Intestinal epithelial cell toll-like receptor 5 regulates the intestinal microbiota to prevent low-grade inflammation and metabolic syndrome in mice

Gastroenterology

Volumn 147, Issue 6, 2014, Pages 1363-1377.e17

  Chassaing, Benoit ^a   Ley, Ruth E ^b   Gewirtz, Andrew T ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

IBD; Intestine; LPS; Mouse Model

Indexed keywords

AMPICILLIN; BACTERIUM LIPOPOLYSACCHARIDE; CRE RECOMBINASE; DEXTRAN SULFATE; FLAGELLIN; GLUCOSE; GLYCOPROTEIN P 15095; INTERLEUKIN 22; NEOMYCIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; VILLIN; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL HOUSING; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREEDING; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE MODEL; FEMALE; GENOTYPE; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LIPID DIET; LOXP SITE; MALE; METABOLIC SYNDROME X; MOUSE; MOUSE MODEL; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIBLING; SPLENOMEGALY; WEANING; ANIMAL; C57BL MOUSE; CYTOLOGY; ENTERITIS; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MICROFLORA; SIGNAL TRANSDUCTION;

ANIMALS; COLITIS; DIET, HIGH-FAT; ENTERITIS; FEMALE; FLAGELLIN; INTESTINAL MUCOSA; MALE; METABOLIC SYNDROME X; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5;

EID: 84913554895     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.08.033     Document Type: Article

References (52)

1. A. Kaser, S. Zeissig, and R.S. Blumberg Inflammatory bowel disease Annu Rev Immunol 28 2010 573 621
2. B. Chassaing, and A. Darfeuille-Michaud The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases Gastroenterology 140 2011 1720 1728
3. F.A. Carvalho, O. Koren, and J.K. Goodrich Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice Cell Host Microbe 12 2012 139 152
4. M. Vijay-Kumar, J.D. Aitken, and F.A. Carvalho Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
5. M. Vijay-Kumar, C.J. Sanders, and R.T. Taylor Deletion of TLR5 results in spontaneous colitis in mice J Clin Invest 117 2007 3909 3921
6. A.M. Caricilli, P.K. Picardi, and L.L. de Abreu Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice PLoS Biol 9 2011 e1001212
7. E. Elinav, T. Strowig, and A.L. Kau NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis Cell 145 2011 745 757
8. C. Ubeda, L. Lipuma, and A. Gobourne Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice J Exp Med 209 2012 1445 1456
9. A.T. Gewirtz, T.A. Navas, and S. Lyons Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression J Immunol 167 2001 1882 1885
10. M.E. Hobert, K.A. Sands, and R.J. Mrsny Cdc42 and Rac1 regulate late events in Salmonella typhimurium-induced interleukin-8 secretion from polarized epithelial cells J Biol Chem 277 2002 51025 51032
11. C.J. Sanders, D.A. Moore III, and I.R. Williams Both radioresistant and hemopoietic cells promote innate and adaptive immune responses to flagellin J Immunol 180 2008 7184 7192
12. M.A. Kinnebrew, C.G. Buffie, and G.E. Diehl Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense Immunity 36 2012 276 287
13. L. Van Maele, C. Carnoy, and D. Cayet TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa J Immunol 185 2010 1177 1185
14. S. Uematsu, M.H. Jang, and N. Chevrier Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells Nat Immunol 7 2006 868 874
15. B. Chassaing, G. Srinivasan, and M.A. Delgado Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation PLoS One 7 2012 e44328
16. M.E. Johansson, M. Phillipson, and J. Petersson The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria Proc Natl Acad Sci U S A 105 2008 15064 15069
17. B. Chassaing, O. Koren, and F.A. Carvalho AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition Gut 63 2014 1069 1080
18. C.W. Png, S.K. Linden, and K.S. Gilshenan Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria Am J Gastroenterol 105 2010 2420 2428
19. M. Joossens, G. Huys, and M. Cnockaert Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives Gut 60 2011 631 637
20. K. Lucke, S. Miehlke, and E. Jacobs Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis J Med Microbiol 55 2006 617 624
21. N. Kim, J. Kunisawa, and M.N. Kweon Oral feeding of Bifidobacterium bifidum (BGN4) prevents CD4(+) CD45RB(high) T cell-mediated inflammatory bowel disease by inhibition of disordered T cell activation Clin Immunol 123 2007 30 39
22. F. Rowan, N.G. Docherty, and M. Murphy Desulfovibrio bacterial species are increased in ulcerative colitis Dis Colon Rectum 53 2010 1530 1536
23. M. Bhatia Role of hydrogen sulfide in the pathology of inflammation Scientifica (Cairo) 2012 2012 159680
24. T.W. Miller, E.A. Wang, and S. Gould Hydrogen sulfide is an endogenous potentiator of T cell activation J Biol Chem 287 2012 4211 4221
25. F.A. Carvalho, J.D. Aitken, and M. Vijay-Kumar Toll-like receptor-gut microbiota interactions: perturb at your own risk! Annu Rev Physiol 74 2012 177 198
26. T.C. Cullender, B. Chassaing, and A. Janzon Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut Cell Host Microbe 14 2013 571 581
27. A.T. Gewirtz, M. Vijay-Kumar, and S.R. Brant Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease Am J Physiol Gastrointest Liver Physiol 290 2006 G1157 G1163
28. F.A. Carvalho, I. Nalbantoglu, and J.D. Aitken Cytosolic flagellin receptor NLRC4 protects mice against mucosal and systemic challenges Mucosal Immunol 5 2012 288 298
29. F.A. Carvalho, I. Nalbantoglu, and S. Ortega-Fernandez Interleukin-1beta (IL-1beta) promotes susceptibility of Toll-like receptor 5 (TLR5) deficient mice to colitis Gut 61 2012 373 384
30. S. Uematsu, M.H. Jang, and N. Chevrier Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells Nat Immunol 7 2006 868 874
31. M. Vijay-Kumar, J.D. Aitken, and F.A. Carvalho Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
32. H. Karsunky, M. Merad, and A. Cozzio Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo J Exp Med 198 2003 305 313
33. B. Chassaing, J.D. Aitken, and M. Malleshappa Dextran sulfate sodium (DSS)-induced colitis in mice Curr Protoc Immunol 104 2014 Unit 15.25
34. M.E. Johansson, and G.C. Hansson Preservation of mucus in histological sections, immunostaining of mucins in fixed tissue, and localization of bacteria with FISH Methods Mol Biol 842 2012 229 235
35. F.E. Castaneda, B. Walia, and M. Vijay-Kumar Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP Gastroenterology 129 2005 1991 2008
36. B. Chassaing, G. Srinivasan, and M.A. Delgado Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation PLoS One 7 2012 e44328
37. F.A. Carvalho, I. Nalbantoglu, and J.D. Aitken Cytosolic flagellin receptor NLRC4 protects mice against mucosal and systemic challenges Mucosal Immunol 5 2012 288 298
38. B. Chassaing, O. Koren, and F.A. Carvalho AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition Gut 63 2014 1069 1080
39. A. Darfeuille-Michaud, J. Boudeau, and P. Bulois High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease Gastroenterology 127 2004 412 421
40. A. Darfeuille-Michaud, C. Neut, and N. Barnich Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease Gastroenterology 115 1998 1405 1413
41. F.A. Carvalho, O. Koren, and J.K. Goodrich Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice Cell Host Microbe 12 2012 139 152
42. F.A. Carvalho, N. Barnich, and A. Sivignon Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM J Exp Med 206 2009 2179 2189
43. J.A. Gilbert, F. Meyer, and J. Jansson The Earth Microbiome Project: meeting report of the "1 EMP meeting on sample selection and acquisition" at Argonne National Laboratory October 6 2010 Stand Genomic Sci 3 2010 249 253
44. J.G. Caporaso, C.L. Lauber, and W.A. Walters Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms ISME J 6 2012 1621 1624
45. J.G. Caporaso, J. Kuczynski, and J. Stombaugh QIIME allows analysis of high-throughput community sequencing data Nat Med 7 2010 335 336
46. R.C. Edgar Search and clustering orders of magnitude faster than BLAST Bioinformatics 26 2010 2460 2461
47. D. McDonald, M.N. Price, and J. Goodrich An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea ISME J 6 2012 610 618
48. M.N. Price, P.S. Dehal, and A.P. Arkin FastTree: computing large minimum evolution trees with profiles instead of a distance matrix Mol Biol Evol 26 2009 1641 1650
49. C. Lozupone, and R. Knight UniFrac: a new phylogenetic method for comparing microbial communities Appl Environ Microbiol 71 2005 8228 8235
50. C. Lozupone, M. Hamady, and R. Knight UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context BMC Bioinformatics 7 2006 371
51. F. Meyer, D. Paarmann, and M. D'Souza The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes BMC Bioinformatics 9 2008 386
52. R. Tibshirani, T. Hastie, and B. Narasimhan Diagnosis of multiple cancer types by shrunken centroids of gene expression Proc Natl Acad Sci U S A 99 2002 6567 6572