Escherichia coli isolates from inflammatory bowel diseases patients survive in macrophages and activate NLRP3 inflammasome

International Journal of Medical Microbiology

Volumn 304, Issue 3-4, 2014, Pages 384-392

  De la Fuente, Marjorie ^a   Franchi, Luigi ^b   Araya, Daniela ^a   Díaz Jiménez, David ^a   Olivares, Mauricio ^a   Álvarez Lobos, Manuel ^c   Golenbock, Douglas ^d   González, María Julieta ^a   López Kostner, Francisco ^e   Quera, Rodrigo ^e   Núñez, Gabriel ^b   Vidal, Roberto ^a   Hermoso, Marcela A ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e CLÍNICA LAS CONDES   (Chile)

Author keywords

Crohn's disease; E. coli; IL 1 ; Inflammasome; NLRP3

Indexed keywords

CD1 ANTIGEN; CD2 ANTIGEN; CD6 ANTIGEN; CD9 ANTIGEN; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR; CARRIER PROTEIN; NLRP3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; COLONY FORMING UNIT; CONTROLLED STUDY; CROHN DISEASE; DISEASE ACTIVITY; ESCHERICHIA COLI; GENE IDENTIFICATION; HUMAN; IMMUNE RESPONSE; IMMUNOBLOTTING; MACROPHAGE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS; ULCERATIVE COLITIS; ADOLESCENT; ADULT; AGED; ANIMAL; BACTERIAL LOAD; BIOPSY; CELL LINE; CYTOSOL; EPITHELIUM CELL; FEMALE; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; ILEUM; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BACTERIAL LOAD; BIOPSY; CARRIER PROTEINS; CELL LINE; CYTOSOL; EPITHELIAL CELLS; ESCHERICHIA COLI; FEMALE; GENOTYPE; HOST-PATHOGEN INTERACTIONS; HUMANS; ILEUM; INFLAMMASOMES; INFLAMMATORY BOWEL DISEASES; MACROPHAGES; MALE; MICE; MICROBIAL VIABILITY; MIDDLE AGED; VIRULENCE FACTORS; YOUNG ADULT;

EID: 84899639501     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.01.002     Document Type: Article

References (53)

1. Abraham C., Cho J.H. Inflammatory bowel disease. New England Journal of Medicine 2009, 361:2066-2078.
2. Barnich N., Carvalho F.A., Glasser A., Darcha C., Jantscheff P., Allez M., Peeters H., Bommelaer G., Desreumaux P., Colombel J., Darfeuille-Michaud A. CEACAM6 acts as a receptor for mucosa colonization in Crohn disease. Journal of Clinical Investigation 2007, 117:1566-1574.
3. Blanco M., Blanco J.E., Alonso M.P., Mora A., Balsalobre C., Muñoa F., Juárez A., Blanco J. Detection of pap, sfa and afa adhesin-encoding operons in uropathogenic Escherichia coli strains: relationship with expression of adhesins and production of toxins. Research in Microbiology 1997, 148:745-755.
4. Boudeau J., Glasser A.L., 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. Infection and Immunity 1999, 67:4499-4509.
5. Boyer H.W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. Journal of Molecular Biology 1969, 41:459-472.
6. Brereton C.F., Sutton C.E., Ross P.J., Iwakura Y., Pizza M., Rappuoli R., Lavelle E.C., Mills K.H.G. Escherichia coli heat-labile enterotoxin promotes protective Th17 responses against infection by driving innate IL-1 and IL-23 production. Journal of Immunology 2011, 186:5896-5906.
7. Carvalho F.A., Barnich N., Sivignon A., Darcha C., Chan C.H.F., Stanners C.P., Darfeuille-Michaud A. Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. Journal of Experimental Medicine 2009, 206:2179-2189.
8. Céspedes S., Salgado P., Valenzuela P., Vidal R., Oñate A.A. Characterization of genomic island 3 and genetic variability of Chilean field strains of Brucella abortus. Journal of Clinical Microbiology 2011, 49:2461-2469.
9. Chassaing B., Rolhion N., De Vallée A., Salim S.Y., Prorok-Hamon M., Neut C., Campbell B.J., Söderholm J.D., Hugot J., Colombel J.-F., Darfeuille-Michaud A. Crohn disease-associated adherent-invasive E. coli bacteria target mouse and human Peyer's patches via long polar fimbriae. Journal of Clinical Investigation 2011, 121:966-975.
10. Clarke D.J., Chaudhuri R.R., Martin H.M., Campbell B.J., Rhodes J.M., Constantinidou C., Pallen M.J., Loman N.J., Cunningham A.F., Browning D.F., Henderson I.R. Complete genome sequence of the Crohn's disease-associated adherent-invasive Escherichia coli strain HM605. Journal of Bacteriology 2011, 193:4540.
11. Clermont O., Bonacorsi S., Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology 2000, 66:4555-4558.
12. Cosnes J., Gower-Rousseau C., Seksik P., Cortot A. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology 2011, 140. 1785-1794.e4.
13. Darfeuille-Michaud A., Boudeau J., Bulois P., Neut C., Glasser A.-L., Barnich N., Bringer M.-A., Swidsinski A., Beaugerie L., Colombel J.-F. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 2004, 127:412-421.
14. Davies J.Q., Gordon S. Isolation and culture of murine macrophages. Methods in Molecular Biology (Clifton, NJ) 2005, 290:91-103.
15. Del Canto F., Botkin D.J., Valenzuela P., Popov V., Ruiz-Perez F., Nataro J.P., Levine M.M., Stine O.C., Pop M., Torres A.G., Vidal R. Identification of Coli Surface Antigen 23, a novel adhesin of enterotoxigenic Escherichia coli. Infection and Immunity 2012, 80:2791-2801.
16. Eaves-Pyles T., Allen C.A., Taormina J., Swidsinski A., Tutt C.B., Jezek G.E., Islas-Islas M., Torres A.G. Escherichia coli isolated from a Crohn's disease patient adheres, invades, and induces inflammatory responses in polarized intestinal epithelial cells. International Journal of Medical Microbiology: IJMM 2008, 298:397-409.
17. Elliott T.R., Hudspith B.N., Wu G., Cooley M., Parkes G., Quiñones B., Randall L., Mandrell R.E., Fagerquist C.K., Brostoff J., Rayment N.B., Boussioutas A., Petrovska L., Sanderson J.D. Quantification and Characterization of mucosa-associated and intracellular Escherichia coli in inflammatory bowel disease. Inflammatory Bowel Diseases 2013, 19:2326-2338.
18. Ewers C., Li G., Wilking H., Kiessling S., Alt K., Antáo E.-M., Laturnus C., Diehl I., Glodde S., Homeier T., Böhnke U., Steinrück H., Philipp H.-C., Wieler L.H. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?. International Journal of Medical Microbiology: IJMM 2007, 297:163-176.
19. Figueroa C., Quera P.R., Valenzuela E.J., Jensen B.C. Inflammatory bowel disease: experience of two Chilean centers. Revista médica de Chile 2005, 133:1295-1304.
20. Franchi L., Muñoz-Planillo R., Núñez G. Sensing and reacting to microbes through the inflammasomes. Nature Immunology 2012, 13:325-332.
21. Glasser A.L., Boudeau J., Barnich N., Perruchot M.H., Colombel J.F., Darfeuille-Michaud A. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death. Infection and Immunity 2001, 69:5529-5537.
22. Guinée P.A., Agterberg C.M., Jansen W.H. Escherichia coli O antigen typing by means of a mechanized microtechnique. Applied Microbiology 1972, 24:127-131.
23. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nature Immunology 2008, 9:857-865.
24. Hansen R., Thomson J.M., El-Omar E.M., Hold G.L. The role of infection in the aetiology of inflammatory bowel disease. Journal of Gastroenterology 2010, 45:266-276.
25. Johnson J.R., Stell L.A. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. Journal of Infectious Diseases 2000, 181:261-272.
26. Kanneganti T.-D., Ozören N., Body-Malapel M., Amer A., Park J.-H., Franchi L., Whitfield J., Barchet W., Colonna M., Vandenabeele P., Bertin J., Coyle A., Grant E.P., Akira S., Núñez G. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 2006, 440:233-236.
27. Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nature Reviews. Microbiology 2004, 2:123-140.
28. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annual Review of Immunology 2010, 28:573-621.
29. Levine M.M., Bergquist E.J., Nalin D.R., Waterman D.H., Hornick R.B., Young C.R., Sotman S. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1978, 1:1119-1122.
30. Louis E., Collard A., Oger A.F., Degroote E., Aboul Nasr El Yafi F.A., Belaiche J. Behaviour of Crohn's disease according to the Vienna classification: changing pattern over the course of the disease. Gut 2001, 49:777-782.
31. Marks D.J.B., Harbord M.W.N., MacAllister R., Rahman F.Z., Young J., Al-Lazikani B., Lees W., Novelli M., Bloom S., Segal A.W. Defective acute inflammation in Crohn's disease: a clinical investigation. Lancet 2006, 367:668-678.
32. Martinez-Medina M., Mora A., Blanco M., López C., Alonso M.P., Bonacorsi S., Nicolas-Chanoine M.-H., Darfeuille-Michaud A., Garcia-Gil J., Blanco J. Similarity and divergence among adherent-invasive Escherichia coli and extraintestinal pathogenic E. coli strains. Journal of Clinical Microbiology 2009, 47:3968-3979.
33. Martinez-Medina M., Aldeguer X., Lopez-Siles M., González-Huix F., López-Oliu C., Dahbi G., Blanco J.E., Blanco J., Garcia-Gil L.J., Darfeuille-Michaud A. Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflammatory Bowel Diseases 2009, 15:872-882.
34. Miquel S., Peyretaillade E., Claret L., De Vallée A., Dossat C., Vacherie B., Zineb E.H., Segurens B., Barbe V., Sauvanet P., Neut C., Colombel J.-F., Medigue C., Mojica F.J.M., Peyret P., Bonnet R., Darfeuille-Michaud A. Complete genome sequence of Crohn's disease-associated adherent-invasive E. coli strain LF82. PLoS ONE 2010, 5. pii: e12714.
35. Moráin C.O., Segal A.A., Walker D., Levi A.J. Abnormalities of neutrophil function do not cause the migration defect in Crohn's disease. Gut 1981, 22:817-822.
36. Moulin-Schouleur M., Schouler C., Tailliez P., Kao M.-R., Brée A., Germon P., Oswald E., Mainil J., Blanco M., Blanco J. Common virulence factors and genetic relationships between O18:K1:H7 Escherichia coli isolates of human and avian origin. Journal of Clinical Microbiology 2006, 44:3484-3492.
37. Nash J.H.E., Villegas A., Kropinski A.M., Aguilar-Valenzuela R., Konczy P., Mascarenhas M., Ziebell K., Torres A.G., Karmali M.A., Coombes B.K. Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes. BMC Genomics 2010, 11:667.
38. Odze R. Diagnostic problems and advances in inflammatory bowel disease. Modern Pathology 2003, 16:347-358.
39. Ozören N., Masumoto J., Franchi L., Kanneganti T.-D., Body-Malapel M., Ertuk I., Jagirdar R., Zhu L., Inohara N., Bertin J., Coyle A., Grant E.P., Nuñez G. Distinct roles of TLR2 and the adaptor ASC in IL-1/IL-18 secretion in response to listeria monocytogenes. Journal of Immunology 2006, 176:4337-4342.
40. Peeters H., Bogaert S., Laukens D., Rottiers P., De Keyser F., Darfeuille-Michaud A., Glasser A.-L., Elewaut D., De Vos M. CARD15 variants determine a disturbed early response of monocytes to adherent-invasive Escherichia coli strain LF82 in Crohn's disease. International Journal of Immunogenetics 2007, 34:181-191.
41. Pereira M.S.F., Morgantetti G.F., Massis L.M., Horta C.V., Hori J.I., Zamboni D.S. Activation of NLRC4 by flagellated bacteria triggers caspase-1-dependent and -independent responses to restrict Legionella pneumophila replication in macrophages and in vivo. Journal of Immunology (Baltimore, Md. 1950) 2011, 187:6447-6455.
42. Saldaña Z., Erdem A.L., Schüller S., Okeke I.N., Lucas M., Sivananthan A., Phillips A.D., Kaper J.B., Puente J.L., Girón J.A. The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. Journal of Bacteriology 2009, 191:3451-3461.
43. Sander L.E., Davis M.J., Boekschoten M.V., Amsen D., Dascher C.C., Ryffel B., Swanson J.A., Müller M., Blander J.M. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011, 474:385-389.
44. Sasaki M., Sitaraman S.V., Babbin B.A., Gerner-Smidt P., Ribot E.M., Garrett N., Alpern J.A., Akyildiz A., Theiss A.L., Nusrat A., Klapproth J.-M.A. Invasive Escherichia coli are a feature of Crohn's disease. Laboratory Investigation 2007, 87:1042-1054.
45. Shen X., Shi R., Zhang H., Li K., Zhao Y., Zhang R. The Toll-like receptor 4 D299G and T399I polymorphisms are associated with Crohn's disease and ulcerative colitis: a meta-analysis. Digestion 2010, 81:69-77.
46. Shih D.Q., Targan S.R. Immunopathogenesis of inflammatory bowel disease. World Journal of Gastroenterology: WJG 2008, 14:390-400.
47. Sokolovska A., Becker C.E., Ip W.K.E., Rathinam V.A.K., Brudner M., Paquette N., Tanne A., Vanaja S.K., Moore K.J., Fitzgerald K.A., Lacy-Hulbert A., Stuart L.M. Activation of caspase-1 by the NLRP3 inflammasome regulates the NADPH oxidase NOX2 to control phagosome function. Nature Immunology 2013, 14:543-553.
48. Strate L.L., Modi R., Cohen E., Spiegel B.M.R. Diverticular disease as a chronic illness: evolving epidemiologic and clinical insights. American Journal of Gastroenterology 2012, 107:1486-1493.
49. Strober W., Fuss I.J. Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology 2011, 140:1756-1767.
50. Tiba M.R., Yano T., Leite D.D.S. Genotypic characterization of virulence factors in Escherichia coli strains from patients with cystitis. Revista do Instituto de Medicina Tropical de São Paulo 2008, 50:255-260.
51. Vidal M., Kruger E., Durán C., Lagos R., Levine M., Prado V., Toro C., Vidal R. Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. Journal of Clinical Microbiology 2005, 43:5362-5365.
52. Villani A.-C., Lemire M., Fortin G., Louis E., Silverberg M.S., Collette C., Baba N., Libioulle C., Belaiche J., Bitton A., Gaudet D., Cohen A., Langelier D., Fortin P.R., Wither J.E., Sarfati M., Rutgeerts P., Rioux J.D., Vermeire S., Hudson T.J., Franchimont D. Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nature Genetics 2009, 41:71-76.
53. Walker A.W., Sanderson J.D., Churcher C., Parkes G.C., Hudspith B.N., Rayment N., Brostoff J., Parkhill J., Dougan G., Petrovska L. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiology 2011, 11:7.