CD103+CD11b+ dendritic cells induce Th17 T cells in Muc2-deficient mice with extensively spread colitis

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Wenzel, Ulf A ^a   Jonstrand, Caroline ^b   Hansson, Gunnar C ^b   Wick, Mary Jo ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; MUCIN 2; TUMOR NECROSIS FACTOR ALPHA; ALPHA E INTEGRINS; ALPHA INTEGRIN; AUTACOID; CD11 ANTIGEN; LEUKOCYTE ANTIGEN; MUC2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; COLITIS; CYTOKINE PRODUCTION; DENDRITIC CELL; DESCENDING COLON; EX VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PHAGOCYTE; TH1 CELL; TH17 CELL; ANIMAL; C57BL MOUSE; CELL COUNT; CELL PROLIFERATION; COLON; DEFICIENCY; IMMUNOLOGY; METABOLISM; NEUTROPHIL; PATHOLOGY; RECTUM;

ANIMALIA; MUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11; ANTIGENS, CD11B; CELL COUNT; CELL PROLIFERATION; COLITIS; COLON; CYTOKINES; DENDRITIC CELLS; INFLAMMATION MEDIATORS; INTEGRIN ALPHA CHAINS; LYMPHOCYTE SUBSETS; MICE, INBRED C57BL; MUCIN-2; NEUTROPHILS; RECTUM; TH17 CELLS;

EID: 84938709278     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130750     Document Type: Article

References (45)

1. Bain CC, Mowat AM (2014) Macrophages in intestinal homeostasis and inflammation. Immunol Rev 260: 102-117. doi: 10.1111/imr.12192 PMID: 24942685
2. - intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells. Mucosal Immunol 8: 327-339. doi: 10.1038/mi.2014.70 PMID: 25138666
3. + T cells with antigen acquired from intestinal epithelial cells. Mucosal Immunol 8: 38-48. doi: 10.1038/mi.2014.40 PMID: 24850430
4. Bain CC, Mowat AM (2011) Intestinal macrophages - specialised adaptation to a unique environment. Eur J Immunol 41: 2494-2498. doi: 10.1002/eji.201141714 PMID: 21952804
5. Maloy KJ, Powrie F (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474: 298-306. doi: 10.1038/nature10208 PMID: 21677746
6. Monteleone I, Platt AM, Jaensson E, Agace WW, Mowat AM (2008) IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur J Immunol 38: 1533-1547. doi: 10.1002/eji.200737909 PMID: 18461564
7. Zigmond E, Bernshtein B, Friedlander G, Walker CR, Yona S, Kim K- W, et al. (2014) Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 40: 720-733. doi: 10.1016/j.immuni.2014.03.012 PMID: 24792913
8. Shouval DS, Biswas A, Goettel JA, McCann K, Conaway E, Redhu NS, et al. (2014) Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40: 706-719. doi: 10.1016/j.immuni.2014.03.011 PMID: 24792912
9. hi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med 209: 139-155. doi: 10.1084/jem.20101387 PMID: 22231304
10. hi monocyte precursors. Mucosal Immunology 6: 498-510. doi: 10.1038/mi.2012.89 PMID: 22990622
11. Tamoutounour S, Henri S, Lelouard H, de Bovis B, de Haar C, van der Woude CJ, et al. (2012) CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur J Immunol 42: 3150-3166. doi: 10.1002/eji.201242847 PMID: 22936024
12. hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37: 1076-1090. doi: 10.1016/j.immuni.2012.08.026 PMID: 23219392
13. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206: 3101-3114. doi: 10.1084/jem.20091925 PMID: 20008524
14. - dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol 6: 104-113. doi: 10.1038/mi.2012.53 PMID: 22718260
15. Bekiaris V, Persson EK, Agace WW (2014) Intestinal dendritic cells in the regulation of mucosal immunity. Immunol Rev 260: 86-101. doi: 10.1111/imr.12194 PMID: 24942684
16. Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, et al. (2009) Origin of the Lamina Propria Dendritic Cell Network. Immunity 31: 513-525. doi: 10.1016/j.immuni.2009.08.010 PMID: 19733489
17. + dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38: 958-969. doi: 10.1016/j.immuni.2013.03.009 PMID: 23664832
18. + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38: 970-983. doi: 10.1016/j.immuni.2013.04.011 PMID: 23706669
19. Welty NE, Staley C, Ghilardi N, Sadowsky MJ, Igyártó BZ, Kaplan DH. (2013) Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism. J Exp Med 210: 2011-2024. doi: 10.1084/jem.20130728 PMID: 24019552
20. Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 105: 15064-15069. doi: 10.1073/pnas.0803124105 PMID: 18806221
21. Johansson MEV, Gustafsson JK, Holmén-Larsson J, Jabbar KS, Xia L, Xu H, et al. (2014) Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 63: 281-291. doi: 10.1136/gutjnl-2012-303207 PMID: 23426893
22. Van der Sluis M, De Koning BAE, De Bruijn ACJM, Velcich A, Meijerink JPP, Van Goudoever JB, et al. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131: 117-129. PMID: 16831596
23. Wenzel UA, Magnusson MK, Rydström A, Jonstrand C, Hengst J, Johansson MEV, et al. (2014) Spontaneous colitis in Muc2-deficient mice reflects clinical and cellular features of active ulcerative colitis. PLoS ONE 9: e100217. doi: 10.1371/journal.pone.0100217 PMID: 24945909
24. Langlet C, Tamoutounour S, Henri S, Luche H, Ardouin L, Grégoir C, et al. (2012) CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 188: 1751-1760. doi: 10.4049/jimmunol.1102744 PMID: 22262658
25. Guilliams M, Bruhns P, Saeys Y, Hammad H, Lambrecht BN (2014) The function of Fcaγ receptors in dendritic cells and macrophages. Nat Rev Immunol 14: 94-108. doi: 10.1038/nri3582 PMID: 24445665
26. + dendritic cells. J Immunol 171: 2797-2803. PMID: 12960300
27. Masterson JC, McNamee EN, Fillon SA, Hosford L, Harris R, Fernando SD, et al. (2014) Eosinophilmediated signalling attenuates inflammatory responses in experimental colitis. Gut doi: 10.1136/gutjnl-2014-306998
28. Mowat AM, Agace WW (2014) Regional specialization within the intestinal immune system. Nat Rev Immunol 14: 667-685. doi: 10.1038/nri3738 PMID: 25234148
29. Dent G, Loweth SC, Hasan AM, Leslie FM (2014) Synergic production of neutrophil chemotactic activity by colonic epithelial cells and eosinophils. Immunobiology 219: 793-797. doi: 10.1016/j.imbio.2014.06.008 PMID: 25097152
30. Denning TL, Norris BA, Medina-Contreras O, Manicassamy S, Geem D, Madan R, et al. (2011) Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J Immunol 187: 733-747. doi: 10.4049/jimmunol.1002701 PMID: 21666057
31. Hu W, Troutman TD, Edukulla R, Pasare C (2011) Priming microenvironments dictate cytokine requirements for T helper 17 cell lineage commitment. Immunity 35: 1010-1022. doi: 10.1016/j.immuni.2011.10.013 PMID: 22137454
32. Shaw MH, Kamada N, Kim Y- G, Núñez G (2012) 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: 251-258. doi: 10.1084/jem.20111703 PMID: 22291094
33. Gutcher I, Donkor MK, Ma Q, Rudensky AY, Flavell RA, Li MO. (2011) Autocrine transforming growth factor-β1 promotes in vivo Th17 cell differentiation. Immunity 34: 396-408. doi: 10.1016/j.immuni.2011.03.005 PMID: 21435587
34. + T cells in colitis. JI 189: 1243-1252.
35. Manicassamy S, Reizis B, Ravindran R, Nakaya H, Salazar-Gonzalez RM, Wang Y-C, et al. (2010) Activation of β-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329: 849-853. doi: 10.1126/science.1188510 PMID: 20705860
36. Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU, Chen K, et al. (2013) Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342: 447-453. doi: 10.1126/science.1237910 PMID: 24072822
37. Ohman L, Dahlén R, Isaksson S, Sjöling A, Wick MJ, Sjövall H, et al. (2013) Serum IL-17A in newly diagnosed treatment-naive patients with ulcerative colitis reflects clinical disease severity and predicts the course of disease. Inflamm Bowel Dis 19: 2433-2439. doi: 10.1097/MIB.0b013e3182a563cb PMID: 23966065
38. Jiang W, Su J, Zhang X, Cheng X, Zhou J, Shi R, et al. (2014) Elevated levels of Th17 cells and Th17-related cytokines are associated with disease activity in patients with inflammatory bowel disease. Inflamm res 63: 943-950. doi: 10.1007/s00011-014-0768-7 PMID: 25129403
39. Rodríguez D, Silvera R, Carrio R, Nadji M, Caso R, Rodríguez G, et al. (2013) Tumor microenvironment profoundly modifies functional status of macrophages: peritoneal and tumor-associated macrophages are two very different subpopulations. Cell Immunol 283: 51-60. doi: 10.1016/j.cellimm.2013.06.008 PMID: 23850963
40. Galdiero MR, Bonavita E, Barajon I, Garlanda C, Mantovani A, Jaillon S. (2013) Tumor associated macrophages and neutrophils in cancer. Immunobiology 218: 1402-1410. doi: 10.1016/j.imbio.2013.06.003 PMID: 23891329
41. Capece D, Fischietti M, Verzella D, Gaggiano A, Cicciarelli G, Tessitore A, et al. (2013) The inflammatory microenvironment in hepatocellular carcinoma: a pivotal role for tumor-associated macrophages. Biomed Res Int 2013: 187204. doi: 10.1155/2013/187204 PMID: 23533994
42. Velcich A, Yang W, Heyer J, Fragale A, Nicholas C, Viani S, et al. (2002) Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295: 1726-1729. PMID: 11872843
43. + dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 202: 1063-1073. PMID: 16216890
44. Flach C- F, Mozer M, Sundquist M, Holmgren J, Raghavan S (2012) Mucosal vaccination increases local chemokine production attracting immune cells to the stomach mucosa of Helicobacter pylori infected mice. Vaccine 30: 1636-1643. doi: 10.1016/j.vaccine.2011.12.111 PMID: 22230589
45. Rydström A, Wick MJ (2007) Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection. J Immunol 178: 5789-5801. PMID: 17442963