Complement activation promotes colitis-associated carcinogenesis through activating intestinal IL-1β/IL-17A axis

Mucosal Immunology

Volumn 8, Issue 6, 2015, Pages 1275-1284

  Ning, C ^a,b   Li, Y Y ^c   Wang, Y ^a   Han, G C ^a,b   Wang, R X ^a,b   Xiao, H ^a,b   Li, X Y ^a   Hou, C M ^a   Ma, Y F ^c   Sheng, D S ^d   Shen, B F ^a,b   Feng, J N ^a,b   Guo, R F ^e   Li, Y ^a,b   Chen, G J ^a,b  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b State Key Laboratory of Toxicology and Medical Countermeasures   (China)

^c HENAN UNIVERSITY   (China)

^d Beijing 307 Hospital   (China)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5A RECEPTOR; DEXTRAN SULFATE; INTERLEUKIN 17; INTERLEUKIN 1BETA; IL1B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; COLITIS; COLON CARCINOGENESIS; COLORECTAL CANCER; COMPLEMENT ACTIVATION; COMPLEMENT DEFICIENCY; COMPLEMENT DEPOSITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DOWN REGULATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CARCINOGENESIS; CELL TRANSFORMATION; COLORECTAL TUMOR; DISEASE COURSE; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INTESTINE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CARCINOGENESIS; CELL TRANSFORMATION, NEOPLASTIC; COLITIS; COLORECTAL NEOPLASMS; COMPLEMENT ACTIVATION; DISEASE PROGRESSION; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTESTINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84937859021     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.18     Document Type: Article

References (46)

1. Mantovani A., Allavena P., Sica A., & Balkwill F. Cancer-related inflammation. Nature 454, 436-444 (2008
2. Itzkowitz S.H., & Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G7-G17 (2004
3. Eaden J.A., Abrams K.R., & Mayberry J.F. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48, 526-535 (2001
4. Popivanova B.K., et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Invest. 118, 560-570 (2008
5. Grivennikov S., et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15, 103-113 (2009
6. Matsumoto S., et al. Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model. J. Immunol. 184, 1543-1551 (2010
7. Hyun Y.S., et al. Role of IL-17A in the development of colitis-associated cancer. Carcinogenesis 33, 931-936 (2012
8. Wang Y., et al. Neutrophil infiltration favors colitis-associated tumorigenesis by activating the interleukin-1 (IL-1)/IL-6 axis. Mucosal Immunol. 7, 1106-1115 (2014
9. Zhang J., Fu S., Sun S., Li Z., & Guo B. Inflammasome activation has an important role in the development of spontaneous colitis. Mucosal Immunol. 7, 1139-1150 (2014
10. Scheinin T., et al. Decreased expression of protectin (CD59) in gut epithelium in ulcerative colitis and Crohn's disease. Hum. Pathol. 30, 1427-1430 (1999
11. Berstad A.E., & Brandtzaeg P. Expression of cell membrane complement regulatory glycoproteins along the normal and diseased human gastrointestinal tract. Gut 42, 522-529 (1998
12. Lin F., Spencer D., Hatala D.A., Levine A.D., & Medof M.E. Decayaccelerating factor deficiency increases susceptibility to dextran sulfate sodium-induced colitis: role for complement in inflammatory bowel disease. J. Immunol. 172, 3836-3841 (2004
13. Lu F., Fernandes S.M., & Davis A.E. 3rd The role of the complement and contact systems in the dextran sulfate sodium-induced colitis model: the effect of C1 inhibitor in inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G878-G883 (2010
14. Woodruff T.M., et al. A potent human C5a receptor antagonist protects against disease pathology in a rat model of inflammatory bowel disease. J. Immunol. 171, 5514-5520 (2003
15. Chen G., et al. Blockade of complement activation product C5a activity using specific antibody attenuates intestinal damage in trinitrobenzene sulfonic acid induced model of colitis. Lab. Invest. 91, 472-483 (2011
16. Johswich K., et al. Role of the C5a receptor (C5aR) in acute and chronic dextran sulfate-induced models of inflammatory bowel disease. Inflam. Bowel Dis. 15, 1812-1823 (2009
17. Guo R.F., et al. Neutrophil C5a receptor and the outcome in a rat model of sepsis. FASEB J. 17, 1889-1891 (2003
18. Coccia M., et al. IL-1beta mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4 Th17 cells. J. Exp. Med. 209, 1595-1609 (2012
19. Shaw M.H., Kamada N., Kim Y.G., & Nunez G. Microbiota-induced IL-1beta, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J. Exp. Med. 209, 251-258 (2012
20. Issuree P.D., Pushparaj P.N., Pervaiz S., & Melendez A.J. Resveratrol attenuates C5a-induced inflammatory responses in vitro and in vivo by inhibiting phospholipase D and sphingosine kinase activities. FASEB J. 23, 2412-2424 (2009
21. Markiewski M.M., et al. Modulation of the antitumor immune response by complement. Nat. Immunol. 9, 1225-1235 (2008
22. Corrales L., et al. Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression. J. Immunol. 189, 4674-4683 (2012
23. Nozaki M., et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc. Natl. Acad. Sci. USA 103, 2328-2333 (2006
24. Cao Q., McIsaac S.M., & Stadnyk A.W. Human colonic epithelial cells detect and respond to C5a via apically expressed C5aR through the ERK pathway. American journal of physiology. Cell Physiol. 302, C1731-C1740 (2012
25. Schauer I.G., et al. Interleukin-1beta promotes ovarian tumorigenesis through a p53/NF-kappaB-mediated inflammatory response in stromal fibroblasts. Neoplasia 15, 409-420 (2013
26. Liu Q., et al. Interleukin-1beta promotes skeletal colonization and progression of metastatic prostate cancer cells with neuroendocrine features. Cancer Res. 73, 3297-3305 (2013
27. Huang Q., et al. IL-1beta-induced activation of p38 promotes metastasis in gastric adenocarcinoma via upregulation of AP-1/c-fos, MMP2 and MMP9. Mol. Cancer 13, 18 (2014
28. Reinecker H.C., et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin. Exp. Immunol. 94, 174-181 (1993
29. McAlindon M.E., Hawkey C.J., & Mahida Y.R. Expression of interleukin 1 beta and interleukin 1 beta converting enzyme by intestinal macrophages in health and inflammatory bowel disease. Gut 42, 214-219 (1998
30. Okayasu I., et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98, 694-702 (1990
31. McCall R.D., et al. Tissue interleukin 1 and interleukin-1 receptor antagonist expression in enterocolitis in resistant and susceptible rats. Gastroenterology 106, 960-972 (1994
32. Siegmund B., Lehr H.A., Fantuzzi G., & Dinarello C.A. IL-1betaconverting enzyme (caspase-1) in intestinal inflammation. Proc. Natl. Acad. Sci. USA 98, 13249-13254 (2001
33. Maeda S., et al. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 307, 734-738 (2005
34. Wu S., et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17Tcell responses. Nat. Med. 15, 1016-1022 (2009
35. Dieleman L.A., et al. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107, 1643-1652 (1994
36. Wu P., et al. gammadeltaT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40, 785-800 (2014
37. Katayama M., et al. Neutrophils are essential as a source of IL-17 in the effector phase of arthritis. PLoS One 8, e62231 (2013
38. Ferretti S., Bonneau O., Dubois G.R., Jones C.E., & Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170, 2106-2112 (2003
39. Li L., et al. IL-17 produced by neutrophils regulates IFN-gamma-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J. Clin. Invest. 120, 331-342 (2010
40. Hoshino A., et al. MPO-ANCA induces IL-17 production by activated neutrophils in vitro via classical complement pathway-dependent manner. J. Autoimmun. 31, 79-89 (2008
41. Bosmann M., Sarma J.V., Atefi G., Zetoune F.S., & Ward P.A. Evidence for anti-inflammatory effects of C5a on the innate IL-17A/IL-23 axis. FASEB J. 26, 1640-1651 (2012
42. Kirchberger S., et al. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 210, 917-931 (2013
43. Longman R.S., et al. CX(3)CR1 mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J. Exp. Med. 211, 1571-1583 (2014
44. Kolls J.K., & Linden A. Interleukin-17 family members and inflammation. Immunity 21, 467-476 (2004
45. Grivennikov S.I., et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491, 254-258 (2012
46. Wirtz S., Neufert C., Weigmann B., & Neurath M.F. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541-546 (2007