14,087
Views
66
CrossRef citations to date
0
Altmetric
Review Article

E. coli and colorectal cancer: a complex relationship that deserves a critical mindset

Pages 619-632 | Received 07 Jun 2017, Accepted 23 May 2018, Published online: 17 Jun 2018

References

  • Abdulamir AS, Hafidh RR, Abu Bakar F. 2011. The association of Streptococcus bovis/gallolyticus with colorectal tumors: the nature and the underlying mechanisms of its etiological role. J Exp Clin Cancer Res. 30:11.
  • Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, Goedert JJ, Hayes RB, Yang L. 2013. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 105:1907–1911.
  • Allen-Vercoe E, Jobin C. 2014. Fusobacterium and Enterobacteriaceae: important players for CRC? Immunol Lett. 162:54–61.
  • Arthur JC, Gharaibeh RZ, Mühlbauer M, Perez-Chanona E, Uronis JM, McCafferty J, Fodor AA, Jobin C. 2014. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 5:4724.
  • Arthur JC, Jobin C. 2013. The complex interplay between inflammation, the microbiota and colorectal cancer. Gut Microbes. 4:253–258.
  • Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB. 2012. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 338:120–123.
  • Balskus EP. 2015. Colibactin: understanding an elusive gut bacterial genotoxin. Nat Prod Rep. 32:1534–1540.
  • Bian X, Fu J, Plaza A, Herrmann J, Pistorius D, Stewart AF, Zhang Y, Müller R. 2013. In vivo evidence for a prodrug activation mechanism during colibactin maturation. Chembiochem. 14:1194–1197.
  • Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, Déchelotte P, Bonnet R, Pezet D, Darfeuille-Michaud A. 2014. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res. 20:859–886.
  • Bossuet-Greif N, Dubois D, Petit C, Tronnet S, Martin P, Bonnet R, Oswald E, Nougayrède JP. 2016. Escherichia coli ClbS is a colibactin resistance protein. Mol Microbiol. 99:897–908.
  • Brader P, Stritzker J, Riedl CC, Zanzonico P, Cai S, Burnazi EM, Ghani ER, Hricak H, Szalay AA, Fong Y, et al. 2008. Escherichia coli Nissle 1917 facilitates tumor detection by positron emission tomography and optical imaging. Clin Cancer Res. 14:2295–2302.
  • Brotherton CA, Balskus EP. 2013. A prodrug resistance mechanism is involved in colibactin biosynthesis and cytotoxicity. J Am Chem Soc. 135:3359–3362.
  • Brotherton CA, Wilson M, Byrd G, Balskus EP. 2015. Isolation of a metabolite from the pks island provides insights into colibactin biosynthesis and activity. Org Lett. 17:1545–1548.
  • Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, Pezet D, Bonnet R. 2013. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 8:e56964.
  • Candela M, Guidotti M, Fabbri A, Brigidi P, Franceschi C, Fiorentini C. 2011. Human intestinal microbiota: cross-talk with the host and its potential role in colorectal cancer. Crit Rev Microbiol. 37:1–14.
  • Caruso ML, Fucci L. 1990. Histological identification of Helicobacter pylori in early and advanced gastric cancer. J Clin Gastroenterol. 12:601–602.
  • Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, et al. 2012. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 22:299–306.
  • Chaudhuri RR, Henderson IR. 2012. The evolution of the Escherichia coli phylogeny. Infect Genet Evol. 12:214–226.
  • Chen W, Liu F, Ling Z, Tong X, Xiang C. 2012. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One. 7:e39743.
  • Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, Sauvanet P, Darcha C, Déchelotte P, Bonnet M, et al. 2014. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype . Gut. 63:1932–1942.
  • Cougnoux A, Gibold L, Robin F, Dubois D, Pradel N, Darfeuille-Michaud A, Dalmasso G, Delmas J, Bonnet R. 2012. Analysis of structure-function relationships in the colibactin-maturating enzyme ClbP. J Mol Biol. 424:203–214.
  • Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrède JP. 2010. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 107:11537–11542.
  • Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R. 2014. The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes. 5:675–680.
  • Danino T, Prindle A, Kwong GA, Skalak M, Li H, Allen K, Hasty J, Bhatia SN. 2015. Programmable probiotics for detection of cancer in urine. Sci Transl Med. 7:289ra84.
  • de Meijere A. 1979. Bonding properties of cyclopropane and their chemical consequences. Angew Chem Int Ed Engl. 18:809–826.
  • Dubois D, Baron O, Cougnoux A, Delmas J, Pradel N, Boury M, Bouchon B, Bringer MA, Nougayrède JP, Oswald E, et al. 2011. ClbP is a prototype of a peptidase subgroup involved in biosynthesis of nonribosomal peptides. J Biol Chem. 286:35562–35570.
  • Escobar-Páramo P, Grenet K, Le Menac’h A, Rode L, Salgado E, Amorin C, Gouriou S, Picard B, Rahimy MC, Andremont A, et al. 2004. Large-scale population structure of human commensal Escherichia coli isolates. Appl Environ Microbiol.70:5698–5700.
  • Fabbri A, Travaglione S, Ballan G, Loizzo S, Fiorentini CT. 2013. The cytotoxic necrotizing factor 1 from E. coli: a Janus toxin playing with cancer regulators. Toxins. 5:1462–1474.
  • Gagnière J, Bonnin V, Jarrousse AS, Cardamone E, Agus A, Uhrhammer N, Sauvanet P, Déchelotte P, Barnich N, Bonnet R, et al. 2017. Interactions between microsatellite instability and human gut colonization by Escherichia coli in colorectal cancer. Clin Sci. 131:471–485.
  • Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, Bringer MA, Pezet D, Bonnet M. 2016. Gut microbiota imbalance and colorectal cancer. World J Gastroenterol. 22:501–518.
  • Grasso F, Frisan T. 2015. Bacterial genotoxins: merging the DNA damage response into infection biology. Biomolecules. 5:1762–1782.
  • Healy AR, Nikolayevskiy H, Patel JR, Crawford JM, Herzon SB. 2016. A mechanistic model for colibactin-induced genotoxicity. J Am Chem Soc. 138:15563–15570.
  • Healy AR, Vizcaino MI, Crawford JM, Herzon SB. 2016. Convergent and modular synthesis of candidate precolibactins. Structural revision of precolibactin A. J Am Chem Soc. 138:5426–5432.
  • Herrinton LJ, Liu L, Levin TR, Allison JE, Lewis JD, Velayos F. 2012. Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010. Gastroenterology. 143:382–389.
  • Hill PJ, Stritzker J, Scadeng M, Geissinger U, Haddad D, Basse-Lüsebrink TC, Gbureck U, Jakob P, Szalay AA. 2011. Magnetic resonance imaging of tumors colonized with bacterial ferritin-expressing Escherichia coli. PLoS One. 6:e25409.
  • Höckel M, Vaupel P. 2001. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 93:266–276.
  • Homburg S, Oswald E, Hacker J, Dobrindt U. 2007. Expression analysis of the colibactin gene cluster coding for a novel polyketide in Escherichia coli. FEMS Microbiol Lett. 275:255–262.
  • Irving AA, Yoshimi K, Hart ML, Parker T, Clipson L, Ford MR, Kuramoto T, Dove WF, Amos-Landgraf JM. 2014. The utility of Apc-mutant rats in modeling human colon cancer. Dis Model Mech. 7:1215–1225.
  • Joeres-Nguyen-Xuan TH, Boehm SK, Joeres L, Schulze J, Kruis W. 2010. Survival of the probiotic Escherichia coli Nissle 1917 (EcN) in the gastrointestinal tract given in combination with oral mesalamine to healthy volunteers. Inflamm Bowel Dis. 16:256–262.
  • Johnson JR, Johnston B, Kuskowski MA, Nougayrède JP, Oswald E. 2008. Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island. J Clin Microbiol. 46:3906–3911.
  • Johnson JR, Oswald E, O’Bryan TT, Kuskowski MA, Spanjaard L. 2002. Phylogenetic distribution of virulence-associated genes among Escherichia coli isolates associated with neonatal bacterial meningitis in the Netherlands. J Infect Dis. 185:774–784.
  • Kim SC, Tonkonogy SL, Albright CA, Tsang J, Balish EJ, Braun J, Huycke MM, Sartor RB. 2005. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 128:891–906.
  • Kipanyula MJ, Seke Etet PF, Vecchio L, Farahna M, Nukenine EN, Nwabo Kamdje AH. 2013. Signaling pathways bridging microbial-triggered inflammation and cancer. Cell Signal. 25:403–416.
  • Kocijancic D, Felgner S, Frahm M, Komoll RM, Iljazovic A, Pawar V, Rohde M, Heise U, Zimmermann K, Gunzer F, et al. 2016. Therapy of solid tumors using probiotic Symbioflor-2: restraints and potential. Oncotarget. 7:22605–22622.
  • Lara-Tejero M, Galán JE. 2000. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science. 290:354–357.
  • Lax AJ. 2005. Opinion: bacterial toxins and cancer-a case to answer? Nat Rev Microbiol. 3:343–349.
  • Li ZR, Li J, Gu JP, Lai JYH, Duggan BM, Zhang WP, Li ZL, Li YX, Tong RB, Xu Y, et al. 2016. Divergent biosynthesis yields a cytotoxic aminomalonate-containing precolibactin. Nat Chem Biol. 12:773–775.
  • Maddocks OD, Short AJ, Donnenberg MS, Bader S, Harrison DJ. 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.
  • Marchès O, Ledger TN, Boury M, Ohara M, Tu X, Goffaux F, Mainil J, Rosenshine I, Sugai M, De Rycke J, et al. 2003. Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol. 50:1553–1567.
  • Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM. 2004. Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology. 127:80–93.
  • Mousa JJ, Newsome RC, Yang Y, Jobin C, Bruner SD. 2017. ClbM is a versatile, cation-promiscuous MATE transporter found in the colibactin biosynthetic gene cluster. Biochem Biophys Res Commun. 482:1233–1239.
  • Mousa JJ, Yang Y, Tomkovich S, Shima A, Newsome RC, Tripathi P, Oswald E, Bruner SD, Jobin C. 2016. MATE transport of the E. coli-derived genotoxin colibactin. Nat Microbiol. 1:15009.
  • Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E, et al. 2006. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 313:848–851.
  • Nougayrède JP, Taieb F, De Rycke J, Oswald E. 2005. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol. 13:103–110.
  • Nowrouzian FL, Oswald E. 2012. Escherichia coli strains with the capacity for long-term persistence in the bowel microbiota carry the potentially genotoxic pks island. Microb Pathog. 53:180–182.
  • Patwa LG, Fan TJ, Tchaptchet S, Liu Y, Lussier YA, Sartor RB, Hansen JJ. 2011. Chronic intestinal inflammation induces stress-response genes in commensal Escherichia coli. Gastroenterology.141:1842–1851.
  • Payros D, Dobrindt U, Martin P, Secher T, Bracarense AP, Boury M, Laffitte J, Pinton P, Oswald E, Oswald IP. 2017. The food contaminant deoxynivalenol exacerbates the genotoxicity of gut microbiota. MBio. 8:e00007–00017.
  • Prilassnig M, Wenisch C, Daxboeck F, Feierl G. 2007. Are probiotics detectable in human feces after oral uptake by healthy volunteers? Wien Klin Wochenschr. 119:456–462.
  • Prorok-Hamon M, Friswell MK, Alswied A, Roberts CL, Song F, Flanagan PK, Knight P, Codling C, Marchesi JR, Winstanley C, 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.
  • Putze J, Hennequin C, Nougayrède JP, Zhang W, Homburg S, Karch H, Bringer MA, Fayolle C, Carniel E, Rabsch W, et al. 2009. Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun. 77:4696–4703.
  • Raisch J, Buc E, Bonnet M, Sauvanet P, Vazeille E, de Vallée A, Déchelotte P, Darcha C, Pezet D, Bonnet R, et al. 2014. Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World J Gastroenterol. 20:6560–6572.
  • Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. 2013. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe. 14:195–206.
  • Sanapareddy N, Legge RM, Jovov B, McCoy A, Burcal L, Araujo-Perez F, Randall TA, Galanko J, Benson A, Sandler RS, et al. 2012. Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans. ISME J. 6:1858–1868.
  • Sandler RS. 1996. Epidemiology and risk factors for colorectal cancer. Gastroenterol Clin North Am. 25:717–735.
  • Schölzel S, Zimmermann W, Schwarzkopf G, Grunert F, Rogaczewski B, Thompson J. 2000. Carcinoembryonic antigen family members CEACAM6 and CEACAM7 are differentially expressed in normal tissues and oppositely deregulated in hyperplastic colorectal polyps and early adenomas. Am J Pathol. 156:595–605.
  • Secher T, Brehin C, Oswald E. 2016. Early settlers: which E. coli strains do you not want at birth? Am J Physiol Gastrointest Liver Physiol. 311:G123–G129.
  • Secher T, Samba-Louaka A, Oswald E, Nougayrède JP. 2013. Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PLoS One. 8:e77157.
  • Selander RK, Caugant DA, Ochman H, Mussser JM, Gilmour MN, Whittam TS. 1986. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol. 51:873–884.
  • Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Tran Van Nhieu J, Furet JP. 2011. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 6:e16393.
  • Stritzker J, Hill PJ, Gentsche I, Szalay AA. 2010. Myristoylation negative msbB-mutants of probiotic E. coli Nissle 1917 retain tumor specific colonization properties but show less side effects in immunocompetent mice. Bioeng Bugs. 1:139–145.
  • Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA. 2007. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int J Med Microbiol. 297:151–162.
  • Stritzker J, Weibel S, Seubert C, Götz A, Tresch A, van Rooijen N, Oelschlaeger TA, Hill PJ, Gentschev I, Szalay AA. 2010. Enterobacterial tumor colonization in mice depends on bacterial metabolism and macrophages but is independent of chemotaxis and motility. Int J Med Microbiol. 300:449–456.
  • Swidsinski A, Khilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber J, Lochs H. 1998. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology.115:281–286.
  • Uronis JM, Mühlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. 2009. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 4:e6026.
  • Vizcaino MI, Crawford JM. 2015. The colibactin warhead crosslinks DNA. Nat Chem. 7:411–417.
  • Vizcaino MI, Engel P, Trautman E, Crawford JM. 2014. Comparative metabolomics and structural characterizations illuminate colibactin pathway-dependent small molecules. J Am Chem Soc. 136:9244–9247.
  • Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, Jia W, Cai S, Zhao L. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6:320–329.
  • Zha L, Wilson MR, Brotherton CA, Balskus EP. 2016. Characterization of polyketide synthase machinery from the pks island facilitates isolation of a candidate precolibactin. ACS Chem Biol. 11:1287–1295.