Interleukin-17 induces an atypical M2-Like macrophage subpopulation that regulates intestinal inflammation

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Nishikawa, Kenichiro ^a   Seo, Naohiro ^a   Torii, Mie ^a,c   Ma, Nei ^b   Muraoka, Daisuke ^a   Tawara, Isao ^a   Masuya, Masahiro ^a   Tanaka, Kyosuke ^a   Takei, Yoshiyuki ^a   Shiku, Hiroshi ^a   Katayama, Naoyuki ^a   Kato, Takuma ^a  

^a MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SUZUKA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; CD11B ANTIGEN; CLODRONIC ACID; CYCLOOXYGENASE 2; DEXTRAN SULFATE; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 17; LIPOSOME; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN 6C; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 2; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ENTERITIS; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IMMUNOREGULATION; KNOCKOUT MOUSE; LAMINA PROPRIA; LEUKOCYTE; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; WILD TYPE; WOUND HEALING; ANIMAL; CELL COUNT; CELL DIFFERENTIATION; CHEMICALLY INDUCED; COLITIS; CYTOLOGY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHENOTYPE; SEVERITY OF ILLNESS INDEX;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, LY; CELL COUNT; CELL DIFFERENTIATION; COLITIS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERLEUKIN-17; MACROPHAGES; MICE; MICE, KNOCKOUT; MONOCYTES; PHENOTYPE; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; TRANSCRIPTION FACTORS;

EID: 84907478536     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108494     Document Type: Article

References (43)

1. Kaser A, Zeissig S, Blumberg RS (2010) Inflammatory bowel disease. Annu Rev Immunol 28: 573-621.
2. Strober W, Fuss IJ, Mannon P (2007) The fundamental basis of inflammatory bowel disease. J Clin Invest 117: 514-521.
3. Iwakura Y, Ishigame H, Saijo S, Nakae S (2011) Functional specialization of interleukin-17 family members. Immunity 34: 149-162.
4. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, et al. (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52: 65-70.
5. Hue S, Ahern PP, Buonocore S, Kullberg MC, Cua DJ, et al. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med 203: 2473-2483.
6. Tang C, Iwakura Y (2012) IL-23 in colitis: targeting the progenitors. Immunity 37: 957-959.
7. Hundorfean G, Neurath MF, Mudter J (2012) Functional relevance of T helper 17 (Th17) cells and the IL-17 cytokine family in inflammatory bowel disease. Inflamm Bowel Dis 18: 180-186.
8. Zhang Z, Zheng M, Bindas J, Schwarzenberger P, Kolls JK (2006) Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm Bowel Dis 12: 382-388.
9. Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, et al. (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464: 1371-1375.
10. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, et al. (2009) CD4 + regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326: 986-991.
11. O'Connor W, Kamanaka M, Booth CJ, Town T, Nakae S, et al. (2009) A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 10: 603-609.
12. Ito R, Kita M, Shin-Ya M, Kishida T, Urano A, et al. (2008) Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice. Biochem Biophys Res Commun 377: 12-16.
13. Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y (2004) Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol 110: 55-62.
14. Yang XO, Chang SH, Park H, Nurieva RI, Shah B, et al. (2008) Regulation of inflammatory responses by IL-17F. J Exp Med 205: 1063-1075.
15. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, et al. (2002) Antigenspecific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387.
16. Schepp-Berglind J, Atkinson C, Elvington M, Qiao F, Mannon P, et al. (2012) Complement-dependent injury and protection in a murine model of acute dextran sulfate sodium-induced colitis. J Immunol 188: 6309-6318.
17. Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, et al. (2009) Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31: 502-512.
18. Wang L, Toda M, Saito K, Hori T, Horii T, et al. (2008) Post-immune UV irradiation induces Tr1-like regulatory T cells that suppress humoral immune responses. Int Immunol 20: 57-70.
19. Torii M, Wang L, Ma N, Saito K, Hori T, et al. (2010) Thioredoxin suppresses airway inflammation independently of systemic Th1/Th2 immune modulation. Eur J Immunol 40: 787-796.
20. Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
21. Monteleone I, Rizzo A, Sarra M, Sica G, Sileri P, et al. (2011) Aryl Hydrocarbon Receptor-Induced Signals Up-regulate IL-22 Production and Inhibit Inflammation in the Gastrointestinal Tract. Gastroenterology 141: 237-248. e231.
22. Hansell CAH, Hurson CE, Nibbs RJB (2011) DARC and D6: silent partners in chemokine regulation? Immunol Cell Biol 89: 197-206.
23. Zigmond E, Jung S (2013) Intestinal macrophages: well educated exceptions from the rule. Trends Immunol 34: 162-168.
24. Tamoutounour S, Henri S, Lelouard H, de Bovis B, de Haar C, 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.
25. Rivollier A, He J, Kole A, Valatas V, Kelsall BL (2012) Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med 209: 139-155.
26. Lawrence T, Natoli G (2011) Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11: 750-761.
27. Perry DG, Martin WJ (1995) Fluorescent liposomes as quantitative markers of phagocytosis by alveolar macrophages. J Immunol Methods 181: 269-285.
28. Leidi M, Gotti E, Bologna L, Miranda E, Rimoldi M, et al. (2009) M2 macrophages phagocytose rituximab-opsonized leukemic targets more efficiently than m1 cells in vitro. J Immunol 182: 4415-4422.
29. Targan SR, Feagan BG, Vermeire S, Panaccione R, Melmed GY, et al. (2012) Mo2083 A Randomized, Double-Blind, Placebo-Controlled Study to Evaluate the Safety, Tolerability, and Efficacy of AMG 827 in Subjects With Moderate to Severe Crohn's Disease. Gastroenterology 143: e26.
30. Hueber W, Sands BE, Lewitzky S, Vandemeulebroecke M, Reinisch W, et al. (2012) Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut.
31. Zizzo G, Hilliard BA, Monestier M, Cohen PL (2012) Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J Immunol 189: 3508-3520.
32. Kostadinova FI, Baba T, Ishida Y, Kondo T, Popivanova BK, et al. (2010) Crucial involvement of the CX3CR1-CX3CL1 axis in dextran sulfate sodiummediated acute colitis in mice. J Leukocyte Biol 88: 133-143.
33. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M (2013) Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 229: 176-185.
34. Vos ACW, Wildenberg ME, Duijvestein M, Verhaar AP, Van Den Brink GR, et al. (2011) Anti-tumor necrosis factor-A antibodies induce regulatory macrophages in an Fc region-dependent manner. Gastroenterology 140: 221-230.
35. Kayama H, Ueda Y, Sawa Y, Jeon SG, Ma JS, et al. (2012) Intestinal CX3C chemokine receptor 1(high) (CX3CR1(high)) myeloid cells prevent T-celldependent colitis. Proc Natl Acad Sci U S A 109: 5010-5015.
36. Qualls JE, Kaplan AM, Van Rooijen N, Cohen DA (2006) Suppression of experimental colitis by intestinal mononuclear phagocytes. J Leukocyte Biol 80: 802-815.
37. Medina-Contreras O, Geem D, Laur O, Williams IR, Lira SA, et al. (2011) CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J Clin Invest 121: 4787-4795.
38. Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, et al. (2013) Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol 6: 498-510.
39. Grainger JR, Wohlfert EA, Fuss IJ, Bouladoux N, Askenase MH, et al. (2013) Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med 19: 713-721.
40. Nair MG, Cochrane DW, Allen JE (2003) Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol Lett 85: 173-180.
41. Chen GH, Olszewski MA, McDonald RA, Wells JC, Paine R 3rd, et al. (2007) Role of granulocyte macrophage colony-stimulating factor in host defense against pulmonary Cryptococcus neoformans infection during murine allergic bronchopulmonary mycosis. Am J Pathol 170: 1028-1040.
42. Liu L, Ge D, Ma L, Mei J, Liu S, et al. (2012) Interleukin-17 and prostaglandin E2 are involved in formation of an M2 macrophage-dominant microenvironment in lung cancer. J Thorac Oncol 7: 1091-1100.
43. Zizzo G, Cohen PL (2013) IL-17 stimulates differentiation of human antiinflammatory macrophages and phagocytosis of apoptotic neutrophils in response to IL-10 and glucocorticoids. J Immunol 190: 5237-5246.