NLRP6 Protects Il10−/− Mice from Colitis by Limiting Colonization of Akkermansia muciniphila

Cell Reports

Volumn 19, Issue 4, 2017, Pages 733-745

  Seregin, Sergey S ^a   Golovchenko, Natasha ^a   Schaf, Bryan ^a   Chen, Jiachen ^a   Pudlo, Nicholas A ^a   Mitchell, Jonathan ^a   Baxter, Nielson T ^a   Zhao, Lili ^b   Schloss, Patrick D ^a   Martens, Eric C ^a   Eaton, Kathryn A ^a   Chen, Grace Y ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Akkermansia; colitis; dysbiosis; IL 10; inflammation; intestine; Microbiota; NLRP6; NLRs; pathobiont

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; INTERLEUKIN 18; NLRP6 PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; CELL SURFACE RECEPTOR; INTERLEUKIN 10; NOD-LIKE RECEPTOR PYRIN DOMAIN-CONTAINING PROTEIN 6, MOUSE;

AKKERMANSIA MUCINIPHILA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; COLITIS; DISEASE PREDISPOSITION; GRAM NEGATIVE BACTERIUM; IMMUNOREGULATION; INFLAMMATORY BOWEL DISEASE; INTESTINE PROTECTION; MOUSE; MOUSE MODEL; NONHUMAN; PROTECTION; PROTEIN DEFICIENCY; PROTEIN FUNCTION; ANIMAL; BACTEROIDES; C57BL MOUSE; CHEMISTRY; COLON; DEFICIENCY; DNA SEQUENCE; FEMALE; GENETICS; HYPERPLASIA; INFLAMMATION; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOLOGY; PHYSIOLOGY; VERRUCOMICROBIA;

ANIMALS; BACTEROIDES; COLITIS; COLON; DISEASE SUSCEPTIBILITY; DNA, BACTERIAL; FEMALE; HYPERPLASIA; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-18; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; RECEPTORS, CELL SURFACE; SEQUENCE ANALYSIS, DNA; VERRUCOMICROBIA;

EID: 85018672799     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.03.080     Document Type: Article

References (48)

1. Baxter, N.T., Zackular, J.P., Chen, G.Y., Schloss, P.D., Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome, 2, 2014, 20.
2. Brown, S.L., Riehl, T.E., Walker, M.R., Geske, M.J., Doherty, J.M., Stenson, W.F., Stappenbeck, T.S., Myd88-dependent positioning of Ptgs2-expressing stromal cells maintains colonic epithelial proliferation during injury. J. Clin. Invest. 117 (2007), 258–269.
3. Chen, G.Y., Liu, M., Wang, F., Bertin, J., Núñez, G., A functional role for Nlrp6 in intestinal inflammation and tumorigenesis. J. Immunol. 186 (2011), 7187–7194.
4. Couturier-Maillard, A., Secher, T., Rehman, A., Normand, S., De Arcangelis, A., Haesler, R., Huot, L., Grandjean, T., Bressenot, A., Delanoye-Crespin, A., et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J. Clin. Invest. 123 (2013), 700–711.
5. Davidson, N.J., Leach, M.W., Fort, M.M., Thompson-Snipes, L., Kühn, R., Müller, W., Berg, D.J., Rennick, D.M., T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J. Exp. Med. 184 (1996), 241–251.
6. Derrien, M., Vaughan, E.E., Plugge, C.M., de Vos, W.M., Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54 (2004), 1469–1476.
7. Elinav, E., Strowig, T., Kau, A.L., Henao-Mejia, J., Thaiss, C.A., Booth, C.J., Peaper, D.R., Bertin, J., Eisenbarth, S.C., Gordon, J.I., Flavell, R.A., NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145 (2011), 745–757.
8. Excoffier, L., Smouse, P.E., Quattro, J.M., Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131 (1992), 479–491.
9. Ganesh, B.P., Klopfleisch, R., Loh, G., Blaut, M., Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS ONE, 8, 2013, e74963.
10. Grenier, J.M., Wang, L., Manji, G.A., Huang, W.J., Al-Garawi, A., Kelly, R., Carlson, A., Merriam, S., Lora, J.M., Briskin, M., 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.
11. Hehemann, J.H., Kelly, A.G., Pudlo, N.A., Martens, E.C., Boraston, A.B., Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc. Natl. Acad. Sci. USA 109 (2012), 19786–19791.
12. Henao-Mejia, J., Elinav, E., Jin, C., Hao, L., Mehal, W.Z., Strowig, T., Thaiss, C.A., Kau, A.L., Eisenbarth, S.C., Jurczak, M.J., et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482 (2012), 179–185.
13. Hirota, S.A., Ng, J., Lueng, A., Khajah, M., Parhar, K., Li, Y., Lam, V., Potentier, M.S., Ng, K., Bawa, M., et al. NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis. Inflamm. Bowel Dis. 17 (2011), 1359–1372.
14. Hooper, L.V., Stappenbeck, T.S., Hong, C.V., Gordon, J.I., Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol. 4 (2003), 269–273.
15. Hoshi, N., Schenten, D., Nish, S.A., Walther, Z., Gagliani, N., Flavell, R.A., Reizis, B., Shen, Z., Fox, J.G., Iwasaki, A., Medzhitov, R., MyD88 signalling in colonic mononuclear phagocytes drives colitis in IL-10-deficient mice. Nat. Commun., 3, 2012, 1120.
16. Hu, S., Peng, L., Kwak, Y.T., Tekippe, E.M., Pasare, C., Malter, J.S., Hooper, L.V., Zaki, M.H., The DNA sensor AIM2 maintains intestinal homeostasis via regulation of epithelial antimicrobial host defense. Cell Rep. 13 (2015), 1922–1936.
17. Johansson, M.E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., Hansson, G.C., The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA 105 (2008), 15064–15069.
18. Johansson, M.E., Gustafsson, J.K., Holmén-Larsson, J., Jabbar, K.S., Xia, L., Xu, H., Ghishan, F.K., Carvalho, F.A., Gewirtz, A.T., Sjövall, H., Hansson, G.C., Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 63 (2014), 281–291.
19. Joossens, M., Huys, G., Cnockaert, M., De Preter, V., Verbeke, K., Rutgeerts, P., Vandamme, P., Vermeire, S., Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 60 (2011), 631–637.
20. Kaplan, G.G., The global burden of IBD: from 2015 to 2025. Nat. Rev. Gastroenterol. Hepatol. 12 (2015), 720–727.
21. Kaser, A., Zeissig, S., Blumberg, R.S., Inflammatory bowel disease. Annu. Rev. Immunol. 28 (2010), 573–621.
22. Keubler, L.M., Buettner, M., Häger, C., Bleich, A., A multihit model: colitis lessons from the interleukin-10-deficient mouse. Inflamm. Bowel Dis. 21 (2015), 1967–1975.
23. Kiesler, P., Fuss, I.J., Strober, W., Experimental models of inflammatory bowel diseases. Cell. Mol. Gastroenterol. Hepatol. 1 (2015), 154–170.
24. Kim, S.C., Tonkonogy, S.L., Albright, C.A., Tsang, J., Balish, E.J., Braun, J., Huycke, M.M., Sartor, R.B., Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128 (2005), 891–906.
25. Knights, D., Silverberg, M.S., Weersma, R.K., Gevers, D., Dijkstra, G., Huang, H., Tyler, A.D., van Sommeren, S., Imhann, F., Stempak, J.M., et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med., 6, 2014, 107.
26. Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K., Schloss, P.D., Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79 (2013), 5112–5120.
27. Levy, M., Thaiss, C.A., Zeevi, D., Dohnalová, L., Zilberman-Schapira, G., Mahdi, J.A., David, E., Savidor, A., Korem, T., Herzig, Y., et al. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163 (2015), 1428–1443.
28. Man, S.M., Zhu, Q., Zhu, L., Liu, Z., Karki, R., Malik, A., Sharma, D., Li, L., Malireddi, R.K., Gurung, P., et al. Critical role for the DNA sensor AIM2 in stem cell proliferation and cancer. Cell 162 (2015), 45–58.
29. Martens, E.C., Lowe, E.C., Chiang, H., Pudlo, N.A., Wu, M., McNulty, N.P., Abbott, D.W., Henrissat, B., Gilbert, H.J., Bolam, D.N., Gordon, J.I., Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol., 9, 2011, e1001221.
30. Nagalingam, N.A., Robinson, C.J., Bergin, I.L., Eaton, K.A., Huffnagle, G.B., Young, V.B., The effects of intestinal microbial community structure on disease manifestation in IL-10-/- mice infected with Helicobacter hepaticus. Microbiome, 1, 2013, 15.
31. Netea, M.G., van de Veerdonk, F.L., van der Meer, J.W., Dinarello, C.A., Joosten, L.A., Inflammasome-independent regulation of IL-1-family cytokines. Annu. Rev. Immunol. 33 (2015), 49–77.
32. Normand, S., Delanoye-Crespin, A., Bressenot, A., Huot, L., Grandjean, T., Peyrin-Biroulet, L., Lemoine, Y., Hot, D., Chamaillard, M., 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.
33. Png, C.W., Lindén, S.K., Gilshenan, K.S., Zoetendal, E.G., McSweeney, C.S., Sly, L.I., McGuckin, M.A., Florin, T.H., Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am. J. Gastroenterol. 105 (2010), 2420–2428.
34. Rajilić-Stojanović, M., Shanahan, F., Guarner, F., de Vos, W.M., Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm. Bowel Dis. 19 (2013), 481–488.
35. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., Medzhitov, R., Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004), 229–241.
36. Rubino, S.J., Selvanantham, T., Girardin, S.E., Philpott, D.J., Nod-like receptors in the control of intestinal inflammation. Curr. Opin. Immunol. 24 (2012), 398–404.
37. Salcedo, R., Worschech, A., Cardone, M., Jones, Y., Gyulai, Z., Dai, R.M., Wang, E., Ma, W., Haines, D., O'hUigin, C., et al. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J. Exp. Med. 207 (2010), 1625–1636.
38. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 (2009), 7537–7541.
39. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S., Huttenhower, C., Metagenomic biomarker discovery and explanation. Genome Biol., 12, 2011, R60.
40. Sellon, R.K., Tonkonogy, S., Schultz, M., Dieleman, L.A., Grenther, W., Balish, E., Rennick, D.M., Sartor, R.B., Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66 (1998), 5224–5231.
41. Seregin, S.S., Golovchenko, N., Schaf, B., Chen, J., Eaton, K.A., Chen, G.Y., NLRP6 function in inflammatory monocytes reduces susceptibility to chemically induced intestinal injury. Mucosal Immunol. 10 (2017), 434–445.
42. Sherwood, R.A., Faecal markers of gastrointestinal inflammation. J. Clin. Pathol. 65 (2012), 981–985.
43. Stappenbeck, T.S., Virgin, H.W., Accounting for reciprocal host-microbiome interactions in experimental science. Nature 534 (2016), 191–199.
44. Takagi, H., Kanai, T., Okazawa, A., Kishi, Y., Sato, T., Takaishi, H., Inoue, N., Ogata, H., Iwao, Y., Hoshino, K., et al. Contrasting action of IL-12 and IL-18 in the development of dextran sodium sulphate colitis in mice. Scand. J. Gastroenterol. 38 (2003), 837–844.
45. White, J.R., Nagarajan, N., Pop, M., Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput. Biol., 5, 2009, e1000352.
46. Willing, B.P., Dicksved, J., Halfvarson, J., Andersson, A.F., Lucio, M., Zheng, Z., Järnerot, G., Tysk, C., Jansson, J.K., Engstrand, L., A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139 (2010), 1844–1854.e1.
47. Zella, G.C., Hait, E.J., Glavan, T., Gevers, D., Ward, D.V., Kitts, C.L., Korzenik, J.R., Distinct microbiome in pouchitis compared to healthy pouches in ulcerative colitis and familial adenomatous polyposis. Inflamm. Bowel Dis. 17 (2011), 1092–1100.
48. Zhang, Y.Z., Li, Y.Y., Inflammatory bowel disease: pathogenesis. World J. Gastroenterol. 20 (2014), 91–99.