The complex role of Fcγ receptors in the pathology of arthritis

Springer Seminars in Immunopathology

Volumn 28, Issue 4, 2006, Pages 339-350

  Boross, Peter ^a   Verbeek, J Sjef ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Animal models; Fc receptors; Immune complexes; Knockout mice; Rheumatoid arthritis

Indexed keywords

ANTIGEN; COLLAGEN; COLLAGEN TYPE 2; FC RECEPTOR; GLUCOSE 6 PHOSPHATE ISOMERASE; IMMUNOGLOBULIN G; PROTEOGLYCAN; ANTIGEN ANTIBODY COMPLEX; AUTOANTIBODY; COMPLEMENT RECEPTOR;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN ANTIBODY COMPLEX; ARTHRITIS; DENDRITIC CELL; EFFECTOR CELL; GENE TARGETING; KNOCKOUT MOUSE; LIGAND BINDING; MOUSE; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; HUMAN; IMMUNOLOGY;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; HUMANS; MICE, KNOCKOUT; RECEPTORS, COMPLEMENT; RECEPTORS, FC; RECEPTORS, IGG;

EID: 33845466170     PISSN: 03444325     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00281-006-0049-9     Document Type: Review

References (85)

1. Feldmann M, Brennan FM, Maini RN (1996) Rheumatoid arthritis. Cell 85:307-310
2. de Vries RR, Huizinga TW, Toes RE (2006) HLA and RA revisited: citrullinated food for the SE hypothesis, the DR6 effect, and NIMA. Hum Immunol 67:454-459
3. Kroot EJ, de Jong BA, van Leeuwen MA, Swinkelsm H, van den Hoogen FH, van't Hof M, van de Putte LB, van Rijswijk MH, van Venrooij WJ, van Riel PL (2000) The prognostic value of anticyclic citrullinated peptide antibody in patients with recent-onset rheumatoid arthritis. Arthritis Rheum 43:1831-1835
4. van Gaalen FA, Linn-Rasker SP, van Venrooij WJ, de Jong BA, Breedveld FC, Verweij CL, Toes RE, Huizinga TW (2004) Autoantibodies to cyclic citrullinated peptides predict progression to rheumatoid arthritis in patients with undifferentiated arthritis: a prospective cohort study. Arthritis Rheum 50:709-715
5. Nielen MM, van Schaardenburg D, Reesink HW, van de Stadt RJ, van der Horst-Bruinsma IE, de Koning MH, Habibuw MR, Vandenbroucke JP, Dijkmans BA (2004) Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 50:380-386
6. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, Sundin U, van Venrooij WJ (2003) Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 48:2741-2749
7. Silverman GJ, Weisman S (2003) Rituximab therapy and autoimmune disorders: prospects for anti-B cell therapy. Arthritis Rheum 48:1484-1492
8. Edwards JC, Cambridge G (2001) Sustained improvement in rheumatoid arthritis following a protocol designed to deplete B lymphocytes. Rheumatology (Oxford) 40:205-211
9. Svensson L, Jirholt J, Holmdahl R, Jansson L (1998) B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol 111:521-526
10. Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, Degott C, Kikutani H, Rajewsky K, Pasquali JL, Benoist C, Mathis D (1999) From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 10:451-461
11. Stuart JM, Dixon FJ (1983) Serum transfer of collagen-induced arthritis in mice. J Exp Med 158:378-392
12. Schubert D, Maier B, Morawietz L, Krenn V, Kamradt T (2004) Immunization with glucose-6-phosphate isomerase induces T cell-dependent peripheral polyarthritis in genetically unaltered mice. J Immunol 172:4503-4509
13. Benoist C, Mathis D (2000) A revival of the B cell paradigm for rheumatoid arthritis pathogenesis? Arthritis Res 2:90-94
14. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV (1994) FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76:519-529
15. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV (2005) FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23:41-51
16. Nimmerjahn F, Ravetch JV (2006) Fcgamma receptors: old friends and new family members. Immunity 24:19-28
17. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV (1996) Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 379:346-349
18. Yuasa T, Kubo S, Yoshino T, Ujike A, Matsumura K, Ono M, Ravetch JV, Takai T (1999) Deletion of fcgamma receptor IIB renders H-2(b) mice susceptible to collagen-induced arthritis. J Exp Med 189:187-194
19. Ioan-Facsinay A, de Kimpe SJ, Hellwig SM, van Lent PL, Hofhuis FM, van Ojik HH, Sedlik C, da Silveira SA, Gerber J, de Jong YF, Roozendaal R, Aarden LA, van den Berg WB, Saito T, Mosser D, Amigorena S, Izui S, van Ommen GJ, van Vugt M, van de Winkel JG, Verbeek JS (2002) FcgammaRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16:391-402
20. Fossati-Jimack L, Ioan-Facsinay A, Reininger L, Chicheportiche Y, Watanabe N, Saito T, Hofhuis FM, Gessner JE, Schiller C, Schmidt RE, Honjo T, Verbeek JS, Izui S (2000) Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an antierythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcgamma receptor III. J Exp Med 191:1293-1302
21. Hazenbos WL, Heijnen IA, Meyer D, Hofhuis FM, Renardel de Lavalette CR, Schmidt RE, Capel PJ, van de Winkel JG, Gessner JE, van den Berg TK, Verbeek JS (1998) Murine IgG1 complexes trigger immune effector functions predominantly via Fc gamma RIII (CD16). J Immunol 161:3026-3032
22. Takai T (2005) Fc receptors and their role in immune regulation and autoimmunity. J Clin Immunol 25:1-18
23. Ji H, Ohmura K, Mahmood U, Lee DM, Hofhuis FM, Boackle SA, Takahashi K, Holers VM, Walport M, Gerard C, Ezekowitz A, Carroll MC, Brenner M, Weissleder R, Verbeek JS, Duchatelle V, Degott C, Benoist C, Mathis D (2002) Arthritis critically dependent on innate immune system players. Immunity 16:157-168
24. Grant EP, Picarella D, Burwell T, Delaney T, Croci A, Avitahl N, Humbles AA, Gutierrez-Ramos JC, Briskin M, Gerard C, Coyle AJ (2002) Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J Exp Med 196:1461-1471
25. Wang Y, Kristan J, Hao L, Lenkoski CS, Shen Y, Matis LA (2002) A role for complement in antibody-mediated inflammation: C5-deficient DBA/1 mice are resistant to collagen-induced arthritis. J Immunol 164:4340-4347
26. Wang Y, Rollins SA, Madri JA, Matis LA (1995) Anti-C5 monoclonal antibody therapy prevents collagen-induced arthritis and ameliorates established disease. Proc Natl Acad Sci U S A 92:8955-8959
27. Schmidt RE, Gessner JE (2005) Fc receptors and their interaction with complement in autoimmunity. Immunol Lett 100:56-67
28. Trcka J, Moroi Y, Clynes RA, Goldberg SM, Bergtold A, Perales MA, Ma M, Ferrone CR, Carroll MC, Ravetch JV, Houghton AN (2002) Redundant and alternative roles for activating Fc receptors and complement in an antibody-dependent model of autoimmune vitiligo. Immunity 16:861-868
29. Hazenbos WL, Gessner JE, Hofhuis FM, Kuipers H, Meyer D, Heijnen IA, Schmidt RE, Sandor M, Capel PJ, Daeron M, van de Winkel JG, Verbeek JS (1996) Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity 5:181-188
30. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, Wong T, Campagnuolo G, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle WJ, Penninger JM (1992) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402:304-309
31. Sivo J, Politis AD, Vogel SN (1993) Differential effects of interferon-gamma and glucocorticoids on Fc gamma R gene expression in murine macrophages. J Leukoc Biol 54:451-457
32. Kannan K, Ortmann RA, Kimpel D (2005) Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology 12:167-181
33. Kouskoff V, Korganow AS, Duchatelle V, Degott C, BenoistC, Mathis D (1996) Organ-specific disease provoked by systemic autoimmunity. Cell 87:811-822
34. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru S, Sakaguchi S (2003) Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 426:454-460
35. Butler DM, Malfait AM, Mason LJ, Warden PJ, Kollias G, Maini RN, Feldmann M, Brennan FM (1997) DBA/1 mice expressing the human TNF-alpha transgene develop a severe, erosive arthritis: characterization of the cytokine cascade and cellular composition. J Immunol 159:2867-2876
36. Horai R, Saijo S, Tanioka H, Nakae S, Sudo K, Okahara A, Ikuse T, Asano M, Iwakura Y (2000) Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J Exp Med 191:313-320
37. van Lent PL, van Vuuren AJ, Blom AB, Holthuysen AE, van de Putte LB, van de Winkel JG, van den Berg WB (2000) Role of Fc receptor gamma chain in inflammation and cartilage damage during experimental antigen-induced arthritis. Arthritis Rheum 43:740-752
38. Nabbe KC, Blom AB, Holthuysen AE, Boross P, Roth J, Verbeek S, van Lent PL, van den Berg WB (2003) Coordinate expression of activating Fc gamma receptors I and III and inhibiting Fc gamma receptor type II in the determination of joint inflammation and cartilage destruction during immune complex-mediated arthritis. Arthritis Rheum 48:255-265
39. Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B (1980) Immunisation against heterologous type II collagen induces arthritis in mice. Nature 283:666-668
40. Kleinau S, Martinsson P, Heyman B (2000) Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J Exp Med 191:1611-1616
41. Diaz DS, Andren M, Martinsson P, Verbeek JS, Kleinau S (2002) Expression of FcgammaRIII is required for development of collagen-induced arthritis. Eur J Immunol 32:2915-2922
42. van Lent PL, Holthuysen AE, Van Den Bersselaar LA, van Rooijen N, Joosten LA, van de Loo FA, van de Putte LB, van den Berg WB (1996) Phagocytic lining cells determine local expression of inflammation in type II collagen-induced arthritis. Arthritis Rheum 39:1545-1555
43. Andren M, Xiang Z, Nilsson G, Kleinau S (2006) FcgammaRIII-expressing macrophages are essential for development of collagen-induced arthritis. Scand J Immunol 63:282-289
44. Kaplan CD, O'Neill SK, Koreny T, Czipri M, Finnegan A (2002) Development of inflammation in proteoglycan-induced arthritis is dependent on Fc gamma R regulation of the cytokine/chemokine environment. J Immunol 169:5851-5859
45. Kaplan CD, Cao Y, Verbeek JS, Tunyogi-Csapo M, Finnegan A (2005) Development of proteoglycan-induced arthritis is critically dependent on Fcgamma receptor type III expression. Arthritis Rheum 52:1612-1619
46. Terato K, Hasty KA, Reife RA, Cremer MA, Kang AH, Stuart JM (1992) Induction of arthritis with monoclonal antibodies to collagen. J Immunol 148:2103-2108
47. Kagari T, Tanaka D, Doi H, Shimozato T (2003) Essential role of Fc gamma receptors in anti-type II collagen antibody-induced arthritis. J Immunol 170:4318-4324
48. Nandakumar KS, Andren M, Martinsson P, Bajtnerm E, Hellstrom S, Holmdahl R, Kleinau S (2003) Induction of arthritis by single monoclonal IgG anti-collagen type II antibodies and enhancement of arthritis in mice lacking inhibitory FcgammaRIIB. Eur J Immunol 33:2269-2277
49. Banda NK, Thurman JM, Kraus D, Wood A, Carroll MC, Arend WP, Holers VM (2006) Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis. J Immunol 177:1904-1912
50. Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM (2004) Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol 172:7694-7702
51. Grant EP, Picarella D, Burwell T, Delaney T, Croci A, Avitahl N, Humbles AA, Gutierrez-Ramos JC, Briskin M, Gerard C, Coyle AJ (2002) Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J Exp Med 196:1461-1471
52. Tanaka D, Kagari T, Doi H, Shimozato T (2006) Essential role of neutrophils in anti-type II collagen antibody and lipopolysaccharide-induced arthritis. Immunology 119(2):195-202
53. Maccioni M, Zeder-Lutz G, Huang H, Ebel C, Gerber P, Hergueux J, Marchal P, Duchatelle V, Degott C, van Regenmortel M, Benoist C, Mathis D (2002) Arthritogenic monoclonal antibodies from K/BxN mice. J Exp Med 195:1071-1077
54. Corr M, Crain B (2002) The role of FcgammaR signaling in the K/B x N serum transfer model of arthritis. J Immunol 169:6604-6609
55. Ji H, Gauguier D, Ohmura K, Gonzalez A, Duchatelle V, Danoy P, Garchon HJ, Degott C, Lathrop M, Benoist C, Mathis D (2001) Genetic influences on the end-stage effector phase of arthritis. J Exp Med 194:321-330
56. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB (2002) Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297:1689-1692
57. Wipke BT, Allen PM (2001) Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 167:1601-1608
58. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, Mahmood U, Weissleder R, Mathis D, Benoist C (2006) Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol 7:284-292
59. Finkelman FD, Rothenberg ME, Brandt EB, Morris SC, Strait RT (2005) Molecular mechanisms of anaphylaxis: lessons from studies with murine models. J Allergy Clin Immunol 115:449-457
60. Ji H, Pettit A, Ohmura K, Ortiz-Lopez A, Duchatelle V, Degott C, Gravallese E, Mathis D, Benoist C (2002) Critical roles for interleukin 1 and tumor necrosis factor alpha in antibody-induced arthritis. J Exp Med 196:77-85
61. van Lent PL, Nabbe K, Blom AB, Holthuysen AE, Sloetjes A, van de Putte LB, Verbeek S, van den Berg WB (2001) Role of activatory Fc gamma RI and Fc gamma RIII and inhibitory Fc gamma RII in inflammation and cartilage destruction during experimental antigen-induced arthritis. Am J Pathol 159:2309-2320
62. van Meurs JB, van Lent PL, Holthuysen AE, Singer II, Bayne EK, van den Berg WB (1999) Kinetics of aggrecanase- and metalloproteinase-induced neoepitopes in various stages of cartilage destruction in murine arthritis. Arthritis Rheum 42:1128-1139
63. van den Broek MF, van den Berg WB, van de Putte LB (1988) The role of mast cells in antigen induced arthritis in mice. J Rheumatol 15:544-551
64. van Lent PL, Holthuysen AE, van Den BL, van Rooijen N, van de Putte LB, van den Berg WB (1995) Role of macrophage-like synovial lining cells in localization and expression of experimental arthritis. Scand J Rheumatol Suppl 101:83-89
65. van Lent P, Nabbe KC, Boross P, Blom AB, Roth J, Holthuysen A, Sloetjes A, Verbeek S, van den Berg W (2003) The inhibitory receptor FcgammaRII reduces joint inflammation and destruction in experimental immune complex-mediated arthritides not only by inhibition of FcgammaRI/III but also by efficient clearance and endocytosis of immune complexes. Am J Pathol 163:1839-1848
66. Blom AB, van Lent PL, van Vuuren H, Holthuysen AE, Jacobs C, van de Putte LB, van de Winkel JG, van den Berg WB (2000) Fc gamma R expression on macrophages is related to severity and chronicity of synovial inflammation and cartilage destruction during experimental immune-complex-mediated arthritis (ICA). Arthritis Res 2:489-503
67. Nabbe KC, Blom AB, Holthuysen AE, Boross P, Roth J, Verbeek S, van Lent PL, van den Berg WB (2003) Coordinate expression of activating Fc gamma receptors I and III and inhibiting Fc gamma receptor type II in the determination of joint inflammation and cartilage destruction during immune complex-mediated arthritis. Arthritis Rheum 48:255-265
68. van Lent PL, van den Hoek AE, Van Den Bersselaar LA, Spanjaards MF, van Rooijen N, Dijkstra CD, van de Putte LB, van den Berg WB (1993) In vivo role of phagocytic synovial lining cells in onset of experimental arthritis. Am J Pathol 143:1226-1237
69. Nabbe KC, van Lent PL, Holthuysen AE, Kolls JK, Verbeek S, van den Berg WB (2003) FcgammaRI up-regulation induced by local adenoviral-mediated interferon-gamma production aggravates chondrocyte death during immune complex-mediated arthritis. Am J Pathol 163:743-752
70. Nabbe KC, Boross P, Holthuysen AE, Sloetjes AW, Kolls JK, Verbeek S, van Lent PL, van den Berg WB (2005) Joint inflammation and chondrocyte death become independent of Fcgamma receptor type III by local overexpression of interferon-gamma during immune complex-mediated arthritis. Arthritis Rheum 52:967-974
71. Nieto A, Caliz R, Pascual M, Mataran L, Garcia S, Martin J (2000) Involvement of Fcgamma receptor IIIA genotypes in susceptibility to rheumatoid arthritis. Arthritis Rheum 43:735-739
72. Chen JY, Wang CM, Wu JM, Ho HH, Luo SF (2006) Association of rheumatoid factor production with FcgammaRIIIa polymorphism in Taiwanese rheumatoid arthritis. Clin Exp Immunol 144:10-16
73. Matsumoto I, Zhang H, Muraki Y, Hayashi T, Yasukochi T, Kori Y, Goto D, Ito S, Tsutsumi A, Sumida T (2005) A functional variant of Fcgamma receptor IIIA is associated with rheumatoid arthritis in individuals who are positive for anti-glucose-6-phosphate isomerase antibodies. Arthritis Res Ther 7:R1183-R1188
74. Kastbom A, Ahmadi A, Soderkvist P, Skogh T (2005) The 158V polymorphism of Fc gamma receptor type IIIA in early rheumatoid arthritis: increased susceptibility and severity in male patients (the Swedish TIRA project). Rheumatology (Oxford) 44:1294-1298
75. Hogarth PM (2002) Fc receptors are major mediators of antibody based inflammation in autoimmunity. Curr Opin Immunol 14:798-802
76. Tan SC, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, Wicks IP, Campbell IK, McKenzie SE, Brooks M, Stevenson AW, Hogarth PM (2005) Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum 52:3220-3229
77. Wijngaarden S, van de Winkel JG, Jacobs KM, Bijlsma JW, Lafeber FP, van Roon JA (2004) A shift in the balance of inhibitory and activating Fcgamma receptors on monocytes toward the inhibitory Fcgamma receptor IIb is associated with prevention of monocyte activation in rheumatoid arthritis. Arthritis Rheum 50:3878-3887
78. Radstake TR, Blom AB, Sloetjes AW, van Gorselen EO, Pesman GJ, Engelen L, Torensma R, van den Berg WB, Figdor CG, van Lent PL, Adema GJ, Barrera P (2004) Increased FcgammaRII expression and aberrant tumor necrosis factor alpha production by mature dendritic cells from patients with active rheumatoid arthritis. Ann Rheum Dis 63:1556-1563
79. Hirano T (2002) Revival of the autoantibody model in rheumatoid arthritis. Nat Immunol 3:342-344
80. Johansson AC, Sundler M, Kjellen P, Johannesson M, Cook A, Lindqvist AK, Nakken B, Bolstad AI, Jonsson R, Alarcon-Riquelme M, Holmdahl R (2001) Genetic control of collagen-induced arthritis in a cross with NOD and C57BL/10 mice is dependent on gene regions encoding complement factor 5 and FcgammaRIIb and is not associated with loci controlling diabetes. Eur J Immunol 31:1847-1856
81. Yanni G, Whelan A, Feighery C, Bresnihan B (1994) Synovial tissue macrophages and joint erosion in rheumatoid arthritis. Ann Rheum Dis 53:39-44
82. van der Helm-van Mil AH, Wesoly JZ, Huizinga TW (2005) Understanding the genetic contribution to rheumatoid arthritis. Curr Opin Rheumatol 17:299-304
83. Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, Mangion J, Roberton-Lowe C, Marshall AJ, Petretto E, Hodges MD, Bhangal G, Patel SG, Sheehan-Rooney K, Duda M, Cook PR, Evans DJ, Domin J, Flint J, Boyle JJ, Pusey CD, Cook HT (2006) Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439:851-855
84. Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S (2006) Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312:1669-1672
85. van Lent PL, Grevers L, Lubberts E, de Vries TJ, Nabbe KC, Verbeek JS, Oppers B, Sloetjes A, Blom AB, van den Berg WB (2006) Fcg receptors directly mediate cartilage but not bone destruction: uncoupling of cartilage damage from bone erosion and joint inflammation. Arthritis Rheum (in press)