gut Microbes 6 194–201. 10.4161/19490976.2014.969979 PubMed DOI PMC

Escobar-Páramo P., Grenet K., Le Menac’h A., Rode L., Salgado E., Amorin C., et al. (2004). Large-scale population structure of human commensal Escherichia coli isolates. Appl. Environ. Microbiol. 70 5698–5700. 10.1128/AEM.70.9.5698-5700.2004 PubMed DOI PMC

European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control (2021). The European Union one health 2019 zoonoses report. EFSA J. 19:6406. 10.2903/j.efsa.2021.6406 PubMed DOI PMC

Feldmann F., Sorsa L. J., Hildinger K., Schubert S. (2007). The salmochelin siderophore receptor IroN contributes to invasion of urothelial cells by extraintestinal pathogenic Escherichia coli in vitro. Infect. Immun. 75 3183–3187. 10.1128/IAI.00656-06 PubMed DOI PMC

Feng Q., Liang S., Jia H., Stadlmayr A., Tang L., Lan Z., et al. (2015). Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun. 6:e6528. 10.1038/ncomms7528 PubMed DOI

Garrett W. S. (2019). The gut microbiota and colon cancer. Science 364 1133–1135. 10.1126/science.aaw2367 PubMed DOI

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. U S A. 100 3677–3682. 10.1073/PNAS.0737682100 PubMed DOI PMC

Iwasaki M., Kanehara R., Yamaji T., Katagiri R., Mutoh M., Tsunematsu Y., et al. (2022). Association of Escherichia coli containing polyketide synthase in the gut microbiota with colorectal neoplasia in Japan. Cancer Sci. 113 277–286. 10.1111/cas.15196 PubMed DOI PMC

Kaper J. B., Nataro J. P., Mobley H. L. T. (2004). Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2 123–140. 10.1038/nrmicro818 PubMed DOI

Kohoutová D., Forstlová M., Moravková P., Cyrany J., Bosák J., Šmajs D., et al. (2020). Bacteriocin production by mucosal bacteria in current and previous colorectal neoplasia. BMC Cancer 20:39. 10.1186/s12885-020-6512-5 PubMed DOI PMC

Kohoutová D., Pejchal J., Bureš J. (2018). Mitotic and apoptotic activity in colorectal neoplasia. BMC Gastroenterol. 18:65. 10.1186/s12876-018-0786-y PubMed DOI PMC

Kohoutová D., Šmajs D., Moravková P., Cyrany J., Moravková M., Forstlová M., et al. (2014). Escherichia coli strains of phylogenetic group B2 and D and bacteriocin production are associated with advanced colorectal neoplasia. BMC Infect. Dis. 14:e733. 10.1186/s12879-014-0733-7 PubMed DOI PMC

Kosek M., Bern C., Guerrant R. L. (2003). The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organ. 81 197–204. 10.1590/S0042-96862003000300010 PubMed DOI PMC

Kotlowski R., Bernstein C. N., Sepehri S., Krause D. O. (2007). High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56 669–675. 10.1136/gut.2006.099796 PubMed DOI PMC

Lopez L. R., Bleich R. M., Arthur J. C. (2021). Microbiota effects on carcinogenesis: initiation, promotion, and progression. Annu. Rev. Med. 72 243–261. 10.1146/annurev-med-080719-091604 PubMed DOI PMC

Maddocks O. D., Short A. J., Donnenberg M. S., Bader S., Harrison D. J. (2009). Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS One 4:e5517. 10.1371/journal.pone.0005517 PubMed DOI PMC

Mahajan D., Downs-Kelly E., Liu X., Pai R. K., Patil D. T., Rybicki L., et al. (2013). Reproducibility of the villous component and high-grade dysplasia in colorectal adenomas <1 cm: implications for endoscopic surveillance. Am. J. Surg. Pathol. 37 427–433. 10.1097/PAS.0b013e31826cf50f PubMed DOI

Martinez-Medina M., Naves P., Blanco J., Aldeguer X., Blanco J. E., Blanco M., et al. (2009). Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol. 9:202. 10.1186/1471-2180-9-202 PubMed DOI PMC

Micenková L., Bosák J., Štaudová B., Kohoutová D., Èejková D., Woznicová V., et al. (2016a). Microcin determinants are associated with B2 phylogroup of human fecal Escherichia coli isolates. Microbiologyopen 5 490–498. 10.1002/mbo3.345 PubMed DOI PMC

Micenková L., Bosák J., Vrba M., Ševèíková A., Šmajs D. (2016b). Human extraintestinal pathogenic Escherichia coli strains differ in prevalence of virulence factors, phylogroups, and bacteriocin determinants. BMC Microbiol. 16:218. 10.1186/s12866-016-0835-z PubMed DOI PMC

Mulvey M. A. (2002). Adhesion and entry of uropathogenic Escherichia coli. Cell. Microbiol. 4 257–271. 10.1046/j.1462-5822.2002.00193.x PubMed DOI

Nakatsu G., Li X., Zhou H., Sheng J., Wong S. H., Wu W. K. K., et al. (2015). Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat. Commun. 6:8727. 10.1038/ncomms9727 PubMed DOI PMC

Nataro J. P., Kaper J. B. (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11 142–201. 10.1128/CMR.11.1.142 PubMed DOI PMC

Nipič D., Podlesek Z., Budiè M., Črnigoj M., Žgur-Bertok D. (2013). Escherichia coli uropathogenic-specific protein, USP, is a bacteriocin-like genotoxin. J. Infect. Dis. 208 1545–1552. 10.1093/infdis/jit480 PubMed DOI

Nouri R., Hasani A., Masnadi Shirazi K., Alivand M. R., Sepehri B., Sotoudeh S., et al. (2021). Mucosa-associated Escherichia coli in colorectal cancer patients and control subjects: variations in the prevalence and attributing features. Can. J. Infect. Dis. Med. Microbiol. 2021:2131787. 10.1155/2021/2131787 PubMed DOI PMC

Nowrouzian F. L., Wold A. E., Adlerberth I. (2005). Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J. Infect. Dis. 191 1078–1083. 10.1086/427996 PubMed DOI

Palmela C., Chevarin C., Xu Z., Torres J., Sevrin G., Hirten R., et al. (2018). Adherent-invasive Escherichia coli in inflammatory bowel disease. Gut 67 574–587. 10.1136/gutjnl-2017-314903 PubMed DOI

Parret A. H. A., De Mot R. (2002). Escherichia coli’s uropathogenic-specific protein: a bacteriocin promoting infectivity? Microbiology 148 1604–1606. 10.1099/00221287-148-6-1604 PubMed DOI

Picard B., Garcia J. S., Gouriou S., Duriez P., Brahimi N., Bingen E., et al. (1999). The link between phylogeny and virulence in Escherichia coli extraintestinal infection? Infect. Immun. 67 546–553. 10.1128/iai.67.2.546-553.1999 PubMed DOI PMC

Prorok-Hamon M., Friswell M. K., Alswied A., Roberts C. L., Song F., Flanagan P. K., et al. (2014). Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut 63 761–770. 10.1136/gutjnl-2013-304739 PubMed DOI PMC

R Core Team (2022). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Raisch J., Buc E., Bonnet M., Sauvanet P., Vazeille E., de Vallée A., et al. (2014). Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World J. Gastroenterol. 20 6560–6572. 10.3748/wjg.v20.i21.6560 PubMed DOI PMC

Rijavec M., Müller-Premru M., Zakotnik B., Žgur-Bertok D. (2008). Virulence factors and biofilm production among Escherichia coli strains causing bacteraemia of urinary tract origin. J. Med. Microbiol. 57 1329–1334. 10.1099/jmm.0.2008/002543-0 PubMed DOI

Riley L. W. (2020). Distinguishing pathovars from nonpathovars: Escherichia coli. Microbiol. Spectr 8:AME0014-2020. 10.1128/microbiolspec.ame-0014-2020 PubMed DOI PMC

Roche-Lima A., Carrasquillo-Carrión K., Gómez-Moreno R., Cruz J. M., Velázquez-Morales D. M., Rogozin I. B., et al. (2018). The presence of genotoxic and/or pro-inflammatory bacterial genes in gut metagenomic databases and their possible link with inflammatory bowel diseases. Front. Genet. 9:116. 10.3389/fgene.2018.00116 PubMed DOI PMC

Russo T. A., Carlino U. B., Johnson J. R. (2001). Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coli. Infect. Immun. 69 6209–6216. 10.1128/IAI.69.10.6209-6216.2001 PubMed DOI PMC

Sarshar M., Scribano D., Marazzato M., Ambrosi C., Aprea M. R., Aleandri M., et al. (2017). Genetic diversity, phylogroup distribution and virulence gene profile of pks positive Escherichia coli colonizing human intestinal polyps. Microb. Pathog. 112 274–278. 10.1016/j.micpath.2017.10.009 PubMed DOI

Sepehri S., Khafipour E., Bernstein C. N., Coombes B. K., Pilar A. V., Karmali M., et al. (2011). Characterization of Escherichia coli isolated from gut biopsies of newly diagnosed patients with inflammatory bowel disease. Inflamm. Bowel Dis. 17 1451–1463. 10.1002/ibd.21509 PubMed DOI

Shimpoh T., Hirata Y., Ihara S., Suzuki N., Kinoshita H., Hayakawa Y., et al. (2017). Prevalence of pks-positive Escherichia coli in Japanese patients with or without colorectal cancer. Gut Pathog. 9:35. 10.1186/s13099-017-0185-x PubMed DOI PMC

Sung H., Ferlay J., Siegel R. L., Laversanne M., Soerjomataram I., Jemal A., et al. (2021). Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA. Cancer J. Clin. 71 209–249. 10.3322/caac.21660 PubMed DOI

Tenaillon O., Skurnik D., Picard B., Denamur E. (2010). The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8 207–217. 10.1038/nrmicro2298 PubMed DOI

Tilg H., Adolph T. E., Gerner R. R., Moschen A. R. (2018). The intestinal microbiota in colorectal cancer. Cancer Cell 33 954–964. 10.1016/j.ccell.2018.03.004 PubMed DOI

Tjalsma H., Boleij A., Marchesi J. R., Dutilh B. E. (2012). A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat. Rev. Microbiol. 10 575–582. 10.1038/nrmicro2819 PubMed DOI

Tseng M., Fratamico P. M., Manning S. D., Funk J. A. (2014). Shiga toxin-producing Escherichia coli in swine: the public health perspective. Anim. Heal. Res. Rev. 15 63–75. 10.1017/S1466252313000170 PubMed DOI PMC

Vieira P. C. G., Espinoza-Culupú A. O., Nepomuceno R., Alves M. R., Lebrun I., Elias W. P., et al. (2020). Secreted autotransporter toxin (Sat) induces cell damage during enteroaggregative Escherichia coli infection. PLoS One 15:e0228959. 10.1371/journal.pone.0228959 PubMed DOI PMC

Viljoen K. S., Dakshinamurthy A., Goldberg P., Blackburn J. M. (2015). Quantitative profiling of colorectal cancer-associated bacteria reveals associations between Fusobacterium spp., enterotoxigenic Bacteroides fragilis (ETBF) and clinicopathological features of colorectal cancer. PLoS One 10:e0119462. 10.1371/journal.pone.0119462 PubMed DOI PMC

Wassenaar T. M. (2018). E. coli and colorectal cancer: a complex relationship that deserves a critical mindset. Crit. Rev. Microbiol. 44 619–632. 10.1080/1040841X.2018.1481013 PubMed DOI

Yamamoto S., Nakano M., Terai A., Yuri K., Nakata K., Nair G. B., et al. (2001). The presence of the virulence island containing the USP gene in uropathogenic Escherichia coli is associated with urinary tract infection in an experimental mouse model. J. Urol. 165 1347–1351. 10.1016/S0022-5347(01)69897-5 PubMed DOI

Zhao W. D., Liu D. X., Wei J. Y., Miao Z. W., Zhang K., Su Z. K., et al. (2018). Caspr1 is a host receptor for meningitis-causing Escherichia coli. Nat. Commun. 9:2296. 10.1038/s41467-018-04637-3 PubMed DOI PMC

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