Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury

Circulation

Volumn 120, Issue 20, 2009, Pages 2012-2024

  Mayadas, Tanya N ^a   Tsokos, George C ^b   Tsuboi, Naotake ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 GLYCOPROTEIN 1; CD40 LIGAND; CHEMOKINE; CHEMOKINE RECEPTOR CXCR2; COMPLEMENT; CYTOKINE; FC RECEPTOR; HYPOCHOLESTEROLEMIC AGENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN;

ANTIGEN ANTIBODY COMPLEX; ARTHRITIS; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; DISEASE ASSOCIATION; ELECTRON BEAM TOMOGRAPHY; GLOMERULUS BASEMENT MEMBRANE; HUMAN; IMMUNOPATHOGENESIS; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; REVIEW; RISK FACTOR; SYSTEMIC LUPUS ERYTHEMATOSUS; TISSUE INJURY;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ATHEROSCLEROSIS; AUTOIMMUNE DISEASES; CHRONIC DISEASE; HUMANS; INFLAMMATION; NEUTROPHIL INFILTRATION; NEUTROPHILS;

EID: 72449160275     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.771170     Document Type: Review

References (156)

1. Roman MJ, Shanker BA, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2399-2406.
2. Asanuma Y, Oeser A, Shintani AK, Turner E, Olsen N, Fazio S, Linton MF, Raggi P, Stein CM. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2407-2415.
3. Avalos I, Rho YH, Chung CP, Stein CM. Atherosclerosis in rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Rheumatol. 2008; 26:S5-S13.
4. Solomon DH, Curhan GC, Rimm EB, Cannuscio CC, Karlson EW. Cardiovascular risk factors in women with and without rheumatoid arthritis. Arthritis Rheum. 2004;50:3444-3449.
5. Salmon JE, Roman MJ. Subclinical atherosclerosis in rheumatoid arthritis and systemic lupus erythematosus. Am J Med. 2008;121:S3-S8.
6. Gonzalez-Gay MA, Gonzalez-Juanatey C, Miranda-Filloy JA, Garcia-Porrua C, Llorca J, Martin J. Cardiovascular disease in rheumatoid arthritis. Biomed Pharmacother. 2006;60:673-677.
7. Gonzalez-Juanatey C, Lopez-Diaz MJ, Martin J, Llorca J, Gonzalez-Gay MA. Atherosclerosis in patients with biopsy-proven giant cell arteritis. Arthritis Rheum. 2007;57:1481-1486. (Pubitemid 350308847)
8. Gonzalez-Gay MA, Vazquez-Rodriguez TR, Gonzalez-Juanatey C, Llorca J. Subclinical atherosclerosis in patients with psoriatic arthritis. J Rheumatol. 2008;35:2070-2071.
9. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L, D'Agostino RB, Kuller LH. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol. 1997;145:408-415.
10. Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, Cote R, Grover SA, Fortin PR, Clarke AE, Senecal JL. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2001; 44:2331-2337.
11. Shoenfeld Y, Gerli R, Doria A, Matsuura E, Cerinic MM, Ronda N, Jara LJ, Abu-Shakra M, Meroni PL, Sherer Y. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation. 2005;112:3337-3347. (Pubitemid 43739380)
12. de Leeuw K, Kallenberg C, Bijl M. Accelerated atherosclerosis in patients with systemic autoimmune diseases. Ann N Y Acad Sci. 2005; 1051:362-371. (Pubitemid 41362766)
13. Sherer Y, Shoenfeld Y. Antiphospholipid syndrome, antiphospholipid antibodies, and atherosclerosis. Curr Atheroscler Rep. 2001;3:328-333.
14. Edwards CJ, Syddall H, Goswami R, Goswami P, Dennison EM, Arden NK, Cooper C. The autoantibody rheumatoid factor may be an independent risk factor for ischaemic heart disease in men. Heart. 2007;93: 1263-1267.
15. Chung CP, Oeser A, Solus JF, Gebretsadik T, Shintani A, Avalos I, Sokka T, Raggi P, Pincus T, Stein CM. Inflammation-associated insulin resistance: differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms. Arthritis Rheum. 2008;58: 2105-2112.
16. Rho YH, Chung CP, Oeser A, Solus J, Raggi P, Gebretsadik T, Shintani A, Stein CM. Novel cardiovascular risk factors in premature coronary atherosclerosis associated with systemic lupus erythematosus. J Rheumatol. 2008;35:1789-1794.
17. Gu L, Weinreb A, Wang XP, Zack DJ, Qiao JH, Weisbart R, Lusis AJ. Genetic determinants of autoimmune disease and coronary vasculitis in the MRL-lpr/lpr mouse model of systemic lupus erythematosus. J Immunol. 1998;161:6999-7006.
18. Mizutani H, Engelman RW, Kinjoh K, Kurata Y, Ikehara S, Good RA. Prevention and induction of occlusive coronary vascular disease in autoimmune (W/B)F1 mice by haploidentical bone marrow transplantation: possible role for anticardiolipin autoantibodies. Blood. 1993;82: 3091-3097.
19. Morel L, Wakeland EK. Susceptibility to lupus nephritis in the NZB/W model system. Curr Opin Immunol. 1998;10:718-725.
20. Wissler RW. Update on the pathogenesis of atherosclerosis. Am J Med. 1991;91:3S-9S.
21. Hernandez-Vargas P, Ortiz-Munoz G, Lopez-Franco O, Suzuki Y, Gallego-Delgado J, Sanjuan G, Lazaro A, Lopez-Parra V, Ortega L, Egido J, Gomez-Guerrero C. Fcgamma receptor deficiency confers protection against atherosclerosis in apolipoprotein E knockout mice. Circ Res. 2006;99:1188-1196.
22. Kaveri SV, Lacroix-Desmazes S, Bayry J. The antiinflammatory IgG. N Engl J Med. 2008;359:307-309.
23. Yuan Z, Kishimoto C, Sano H, Shioji K, Xu Y, Yokode M. Immunoglobulin treatment suppresses atherosclerosis in apolipoprotein E-deficient mice via the Fc portion. Am J Physiol Heart Circ Physiol. 2003;285:H899-H906.
24. Virella G, Lopes-Virella MF. Atherogenesis and the humoral immune response to modified lipoproteins. Atherosclerosis. 2008;200:239-246.
25. Lopes-Virella MF, Binzafar N, Rackley S, Takei A, La Via M, Virella G. The uptake of LDL-IC by human macrophages: predominant involvement of the Fc gamma RI receptor. Atherosclerosis. 1997;135: 161-170.
26. Feng X, Li H, Rumbin AA, Wang X, La Cava A, Brechtelsbauer K, Castellani LW, Witztum JL, Lusis AJ, Tsao BP. ApoE-/-Fas-/- C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis, and osteopenia. J Lipid Res. 2007;48: 794-805.
27. Aprahamian T, Bonegio R, Rizzo J, Perlman H, Lefer DJ, Rifkin IR, Walsh K. Simvastatin treatment ameliorates autoimmune disease associated with accelerated atherosclerosis in a murine lupus model. J Immunol. 2006;177:3028-3034.
28. Stanic AK, Stein CM, Morgan AC, Fazio S, Linton MF, Wakeland EK, Olsen NJ, Major AS. Immune dysregulation accelerates atherosclerosis and modulates plaque composition in systemic lupus erythematosus. Proc Natl Acad Sci USA. 2006;103:7018-7023.
29. Pryshchep O, Ma-Krupa W, Younge BR, Goronzy JJ, Weyand CM. Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation. 2008;118:1276-1284.
30. Sato K, Niessner A, Kopecky SL, Frye RL, Goronzy JJ, Weyand CM. TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque. J Exp Med. 2006;203:239-250.
31. Li X, Su K, Ji C, Szalai AJ, Wu J, Zhang Y, Zhou T, Kimberly RP, Edberg JC. Immune opsonins modulate BLyS/BAFF release in a receptor-specific fashion. J Immunol. 2008;181:1012-1018.
32. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science. 2001;294:1540-1543.
33. Nigrovic PA, Lee DM. Innate immunity and immune complexes in rheumatoid arthritis. In: Firestein GS, Panayi G, Wollheim K, eds. Rheumatoid Arthritis. New York, NY: Oxford University Press; 2006: 135-155.
34. Segerer S, Henger A, Schmid H, Kretzler M, Draganovici D, Brandt U, Noessner E, Nelson PJ, Kerjaschki D, Schlondorff D, Regele H. Expression of the chemokine receptor CXCR1 in human glomerular diseases. Kidney Int. 2006;69:1765-1773.
35. Fu Y, Du Y, Mohan C. Experimental anti-GBM disease as a tool for studying spontaneous lupus nephritis. Clin Immunol. 2007;124: 109-118.
36. Quinn K, Henriques M, Parker T, Slutsky AS, Zhang H. Human neutrophil peptides: a novel potential mediator of inflammatory cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2008;295: H1817-H1824.
37. Packard RR, Lichtman AH, Libby P. Innate and adaptive immunity in atherosclerosis. Semin Immunopathol. 2009;31:5-22.
38. Rotzius P, Soehnlein O, Kenne E, Lindbom L, Nystrom K, Thams S, Eriksson EE. ApoE(-/- )/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis. 2009;202:111-118.
39. van Leeuwen M, Gijbels MJ, Duijvestijn A, Smook M, van de Gaar MJ, Heeringa P, de Winther MP, Tervaert JW. Accumulation of myeloperoxidase-positive neutrophils in atherosclerotic lesions in LDLR-/- mice. Arterioscler Thromb Vasc Biol. 2008;28:84-89.
40. Zernecke A, Bot I, Djalali-Talab Y, Shagdarsuren E, Bidzhekov K, Meiler S, Krohn R, Schober A, Sperandio M, Soehnlein O, Bornemann J, Tacke F, Biessen EA, Weber C. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102:209-217.
41. Nagarajan S. Anti-OxLDL IgG blocks OxLDL interaction with CD36, but promotes FcgammaR, CD32A-dependent inflammatory cell adhesion. Immunol Lett. 2007;108:52-61.
42. Clavel C, Nogueira L, Laurent L, Iobagiu C, Vincent C, Sebbag M, Serre G. Induction of macrophage secretion of tumor necrosis factor alpha through Fcgamma receptor IIa engagement by rheumatoid arthritis-specific autoantibodies to citrullinated proteins complexed with fibrinogen. Arthritis Rheum. 2008;58:678-688.
43. Cobb RR, Molony JL. Interleukin-1beta expression is induced by adherence and is enhanced by Fc-receptor binding to immune complex in THP-1 cells. FEBS Lett. 1996;394:241-246.
44. Curtiss LK, Tobias PS. Emerging role of Toll-like receptors in atherosclerosis. J Lipid Res. 2009;50(suppl):S340-S345.
45. Kim WU, Sreih A, Bucala R. Toll-like receptors in systemic lupus erythematosus: prospects for therapeutic intervention. Autoimmun Rev. 2009;8:204-208.
46. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol. 2006;6:823-835.
47. Means TK, Latz E, Hayashi F, Murali MR, Golenbock DT, Luster AD. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J Clin Invest. 2005;115:407-417.
48. Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M, Forsbach A, Akira S, Kelly KM, Reeves WH, Bauer S, Krieg AM. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med. 2005;202:1575-1585.
49. Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood. 2003;102:2660-2669.
50. Kurt-Jones EA, Mandell L, Whitney C, Padgett A, Gosselin K, New-burger PE, Finberg RW. Role of toll-like receptor 2 (TLR2) in neu-trophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils. Blood. 2002;100: 1860-1868.
51. Sabroe I, Prince LR, Jones EC, Horsburgh MJ, Foster SJ, Vogel SN, Dower SK, Whyte MK. Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol. 2003;170:5268-5275.
52. Brumeanu TD, Goldstein R, Casares S. Down-regulation of autoreactive T-cells by HMG CoA reductase inhibitors. Clin Immunol. 2006; 119:1-12.
53. Fleming SD, Monestier M, Tsokos GC. Accelerated ischemia/ reperfusion-induced injury in autoimmunity-prone mice. J Immunol. 2004;173:4230-4235.
54. Neale TJ, Wilson CB. Glomerular antigens in glomerulonephritis. Springer Semin Immunopathol. 1982;5:221-249.
55. Belmont HM, Abramson SB, Lie JT. Pathology and pathogenesis of vascular injury in systemic lupus erythematosus: interactions of inflammatory cells and activated endothelium. Arthritis Rheum. 1996;39:9-22.
56. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678-689.
57. Downey GP, Fukushima T, Fialkow L, Waddell TK. Intracellular signaling in neutrophil priming and activation. Semin Cell Biol. 1995;6: 345-356.
58. Swain SD, Rohn TT, Quinn MT. Neutrophil priming in host defense: role of oxidants as priming agents. Antioxid Redox Signal. 2002;4: 69-83.
59. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, Silliman CC. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J Leukoc Biol. 2005;78:1025-1042.
60. Cai TQ, Wright SD. Human leukocyte elastase is an endogenous ligand for the integrin CR3 (CD11b/CD18, Mac-1, alpha M beta 2) and modulates polymorphonuclear leukocyte adhesion. J Exp Med. 1996;184: 1213-1223.
61. Adkison AM, Raptis SZ, Kelley DG, Pham CT. Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J Clin Invest. 2002;109:363-371.
62. Raptis SZ, Shapiro SD, Simmons PM, Cheng AM, Pham CT. Serine protease cathepsin G regulates adhesion-dependent neutrophil effector functions by modulating integrin clustering. Immunity. 2005;22: 679-691.
63. Kessenbrock K, Frohlich L, Sixt M, Lammermann T, Pfister H, Bateman A, Belaaouaj A, Ring J, Ollert M, Fassler R, Jenne DE. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating anti-inflammatory progranulin. J Clin Invest. 2008;118:2438-2447.
64. Fialkow L, Wang Y, Downey GP. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med. 2007;42:153-164.
65. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006;6:173-182.
66. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc Natl Acad Sci U S A. 2002;99:6901-6906.
67. von Vietinghoff S, Ley K. Homeostatic regulation of blood neutrophil counts. J Immunol. 2008;181:5183-5188.
68. Jennette JC, Falk RJ. New insight into the pathogenesis of vasculitis associated with antineutrophil cytoplasmic autoantibodies. Curr Opin Rheumatol. 2008;20:55-60.
69. Harper L, Savage CO. Pathogenesis of ANCA-associated systemic vas-culitis. J Pathol. 2000;190:349-359.
70. Xiao H, Heeringa P, Hu P, Liu Z, Zhao M, Aratani Y, Maeda N, Falk RJ, Jennette JC. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest. 2002;110:955-963.
71. Nolan SL, Kalia N, Nash GB, Kamel D, Heeringa P, Savage CO. Mechanisms of ANCA-mediated leukocyte-endothelial cell interactions in vivo. J Am Soc Nephrol. 2008;19:973-984.
72. Praprotnik S, Blank M, Meroni PL, Rozman B, Eldor A, Shoenfeld Y. Classification of anti-endothelial cell antibodies into antibodies against microvascular and macrovascular endothelial cells: the pathogenic and diagnostic implications. Arthritis Rheum. 2001;44:1484-1494.
73. Damianovich M, Gilburd B, George J, Del Papa N, Afek A, Goldberg I, Kopolovic Y, Roth D, Barkai G, Meroni PL, Shoenfeld Y. Pathogenic role of anti-endothelial cell antibodies in vasculitis: an idiotypic experimental model. J Immunol. 1996;156:4946-4951. (Pubitemid 26174484)
74. Meroni P, Ronda N, Raschi E, Borghi MO. Humoral autoimmunity against endothelium: theory or reality? Trends Immunol. 2005;26: 275-281.
75. Benoit FL, Rulon DB, Theil GB, Doolan PD, Watten RH. Goodpasture's syndrome: a clinicopathologic entity. Am J Med. 1964;37:424-444.
76. Wilson CB, Dixon FJ. Anti-glomerular basement membrane antibody-induced glomerulonephritis. Kidney Int. 1973;3:74-89.
77. Hudson BG, Kalluri R, Gunwar S, Noelken ME, Mariyama M, Reeders ST. Molecular characteristics of the Goodpasture autoantigen. Kidney Int. 1993;43:135-139.
78. Borza DB, Neilson EG, Hudson BG. Pathogenesis of Goodpasture syndrome: a molecular perspective. Semin Nephrol. 2003;23:522-531.
79. Meyers KE, Allen J, Gehret J, Jacobovits A, Gallo M, Neilson EG, Hopfer H, Kalluri R, Madaio MP. Human antiglomerular basement membrane autoantibody disease in XenoMouse II. Kidney Int. 2002;61: 1666-1673.
80. Suzuki Y, Gomez-Guerrero C, Shirato I, Lopez-Franco O, Gallego-Delgado J, Sanjuan G, Lazaro A, Hernandez-Vargas P, Okumura K, Tomino Y, Ra C, Egido J. Pre-existing glomerular immune complexes induce polymorphonuclear cell recruitment through an Fc receptor-dependent respiratory burst: potential role in the perpetuation of immune nephritis. J Immunol. 2003;170:3243-3253.
81. Gwinner W, Grone HJ. Role of reactive oxygen species in glomerulo-nephritis. Nephrol Dial Transplant. 2000;15:1127-1132.
82. Hooke DH, Gee DC, Atkins RC. Leukocyte analysis using monoclonal antibodies in human glomerulonephritis. Kidney Int. 1987;31:964-972.
83. Camussi G, Cappio FC, Messina M, Coppo R, Stratta P, Vercellone A. The polymorphonuclear neutrophil (PMN) immunohistological technique: detection of immune complexes bound to the PMN membrane in acute poststreptococcal and lupus nephritis. Clin Nephrol. 1980;14: 280-287.
84. Cream JJ, Bryceson AD, Ryder G. Disappearance of immunoglobulin and complement from the Arthus reaction and its relevance to studies of vasculitis in man. Br J Dermatol. 1971;84:106-109.
85. Cream JJ, Turk L. A review of the evidence for immune-complex deposition as a cause of skin diseases in man. Clin Allergy. 1971;1: 235-247.
86. Movat HZ, Fernando NV. Allergic inflammation, I: the earliest fine structural changes at the blood-tissue barrier during antigen-antibody interaction. Am J Pathol. 1963;42:41-59.
87. Cochrane CG. Studies on the localization of circulating antigen-antibody complexes and other macromolecules in vessels, II: pathogenetic and pharmacodynamic studies. J Exp Med. 1963;118:503-513.
88. Stokol T, O'Donnell P, Xiao L, Knight S, Stavrakis G, Botto M, von Andrian UH, Mayadas TN. C1q governs deposition of circulating immune complexes and leukocyte Fcgamma receptors mediate subsequent neutrophil recruitment. J Exp Med. 2004;200:835-846.
89. Norman MU, Van De Velde NC, Timoshanko JR, Issekutz A, Hickey MJ. Overlapping roles of endothelial selectins and vascular cell adhesion molecule-1 in immune complex-induced leukocyte recruitment in the cremasteric microvasculature. Am J Pathol. 2003;163:1491-1503.
90. Jancar S, Sanchez Crespo M. Immune complex-mediated tissue injury: a multistep paradigm. Trends Immunol. 2005;26:48-55.
91. Weis SM. Vascular permeability in cardiovascular disease and cancer. Curr Opin Hematol. 2008;15:243-249.
92. Bozic CR, Lu B, Hopken UE, Gerard C, Gerard NP. Neurogenic amplification of immune complex inflammation. Science. 1996;273: 1722-1725.
93. Kyburz D, Corr M. The KRN mouse model of inflammatory arthritis. Springer Semin Immunopathol. 2003;25:79-90.
94. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, Mahmood U, Weissleder R, Mathis D, Benoist C. Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol. 2006;7:284-292.
95. Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM. Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol. 2004;172:7694-7702.
96. Gauthier VJ, Abrass CK. Circulating immune complexes in renal injury. Semin Nephrol. 1992;12:379-394.
97. Coimbra TM, Gouveia MA, Ebisui L, Barbosa JE, Lachat JJ, de Carvalho IF. Influence of antigen charge in the pathogenicity of immune complexes in rats. Br J Exp Pathol. 1985;66:595-603.
98. Michelin MA, Crott LS, Assis-Pandochi AI, Coimbra TM, Teixeira JE, Barbosa JE. Influence of the electric charge of the antigen and the immune complex (IC) lattice on the IC activation of human complement. Int J Exp Pathol. 2002;83:105-110.
99. Daha MR, Miltenburg AM, Hiemstra PS, Klar-Mohamad N, Van Es LA, Van Hinsbergh VW. The complement subcomponent C1q mediates binding of immune complexes and aggregates to endothelial cells in vitro. Eur J Immunol. 1988;18:783-787.
100. Beynon HL, Davies KA, Haskard DO, Walport MJ. Erythrocyte complement receptor type 1 and interactions between immune complexes, neutrophils, and endothelium. J Immunol. 1994;153:3160-3167.
101. Bohnsack JF, Tenner AJ, Laurie GW, Kleinman HK, Martin GR, Brown EJ. The C1q subunit of the first component of complement binds to laminin: a mechanism for the deposition and retention of immune complexes in basement membrane. Proc Natl Acad Sci U S A. 1985;82: 3824-3828.
102. Rostagno AA, Gallo G, Gold LI. Binding of polymeric IgG to fibronectin in extracellular matrices: an in vitro paradigm for immune-complex deposition. Mol Immunol. 2002;38:1101-1111.
103. Schifferli JA, Taylor RP. Physiological and pathological aspects of circulating immune complexes. Kidney Int. 1989;35:993-1003.
104. Walport MJ. Complement: first of two parts. N Engl J Med. 2001;344: 1058-1066.
105. 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. Arthritis critically dependent on innate immune system players. Immunity. 2002;16:157-168.
106. Schmidt RE, Gessner JE. Fc receptors and their interaction with complement in autoimmunity. Immunol Lett. 2005;100:56-67.
107. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol. 2008;8:34-47.
108. Su K, Yang H, Li X, Li X, Gibson AW, Cafardi JM, Zhou T, Edberg JC, Kimberly RP. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol. 2007;178: 3272-3280.
109. Boruchov AM, Heller G, Veri MC, Bonvini E, Ravetch JV, Young JW. Activating and inhibitory IgG Fc receptors on human DCs mediate opposing functions. J Clin Invest. 2005;115:2914-2923.
110. Veri MC, Gorlatov S, Li H, Burke S, Johnson S, Stavenhagen J, Stein KE, Bonvini E, Koenig S. Monoclonal antibodies capable of discriminating the human inhibitory Fcgamma-receptor IIB (CD32B) from the activating Fcgamma-receptor IIA (CD32A): biochemical, biological and functional characterization. Immunology. 2007;121:392-404.
111. Hogarth PM. Fc receptors are major mediators of antibody based inflammation in autoimmunity. Curr Opin Immunol. 2002;14:798-802.
112. Selvaraj P, Fifadara N, Nagarajan S, Cimino A, Wang G. Functional regulation of human neutrophil Fc gamma receptors. Immunol Res. 2004;29:219-230.
113. Nimmerjahn F. Activating and inhibitory FcgammaRs in autoimmune disorders. Springer Semin Immunopathol. 2006;28:305-319.
114. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity. 2006;24:19-28.
115. Fodor S, Jakus Z, Mocsai A. ITAM-based signaling beyond the adaptive immune response. Immunol Lett. 2006;104:29-37.
116. Baumann U, Kohl J, Tschernig T, Schwerter-Strumpf K, Verbeek JS, Schmidt RE, Gessner JE. A codominant role of Fc gamma RI/III and C5aR in the reverse Arthus reaction. J Immunol. 2000;164:1065-1070.
117. Baumann U, Chouchakova N, Gewecke B, Kohl J, Carroll MC, Schmidt RE, Gessner JE. Distinct tissue site-specific requirements of mast cells and complement components C3/C5a receptor in IgG immune complex-induced injury of skin and lung. J Immunol. 2001;167:1022-1027.
118. Welch TR. Complement in glomerulonephritis. Nat Genet. 2002;31: 333-334.
119. Bao L, Osawe I, Puri T, Lambris JD, Haas M, Quigg RJ. C5a promotes development of experimental lupus nephritis which can be blocked with a specific receptor antagonist. Eur J Immunol. 2005;35:2496-2506.
120. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, Gebhard F, Younger JG, Drouin SM, Wetsel RA, Ward PA. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med. 2006;12:682-687.
121. Shushakova N, Skokowa J, Schulman J, Baumann U, Zwirner J, Schmidt RE, Gessner JE. C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J Clin Invest. 2002;110:1823-1830.
122. Lewis MJ, Botto M. Complement deficiencies in humans and animals: links to autoimmunity. Autoimmunity. 2006;39:367-378.
123. Bao L, Quigg RJ. Complement in lupus nephritis: the good, the bad, and the unknown. Semin Nephrol. 2007;27:69-80.
124. Karp DR. Complement and systemic lupus erythematosus. Curr Opin Rheumatol. 2005;17:538-542.
125. Trouw LA, Groeneveld TW, Seelen MA, Duijs JM, Bajema IM, Prins FA, Kishore U, Salant DJ, Verbeek JS, van Kooten C, Daha MR. Anti-C1q autoantibodies deposit in glomeruli but are only pathogenic in combination with glomerular C1q-containing immune complexes. J Clin Invest. 2004;114:679-688.
126. Trendelenburg M, Fossati-Jimack L, Cortes-Hernandez J, Turnberg D, Lewis M, Izui S, Cook HT, Botto M. The role of complement in cryoglobulin-induced immune complex glomerulonephritis. J Immunol. 2005;175:6909-6914.
127. Norman MU, Lister KJ, Yang YH, Issekutz A, Hickey MJ. TNF regulates leukocyte-endothelial cell interactions and microvascular dysfunction during immune complex-mediated inflammation. Br J Pharmacol. 2005;144:265-274.
128. Coxon A, Cullere X, Knight S, Sethi S, Wakelin MW, Stavrakis G, Luscinskas FW, Mayadas TN. Fc gamma RIII mediates neutrophil recruitment to immune complexes. a mechanism for neutrophil accumulation in immune-mediated inflammation. Immunity. 2001;14:693-704.
129. Florey OJ, Johns M, Esho OO, Mason JC, Haskard DO. Antiendothelial cell antibodies mediate enhanced leukocyte adhesion to cytokine-acti-vated endothelial cells through a novel mechanism requiring cooperation between FcγRIIa and CXCR1/2. Blood. 2007;109:3881-3889.
130. Lauterbach M, O'Donnell P, Asano K, Mayadas TN. Role of TNF priming and adhesion molecules in neutrophil recruitment to intra-vascular immune complexes. J Leukoc Biol. 2008;83:1423-1430.
131. Crockett-Torabi E, Smith CW, Kateley JR, Patterson R, Tsai P, Fantone JC. Insoluble immune complex-stimulated neutrophil leukotriene B4 production is dependent on Fc gamma RII and Fc gamma RIII and independent of pertussis toxin-sensitive signal transduction pathways. Am J Pathol. 1992;140:613-620.
132. Unkeless JC, Shen Z, Lin CW, DeBeus E. Function of human Fc gamma RIIA and Fc gamma RIIIB. Semin Immunol. 1995;7:37-44.
133. Utomo A, Hirahashi J, Mekala D, Asano K, Glogauer M, Cullere X, Mayadas TN. Requirement for Vav proteins in post-recruitment neu-trophil cytotoxicity in IgG but not complement C3-dependent injury. J Immunol. 2008;180:6279-6287.
134. Worth RG, Chien CD, Chien P, Reilly MP, McKenzie SE, Schreiber AD. Platelet FcgammaRIIA binds and internalizes IgG-containing complexes. Exp Hematol. 2006;34:1490-1495.
135. McKenzie SE, Taylor SM, Malladi P, Yuhan H, Cassel DL, Chien P, Schwartz E, Schreiber AD, Surrey S, Reilly MP. The role of the human Fc receptor Fc gamma RIIA in the immune clearance of platelets: a transgenic mouse model. J Immunol. 1999;162:4311-4318.
136. Tan Sardjono C, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, Wicks IP, Campbell IK, McKenzie SE, Brooks M, Stevenson AW, Hogarth PM. Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum. 2005;52:3220-3229.
137. Tsuboi N, Asano K, Lauterbach M, Mayadas TN. Human neutrophil Fcgamma receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity. 2008;28:833-846.
138. Lister KJ, James WG, Hickey MJ. Immune complexes mediate rapid alterations in microvascular permeability: roles for neutrophils, complement, and platelets. Microcirculation. 2007;14:709-722.
139. 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. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature. 2006;439:851-855.
140. Willcocks LC, Lyons PA, Clatworthy MR, Robinson JI, Yang W, Newland SA, Plagnol V, McGovern NN, Condliffe AM, Chilvers ER, Adu D, Jolly EC, Watts R, Lau YL, Morgan AW, Nash G, Smith KG. Copy number of FCGR3B, which is associated with systemic lupus erythematosus, correlates with protein expression and immune complex uptake. J Exp Med. 2008;205:1573-1582.
141. Fanciulli M, Norsworthy PJ, Petretto E, Dong R, Harper L, Kamesh L, Heward JM, Gough SC, de Smith A, Blakemore AI, Froguel P, Owen CJ, Pearce SH, Teixeira L, Guillevin L, Graham DS, Pusey CD, Cook HT, Vyse TJ, Aitman TJ. FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat Genet. 2007;39:721-723.
142. Zhang Y, Ramos BF, Jakschik BA. Augmentation of reverse Arthus reaction by mast cells in mice. J Clin Invest. 1991;88:841-846.
143. Sylvestre DL, Ravetch JV. A dominant role for mast cell Fc receptors in the Arthus reaction. Immunity. 1996;5:387-390.
144. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science. 2002;297:1689-1692.
145. Zhou JS, Xing W, Friend DS, Austen KF, Katz HR. Mast cell deficiency in Kit(W-sh) mice does not impair antibody-mediated arthritis. J Exp Med. 2007;204:2797-2802.
146. Nigrovic PA, Gray DH, Jones T, Hallgren J, Kuo FC, Chaletzky B, Gurish M, Mathis D, Benoist C, Lee DM. Genetic inversion in mast cell-deficient (W(sh)) mice interrupts corin and manifests as hemato-poietic and cardiac aberrancy. Am J Pathol. 2008;173:1693-1701.
147. Nigrovic PA, Lee DM. Synovial mast cells: role in acute and chronic arthritis. Immunol Rev. 2007;217:19-37.
148. Duffield JS, Tipping PG, Kipari T, Cailhier JF, Clay S, Lang R, Bon-ventre JV, Hughes J. Conditional ablation of macrophages halts progression of crescentic glomerulonephritis. Am J Pathol. 2005;167: 1207-1219.
149. Bergtold A, Gavhane A, D'Agati V, Madaio M, Clynes R. FcR-bearing myeloid cells are responsible for triggering murine lupus nephritis. J Immunol. 2006;177:7287-7295.
150. Braselmann S, Taylor V, Zhao H, Wang S, Sylvain C, Baluom M, Qu K, Herlaar E, Lau A, Young C, Wong BR, Lovell S, Sun T, Park G, Argade A, Jurcevic S, Pine P, Singh R, Grossbard EB, Payan DG, Masuda ES. R406, an orally available spleen tyrosine kinase inhibitor blocks fc receptor signaling and reduces immune complex-mediated inflammation. J Pharmacol Exp Ther. 2006;319:998-1008.
151. Pine PR, Chang B, Schoettler N, Banquerigo ML, Wang S, Lau A, Zhao F, Grossbard EB, Payan DG, Brahn E. Inflammation and bone erosion are suppressed in models of rheumatoid arthritis following treatment with a novel Syk inhibitor. Clin Immunol. 2007;124:244-257.
152. Bahjat FR, Pine PR, Reitsma A, Cassafer G, Baluom M, Grillo S, Chang B, Zhao FF, Payan DG, Grossbard EB, Daikh DI. An orally bioavailable spleen tyrosine kinase inhibitor delays disease progression and prolongs survival in murine lupus. Arthritis Rheum. 2008;58:1433-1444.
153. Weinblatt ME, Kavanaugh A, Burgos-Vargas R, Dikranian AH, Medrano-Ramirez G, Morales-Torres JL, Murphy FT, Musser TK, Straniero N, Vicente-Gonzales AV, Grossbard E. Treatment of rheumatoid arthritis with a syk kinase inhibitor: a twelve-week, randomized, placebo-controlled trial. Arthritis Rheum. 2008;58:3309-3318.
154. Kyttaris VC, Tsokos GC. Syk kinase as a treatment target for therapy in autoimmune diseases. Clin Immunol. 2007;124:235-237.
155. Peer D, Park EJ, Morishita Y, Carman CV, Shimaoka M. Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target. Science. 2008;319:627-630.
156. Peer D, Zhu P, Carman CV, Lieberman J, Shimaoka M. Selective gene silencing in activated leukocytes by targeting siRNAs to the integrin lymphocyte function-associated antigen-1. Proc Natl Acad Sci U S A. 2007;104:4095-4100.