The C5a receptor antagonist PMX205 ameliorates experimentally induced colitis associated with increased IL-4 and IL-10

British Journal of Pharmacology

Volumn 168, Issue 2, 2013, Pages 488-501

  Jain, U ^a   Woodruff, T M ^b   Stadnyk, Andrew ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

anaphylatoxin; C5a; CD88; complement; DSS; IBD; PMX205

Indexed keywords

ARGINASE 1; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; CXCL2 CHEMOKINE; DEXTRAN SULFATE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; PMX 205; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; COLITIS; COLON; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIARRHEA; DRUG EFFICACY; INFLAMMATION; MOUSE; NONHUMAN; OCCULT BLOOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; WEIGHT REDUCTION; WESTERN BLOTTING;

ANIMALS; ANTI-INFLAMMATORY AGENTS; COLITIS; COMPLEMENT C3A; COMPLEMENT C5A; CYTOKINES; DEXTRAN SULFATE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDES, CYCLIC; RECEPTOR, ANAPHYLATOXIN C5A;

EID: 84871575617     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02183.x     Document Type: Article

References (52)

1. Alexander SPH, Mathie A, Peters JA, (2011). Guide to receptors and channels (GRAC), 5th edn. Br J Pharmacol 164 (Suppl. 1): S1-S324.
2. Arumugam TV, Woodruff TM, Stocks SZ, Proctor LM, Pollitt S, Shiels IA, et al,. (2004). Protective effect of a human C5a receptor antagonist against hepatic ischaemia-reperfusion injury in rats. J Hepatol 40: 934-941.
3. Baelder R, Fuchs B, Bautsch W, Zwirner J, Köhl J, Hoymann HG, et al,. (2005). Pharmacological targeting of anaphylatoxin receptors during the effector phase of allergic asthma suppresses airway hyperresponsiveness and airway inflammation. J Immunol 174: 783-789.
4. Chen G, Yang Y, Gao X, Dou Y, Wang H, Han G, et al,. (2011). 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.
5. Czermak BJ, Sarma V, Pierson CL, Warner RL, Huber-Lang M, Bless NM, et al,. (1999). Protective effects of C5a blockade in sepsis. Nat Med 5: 788-792.
6. Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, Elson CO, (1994). Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107: 1643-1652.
7. DiScipio RG, Schraufstatter IU, Sikora L, Zuraw BL, Sriramarao P, (2006). C5a mediates secretion and activation of matrix metalloproteinase 9 from human eosinophils and neutrophils. Int Immunopharmacol 6: 1109-1118.
8. Ehrnthaller C, Ignatius A, Gebhard F, Huber-Lang M, (2011). New insights of an old defense system: structure, function, and clinical relevance of the complement system. Mol Med 17: 317-329.
9. Fonseca MI, Ager RR, Chu SH, Yazan O, Sanderson SD, LaFerla FM, et al,. (2009). Treatment with a C5aR antagonist decreases pathology and enhances behavioral performance in murine models of Alzheimer's disease. J Immunol 183: 1375-1383.
10. Gordon S, (2003). Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
11. Halstensen TS, Brandtzaeg P, (1991). Local complement activation in inflammatory bowel disease. Immunol Res 10: 485-492.
12. Hanauer SB, (2006). Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis 12: S3-S9.
13. Hawlisch H, Wills-Karp M, Karp CL, Köhl J, (2004). The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol Immunol 41: 123-131.
14. Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen M, Beck PL, et al,. (2010). In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138: 1395-1405.
15. Johswich K, Martin M, Bleich A, Kracht M, Dittrich-Breiholz O, Gessner JE, et al,. (2009). Role of the C5a receptor (C5aR) in acute and chronic dextran sulfate-induced models of inflammatory bowel disease. Inflamm Bowel Dis 15: 1812-1823.
16. Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W, (1993). Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
17. Langer HF, Chung KJ, Orlova VV, Choi EY, Kaul S, Kruhlak MJ, et al,. (2010). Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 116: 4395-4403.
18. Lin F, Spencer D, Hatala DA, Levine AD, Medof ME, (2004). Decay-accelerating factor deficiency increases susceptibility to dextran sulfate sodium-induced colitis: role for complement in inflammatory bowel disease. J Immunol 172: 3836-3841.
19. Lindsay J, Van Montfrans C, Brennan F, Van Deventer S, Drillenburg P, Hodgson H, et al,. (2002). IL-10 gene therapy prevents TNBS-induced colitis. Gene Ther 9: 1715-1721.
20. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
21. McKeage K, (2011). Eculizumab: a review of its use in paroxysmal nocturnal haemoglobinuria. Drugs 71: 2327-2345.
22. Mañé J, Lorén V, Pedrosa E, Ojanguren I, Xaus J, Cabré E, et al,. (2009). Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflamm Bowel Dis 15: 1155-1163.
23. Melgar S, Karlsson A, Michaelsson E, (2005). Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol Gastrointest Liver Physiol 288: G1328-G1338.
24. Melgar S, Karlsson L, Rehnstrom E, Arlsson A, Utkovic H, Jansson L, et al,. (2008). Validation of murine dextran sulfate sodium-induced colitis using four therapeutic agents for human inflammatory bowel disease. Int Immunopharmacol 8: 836-844.
25. Molodecky NA, Kaplan GG, (2010). Environmental risk factors for inflammatory bowel disease. Gastroenterol Hepatol (N Y) 6: 339-346.
26. Monk PN, Scola AM, Madala P, Fairlie DP, (2007). Function, structure and therapeutic potential of complement C5a receptors. Br J Pharmacol 152: 429-448.
27. Monsinjon T, Gasque P, Chan P, Ischenko A, Brady JJ, Fontaine MC, (2003). Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J 17: 1003-1014.
28. Munder M, (2009). Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158: 638-651.
29. Myers KJ, Murthy S, Flanigan A, Witchell DR, Butler M, Murray S, et al,. (2003). Antisense oligonucleotide blockade of tumor necrosis factor-alpha in two murine models of colitis. J Pharmacol Exp Ther 304: 411-424.
30. Naito Y, Yakagi T, Handa O, Ishikawa T, Nakagawa S, Yamaguchi T, et al,. (2003). Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice. J Gastroenterol Hepatol 18: 560-569.
31. Pavlovski D, Thundyil J, Monk PN, Wetsel RA, Taylor SM, Woodruff TM, (2012). Generation of complement component C5a by ischemic neurons promotes neuronal apoptosis. FASEB J 9: 3680-3690.
32. Perianayagam MC, Balakrishnan VS, King AJ, Pereira BJ, Jaber BL, (2002). C5a delays apoptosis of human neutrophils by a phosphatidylinositol 3-kinase-signaling pathway. Kidney Int 61: 456-463.
33. Ricklin D, Lambris JD, (2007). Complement-targeted therapeutics. Nat Biotechnol 25: 1265-1275.
34. Riedemann NC, Guo RF, Sarma VJ, Laudes IJ, Huber-Lang M, Warner RL, et al,. (2002). Expression and function of the C5a receptor in rat alveolar epithelial cells. J Immunol 168: 1919-1925.
35. Satsangi J, Morecroft J, Shah NB, Nimmo E, (2003). Genetics of inflammatory bowel disease: scientific and clinical implications. Best Pract Res Clin Gastroenterol 17: 3-18.
36. Sivaram G, Tiwari SK, Bardia A, Manoj G, Santhosh B, Saikant R, et al,. (2011). Association of genetic variants of mannan-binding (MBL) lectin-2 gene, MBL levels and function in ulcerative colitis and Crohn's disease. Innate Immun 17: 526-531.
37. Snyderman R, Phillips J, Mergenhagen SE, (1970). Polymorphonuclear leukocyte chemotactic activity in rabbit serum and Guinea pig serum treated with immune complexes: evidence for C5a as the major chemotactic factor. Infect Immun 1: 521-525.
38. Snyderman R, Pike M, McCarley D, Lang L, (1975). Quantification of mouse macrophage chemotaxis in vitro: role of C5 for the production of chemotactic activity. Infect Immun 11: 488-492.
39. Solomon L, Mansor S, Mallon P, Donnelly E, Hoper M, Loughrey M, et al,. (2010). The dextran sulphate sodium (DSS) model of colitis: an overview. Comp Clin Pathol 19: 235-239.
40. Stallmach A, Hagel S, Bruns T, (2010). Adverse effects of biologics used for treating IBD. Best Pract Res Clin Gastroenterol 24: 167-182.
41. Stevceva L, Pavli P, Husband A, Doe W, (2001). The inflammatory infiltrate in the acute stage of the dextran sulphate sodium induced colitis: B cell response differs depending on the percentage of DSS used to induce it. BMC Clin Pathol 1: 3.
42. Stillie R, Stadnyk AW, (2009). Role of TNF receptors, TNFR1 and TNFR2, in dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 15: 1515-1525.
43. Tomoyose M, Mitsuyama K, Ishida H, Toyonaga A, Tanikawa K, (1998). Role of interleukin-10 in a murine model of dextran sulfate sodium-induced colitis. Scand J Gastroenterol 33: 435-440.
44. Tsuji RF, Kawikova I, Ramabhadran R, Akahira-Azuma M, Taub D, Hugli TE, et al,. (2000). Early local generation of C5a initiates the elicitation of contact sensitivity by leading to early T cell recruitment. J Immunol 165: 1588-1598.
45. Wirtz S, Neufert C, Weigmann B, Neurath MF, (2007). Chemically induced mouse models of intestinal inflammation. Nat Protoc 2: 541-546.
46. Woodruff TM, Arumugam TV, Shiels IA, Reid RC, Fairlie DP, Taylor SM, (2003). A potent human C5a receptor antagonist protects against disease pathology in a rat model of inflammatory bowel disease. J Immunol 171: 5514-5520.
47. Woodruff TM, Pollitt S, Proctor LM, Stocks SZ, Manthey HD, Williams HM, et al,. (2005). Increased potency of a novel complement factor 5a receptor antagonist in a rat model of inflammatory bowel disease. J Pharmacol Exp Ther 314: 811-817.
48. Woodruff TM, Crane JW, Proctor LM, Buller KM, Shek AB, de, Vos K, et al,. (2006). Therapeutic activity of C5a receptor antagonists in a rat model of neurodegeneration. FASEB J 2006: 1407-1417.
49. Woodruff TM, Costantini KJ, Crane JW, Atkin JD, Monk PN, Taylor SM, et al,. (2008). The complement factor C5a contributes to pathology in a rat model of amyotrophic lateral sclerosis. J Immunol 181: 8727-8734.
50. Woodruff TM, Nandakumar KS, Tedesco F, (2011). Inhibiting the C5-C5a receptor axis. Mol Immunol 48: 1631-1642.
51. Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV, et al,. (2009). Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. Plos ONE 4: e6073.
52. Yang YJ, Macneil AJ, Junkins R, Carrigan SO, Tang JT, Forward N, et al,. (2011). Regulator of calcineurin 1 (Rcan1) is required for the development of pulmonary eosinophilia in allergic inflammation in mice. Am J Pathol 179: 1199-1210.