NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis

Cell

Volumn 145, Issue 5, 2011, Pages 745-757

  Elinav, Eran ^a   Strowig, Till ^a   Kau, Andrew L ^b   Henao Mejia, Jorge ^a   Thaiss, Christoph A ^a   Booth, Carmen J ^a   Peaper, David R ^a   Bertin, John ^c   Eisenbarth, Stephanie C ^a   Gordon, Jeffrey I ^b   Flavell, Richard A ^a,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GLAXOSMITHKLINE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN; CIPROFLOXACIN; CYTOKINE; DEXTRAN SULFATE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; METRONIDAZOLE; NLRP6 PROTEIN; RANTES; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTEROIDETES; COLITIS; COLON FLORA; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE TRANSMISSION; ELECTRON MICROSCOPY; FECES MICROFLORA; GENE DELETION; INFLAMMATORY CELL; MOLECULAR ECOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; WILD TYPE;

BACTERIA (MICROORGANISMS); BACTEROIDETES; MUS; PREVOTELLACEAE;

EID: 79957576718     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.04.022     Document Type: Article

References (69)

1. L. Agostini, F. Martinon, K. Burns, M.F. McDermott, P.N. Hawkins, and J. Tschopp NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder Immunity 20 2004 319 325 (Pubitemid 38388233)
2. I.C. Allen, E.M. TeKippe, R.M. Woodford, J.M. Uronis, E.K. Holl, A.B. Rogers, H.H. Herfarth, C. Jobin, and J.P. Ting The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer J. Exp. Med. 207 2010 1045 1056
3. J.C. Arthur, J.D. Lich, Z. Ye, I.C. Allen, D. Gris, J.E. Wilson, M. Schneider, K.E. Roney, B.P. O'Connor, and C.B. Moore Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity J. Immunol. 185 2010 4515 4519
4. C. Bauer, P. Duewell, C. Mayer, H.A. Lehr, K.A. Fitzgerald, M. Dauer, J. Tschopp, S. Endres, E. Latz, and M. Schnurr Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome Gut 59 2010 1192 1199
5. C. Becker, M.C., Fantini, and M.F. Neurath High resolution colonoscopy in live mice Nat. Protoc. 1 2006 2900 2904
6. J. Bérubé, C. Bourdon, Y. Yao, and S. Rousseau Distinct intracellular signaling pathways control the synthesis of IL-8 and RANTES in TLR1/TLR2, TLR3 or NOD1 activated human airway epithelial cells Cell. Signal. 21 2009 448 456
7. B. Björkstén The environmental influence on childhood asthma Allergy 54 Suppl 49 1999 17 23 (Pubitemid 29292488)
8. M.A. Breban, M.C. Moreau, C. Fournier, R. Ducluzeau, and M.F. Kahn Influence of the bacterial flora on collagen-induced arthritis in susceptible and resistant strains of rats Clin. Exp. Rheumatol. 11 1993 61 64 (Pubitemid 23050855)
9. M.M. Brinig, P.W. Lepp, C.C. Ouverney, G.C. Armitage, and D.A. Relman Prevalence of bacteria of division TM7 in human subgingival plaque and their association with disease Appl. Environ. Microbiol. 69 2003 1687 1694 (Pubitemid 36314312)
10. J.G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Peña, J.K. Goodrich, and J.I. Gordon QIIME allows analysis of high-throughput community sequencing data Nat. Methods 7 2010 335 336
11. A. Darfeuille-Michaud, J. Boudeau, P. Bulois, C. Neut, A.L. Glasser, N. Barnich, M.A. Bringer, A. Swidsinski, L. Beaugerie, and J.F. Colombel High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease Gastroenterology 127 2004 412 421 (Pubitemid 39091889)
12. J. Dupaul-Chicoine, G. Yeretssian, K. Doiron, K.S. Bergstrom, C.R. McIntire, P.M. LeBlanc, C. Meunier, C. Turbide, P. Gros, and N. Beauchemin Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases Immunity 32 2010 367 378
13. T.B. Geijtenbeek, S.J. van Vliet, A. Engering, B.A. 't Hart, and Y. van Kooyk Self- and nonself-recognition by C-type lectins on dendritic cells Annu. Rev. Immunol. 22 2004 33 54 (Pubitemid 38680417)
14. J.M. Grenier, L. Wang, G.A. Manji, W.J. Huang, A. Al-Garawi, R. Kelly, A. Carlson, S. Merriam, J.M. Lora, and M. Briskin Functional screening of five PYPAF family members identifies PYPAF5 as a novel regulator of NF-kappaB and caspase-1 FEBS Lett. 530 2002 73 78 (Pubitemid 35248189)
15. S.A. Hirota, J. Ng, A. Lueng, M. Khajah, K. Parhar, Y. Li, V. Lam, M.S. Potentier, K. Ng, and M. Bawa NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis Inflamm. Bowel Dis. 2010 10.1002/ibd.21478 in press. Published online September 24, 2010
16. B. Hu, E. Elinav, S. Huber, C.J. Booth, T. Strowig, C. Jin, S.C. Eisenbarth, and R.A. Flavell Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4 Proc. Natl. Acad. Sci. USA 107 2010 21635 21640
17. P. Hugenholtz, G.W. Tyson, R.I. Webb, A.M. Wagner, and L.L. Blackall Investigation of candidate division TM7, a recently recognized major lineage of the domain Bacteria with no known pure-culture representatives Appl. Environ. Microbiol. 67 2001 411 419 (Pubitemid 32044445)
18. C.A. Janeway Jr., and R. Medzhitov Innate immune recognition Annu. Rev. Immunol. 20 2002 197 216 (Pubitemid 34293424)
19. S.L. Kempster, G. Belteki, A.J. Forhead, A.L. Fowden, R.D. Catalano, B.Y. Lam, I. McFarlane, D.S. Charnock-Jones, and G.C. Smith Developmental control of the Nlrp6 inflammasome and a substrate, IL-18, in mammalian intestine Am. J. Physiol. Gastrointest. Liver Physiol. 300 2011 G253 G263
20. B. Kleessen, A.J. Kroesen, H.J. Buhr, and M. Blaut Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls Scand. J. Gastroenterol. 37 2002 1034 1041
21. T. Kuehbacher, A. Rehman, P. Lepage, S. Hellmig, U.R. Fölsch, S. Schreiber, and S.J. Ott Intestinal TM7 bacterial phylogenies in active inflammatory bowel disease J. Med. Microbiol. 57 2008 1569 1576
22. T.A. Kufer, and P.J. Sansonetti NLR functions beyond pathogen recognition Nat. Immunol. 12 2011 121 128
23. P.S. Kumar, A.L. Griffen, J.A. Barton, B.J. Paster, M.L. Moeschberger, and E.J. Leys New bacterial species associated with chronic periodontitis J. Dent. Res. 82 2003 338 344 (Pubitemid 41756823)
24. Y.K. Lee, J.S. Menezes, Y. Umesaki, and S.K. Mazmanian Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. USA 108 Suppl 1 2010 4615 4622
25. C. Lozupone, and R. Knight UniFrac: a new phylogenetic method for comparing microbial communities Appl. Environ. Microbiol. 71 2005 8228 8235 (Pubitemid 41803949)
26. K. Lucke, S. Miehlke, E. Jacobs, and M. Schuppler Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis J. Med. Microbiol. 55 2006 617 624
27. A.J. Macpherson, and T. Uhr Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria Science 303 2004 1662 1665 (Pubitemid 38338323)
28. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol. 25 2004 677 686 (Pubitemid 39457982)
29. Y. Marcy, C. Ouverney, E.M. Bik, T. Lösekann, N. Ivanova, H.G. Martin, E. Szeto, D. Platt, P. Hugenholtz, D.A. Relman, and S.R. Quake Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth Proc. Natl. Acad. Sci. USA 104 2007 11889 11894 (Pubitemid 47185600)
30. F. Martinon, K. Burns, and J. Tschopp The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta Mol. Cell 10 2002 417 426 (Pubitemid 35007355)
31. P. Matzinger Friendly and dangerous signals: is the tissue in control? Nat. Immunol. 8 2007 11 13 (Pubitemid 46242350)
32. S.K. Mazmanian, J.L. Round, and D.L. Kasper A microbial symbiosis factor prevents intestinal inflammatory disease Nature 453 2008 620 625 (Pubitemid 351769307)
33. J.H. Niess, S. Brand, X. Gu, L. Landsman, S. Jung, B.A. McCormick, J.M. Vyas, M. Boes, H.L. Ploegh, and J.G. Fox CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance Science 307 2005 254 258 (Pubitemid 40116240)
34. C.C. Ouverney, G.C. Armitage, and D.A. Relman Single-cell enumeration of an uncultivated TM7 subgroup in the human subgingival crevice Appl. Environ. Microbiol. 69 2003 6294 6298 (Pubitemid 37280358)
35. J. Penders, E.E. Stobberingh, P.A. van den Brandt, and C. Thijs The role of the intestinal microbiota in the development of atopic disorders Allergy 62 2007 1223 1236 (Pubitemid 47537504)
36. J. Qin, R. Li, J. Raes, M. Arumugam, K.S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada MetaHIT Consortium A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 2010 59 65
37. S. Rakoff-Nahoum, J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis Cell 118 2004 229 241 (Pubitemid 38962578)
38. M. Rescigno, M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J.P. Kraehenbuhl, and P. Ricciardi-Castagnoli Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria Nat. Immunol. 2 2001 361 367 (Pubitemid 33706348)
39. K. Schroder, and J. Tschopp The inflammasomes Cell 140 2010 821 832
40. B. Siegmund Interleukin-18 in intestinal inflammation: friend and foe? Immunity 32 2010 300 302
41. B. Siegmund, H.A. Lehr, G. Fantuzzi, and C.A. Dinarello IL-1 beta -converting enzyme (caspase-1) in intestinal inflammation Proc. Natl. Acad. Sci. USA 98 2001 13249 13254 (Pubitemid 33051348)
42. Z. Sinkorová, J. Capková, J. Niederlová, R. Stepánková, and J. Sinkora Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice Hum. Immunol. 69 2008 845 850
43. H. Sokol, B. Pigneur, L. Watterlot, O. Lakhdari, L.G. Bermúdez-Humarán, J.J. Gratadoux, S. Blugeon, C. Bridonneau, J.P. Furet, and G. Corthier Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients Proc. Natl. Acad. Sci. USA 105 2008 16731 16736
44. K. Suzuki, B. Meek, Y. Doi, M. Muramatsu, T. Chiba, T. Honjo, and S. Fagarasan Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut Proc. Natl. Acad. USA 101 2004 1981 1986 (Pubitemid 38229001)
45. H.H. Tsai, A.D. Dwarakanath, C.A. Hart, J.D. Milton, and J.M. Rhodes Increased faecal mucin sulphatase activity in ulcerative colitis: a potential target for treatment Gut 36 1995 570 576
46. P.J. Turnbaugh, M. Hamady, T. Yatsunenko, B.L. Cantarel, A. Duncan, R.E. Ley, M.L. Sogin, W.J. Jones, B.A. Roe, and J.P. Affourtit A core gut microbiome in obese and lean twins Nature 457 2009 480 484
47. J. Vaahtovuo, E. Munukka, M. Korkeamäki, R. Luukkainen, and P. Toivanen Fecal microbiota in early rheumatoid arthritis J. Rheumatol. 35 2008 1500 1505
48. S. Vaishnava, C.L. Behrendt, A.S. Ismail, L. Eckmann, and L.V. Hooper Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface Proc. Natl. Acad. Sci. USA 105 2008 20858 20863
49. L. Wang, G.A. Manji, J.M. Grenier, A. Al-Garawi, S. Merriam, J.M. Lora, B.J. Geddes, M. Briskin, P.S. DiStefano, and J. Bertin PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing J. Biol. Chem. 277 2002 29874 29880
50. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, A.C. Stonebraker, C. Hu, F.S. Wong, G.L. Szot, and J.A. Bluestone Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
51. C. Werts, L. le Bourhis, J. Liu, J.G. Magalhaes, L.A. Carneiro, J.H. Fritz, S. Stockinger, V. Balloy, M. Chignard, and T. Decker Nod1 and Nod2 induce CCL5/RANTES through the NF-kappaB pathway Eur. J. Immunol. 37 2007 2499 2508 (Pubitemid 47423619)
52. D.P. Wright, D.I. Rosendale, and A.M. Robertson Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucin FEMS Microbiol. Lett. 190 2000 73 79 (Pubitemid 30645838)
53. H.J. Wu, I.I. Ivanov, J. Darce, K. Hattori, T. Shima, Y. Umesaki, D.R. Littman, C. Benoist, and D. Mathis Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells Immunity 32 2010 815 827
54. M.H. Zaki, K.L. Boyd, P. Vogel, M.B. Kastan, M. Lamkanfi, and T.D. Kanneganti The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis Immunity 32 2010 379 391
55. Arthur, J.C., Lich, J.D., Ye, Z., Allen, I.C., Gris, D., Wilson, J.E., Schneider, M., Roney, K.E., O'Connor, B.P., Moore, C.B., et al. (2010). Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J. Immunol. 185, 4515-4519.
56. Bjöersdorff, A., Bagert, B., Massung, R.F., Gusa, A., and Eliasson, I. (2002). Isolation and characterization of two European strains of Ehrlichia phagocytophila of equine origin. Clin. Diagn. Lab. Immunol. 9, 341-343. (Pubitemid 34226028)
57. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.
58. Dalwai, F., Spratt, D.A., and Pratten, J. (2007). Use of quantitative PCR and culture methods to characterize ecological flux in bacterial biofilms. J. Clin. Microbiol. 45, 3072-3076. (Pubitemid 47417359)
59. Glaccum, M.B., Stocking, K.L., Charrier, K., Smith, J.L., Willis, C.R., Maliszewski, C., Livingston, D.J., Peschon, J.J., and Morrissey, P.J. (1997). Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J. Immunol. 159, 3364-3371. (Pubitemid 127482095)
60. Haas, B.J., Gevers, D., Earl, A.M., Feldgarden, M., Ward, D.V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S.K., Sodergren, E., et al; Human Microbiome Consortium. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494-504.
61. Hu, B., Elinav, E., Huber, S., Booth, C.J., Strowig, T., Jin, C., Eisenbarth, S.C., and Flavell, R.A. (2010). Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc. Natl. Acad. Sci. USA 107, 21635-21640.
62. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S., and Flavell, R.A. (1995). Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267, 2000-2003.
63. Lara-Tejero, M., Sutterwala, F.S., Ogura, Y., Grant, E.P., Bertin, J., Coyle, A.J., Flavell, R.A., and Galán, J.E. (2006). Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412. (Pubitemid 43877602)
64. O'Connor, W., Jr., Kamanaka, M., Booth, C.J., Town, T., Nakae, S., Iwakura, Y., Kolls, J.K., and Flavell, R.A. (2009). A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10, 603-609.
65. Rathinam, V.A., Jiang, Z., Waggoner, S.N., Sharma, S., Cole, L.E., Waggoner, L., Vanaja, S.K., Monks, B.G., Ganesan, S., Latz, E., et al. (2010). The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395-402.
66. Sutterwala, F.S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G.S., Grant, E.P., Bertin, J., Coyle, A.J., Galán, J.E., Askenase, P.W., and Flavell, R.A. (2006). Critical role for NALP3/CIAS1/ Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327.
67. Takeda, K., Tsutsui, H., Yoshimoto, T., Adachi, O., Yoshida, N., Kishimoto, T., Okamura, H., Nakanishi, K., and Akira, S. (1998). Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8, 383-390. (Pubitemid 28188898)
68. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., et al. (2009). A core gut microbiome in obese and lean twins. Nature 457, 480-484.
69. Zheng, H., Fletcher, D., Kozak, W., Jiang, M., Hofmann, K.J., Conn, C.A., Soszynski, D., Grabiec, C., Trumbauer, M.E., Shaw, A., et al. (1995). Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 3, 9-19.