Microbiota Sensing by Mincle-Syk Axis in Dendritic Cells Regulates Interleukin-17 and -22 Production and Promotes Intestinal Barrier Integrity

Immunity

Volumn 50, Issue 2, 2019, Pages 446-461.e9

  Martínez López, María ^a   Iborra, Salvador ^a,b   Conde Garrosa, Ruth ^a   Mastrangelo, Annalaura ^a   Danne, Camille ^c   Mann, Elizabeth R ^d,e   Reid, Delyth M ^f   Gaboriau Routhiau, Valérie ^g,h,i   Chaparro, Maria ^j   Lorenzo, María P ^k   Minnerup, Lara ^l   Saz Leal, Paula ^a   Slack, Emma ^m   Kemp, Benjamin ⁿ   Gisbert, Javier P ^j   Dzionek, Andrzej ^l   Robinson, Matthew J ⁿ   Rupérez, Francisco J ^k   Cerf Bensussan, Nadine ^h,i   Brown, Gordon D ^f   Bernardo, David ^j   LeibundGut Landmann, Salomé ^o   Sancho, David ^a   more..

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

^g UNIVERSITÉ PARIS SACLAY   (France)

^h IMAGINE INSTITUTE   (France)

ⁱ UNIVERSITÉ PARIS DESCARTES   (France)

^j Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

^k UNIVERSIDAD SAN PABLO CEU   (Spain)

^l MILTENYI BIOTEC GMBH   (Germany)

^m ETH ZURICH   (Switzerland)

ⁿ MEDIMMUNE LTD   (United Kingdom)

^o UNIVERSITY OF ZURICH   (Switzerland)

more..

Author keywords

antimicrobial defense; dendritic cell; gut microbiota translocation; IL 17; IL 22; innate lymphoid cells; intestinal barrier; lipid metabolism; liver inflammation; Mincle; Syk kinase; T lymphocyte

Indexed keywords

CHOLECYSTOKININ OCTAPEPTIDE; CIMETIDINE; IMMUNOGLOBULIN A; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23P19; INTERLEUKIN 6; LECTIN RECEPTOR; MINCLE PROTEIN; PROTEIN; PROTEIN KINASE SYK; REGIII GAMMA PROTEIN; UNCLASSIFIED DRUG; CLECSF8 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; LECTIN; MEMBRANE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; COMMENSALISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HEPATITIS; HOST MICROBE INTERACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNODETECTION; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LACTOBACILLUS PLANTARUM; LIPID METABOLISM; LYMPHOID CELL; MALE; MIDDLE AGED; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NORMAL HUMAN; PEYER PATCH; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TH17 CELL; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; DENDRITIC CELLS; GASTROINTESTINAL MICROBIOME; HUMANS; INTERLEUKIN-17; INTERLEUKINS; INTESTINAL MUCOSA; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; PEYER'S PATCHES; SIGNAL TRANSDUCTION; SYK KINASE; TH17 CELLS;

EID: 85061393496     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2018.12.020     Document Type: Article

References (68)

1. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., Akira, S., Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9 (1998), 143–150.
2. Allen, J.N., Dey, A., Nissly, R., Fraser, J., Yu, S., Balandaram, G., Peters, J.M., Hankey-Giblin, P.A., Isolation, characterization, and purification of macrophages from tissues affected by obesity-related inflammation. J. Vis. Exp.(122), 2017.
3. Atarashi, K., Tanoue, T., Ando, M., Kamada, N., Nagano, Y., Narushima, S., Suda, W., Imaoka, A., Setoyama, H., Nagamori, T., et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 163 (2015), 367–380.
4. Bäumler, A.J., Sperandio, V., Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535 (2016), 85–93.
5. Behler, F., Maus, R., Bohling, J., Knippenberg, S., Kirchhof, G., Nagata, M., Jonigk, D., Izykowski, N., Mägel, L., Welte, T., et al. Macrophage-inducible C-type lectin Mincle-expressing dendritic cells contribute to control of splenic Mycobacterium bovis BCG infection in mice. Infect. Immun. 83 (2015), 184–196.
6. Bekiaris, V., Persson, E.K., Agace, W.W., Intestinal dendritic cells in the regulation of mucosal immunity. Immunol. Rev. 260 (2014), 86–101.
7. Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
8. Bonnardel, J., Da Silva, C., Henri, S., Tamoutounour, S., Chasson, L., Montañana-Sanchis, F., Gorvel, J.P., Lelouard, H., Innate and adaptive immune functions of peyer's patch monocyte-derived cells. Cell Rep. 11 (2015), 770–784.
9. Bunker, J.J., Flynn, T.M., Koval, J.C., Shaw, D.G., Meisel, M., McDonald, B.D., Ishizuka, I.E., Dent, A.L., Wilson, P.C., Jabri, B., et al. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43 (2015), 541–553.
10. 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. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
11. Cohen, P.S., Laux, D.C., Bacterial adhesion to and penetration of intestinal mucus in vitro. Methods Enzymol. 253 (1995), 309–314.
12. Cullender, T.C., Chassaing, B., Janzon, A., Kumar, K., Muller, C.E., Werner, J.J., Angenent, L.T., Bell, M.E., Hay, A.G., Peterson, D.A., et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14 (2013), 571–581.
13. Da Silva, C., Wagner, C., Bonnardel, J., Gorvel, J.P., Lelouard, H., The Peyer's patch mononuclear phagocyte system at steady state and during infection. Front. Immunol., 8, 2017, 1254.
14. Donaldson, G.P., Lee, S.M., Mazmanian, S.K., Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14 (2016), 20–32.
15. Eriksson, M., Johannssen, T., von Smolinski, D., Gruber, A.D., Seeberger, P.H., Lepenies, B., The C-Type lectin receptor SIGNR3 binds to fungi present in commensal microbiota and influences immune regulation in experimental colitis. Front. Immunol., 4, 2013, 196.
16. Fung, T.C., Artis, D., Sonnenberg, G.F., Anatomical localization of commensal bacteria in immune cell homeostasis and disease. Immunol. Rev. 260 (2014), 35–49.
17. Gaboriau-Routhiau, V., Rakotobe, S., Lécuyer, E., Mulder, I., Lan, A., Bridonneau, C., Rochet, V., Pisi, A., De Paepe, M., Brandi, G., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31 (2009), 677–689.
18. Geijtenbeek, T.B., Gringhuis, S.I., C-type lectin receptors in the control of T helper cell differentiation. Nat. Rev. Immunol. 16 (2016), 433–448.
19. González-Peña, D., Dudzik, D., García, A., Ancos, B., Barbas, C., Sánchez-Moreno, C., Metabolomic fingerprinting in the comprehensive study of liver changes associated with onion supplementation in hypercholesterolemic wistar rats. Int. J. Mol. Sci., 18, 2017, 18.
20. Goodyear, A.W., Kumar, A., Dow, S., Ryan, E.P., Optimization of murine small intestine leukocyte isolation for global immune phenotype analysis. J. Immunol. Methods 405 (2014), 97–108.
21. Helft, J., Böttcher, J., Chakravarty, P., Zelenay, S., Huotari, J., Schraml, B.U., Goubau, D., Reis e Sousa, C., GM-CSF mouse bone marrow cultures comprise a heterogeneous population of CD11c(+)MHCII(+) macrophages and dendritic cells. Immunity 42 (2015), 1197–1211.
22. Hirota, K., Turner, J.E., Villa, M., Duarte, J.H., Demengeot, J., Steinmetz, O.M., Stockinger, B., Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat. Immunol. 14 (2013), 372–379.
23. Honda, K., Littman, D.R., The microbiota in adaptive immune homeostasis and disease. Nature 535 (2016), 75–84.
24. Hu, W., Troutman, T.D., Edukulla, R., Pasare, C., Priming microenvironments dictate cytokine requirements for T helper 17 cell lineage commitment. Immunity 35 (2011), 1010–1022.
25. Iborra, S., Sancho, D., Signalling versatility following self and non-self sensing by myeloid C-type lectin receptors. Immunobiology 220 (2015), 175–184.
26. Iborra, S., Izquierdo, H.M., Martínez-López, M., Blanco-Menéndez, N., Reis e Sousa, C., Sancho, D., The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J. Clin. Invest. 122 (2012), 1628–1643.
27. Iborra, S., Martínez-López, M., Cueto, F.J., Conde-Garrosa, R., Del Fresno, C., Izquierdo, H.M., Abram, C.L., Mori, D., Campos-Martín, Y., Reguera, R.M., et al. Leishmania uses mincle to target an inhibitory ITAM signaling pathway in dendritic cells that dampens adaptive immunity to infection. Immunity 45 (2016), 788–801.
28. Iida, N., Dzutsev, A., Stewart, C.A., Smith, L., Bouladoux, N., Weingarten, R.A., Molina, D.A., Salcedo, R., Back, T., Cramer, S., et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342 (2013), 967–970.
29. Ivanov, I.I., McKenzie, B.S., Zhou, L., Tadokoro, C.E., Lepelley, A., Lafaille, J.J., Cua, D.J., Littman, D.R., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126 (2006), 1121–1133.
30. Ivanov, I.I., Frutos, Rde.L., Manel, N., Yoshinaga, K., Rifkin, D.B., Sartor, R.B., Finlay, B.B., Littman, D.R., Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4 (2008), 337–349.
31. Ivanov, I.I., Atarashi, K., Manel, N., Brodie, E.L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K.C., Santee, C.A., Lynch, S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139 (2009), 485–498.
32. Klose, C.S., Artis, D., Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat. Immunol. 17 (2016), 765–774.
33. + conventional dendritic cells induce T follicular helper cell-dependent antibody responses. Sci. Immunol., 2, 2017, 2.
34. Kruglov, A.A., Grivennikov, S.I., Kuprash, D.V., Winsauer, C., Prepens, S., Seleznik, G.M., Eberl, G., Littman, D.R., Heikenwalder, M., Tumanov, A.V., Nedospasov, S.A., Nonredundant function of soluble LTα3 produced by innate lymphoid cells in intestinal homeostasis. Science 342 (2013), 1243–1246.
35. Lécuyer, E., Rakotobe, S., Lengliné-Garnier, H., Lebreton, C., Picard, M., Juste, C., Fritzen, R., Eberl, G., McCoy, K.D., Macpherson, A.J., et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 40 (2014), 608–620.
36. LeibundGut-Landmann, S., Gross, O., Robinson, M.J., Osorio, F., Slack, E.C., Tsoni, S.V., Schweighoffer, E., Tybulewicz, V., Brown, G.D., Ruland, J., Reis e Sousa, C., Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8 (2007), 630–638.
37. Lochner, M., Ohnmacht, C., Presley, L., Bruhns, P., Si-Tahar, M., Sawa, S., Eberl, G., Microbiota-induced tertiary lymphoid tissues aggravate inflammatory disease in the absence of RORgamma t and LTi cells. J. Exp. Med. 208 (2011), 125–134.
38. Longman, R.S., Diehl, G.E., Victorio, D.A., Huh, J.R., Galan, C., Miraldi, E.R., Swaminath, A., Bonneau, R., Scherl, E.J., Littman, D.R., CX₃CR1⁺ mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J. Exp. Med. 211 (2014), 1571–1583.
39. Marakalala, M.J., Vautier, S., Potrykus, J., Walker, L.A., Shepardson, K.M., Hopke, A., Mora-Montes, H.M., Kerrigan, A., Netea, M.G., Murray, G.I., et al. Differential adaptation of Candida albicans in vivo modulates immune recognition by dectin-1. PLoS Pathog., 9, 2013, e1003315.
40. Mastrangelo, A., Ferrarini, A., Rey-Stolle, F., García, A., Barbas, C., From sample treatment to biomarker discovery: A tutorial for untargeted metabolomics based on GC-(EI)-Q-MS. Anal. Chim. Acta 900 (2015), 21–35.
41. McGeachy, M.J., Bak-Jensen, K.S., Chen, Y., Tato, C.M., Blumenschein, W., McClanahan, T., Cua, D.J., TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8 (2007), 1390–1397.
42. Nakamoto, N., Amiya, T., Aoki, R., Taniki, N., Koda, Y., Miyamoto, K., Teratani, T., Suzuki, T., Chiba, S., Chu, P.S., et al. Commensal lactobacillus controls immune tolerance during acute liver injury in mice. Cell Rep. 21 (2017), 1215–1226.
43. Persson, E.K., Uronen-Hansson, H., Semmrich, M., Rivollier, A., Hägerbrand, K., Marsal, J., Gudjonsson, S., Håkansson, U., Reizis, B., Kotarsky, K., Agace, W.W., IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38 (2013), 958–969.
44. Pierantonelli, I., Rychlicki, C., Agostinelli, L., Giordano, D.M., Gaggini, M., Fraumene, C., Saponaro, C., Manghina, V., Sartini, L., Mingarelli, E., et al. Author Correction: Lack of NLRP3-inflammasome leads to gut-liver axis derangement, gut dysbiosis and a worsened phenotype in a mouse model of NAFLD. Sci. Rep., 7, 2017, 17568.
45. Plant, L., Conway, P., Association of Lactobacillus spp. with Peyer's patches in mice. Clin. Diagn. Lab. Immunol. 8 (2001), 320–324.
46. 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.
47. Revy, P., Muto, T., Levy, Y., Geissmann, F., Plebani, A., Sanal, O., Catalan, N., Forveille, M., Dufourcq-Labelouse, R., Gennery, A., et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102 (2000), 565–575.
48. Rios, D., Wood, M.B., Li, J., Chassaing, B., Gewirtz, A.T., Williams, I.R., Antigen sampling by intestinal M cells is the principal pathway initiating mucosal IgA production to commensal enteric bacteria. Mucosal Immunol. 9 (2016), 907–916.
49. Saijo, S., Ikeda, S., Yamabe, K., Kakuta, S., Ishigame, H., Akitsu, A., Fujikado, N., Kusaka, T., Kubo, S., Chung, S.H., et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32 (2010), 681–691.
50. Sano, T., Huang, W., Hall, J.A., Yang, Y., Chen, A., Gavzy, S.J., Lee, J.-Y., Ziel, J.W., Miraldi, E.R., Domingos, A.I., et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid a to promote local effector Th17 responses. Cell 163 (2015), 381–393.
51. Sanos, S.L., Bui, V.L., Mortha, A., Oberle, K., Heners, C., Johner, C., Diefenbach, A., RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10 (2009), 83–91.
52. Sato, A., Hashiguchi, M., Toda, E., Iwasaki, A., Hachimura, S., Kaminogawa, S., CD11b+ Peyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J. Immunol. 171 (2003), 3684–3690.
53. Satoh-Takayama, N., Vosshenrich, C.A., Lesjean-Pottier, S., Sawa, S., Lochner, M., Rattis, F., Mention, J.J., Thiam, K., Cerf-Bensussan, N., Mandelboim, O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29 (2008), 958–970.
54. Satpathy, A.T., Briseño, C.G., Lee, J.S., Ng, D., Manieri, N.A., Kc, W., Wu, X., Thomas, S.R., Lee, W.L., Turkoz, M., et al. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat. Immunol. 14 (2013), 937–948.
55. Sawa, S., Cherrier, M., Lochner, M., Satoh-Takayama, N., Fehling, H.J., Langa, F., Di Santo, J.P., Eberl, G., Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330 (2010), 665–669.
56. Schlitzer, A., McGovern, N., Teo, P., Zelante, T., Atarashi, K., Low, D., Ho, A.W.S., See, P., Shin, A., Wasan, P.S., et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38 (2013), 970–983.
57. Sengupta, R., Altermann, E., Anderson, R.C., McNabb, W.C., Moughan, P.J., Roy, N.C., The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators Inflamm., 2013, 2013, 237921.
58. Shah, S., Nagata, M., Yamasaki, S., Williams, S.J., Total synthesis of a cyclopropane-fatty acid α-glucosyl diglyceride from Lactobacillus plantarum and identification of its ability to signal through Mincle. Chem. Commun. (Camb.) 52 (2016), 10902–10905.
59. Shaw, M.H., Kamada, N., Kim, Y.G., Núñez, G., Microbiota-induced IL-1β, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J. Exp. Med. 209 (2012), 251–258.
60. Sonnenberg, G.F., Monticelli, L.A., Alenghat, T., Fung, T.C., Hutnick, N.A., Kunisawa, J., Shibata, N., Grunberg, S., Sinha, R., Zahm, A.M., et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336 (2012), 1321–1325.
61. Sun, Z., Unutmaz, D., Zou, Y.R., Sunshine, M.J., Pierani, A., Brenner-Morton, S., Mebius, R.E., Littman, D.R., Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288 (2000), 2369–2373.
62. Talukdar, S., Oh, D.Y., Bandyopadhyay, G., Li, D., Xu, J., McNelis, J., Lu, M., Li, P., Yan, Q., Zhu, Y., et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat. Med. 18 (2012), 1407–1412.
63. Vaishnava, S., Yamamoto, M., Severson, K.M., Ruhn, K.A., Yu, X., Koren, O., Ley, R., Wakeland, E.K., Hooper, L.V., The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334 (2011), 255–258.
64. Veal, D.A., Deere, D., Ferrari, B., Piper, J., Attfield, P.V., Fluorescence staining and flow cytometry for monitoring microbial cells. J. Immunol. Methods 243 (2000), 191–210.
65. Weiss, G., Maaetoft-Udsen, K., Stifter, S.A., Hertzog, P., Goriely, S., Thomsen, A.R., Paludan, S.R., Frøkiær, H., MyD88 drives the IFN-β response to Lactobacillus acidophilus in dendritic cells through a mechanism involving IRF1, IRF3, and IRF7. J. Immunol. 189 (2012), 2860–2868.
66. Wells, C.A., Salvage-Jones, J.A., Li, X., Hitchens, K., Butcher, S., Murray, R.Z., Beckhouse, A.G., Lo, Y.-L.-S., Manzanero, S., Cobbold, C., et al. The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J. Immunol. 180 (2008), 7404–7413.
67. Whitney, P.G., Bär, E., Osorio, F., Rogers, N.C., Schraml, B.U., Deddouche, S., LeibundGut-Landmann, S., Reis e Sousa, C., Syk signaling in dendritic cells orchestrates innate resistance to systemic fungal infection. PLoS Pathog., 10, 2014, e1004276.
68. Zeng, M.Y., Cisalpino, D., Varadarajan, S., Hellman, J., Warren, H.S., Cascalho, M., Inohara, N., Núñez, G., Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44 (2016), 647–658.