A pathobiont of the microbiota balances host colonization and intestinal inflammation

Cell Host and Microbe

Volumn 7, Issue 4, 2010, Pages 265-276

  Chow, Janet ^a   Mazmanian, Sarkis K ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; BACTERIAL DNA; BACTERIAL PROTEIN; MEMBRANE PROTEIN;

ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENTERITIS; GENE EXPRESSION; HELICOBACTER HEPATICUS; INTESTINE EPITHELIUM; MICROFLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BACTERIAL COUNT; BIOLOGICAL MODEL; BIOSYNTHESIS; C3H MOUSE; C57BL MOUSE; CHEMISTRY; DNA SEQUENCE; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; MACROMOLECULE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); HELICOBACTER HEPATICUS; MAMMALIA; MUS; NEGIBACTERIA;

ANIMALS; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; HELICOBACTER HEPATICUS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERLEUKIN-17; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 77954607064     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.03.004     Document Type: Article

References (44)

1. Bingle, L. E., Bailey, CM., and Pallen, M. J. (2008). Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11, 3-8.
2. Bladergroen, M. R., Badelt, K., and Spaink, HP. (2003). Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol. Plant Microbe Interact. 16, 53-64.
3. Bland, P. W., and Warren, LG. (1986). Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-la antisera. Immunology 58, 1-7.
4. Bohr, U. R., Glasbrenner, B., Primus, A., Zagoura, A., Wex, T., and Malfertheiner, P. (2004). Identification of enterohepatic Helicobacter species in patients suffering from inflammatory bowel disease. J. Clin. Microbiol. 42, 2766-2768.
5. Das, S., Chakrabortty, A., Banerjee, R., and Chaudhuri, K. (2002). Involvement of in vivo induced icmF gene of Vibrio cholerae in motility, adherence to epithelial cells, and conjugation frequency. Biochem. Biophys. Res. Commun. 295, 922-928.
6. Dudley, E. G., Thomson, N. R., Parkhill, J., Morin, N. P., and Nataro, J. P. (2006). Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol. Microbiol. 61, 1267-1282.
7. Duerr, R. H., Taylor, K. D., Brant, S. R., Rioux, J. D., Silverberg, M. S., Daly, M. J., Steinhart, A. H., Abraham, C., Regueiro, M., Griffiths, A., et al. (2006). A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314, 1461-1463.
8. Erdman, S. E., Rao, V. P., Poutahidis, T., Rogers, A. B., Taylor, C. L., Jackson, E. A., Ge, Z., Lee, C. W., Schauer, D. B., Wogan, G. N., et al. (2009). Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc. Natl. Acad. Sci. USA 106, 1027-1032.
9. Flores, B. M., Fennell, C. L., Kuller, L., Bronsdon, M. A., Morton, W. R., and Stamm, W. E. (1990). Experimental infection of pig-tailed macaques (Macaca nemestrina) with Campylobacter cinaedi and Campylobacter fennelliae. Infect. Immun. 58, 3947-3953.
10. Fox, J. G., Chien, C. C., Dewhirst, F. E., Paster, B. J., Shen, Z., Melito, P. L., Woodward, D. L., and Rodgers, F. G. (2000). Helicobacter canadensis sp. nov. isolated from humans with diarrhea as an example of an emerging pathogen. J. Clin. Microbiol. 38, 2546-2549.
11. Frank, D. N., St Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., and Pace, N. R. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104, 13780-13785.
12. Galan, J. E., and Wolf-Watz, H. (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567-573.
13. Ge, Z., Sterzenbach, T., Whary, M. T., Rickman, B. H., Rogers, A. B., Shen, Z., Taylor, N. S., Schauer, D. B., Josenhans, C., Suerbaum, S., et al. (2008). Helicobacter hepaticus HHGI1 is a pathogenicity island associated with typhlocolitis in B6.129-IL10 tmlCgn mice. Microbes Infect. 10, 726-733.
14. Hampe, J., Cuthbert, A., Croucher, P. J., Mirza, M. M., Mascheretti, S., Fisher, S., Frenzel, H., King, K., Hasselmeyer, A., MacPherson, A. J., et al. (2001). Association between insertion mutation in NOD2 gene and Crohn's disease in German and British populations. Lancet 357, 1925-1928.
15. Hampe, J., Franke, A., Rosenstiel, P., Till, A., Teuber, M., Huse, K., Albrecht, M., Mayr, G., De La Vega, F. M., Briggs, J., et al. (2007). A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39, 207-211. (Pubitemid 46184351)
16. Hooper, L. V., and Gordon, J. I. (2001). Commensal host-bacterial relationships in the gut. Science 292, 1115-1118.
17. Hue, S., Ahern, P., Buonocore, S., Kullberg, M. C., Cua, D. J., McKenzie, B. S., Powrie, F., and Maloy, K. J. (2006). Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
18. Kinross, J. M., von Roon, A. C., Holmes, E., Darzi, A., and Nicholson, J. K. (2008). The human gut microbiome: implications for future health care. Curr. Gastroenterol. Rep. 10, 396-403.
19. Kullberg, M. C., Rothfuchs, A. G., Jankovic, D., Caspar, P., Wynn, T. A., Gorelick, P. L., Cheever, A. W., and Sher, A. (2001). Helicobacter hepaticusinduced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation. Infect. Immun. 69, 4232-4241.
20. Kullberg, M. C., Jankovic, D., Gorelick, P. L., Caspar, P., Letterio, J. J., Cheever, A. W., and Sher, A. (2002). Bacteria-triggered CD4 (+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196, 505-515.
21. Laharie, D., Asencio, C., Asselineau, J., Bulois, P., Bourreille, A., Moreau, J., Bonjean, P., Lamarque, D., Pariente, A., Soule, J. C., et al. (2009). Association between entero-hepatic Helicobacter species and Crohn's disease: a prospective cross-sectional study. Aliment. Pharmacol. Ther. 30, 283-293.
22. Ley, R. E., Peterson, D. A., and Gordon, J. I. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848.
23. Ma, AT., McAuley, S., Pukatzki, S., and Mekalanos, J. J. (2009). Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5, 234-243.
24. Mayer, L., Eisenhardt, D., Salomon, P., Bauer, W., Pious, R., and Piccinini, L. (1991). Expression of class II molecules on intestinal epithelial cells in humans. Differences between normal and inflammatory bowel disease. Gastroenterology 100, 3-12.
25. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., and Kasper, D. L. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107-118.
26. Mazmanian, S. K., Round, J. L., and Kasper, D. L. (2008). A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625.
27. Mehta, N. S., Benoit, S. L., Mysore, J., and Maier, R. J. (2007). In vitro and in vivo characterization of alkyl hydroperoxide reductase mutant strains of Helicobacter hepaticus. Biochim. Biophys. Acta 1770, 257-265.
28. Mougous, J. D., Cuff, M. E., Raunser, S., Shen, A., Zhou, M., Gifford, C. A., Goodman, A. L., Joachimiak, G., Ordonez, C. L., Lory, S., et al. (2006). A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530.
29. Nanda Kumar, N. S., Balamurugan, R., Jayakanthan, K., Pulimood, A., Pugazhendhi, S., and Ramakrishna, B. S. (2008). Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J. Gastroenterol. Hepatol. 23, 1834-1839.
30. O'Hara, A. M., and Shanahan, F. (2006). The gut flora as a forgotten organ. EMBO Rep. 7, 688-693.
31. Packey, C. D., and Sartor, R. B. (2009). Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr. Opin. Infect. Dis. 22, 292-301.
32. Parsons, D. A., and Heffron, F. (2005). sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect. Immun. 73, 4338-4345.
33. Penders, J., Stobberingh, E. E., van den Brandt, P. A., and Thijs, C. (2007). The role of the intestinal microbiota in the development of atopic disorders. Allergy 62, 1223-1236.
34. Pukatzki, S., Ma, AT., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., Heidelberg, J. F., and Mekalanos, J. J. (2006). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103, 1528-1533.
35. Raskin, D. M., Seshadri, R., Pukatzki, S. U., and Mekalanos, J. J. (2006). Bacterial genomics and pathogen evolution. Cell 124, 703-714.
36. Round, J. L., and Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323.
37. Scanlan, P. D., Shanahan, F., O'Mahony, C., and Marchesi, J. R. (2006). Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease. J. Clin. Microbiol. 44, 3980-3988.
38. Solnick, J. V., and Schauer, D. B. (2001). Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin. Microbiol. Rev. 14, 59-97.
39. Sterzenbach, T., Lee, S. K., Brenneke, B., von Goetz, F., Schauer, D. B., Fox, J. G., Suerbaum, S., and Josenhans, C. (2007). Inhibitory effect of enterohepatic Helicobacter hepaticus on innate immune responses of mouse intestinal epithelial cells. Infect. Immun. 75, 2717-2728.
40. Suarez, G., Sierra, J. C., Sha, J., Wang, S., Erova, T. E., Fadl, A. A., Foltz, S. M., Horneman, A. J., and Chopra, A. K. (2008). Molecular characterization of afunctional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 44, 344-361.
41. Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., Droge, M., Fartmann, B., Fischer, H. P., Ge, Z., et al. (2003). The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. USA 100, 7901-7906.
42. Vidal, K., Grosjean, I., evillard, J. P., Gespach, C., and Kaiserlian, D. (1993). Immortalization of mouse intestinal epithelial cells by the SV40-large T gene. Phenotypic and immune characterization of the MODE-K cell line. J. Immunol. Methods 166, 63-73.
43. Wen, L., Ley, R. E., Volchkov, P. Y., Stranges, P. B., Avanesyan, L., Stonebraker, A. C., Hu, C., Wong, F. S., Szot, G. L., Bluestone, J. A., et al. (2008). Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455, 1109-1113.
44. Westendorf, A. M., Fleissner, D., Groebe, L., Jung, S., Gruber, A. D., Hansen, W., and Buer, J. (2009). CD4+Foxp3+ regulatory T cell expansion induced by antigen-driven interaction with intestinal epithelial cells independent of local dendritic cells. Gut 58, 211-219.