Microbiota-Modulated Metabolites Shape the Intestinal Microenvironment by Regulating NLRP6 Inflammasome Signaling

Cell

Volumn 163, Issue 6, 2015, Pages 1428-1443

  Levy, Maayan ^a   Thaiss, Christoph A ^a   Zeevi, David ^a   Dohnalová, Lenka ^a   Zilberman Schapira, Gili ^a   Mahdi, Jemal Ali ^a,b   David, Eyal ^a   Savidor, Alon ^a   Korem, Tal ^a   Herzig, Yonatan ^a   Pevsner Fischer, Meirav ^a   Shapiro, Hagit ^a   Christ, Anette ^c,d   Harmelin, Alon ^a   Halpern, Zamir ^e,f   Latz, Eicke ^c,d   Flavell, Richard A ^g   Amit, Ido ^a   Segal, Eran ^a   Elinav, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e TEL AVIV UNIVERSITY   (Israel)

^f TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTAMINE; INFLAMMASOME; INTERLEUKIN 18; NLRP6 PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; SPERMINE; TAURINE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CELL SURFACE RECEPTOR; NOD-LIKE RECEPTOR PYRIN DOMAIN-CONTAINING PROTEIN 6, MOUSE;

ARTICLE; COLITIS; CYTOKINE RELEASE; HOST PATHOGEN INTERACTION; IMMUNOMODULATION; INTESTINE FLORA; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLON; DYSBIOSIS; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASES; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; COLITIS; COLON; DYSBIOSIS; GERM-FREE LIFE; INFLAMMASOMES; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-18; MICE; MICE, INBRED C57BL; MICROBIOTA; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TAURINE;

EID: 84949255269     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.10.048     Document Type: Article

References (34)

1. P.K. Anand, and T.D. Kanneganti Targeting NLRP6 to enhance immunity against bacterial infections Future Microbiol. 7 2012 1239 1242
2. D. Artis, M.L. Wang, S.A. Keilbaugh, W. He, M. Brenes, G.P. Swain, P.A. Knight, D.D. Donaldson, M.A. Lazar, H.R. Miller, and et al. RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract Proc. Natl. Acad. Sci. USA 101 2004 13596 13600
3. J.R. Brestoff, and D. Artis Commensal bacteria at the interface of host metabolism and the immune system Nat. Immunol. 14 2013 676 684
4. J.G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Peña, J.K. Goodrich, J.I. Gordon, and et al. QIIME allows analysis of high-throughput community sequencing data Nat. Methods 7 2010 335 336
5. G.Y. Chen, M. Liu, F. Wang, J. Bertin, and G. Núñez A functional role for Nlrp6 in intestinal inflammation and tumorigenesis J. Immunol. 186 2011 7187 7194
6. A. Couturier-Maillard, T. Secher, A. Rehman, S. Normand, A. De Arcangelis, R. Haesler, L. Huot, T. Grandjean, A. Bressenot, A. Delanoye-Crespin, and et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer J. Clin. Invest. 123 2013 700 711
7. L.A. David, C.F. Maurice, R.N. Carmody, D.B. Gootenberg, J.E. Button, B.E. Wolfe, A.V. Ling, A.S. Devlin, Y. Varma, M.A. Fischbach, and et al. Diet rapidly and reproducibly alters the human gut microbiome Nature 505 2014 559 563
8. S. Devkota, Y. Wang, M.W. Musch, V. Leone, H. Fehlner-Peach, A. Nadimpalli, D.A. Antonopoulos, B. Jabri, and E.B. Chang Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice Nature 487 2012 104 108
9. E. Elinav, T. Strowig, A.L. Kau, J. Henao-Mejia, C.A. Thaiss, C.J. Booth, D.R. Peaper, J. Bertin, S.C. Eisenbarth, J.I. Gordon, and R.A. Flavell NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis Cell 145 2011 745 757
10. W.S. Garrett, G.M. Lord, S. Punit, G. Lugo-Villarino, S.K. Mazmanian, S. Ito, J.N. Glickman, and L.H. Glimcher Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system Cell 131 2007 33 45
11. J.K. Goodrich, J.L. Waters, A.C. Poole, J.L. Sutter, O. Koren, R. Blekhman, M. Beaumont, W. Van Treuren, R. Knight, J.T. Bell, and et al. Human genetics shape the gut microbiome Cell 159 2014 789 799
12. G. Gremel, A. Wanders, J. Cedernaes, L. Fagerberg, B. Hallstrom, K. Edlund, E. Sjostedt, M. Uhlen, and F. Ponten The human gastrointestinal tract-specific transcriptome and proteome as defined by RNA sequencing and antibody-based profiling J. Gastroenterol. 50 2015 46 57
13. J.M. Grenier, L. Wang, G.A. Manji, W.J. Huang, A. Al-Garawi, R. Kelly, A. Carlson, S. Merriam, J.M. Lora, M. Briskin, and et al. 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
14. J. Henao-Mejia, E. Elinav, C. Jin, L. Hao, W.Z. Mehal, T. Strowig, C.A. Thaiss, A.L. Kau, S.C. Eisenbarth, M.J. Jurczak, and et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 482 2012 179 185
15. L.V. Hooper, T.S. Stappenbeck, C.V. Hong, and J.I. Gordon Angiogenins: a new class of microbicidal proteins involved in innate immunity Nat. Immunol. 4 2003 269 273
16. L.V. Hooper, D.R. Littman, and A.J. Macpherson Interactions between the microbiota and the immune system Science 336 2012 1268 1273
17. B. Hu, E. Elinav, S. Huber, T. Strowig, L. Hao, A. Hafemann, C. Jin, C. Wunderlich, T. Wunderlich, S.C. Eisenbarth, and R.A. Flavell Microbiota-induced activation of epithelial IL-6 signaling links inflammasome-driven inflammation with transmissible cancer Proc. Natl. Acad. Sci. USA 110 2013 9862 9867
18. T. Ikuta, Y. Kobayashi, M. Kitazawa, K. Shiizaki, N. Itano, T. Noda, S. Pettersson, L. Poellinger, Y. Fujii-Kuriyama, S. Taniguchi, and K. Kawajiri ASC-associated inflammation promotes cecal tumorigenesis in aryl hydrocarbon receptor-deficient mice Carcinogenesis 34 2013 1620 1627
19. I.I. Ivanov, K. Atarashi, N. Manel, E.L. Brodie, T. Shima, U. Karaoz, D. Wei, K.C. Goldfarb, C.A. Santee, S.V. Lynch, and et al. Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 2009 485 498
20. 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
21. C. Lupp, M.L. Robertson, M.E. Wickham, I. Sekirov, O.L. Champion, E.C. Gaynor, and B.B. Finlay Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae Cell Host Microbe 2 2007 204
22. F. Martinon, A. Mayor, and J. Tschopp The inflammasomes: guardians of the body Annu. Rev. Immunol. 27 2009 229 265
23. H. Miyoshi, and T.S. Stappenbeck In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture Nat. Protoc. 8 2013 2471 2482
24. C. Moon, M.T. Baldridge, M.A. Wallace, C.A. Burnham, H.W. Virgin, and T.S. Stappenbeck Vertically transmitted faecal IgA levels determine extra-chromosomal phenotypic variation Nature 521 2015 90 93
25. S. Normand, A. Delanoye-Crespin, A. Bressenot, L. Huot, T. Grandjean, L. Peyrin-Biroulet, Y. Lemoine, D. Hot, and M. Chamaillard Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury Proc. Natl. Acad. Sci. USA 108 2011 9601 9606
26. R. Nowarski, R. Jackson, N. Gagliani, M.R. de Zoete, N.W. Palm, W. Bailis, J.S. Low, C.C.D. Harman, M. Graham, E. Elinav, and R.A. Flavell Epithelial IL-18 equilibrium controls barrier function in colitis Cell 163 2015 1444 1456 this issue
27. H. Shapiro, C.A. Thaiss, M. Levy, and E. Elinav The cross talk between microbiota and the immune system: metabolites take center stage Curr. Opin. Immunol. 30 2014 54 62
28. M. Shimizu, Z. Zhao, Y. Ishimoto, and H. Satsu Dietary taurine attenuates dextran sulfate sodium (DSS)-induced experimental colitis in mice Adv. Exp. Med. Biol. 643 2009 265 271
29. B. Stecher, R. Robbiani, A.W. Walker, A.M. Westendorf, M. Barthel, M. Kremer, S. Chaffron, A.J. Macpherson, J. Buer, J. Parkhill, and et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota PLoS Biol. 5 2007 2177 2189
30. C.A. Thaiss, and E. Elinav Exploring new horizons in microbiome research Cell Host Microbe 15 2014 662 667
31. S. Tsuji, J. Uehori, M. Matsumoto, Y. Suzuki, A. Matsuhisa, K. Toyoshima, and T. Seya Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall J. Biol. Chem. 276 2001 23456 23463
32. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, and J.I. Gordon An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 2006 1027 1031
33. M. Wlodarska, C.A. Thaiss, R. Nowarski, J. Henao-Mejia, J.P. Zhang, E.M. Brown, G. Frankel, M. Levy, M.N. Katz, W.M. Philbrick, and et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion Cell 156 2014 1045 1059
34. Z. Zhao, H. Satsu, M. Fujisawa, M. Hori, Y. Ishimoto, M. Totsuka, A. Nambu, S. Kakuta, H. Ozaki, and M. Shimizu Attenuation by dietary taurine of dextran sulfate sodium-induced colitis in mice and of THP-1-induced damage to intestinal Caco-2 cell monolayers Amino Acids 35 2008 217 224