A Large Polysaccharide Produced by Helicobacter hepaticus Induces an Anti-inflammatory Gene Signature in Macrophages

Cell Host and Microbe

Volumn 22, Issue 6, 2017, Pages 733-745.e5

  Danne, Camille ^a   Ryzhakov, Grigory ^a   Martínez López, Maria ^b   Ilott, Nicholas Edward ^a   Franchini, Fanny ^a   Cuskin, Fiona ^c   Lowe, Elisabeth C ^c   Bullers, Samuel J ^a   Arthur, J Simon C ^d   Powrie, Fiona ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

anti inflammatory gene signature; CREB; Helicobacter hepaticus; host microbe interactions; inflammatory bowel disease; macrophage; MSK1 2; mutualism; polysaccharide; TLR2

Indexed keywords

INTERLEUKIN 10; MYELOID DIFFERENTIATION FACTOR 88; POLYSACCHARIDE; TOLL LIKE RECEPTOR 2; BACTERIAL POLYSACCHARIDE; IL10 PROTEIN, MOUSE; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 23; TLR2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CECUM; COLON; CONTROLLED STUDY; GENE; HELICOBACTER HEPATICUS; HOST PATHOGEN INTERACTION; IMMUNOCOMPETENT CELL; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUPERNATANT; SYMBIOSIS; ANIMAL; DRUG EFFECT; IMMUNOLOGY; METABOLISM;

ANIMALS; HELICOBACTER HEPATICUS; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-10; INTERLEUKIN-23; MACROPHAGES; MICE; POLYSACCHARIDES, BACTERIAL; SYMBIOSIS; TOLL-LIKE RECEPTOR 2;

EID: 85040777312     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.11.002     Document Type: Article

References (61)

1. Ananieva, O., Darragh, J., Johansen, C., Carr, J.M., McIlrath, J., Park, J.M., Wingate, A., Monk, C.E., Toth, R., Santos, S.G., et al. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9 (2008), 1028–1036.
2. Arnold, I.C., Mathisen, S., Schulthess, J., Danne, C., Hegazy, A.N., Powrie, F., CD11c(+) monocyte/macrophages promote chronic Helicobacter hepaticus-induced intestinal inflammation through the production of IL-23. Mucosal Immunol. 9 (2016), 352–363.
3. Asquith, M.J., Boulard, O., Powrie, F., Maloy, K.J., Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease. Gastroenterology 139 (2010), 519–529 e511–512.
4. Boulard, O., Asquith, M.J., Powrie, F., Maloy, K.J., TLR2-independent induction and regulation of chronic intestinal inflammation. Eur. J. Immunol. 40 (2010), 516–524.
5. Cahill, R.J., Foltz, C.J., Fox, J.G., Dangler, C.A., Powrie, F., Schauer, D.B., Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect. Immun. 65 (1997), 3126–3131.
6. Chang, H.H., Miaw, S.C., Tseng, W., Sun, Y.W., Liu, C.C., Tsao, H.W., Ho, I.C., PTPN22 modulates macrophage polarization and susceptibility to dextran sulfate sodium-induced colitis. J. Immunol. 191 (2013), 2134–2143.
7. Cheluvappa, R., Eri, R., Luo, A.S., Grimm, M.C., Endothelin and vascular remodelling in colitis pathogenesis–appendicitis and appendectomy limit colitis by suppressing endothelin pathways. Int. J. Colorectal Dis. 29 (2014), 1321–1328.
8. Chen, L., Flies, D.B., Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13 (2013), 227–242.
9. Cohen, P., The TLR and IL-1 signalling network at a glance. J. Cell Sci. 127 (2014), 2383–2390.
10. Cohen-Poradosu, R., McLoughlin, R.M., Lee, J.C., Kasper, D.L., Bacteroides fragilis-stimulated interleukin-10 contains expanding disease. J. Infect. Dis. 204 (2011), 363–371.
11. Darragh, J., Ananieva, O., Courtney, A., Elcombe, S., Arthur, J.S., MSK1 regulates the transcription of IL-1ra in response to TLR activation in macrophages. Biochem. J. 425 (2010), 595–602.
12. Dasgupta, S., Erturk-Hasdemir, D., Ochoa-Reparaz, J., Reinecker, H.C., Kasper, D.L., Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe 15 (2014), 413–423.
13. De Nardo, D., Labzin, L.I., Kono, H., Seki, R., Schmidt, S.V., Beyer, M., Xu, D., Zimmer, S., Lahrmann, C., Schildberg, F.A., et al. High-density lipoprotein mediates anti-inflammatory reprogramming of macrophages via the transcriptional regulator ATF3. Nat. Immunol. 15 (2014), 152–160.
14. Elcombe, S.E., Naqvi, S., Van Den Bosch, M.W., MacKenzie, K.F., Cianfanelli, F., Brown, G.D., Arthur, J.S., Dectin-1 regulates IL-10 production via a MSK1/2 and CREB dependent pathway and promotes the induction of regulatory macrophage markers. PLoS One, 8, 2013, e60086.
15. Erdman, S.E., Poutahidis, T., Tomczak, M., Rogers, A.B., Cormier, K., Plank, B., Horwitz, B.H., Fox, J.G., CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am. J. Pathol. 162 (2003), 691–702.
16. Ferwerda, G., Meyer-Wentrup, F., Kullberg, B.J., Netea, M.G., Adema, G.J., Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages. Cell. Microbiol. 10 (2008), 2058–2066.
17. Gantner, B.N., Simmons, R.M., Canavera, S.J., Akira, S., Underhill, D.M., Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197 (2003), 1107–1117.
18. Ginhoux, F., Schultze, J.L., Murray, P.J., Ochando, J., Biswas, S.K., New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nat. Immunol. 17 (2016), 34–40.
19. Glocker, E.O., Kotlarz, D., Boztug, K., Gertz, E.M., Schäffer, A.A., Noyan, F., Perro, M., Diestelhorst, J., Allroth, A., Murugan, D., et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 361 (2009), 2033–2045.
20. Griseri, T., McKenzie, B.S., Schiering, C., Powrie, F., Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23-driven chronic intestinal inflammation. Immunity 37 (2012), 1116–1129.
21. Hue, S., Ahern, P., Buonocore, S., Kullberg, M.C., Cua, D.J., McKenzie, B.S., Powrie, F., Maloy, K.J., Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203 (2006), 2473–2483.
22. Hynes, S.O., Ferris, J.A., Szponar, B., Wadström, T., Fox, J.G., O'Rourke, J., Larsson, L., Yaquian, E., Ljungh, Å., Clyne, M., Andersen, L.P., Moran, A.P., Comparative chemical and biological characterization of the lipopolysaccharides of gastric and enterohepatic Helicobacters. Helicobacter 9 (2004), 313–323.
23. Junkins, R.D., MacNeil, A.J., Wu, Z., McCormick, C., Lin, T.J., Regulator of calcineurin 1 suppresses inflammation during respiratory tract infections. J. Immunol. 190 (2013), 5178–5186.
24. Kaser, A., Zeissig, S., Blumberg, R.S., Inflammatory bowel disease. Annu. Rev. Immunol. 28 (2010), 573–621.
25. Kotlarz, D., Beier, R., Murugan, D., Diestelhorst, J., Jensen, O., Boztug, K., Pfeifer, D., Kreipe, H., Pfister, E.D., Baumann, U., et al. Loss of interleukin-10 signaling and infantile inflammatory bowel disease: implications for diagnosis and therapy. Gastroenterology 143 (2012), 347–355.
26. Krausgruber, T., Schiering, C., Adelmann, K., Harrison, O.J., Chomka, A., Pearson, C., Ahern, P.P., Shale, M., Oukka, M., Powrie, F., T-bet is a key modulator of IL-23-driven pathogenic CD4(+) T cell responses in the intestine. Nat. Commun., 7, 2016, 11627.
27. Kullberg, M.C., Ward, J.M., Gorelick, P.L., Caspar, P., Hieny, S., Cheever, A., Jankovic, D., Sher, A., Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66 (1998), 5157–5166.
28. Kullberg, M.C., Jankovic, D., Gorelick, P.L., Caspar, P., Letterio, J.J., Cheever, A.W., Sher, A., Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196 (2002), 505–515.
29. Kullberg, M.C., Jankovic, D., Feng, C.G., Hue, S., Gorelick, P.L., McKenzie, B.S., Cua, D.J., Powrie, F., Cheever, A.W., Maloy, K.J., Sher, A., IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203 (2006), 2485–2494.
30. Lawrence, T., Natoli, G., Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 11 (2011), 750–761.
31. Lebedeva, T., Dustin, M.L., Sykulev, Y., ICAM-1 co-stimulates target cells to facilitate antigen presentation. Curr. Opin. Immunol. 17 (2005), 251–258.
32. Liu, Y., Chen, K., Wang, C., Gong, W., Yoshimura, T., Liu, M., Wang, J.M., Cell surface receptor FPR2 promotes antitumor host defense by limiting M2 polarization of macrophages. Cancer Res. 73 (2013), 550–560.
33. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M., Henrissat, B., The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42 (2014), D490–D495.
34. Maloy, K.J., Powrie, F., Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474 (2011), 298–306.
35. Maloy, K.J., Salaun, L., Cahill, R., Dougan, G., Saunders, N.J., Powrie, F., CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197 (2003), 111–119.
36. Mandell, L., Moran, A.P., Cocchiarella, A., Houghton, J., Taylor, N., Fox, J.G., Wang, T.C., Kurt-Jones, E.A., Intact gram-negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus bacteria activate innate immunity via toll-like receptor 2 but not toll-like receptor 4. Infect. Immun. 72 (2004), 6446–6454.
37. Mazmanian, S.K., Round, J.L., Kasper, D.L., A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453 (2008), 620–625.
38. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001), 683–765.
39. Morrison, P.J., Bending, D., Fouser, L.A., Wright, J.F., Stockinger, B., Cooke, A., Kullberg, M.C., Th17-cell plasticity in Helicobacter hepaticus-induced intestinal inflammation. Mucosal Immunol. 6 (2013), 1143–1156.
40. Murray, P.J., Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6 (2006), 379–386.
41. Neff, C.P., Rhodes, M.E., Arnolds, K.L., Collins, C.B., Donnelly, J., Nusbacher, N., Jedlicka, P., Schneider, J.M., McCarter, M.D., Shaffer, M., et al. Diverse intestinal bacteria contain putative Zwitterionic capsular polysaccharides with anti-inflammatory properties. Cell Host Microbe 20 (2016), 535–547.
42. Nemati, M., Larussa, T., Khorramdelazad, H., Mahmoodi, M., Jafarzadeh, A., Toll-like receptor 2: An important immunomodulatory molecule during Helicobacter pylori infection. Life Sci. 178 (2017), 17–29.
43. Oliveira-Nascimento, L., Massari, P., Wetzler, L.M., The role of TLR2 in infection and immunity. Front. Immunol., 3, 2012, 79.
44. 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.
45. Reyskens, K.M., Arthur, J.S., Emerging roles of the mitogen and stress activated kinases MSK1 and MSK2. Front. Cell Dev. Biol., 4, 2016, 56.
46. Round, J.L., Lee, S.M., Li, J., Tran, G., Jabri, B., Chatila, T.A., Mazmanian, S.K., The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332 (2011), 974–977.
47. Safford, M., Collins, S., Lutz, M.A., Allen, A., Huang, C.T., Kowalski, J., Blackford, A., Horton, M.R., Drake, C., Schwartz, R.H., Powell, J.D., Egr-2 and Egr-3 are negative regulators of T cell activation. Nat. Immunol. 6 (2005), 472–480.
48. Sanin, D.E., Prendergast, C.T., Mountford, A.P., IL-10 production in macrophages is regulated by a TLR-driven CREB-mediated mechanism that is linked to genes involved in cell metabolism. J. Immunol. 195 (2015), 1218–1232.
49. Schiering, C., Krausgruber, T., Chomka, A., Fröhlich, A., Adelmann, K., Wohlfert, E.A., Pott, J., Griseri, T., Bollrath, J., Hegazy, A.N., et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513 (2014), 564–568.
50. Shi, C., Pamer, E.G., Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11 (2011), 762–774.
51. Shouval, D.S., Biswas, A., Goettel, J.A., McCann, K., Conaway, E., Redhu, N.S., Mascanfroni, I.D., Al Adham, Z., Lavoie, S., Ibourk, M., et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40 (2014), 706–719.
52. Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., Droge, M., Fartmann, B., Fischer, H.P., Ge, Z., et al. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. USA 100 (2003), 7901–7906.
53. Surana, N.K., Kasper, D.L., The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA. Immunol. Rev. 245 (2012), 13–26.
54. Tomczak, M.F., Gadjeva, M., Wang, Y.Y., Brown, K., Maroulakou, I., Tsichlis, P.N., Erdman, S.E., Fox, J.G., Horwitz, B.H., Defective activation of ERK in macrophages lacking the p50/p105 subunit of NF-kappaB is responsible for elevated expression of IL-12 p40 observed after challenge with Helicobacter hepaticus. J. Immunol. 176 (2006), 1244–1251.
55. Toriseva, M., Laato, M., Carpén, O., Ruohonen, S.T., Savontaus, E., Inada, M., Krane, S.M., Kähäri, V.M., MMP-13 regulates growth of wound granulation tissue and modulates gene expression signatures involved in inflammation, proteolysis, and cell viability. PLoS One, 7, 2012, e42596.
56. Uhlig, H.H., Schwerd, T., Koletzko, S., Shah, N., Kammermeier, J., Elkadri, A., Ouahed, J., Wilson, D.C., Travis, S.P., Turner, D., et al. The diagnostic approach to monogenic very early onset inflammatory bowel disease. Gastroenterology 147 (2014), 990–1007.e3.
57. Wei, J., Zhou, Y., Besner, G.E., Heparin-binding EGF-like growth factor and enteric neural stem cell transplantation in the prevention of experimental necrotizing enterocolitis in mice. Pediatr. Res. 78 (2015), 29–37.
58. Wen, A.Y., Sakamoto, K.M., Miller, L.S., The role of the transcription factor CREB in immune function. J. Immunol. 185 (2010), 6413–6419.
59. Wexler, H.M., Bacteroides: the good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20 (2007), 593–621.
60. Wingate, A.D., Martin, K.J., Hunter, C., Carr, J.M., Clacher, C., Arthur, J.S., Generation of a conditional CREB Ser133Ala knockin mouse. Genesis 47 (2009), 688–696.
61. Zigmond, E., Bernshtein, B., Friedlander, G., Walker, C.R., Yona, S., Kim, K.W., Brenner, O., Krauthgamer, R., Varol, C., Müller, W., Jung, S., Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 40 (2014), 720–733.