Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation

World Journal of Gastroenterology

Volumn 20, Issue 21, 2014, Pages 6560-6572

  Raisch, Jennifer ^a   Buc, Emmanuel ^b   Bonnet, Mathilde ^a   Sauvanet, Pierre ^b   Vazeille, Emilie ^b   de Vallée, Amélie ^a   Déchelotte, Pierre ^b   Darcha, Claude ^b   Pezet, Denis ^b   Bonnet, Richard ^b   Bringer, Marie Agnès ^a   Darfeuille Michaud, Arlette ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

B2 Escherichia coli; Carcinoembryonic antigen related cell adhesion molecule 6; Cell proliferation

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 6; CEFOXITIN; CYCLINE; CEACAM10 PROTEIN, MOUSE; CEACAM6 PROTEIN, HUMAN; CELL ADHESION MOLECULE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; KI 67 ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BIOFILM; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; COLITIS; COLON CANCER; COLON DIVERTICULOSIS; COLONY FORMING UNIT; CONTROLLED STUDY; CYCLOMODULIN ENCODING GENE; DISEASE ASSOCIATION; ENTERITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM CELL; MAJOR CLINICAL STUDY; MALE; MOLECULAR PHYLOGENY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PREVALENCE; PROTEIN EXPRESSION; SKIN DEFECT; WESTERN BLOTTING; ANIMAL; COLON TUMOR; DIVERTICULOSIS; GENETICS; INFLAMMATION; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PATHOGENICITY; TRANSGENIC MOUSE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, CD; BIOFILMS; CELL ADHESION MOLECULES; CELL PROLIFERATION; COLONIC NEOPLASMS; DIVERTICULUM; ESCHERICHIA COLI; FEMALE; GPI-LINKED PROTEINS; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; KI-67 ANTIGEN; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; POLYMERASE CHAIN REACTION; PROLIFERATING CELL NUCLEAR ANTIGEN;

EID: 84902106895     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i21.6560     Document Type: Article

References (51)

1. World Health Organization World. WHO Global Malaria Programme. Switzerland: World Health Organization, 2011. Available from: URL: http://www.who.int/malaria/world_malaria_report_2011/9789241564403_eng.pdf
2. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL. Genetic alterations during colorectal-tumor development. N Engl J Med 1988; 319: 525-532 [PMID: 2841597 DOI: 10.1056/ NEJM198809013190901]
3. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB, Rhodes JM, Stintzi A, Simpson KW, Hansen JJ, Keku TO, Fodor AA, Jobin C. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338: 120-123 [PMID: 22903521 DOI: 10.1126/science.1224820]
4. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454: 436-444 [PMID: 18650914 DOI: 10.1038/nature07205]
5. Uronis JM, Jobin C. Microbes and colorectal cancer: is there a relationship? Curr Oncol 2009; 16: 22-24 [PMID: 19672421]
6. Sears CL, Pardoll DM. Perspective: alpha-bugs, their microbial partners, and the link to colon cancer. J Infect Dis 2011; 203: 306-311 [PMID: 21208921 DOI: 10.1093/jinfdis/jiq061]
7. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 2012; 10: 575-582 [PMID: 22728587 DOI: 10.1038/nrmicro2819]
8. Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Tran Van Nhieu J, Furet JP. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One 2011; 6: e16393 [PMID: 21297998 DOI: 10.1371/journal. pone.0016393]
9. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, Baselga J, Liu C, Shivdasani RA, Ogino S, Birren BW, Huttenhower C, Garrett WS, Meyerson M. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012; 22: 292-298 [PMID: 22009990 DOI: 10.1101/ gr.126573.111]
10. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 2004; 127: 80-93 [PMID: 15236175]
11. Maddocks OD, Short AJ, Donnenberg MS, Bader S, Harrison DJ. Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS One 2009; 4: e5517 [PMID: 19436735 DOI: 10.1371/journal. pone.0005517]
12. Swidsinski A, Khilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber J, Lochs H. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 1998; 115: 281-286 [PMID: 9679033]
13. Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006; 313: 848-851 [PMID: 16902142 DOI: 10.1126/science.1127059]
14. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, Housseau F, Pardoll DM, Sears CL. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009; 15: 1016-1022 [PMID: 19701202 DOI: 10.1038/nm.2015]
15. Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X, Murray-Stewart TR, Hacker-Prietz A, Rabizadeh S, Woster PM, Sears CL, Casero RA. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA 2011; 108: 15354-15359 [PMID: 21876161 DOI: 10.1073/pnas.1010203108]
16. Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population- based study. Cancer 2001; 91: 854-862 [PMID: 11241255]
17. Ullman TA, Itzkowitz SH. Intestinal inflammation and cancer. Gastroenterology 2011; 140: 1807-1816 [PMID: 21530747 DOI: 10.1053/j.gastro.2011.01.057]
18. Martinez-Medina M, Aldeguer X, Gonzalez-Huix F, Acero D, Garcia-Gil LJ. Abnormal microbiota composition in the ileocolonic mucosa of Crohn's disease patients as revealed by polymerase chain reaction-denaturing gradient gel electrophoresis. Inflamm Bowel Dis 2006; 12: 1136-1145 [PMID: 17119388 DOI: 10.1097/01.mib.0000235828.09305.0c]
19. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007; 104: 13780-13785 [PMID: 17699621 DOI: 10.1073/pnas.0706625104]
20. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez- Humarán LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottière HM, Doré J, Marteau P, Seksik P, Langella P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008; 105: 16731-16736 [PMID: 18936492 DOI: 10.1073/ pnas.0804812105]
21. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening- Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H. Mucosal flora in inflammatory bowel disease. Gastroenterology 2002; 122: 44-54 [PMID: 11781279]
22. 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: 481-487 [PMID: 15867588]
23. 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: 403-418 [PMID: 18043660 DOI: 10.1038/ ismej.2007.52]
24. 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: 669-675 [PMID: 17028128 DOI: 10.1136/gut.2006.099796]
25. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel JF. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 1998; 115: 1405-1413 [PMID: 9834268]
26. Boudeau J, Glasser AL, Masseret E, Joly B, Darfeuille-Michaud A. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 1999; 67: 4499-4509 [PMID: 10456892]
27. 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: 412-421 [PMID: 15300573]
28. Barnich N, Carvalho FA, Glasser AL, Darcha C, Jantscheff P, Allez M, Peeters H, Bommelaer G, Desreumaux P, Colombel JF, Darfeuille-Michaud A. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest 2007; 117: 1566-1574 [PMID: 17525800 DOI: 10.1172/JCI30504]
29. Schölzel S, Zimmermann W, Schwarzkopf G, Grunert F, Rogaczewski B, Thompson J. 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 2000; 156: 595-605 [PMID: 10666389 DOI: 10.1016/ S0002-9440(10)64764-5]
30. Kim KS, Kim JT, Lee SJ, Kang MA, Choe IS, Kang YH, Kim SY, Yeom YI, Lee YH, Kim JH, Kim KH, Kim CN, Kim JW, Nam MS, Lee HG. Overexpression and clinical significance of carcinoembryonic antigen-related cell adhesion molecule 6 in colorectal cancer. Clin Chim Acta 2013; 415: 12-19 [PMID: 22975528 DOI: 10.1016/j.cca.2012.09.003]
31. Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991; 19: 6823-6831 [PMID: 1762913]
32. Wang G, Whittam TS, Berg CM, Berg DE. RAPD (arbitrary primer) PCR is more sensitive than multilocus enzyme electrophoresis for distinguishing related bacterial strains. Nucleic Acids Res 1993; 21: 5930-5933 [PMID: 8290354]
33. Bidet P, Metais A, Mahjoub-Messai F, Durand L, Dehem M, Aujard Y, Bingen E, Nassif X, Bonacorsi S. Detection and identification by PCR of a highly virulent phylogenetic subgroup among extraintestinal pathogenic Escherichia coli B2 strains. Appl Environ Microbiol 2007; 73: 2373-2377 [PMID: 17293507 DOI: 10.1128/AEM.02341-06]
34. Chassaing B, Darfeuille-Michaud A. The σE pathway is involved in biofilm formation by Crohn's disease-associated adherent-invasive Escherichia coli. J Bacteriol 2013; 195: 76-84 [PMID: 23104802 DOI: 10.1128/JB.01079-12]
35. Chan CH, Stanners CP. Novel mouse model for carcinoembryonic antigen-based therapy. Mol Ther 2004; 9: 775-785 [PMID: 15194045 DOI: 10.1016/j.ymthe.2004.03.009]
36. Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CH, Stanners CP, Darfeuille-Michaud A. Crohn's disease ad-herent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 2009; 206: 2179-2189 [PMID: 19737864 DOI: 10.1084/jem.20090741]
37. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL. IBDwhat role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 2012; 9: 219-230 [PMID: 22349170 DOI: 10.1038/nrgastro. 2012.14]
38. Sears CL. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin Microbiol Rev 2009; 22: 349-369, Table of Contents [PMID: 19366918 DOI: 10.1128/CMR.00053-08]
39. Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T, Soyletir G. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect 2006; 12: 782-786 [PMID: 16842574 DOI: 10.1111/ j.1469-0691.2006.01494.x]
40. Nougayrède JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005; 13: 103-110 [PMID: 15737728 DOI: 10.1016/j.tim.2005.01.002]
41. Collins D, Hogan AM, Winter DC. Microbial and viral pathogens in colorectal cancer. Lancet Oncol 2011; 12: 504-512 [PMID: 21067973 DOI: 10.1016/S1470-2045(10)70186-8]
42. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, Elion J, Denamur E. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 1999; 67: 546-553 [PMID: 9916057]
43. Nowrouzian FL, Adlerberth I, Wold AE. Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells. Microbes Infect 2006; 8: 834-840 [PMID: 16483819 DOI: 10.1016/j.micinf.2005.10.011]
44. Ilantzis C, DeMarte L, Screaton RA, Stanners CP. Deregulated expression of the human tumor marker CEA and CEA family member CEACAM6 disrupts tissue architecture and blocks colonocyte differentiation. Neoplasia 2002; 4: 151-163 [PMID: 11896570 DOI: 10.1038/sj/neo/7900201]
45. Bos MP, Grunert F, Belland RJ. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect Immun 1997; 65: 2353-2361 [PMID: 9169774]
46. Guignot J, Hudault S, Kansau I, Chau I, Servin AL. Human decay-accelerating factor and CEACAM receptor-mediated internalization and intracellular lifestyle of Afa/Dr diffusely adhering Escherichia coli in epithelial cells. Infect Immun 2009; 77: 517-531 [PMID: 19015254 DOI: 10.1128/ IAI.00695-08]
47. Wu S, Morin PJ, Maouyo D, Sears CL. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 2003; 124: 392-400 [PMID: 12557145 DOI: 10.1053/gast.2003.50047]
48. Chochi K, Ichikura T, Kinoshita M, Majima T, Shinomiya N, Tsujimoto H, Kawabata T, Sugasawa H, Ono S, Seki S, Mochizuki H. Helicobacter pylori augments growth of gastric cancers via the lipopolysaccharide-toll-like receptor 4 pathway whereas its lipopolysaccharide attenuates antitumor activities of human mononuclear cells. Clin Cancer Res 2008; 14: 2909-2917 [PMID: 18483357 DOI: 10.1158/1078-0432. CCR-07-4467]
49. Le Bouguénec C, Lalioui L, du Merle L, Jouve M, Courcoux P, Bouzari S, Selvarangan R, Nowicki BJ, Germani Y, Andremont A, Gounon P, Garcia MI. Characterization of AfaE adhesins produced by extraintestinal and intestinal human Escherichia coli isolates: PCR assays for detection of Afa adhesins that do or do not recognize Dr blood group antigens. J Clin Microbiol 2001; 39: 1738-1745 [PMID: 11325983 DOI: 10.1128/JCM.39.5.1738-1745.2001]
50. Bernier C, Gounon P, Le Bouguénec C. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun 2002; 70: 4302-4311 [PMID: 12117939]
51. Dubois D, Delmas J, Cady A, Robin F, Sivignon A, Oswald E, Bonnet R. Cyclomodulins in urosepsis strains of Escherichia coli. J Clin Microbiol 2010; 48: 2122-2129 [PMID: 20375237 DOI: 10.1128/JCM.02365-09]