Fc gamma receptor CD64 modulates the inhibitory activity of infliximab

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Wojtal, Kacper A ^a   Rogler, Gerhard ^a,b   Scharl, Michael ^a   Biedermann, Luc ^a   Frei, Pascal ^a   Fried, Michael ^a   Weber, Achim ^a   Eloranta, Jyrki J ^a   Kullak Ublick, Gerd A ^a   Vavricka, Stephan R ^a,b,c  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b Of behalf of the SwissIBD Cohort Study ^*  (Switzerland)

^c TRIEMLI HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; CD64 ANTIGEN; CERTOLIZUMAB PEGOL; FC RECEPTOR; GAMMA INTERFERON; GOLIMUMAB; INFLIXIMAB; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; MESSENGER RNA; PHOSPHOTYROSINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CELL TYPE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CROHN DISEASE; CYTOKINE PRODUCTION; DRUG EFFICACY; EX VIVO STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; IN VITRO STUDY; INTESTINE BIOPSY; INTESTINE CELL; MACROPHAGE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PREDICTION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; ULCERATIVE COLITIS; WESTERN BLOTTING;

ADULT; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE; CELLS, CULTURED; FEMALE; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; INFLAMMATORY BOWEL DISEASES; LEUKOCYTES, MONONUCLEAR; MALE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; POLYETHYLENE GLYCOLS; RECEPTORS, IGG; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84865293881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043361     Document Type: Article

References (58)

1. Waetzig GH, Seegert D, Rosenstiel P, Nikolaus S, Schreiber S, (2002) p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J Immunol 168: 5342-5351.
2. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, et al. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385: 729-733.
3. Rogler G, Andus T, (1998) Cytokines in inflammatory bowel disease. World J Surg 22: 382-389.
4. Chang JT, Lichtenstein GR, (2006) Drug Insight: antagonists of tumor-necrosis factor-α in the treatment of inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol 3: 220-228.
5. Lloyd S, Bujkiewicz S, Wailoo AJ, Sutton AJ, Scott D, (2010) The effectiveness of anti-TNF-{alpha} therapies when used sequentially in rheumatoid arthritis patients: a systematic review and meta-analysis. Rheumatology (Oxford) 49: 2313-2321.
6. Mitoma H, Horiuchi T, Hatta N, Tsukamoto H, Harashima S, et al. (2005) Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-alpha. Gastroenterology 128: 376-392.
7. Mitoma H, Horiuchi T, Tsukamoto H, Tamimoto Y, Kimoto Y, et al. (2008) Mechanisms for cytotoxic effects of anti-tumor necrosis factor agents on transmembrane tumor necrosis factor alpha-expressing cells: comparison among infliximab, etanercept, and adalimumab. Arthritis Rheum 58: 1248-1257.
8. Horiuchi T, Mitoma H, Harashima SI, Tsukamoto H, Shimoda T, et al. (2010) Transmembrane TNF-{alpha}: structure, function and interaction with anti-TNF agents. Rheumatology (Oxford) 49: 1215-1228.
9. Lügering A, Schmidt M, Lügering N, Pauels HG, Domeschke D, et al. (2001) Infliximab induces apoptosis in monocytes from patients with chronic active Crohn's disease by using a caspase-dependent pathway. Gastroenterology 121: 1145-1157.
10. Shen C, Assche GV, Colpaert S, Maerten P, Geboes K, et al. (2005) Adalimumab induces apoptosis of human monocytes: a comparative study with infliximab and etanercept. Aliment Pharmacol Ther 21: 251-258.
11. Nesbitt A, Fossati G, Bergin M, Stephens P, Stephens S, et al. (2007) Mechanism of action of certolizumab pegol (CDP870): in vitro comparison with other anti-tumor necrosis factor alpha agents. Inflamm Bowel Dis 13: 1323-1332.
12. Kaymakcalan Z, Sakorafas P, Bose S, Scesney S, Xiong L, et al. (2009) Comparisons of affinities, avidities, and complement activation of adalimumab, infliximab, and etanercept in binding to soluble and membrane tumor necrosis factor. Clin Immunol 131: 308-316.
13. Fries W, Muja C, Crisafulli C, Costantino G, Longo G, et al. (2008) Infliximab and etanercept are equally effective in reducing enterocyte APOPTOSIS in experimental colitis. Int J Med Sci 5: 169-180.
14. Arora T, Padaki R, Liu L, Hamburger AE, Ellison AR, et al. (2009) Differences in binding and effector functions between classes of TNF antagonists. Cytokine 45: 124-131.
15. Vos AC, Wildenberg ME, Duijvestein M, Verhaar AP, van den Brink GR, et al. (2011) Anti-TNFα antibodies induce regulatory macrophages in an Fc region-dependent manner. Gastroenterology 140: 221-230.
16. Vos AC, Wildenberg ME, Arijs I, Duijvestein M, Verhaar AP, et al. (2012) Regulatory macrophages induced by infliximab are involved in healing in vivo and in vitro. Inflamm Bowel Dis 18: 401-408.
17. Nimmerjahn F, Ravetch JV, (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8: 34-47.
18. Sibéril S, Dutertre CA, Boix C, Bonnin E, Ménez R, et al. (2006) Molecular aspects of human FcgammaR interactions with IgG: functional and therapeutic consequences. Immunol Lett 106: 111-118.
19. Jiang XR, Song A, Bergelson S, Arroll T, Parekh B, et al. (2011) Advances in the assessment and control of the effector functions of therapeutic antibodies. Nat Rev Drug Discov 10: 101-111.
20. Rahman AA, Teschner M, Sethi KK, Brandis H, (1976) Appearance of IgG (Fc) receptor(s) on cultured human fibroblasts infected with human cytomegalovirus. J Immunol 117: 253-258.
21. Keller R, Peitchel R, Goldman JN, Goldman M, (1976) An IgG-Fc receptor induced in cytomegalovirus-infected human fibroblasts. J Immunol 116: 772-777.
22. Hanai H, Iida T, Takeuchi K, Watanabe F, Yamada M, et al. (2008) Adsorptive depletion of elevated proinflammatory CD14+CD16+DR++ monocytes in patients with inflammatory bowel disease. Am J Gastroenterol 103: 1210-1216.
23. Tanaka M, Krutzik SR, Sieling PA, Lee DJ, Rea TH, et al. (2009) Activation of Fc gamma RI on monocytes triggers differentiation into immature dendritic cells that induce autoreactive T cell responses. J Immunol 183: 2349-2355.
24. Marsh CB, Gadek JE, Kindt GC, Moore SA, Wewers MD, (1995) Monocyte Fc gamma receptor cross-linking induces IL-8 production. J Immunol 155: 3161-3167.
25. Alonso A, Bayón Y, Renedo M, Crespo MS, (2000) Stimulation of Fc gamma R receptors induces monocyte chemoattractant protein-1 in the human monocytic cell line THP-1 by a mechanism involving I kappa B-alpha degradation and formation of p50/p65 NF-kappa B/Rel complexes. Int Immunol 12: 547-554.
26. Pan LY, Mendel DB, Zurlo J, Guyre PM, (1990) Regulation of the steady state level of Fc gamma RI mRNA by IFN-gamma and dexamethasone in human monocytes, neutrophils, and U-937 cells. J Immunol 145: 267-275.
27. Boltz-Nitulescu G, Willheim M, Spittler A, Leutmezer F, Tempfer C, et al. (1995) Modulation of IgA, IgE, and IgG Fc receptor expression on human mononuclear phagocytes by 1 alpha,25-dihydroxyvitamin D3 and cytokines. J Leukoc Biol 58: 256-262.
28. Miller DM, Rahill BM, Boss JM, Lairmore MD, Durbin JE, et al. (1998) Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J Exp Med 187: 675-683.
29. Auwerx J, Staels B, Van Vaeck F, Ceuppens JL, (1992) Changes in IgG Fc receptor expression induced by phorbol 12-myristate 13-acetate treatment of THP-1 monocytic leukemia cells. Leuk Res 16: 317-327.
30. An Z. (2009) Therapeutic monoclonal antibodies: from the bench to the clinic. In: Mimura Y, Jefferis R, Mimura-Kimura Y, Abrahams J, Rudd PM, editors. Glycosylation of Therapeutics IgGs. Willey. pp. 73-75.
31. Lund J, Takahashi N, Pound JD, Goodall M, Nakagawa H, et al. (1995) Oligosaccharide-protein interactions in IgG can modulate recognition by Fc gamma receptors. FASEB J 9: 115-119.
32. Sandborn WJ, Schreiber S, Feagan BG, Rutgeerts P, Younes ZH, et al. (2011) Certolizumab pegol for active Crohn's disease: a placebo-controlled, randomized trial. Clin Gastroenterol Hepatol 9: 670-678.
33. Chen X, Feng BS, Zheng PY, Liao XQ, Chong J, et al. (2008) Fc gamma receptor signaling in mast cells links microbial stimulation to mucosal immune inflammation in the intestine. Am J Pathol 173: 1647-1656.
34. Kobayashi R, Okamura S, Ohno T, Saito H, Mori M, et al. (2007) Hyperexpression of FcgammaRI and Toll-like receptor 4 in the intestinal mast cells of Crohn's disease patients. Clin Immunol 125: 149-158.
35. Tillinger W, Jilch R, Jilma B, Brunner H, Koeller U, et al. (2009) Expression of the high-affinity IgG receptor FcRI (CD64) in patients with inflammatory bowel disease: a new biomarker for gastroenterologic diagnostics. Am J Gastroenterol 104: 102-109.
36. Davis PM, Abraham R, Xu L, Nadler SG, Suchard SJ, (2007) Abatacept binds to the Fc receptor CD64 but does not mediate complement-dependent cytotoxicity or antibody-dependent cellular cytotoxicity. J Rheumatol 34: 2204-2210.
37. Louis E, El GZ, Vermeire S, Dall'Ozzo S, Rutgeerts P, et al. (2004) Association between polymorphism in IgG Fc receptor IIIa coding gene and biological response to infliximab in Crohn's disease. Aliment Pharmacol Ther 19: 511-519.
38. Tomita K, Chiba T, Sugai T, Habano W, (2010) Association between tumor necrosis factor-alpha and Fc-gamma receptor polymorphisms with infliximab in Crohn's disease. Hepatogastroenterology 57: 535-539.
39. Okuyama A, Nagasawa H, Suzuki K, Kameda H, Kondo H, et al. (2011) Fcγ receptor IIIb polymorphism and use of glucocorticoids at baseline are associated with infusion reactions to infliximab in patients with rheumatoid arthritis. Ann Rheum Dis 70: 299-304.
40. Cañete JD, Suárez B, Hernández MV, Sanmartí R, Rego I, et al. (2009) Influence of variants of Fc gamma receptors IIA and IIIA on the American College of. Rheumatology and European League Against Rheumatism responses to anti-tumour necrosis factor alpha therapy in rheumatoid arthritis. Ann Rheum Dis 68: 1547-1552.
41. Ericson SG, Zhao Y, Gao H, Miller KL, Gibson LF, et al. (1998) Interleukin-6 production by human neutrophils after Fc-receptor cross-linking or exposure to granulocyte colony-stimulating factor. Blood 91: 2099-2107.
42. Krutmann J, Kirnbauer R, Köck A, Schwarz T, Schöpf E, et al. (1990) Cross-linking Fc receptors on monocytes triggers IL-6 production. Role in anti-CD3-induced T cell activation. J Immunol 145: 1337-1342.
43. Fleit HB, Kobasiuk CD, (1991) The human monocyte-like cell line THP-1 expresses Fc gamma RI and Fc gamma RII. J Leukoc Biol 49: 556-565.
44. van Vugt MJ, Kleijmeer MJ, Keler T, Zeelenberg I, van Dijk MA, et al. (1999) The FcgammaRIa (CD64) ligand binding chain triggers major histocompatibility complex class II antigen presentation independently of its associated FcR gamma-chain. Blood 94: 808-817.
45. Grip O, Bredberg A, Lindgren S, Henriksson G, (2007) GIn creased subpopulations of CD16(+) and CD56(+) blood monocytes in patients with active Crohn's disease. Inflamm Bowel Dis 13: 566-572.
46. Koch S, Kucharzik T, Heidemann J, Nusrat A, Luegering A, (2010) Investigating the role of proinflammatory CD16+ monocytes in the pathogenesis of inflammatory bowel disease. Clin Exp Immunol 161: 332-341.
47. Rogler G, Andus T, Aschenbrenner E, Vogl D, Falk W, et al. (1997) Alterations of the phenotype of colonic macrophages in inflammatory bowel disease. Eur J Gastroenterol Hepatol 9: 893-899.
48. Steel AW, Mela CM, Lindsay JO, Gazzard BG, Goodier MR, (2011) Increased proportion of CD16(+) NK cells in the colonic lamina propria of inflammatory bowel disease patients, but not after azathioprine treatment. Aliment Pharmacol Ther 33: 115-126.
49. Hommes DW, Meenan J, de Haas M, ten Kate FJ, von dem Borne AE, et al. (1996) Soluble Fc gamma receptor III (CD 16) and eicosanoid concentrations in gut lavage fluid from patients with inflammatory bowel disease: reflection of mucosal inflammation. Gut 38: 564-567.
50. Kuwabara A, Okamoto H, Suda T, Ajioka Y, Hatakeyama K, (2007) Clinicopathologic characteristics of clinically relevant cytomegalovirus infection in inflammatory bowel disease. J Gastroenterol 42: 823-829.
51. Lévêque N, Brixi-Benmansour H, Reig T, Renois F, Talmud D, et al. (2010) Low frequency of cytomegalovirus infection during exacerbations of inflammatory bowel diseases. J Med Virol 82: 1694-700.
52. Lawlor G, Moss AC, (2010) Cytomegalovirus in inflammatory bowel disease: pathogen or innocent bystander? Inflamm Bowel Dis 16: 1620-1627.
53. Murayama T, Natsuume-Sakai S, Shimokawa K, Furukawa T, (1986) Fc receptor(s) induced by human cytomegalovirus bind differentially with human immunoglobulin G subclasses. J Gen Virol 67: 1475-1478.
54. Roblin X, Pillet S, Oussalah A, Berthelot P, Del Tedesco E, et al. (2011) Cytomegalovirus load in inflamed intestinal tissue is predictive of resistance to immunosuppressive therapy in ulcerative colitis. Am J Gastroenterol 106: 2001-2008.
55. Habbal W, Monem F, Gärtner BC, (2009) Comparative evaluation of published cytomegalovirus primers for rapid real-time PCR: which are the most sensitive? J Med Microbiol 58: 878-883.
56. Brenmoehl J, Miller SN, Hofmann C, Vogl D, Falk W, et al. (2009) Transforming growth factor-beta 1 induces intestinal myofibroblast differentiation and modulates their migration. World J Gastroenterol 15: 1431-1442.
57. Ryan MH, Petrone D, Nemeth JF, Barnathan E, Björck L, et al. (2008) Proteolysis of purified IgGs by human and bacterial enzymes in vitro and the detection of specific proteolytic fragments of endogenous IgG in rheumatoid synovial fluid. Mol Immunol 45: 1837-1846.
58. Ravetch JV, Bolland S, (2001) IgG Fc receptors. Annu Rev Immunol 19: 275-290.