FcγRIIB and autoimmunity

Immunological Reviews

Volumn 269, Issue 1, 2016, Pages 194-211

  Espéli, Marion ^a   Smith, Kenneth G C ^b   Clatworthy, Menna R ^b  

^a Universite Paris Sud   (France)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Autoantibodies; Dendritic cells; Fc receptors; Germinal center B cells; Lymphangiogenesis; Macrophages

Indexed keywords

AUTOANTIBODY; COMPLEMENT RECEPTOR; FC RECEPTOR IIB; TOLL LIKE RECEPTOR; FC RECEPTOR; FCGR2B PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MIGRATION; DENDRITIC CELL; GENETIC VARIABILITY; GERMINAL CENTER; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHANGIOGENESIS; MACROPHAGE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; AUTOIMMUNE DISEASE; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; GENETICS; HOMEOSTASIS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; IMMUNOMODULATION; MOUSE;

ADAPTIVE IMMUNITY; ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTES; GENETIC PREDISPOSITION TO DISEASE; HOMEOSTASIS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; IMMUNOMODULATION; MICE; POLYMORPHISM, GENETIC; RECEPTORS, IGG;

EID: 84950122029     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12368     Document Type: Article

References (176)

1. Krause RM, Dimmock NJ, Morens DM. Summary of antibody workshop: the role of humoral immunity in the treatment and prevention of emerging and extant infectious diseases. J Infect Dis 1997;176:549-559.
2. Joller N, Weber SS, Oxenius A. Antibody-Fc receptor interactions in protection against intracellular pathogens. Eur J Immunol 2011;41:889-897.
3. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol 2001;19:275-290.
4. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 2008;105:19571-19578.
5. Smith KG, Clatworthy MR. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat Rev Immunol 2010;10:328-343.
6. Clatworthy MR. Fcy receptor polymorphisms and susceptibility to infection. In: Ackerman Men F ed. Antibody Fc Linking Adaptive and Innate Immunity. London: Academic Press, Elsevier, 2014:217-238.
7. Shields RL, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002;277:26733-26740.
8. Ferrara C, Stuart F, Sondermann P, Brunker P, Umana P. The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 2006;281:5032-5036.
9. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 2007;25:21-50.
10. Lux A, Nimmerjahn F. Impact of differential glycosylation on IgG activity. Adv Exp Med Biol 2011;780:113-124.
11. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 2005;310:1510-1512.
12. Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1995;1:237-243.
13. Dong X, Storkus WJ, Salter RD. Binding and uptake of agalactosyl IgG by mannose receptor on macrophages and dendritic cells. J Immunol 1999;163:5427-5434.
14. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol 2007;44:1524-1534.
15. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006;313:670-673.
16. Ahmed AA, et al. Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J Mol Biol 2014;426:3166-3179.
17. Pincetic A, et al. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 2014;15:707-716.
18. Yamada E, Tsukamoto Y, Sasaki R, Yagyu K, Takahashi N. Structural changes of immunoglobulin G oligosaccharides with age in healthy human serum. Glycoconj J 1997;14:401-405.
19. Selman MH, et al. Changes in antigen-specific IgG1 Fc N-glycosylation upon influenza and tetanus vaccination. Mol Cell Proteomics 2012;11:M111 014563.
20. Parekh RB, Roitt IM, Isenberg DA, Dwek RA, Ansell BM, Rademacher TW. Galactosylation of IgG associated oligosaccharides: reduction in patients with adult and juvenile onset rheumatoid arthritis and relation to disease activity. Lancet 1988;1:966-969.
21. Lauc G, et al. Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet 2013;9:e1003225.
22. Vuckovic F, et al. Systemic lupus erythematosus associates with the decreased immunosuppressive potential of the IgG glycome. Arthritis Rheumatol 2015;doi: 10.1002/art.39273. [Epub ahead of print].
23. Albrecht S, Unwin L, Muniyappa M, Rudd PM. Glycosylation as a marker for inflammatory arthritis. Cancer Biomark 2014;14:17-28.
24. Bernard NJ. Rheumatoid arthritis: changes in ACPA Fc glycosylation patterns prior to RA onset. Nat Rev Rheumatol 2013;9:697.
25. Rombouts Y, et al. Anti-citrullinated protein antibodies acquire a pro-inflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis. Ann Rheum Dis 2015;74:234-241.
26. Harre U, et al. Glycosylation of immunoglobulin G determines osteoclast differentiation and bone loss. Nat Commun 2015;6:6651.
27. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 2011;475:110-113.
28. Lehrnbecher T, et al. Variant genotypes of the low-affinity Fcgamma receptors in two control populations and a review of low-affinity Fcgamma receptor polymorphisms in control and disease populations. Blood 1999;94:4220-4232.
29. Floto RA, et al. Loss of function of a lupus-associated FcgammaRIIb polymorphism through exclusion from lipid rafts. Nat Med 2005;11:1056-1058.
30. Kono H, et al. FcgammaRIIB Ile232Thr transmembrane polymorphism associated with human systemic lupus erythematosus decreases affinity to lipid rafts and attenuates inhibitory effects on B cell receptor signaling. Hum Mol Genet 2005;14:2881-2892.
31. Clatworthy MR, et al. Systemic lupus erythematosus-associated defects in the inhibitory receptor FcgammaRIIb reduce susceptibility to malaria. Proc Natl Acad Sci USA 2007;104:7169-7174.
32. Chen JY, et al. Association of a transmembrane polymorphism of Fcgamma receptor IIb (FCGR2B) with systemic lupus erythematosus in Taiwanese patients. Arthritis Rheum 2006;54:3908-3917.
33. Chu ZT, et al. Association of Fcgamma receptor IIb polymorphism with susceptibility to systemic lupus erythematosus in Chinese: a common susceptibility gene in the Asian populations. Tissue Antigens 2004;63:21-27.
34. Kyogoku C, et al. Fcgamma receptor gene polymorphisms in Japanese patients with systemic lupus erythematosus: contribution of FCGR2B to genetic susceptibility. Arthritis Rheum 2002;46:1242-1254.
35. Siriboonrit U, et al. Association of Fcgamma receptor IIb and IIIb polymorphisms with susceptibility to systemic lupus erythematosus in Thais. Tissue Antigens 2003;61:374-383.
36. Su K, et al. A promoter haplotype of the immunoreceptor tyrosine-based inhibitory motif-bearing FcgammaRIIb alters receptor expression and associates with autoimmunity. I. Regulatory FCGR2B polymorphisms and their association with systemic lupus erythematosus. J Immunol 2004;172:7186-7191.
37. Su K, et al. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol 2007;178:3272-3280.
38. Blank MC, et al. Decreased transcription of the human FCGR2B gene mediated by the -343 G/C promoter polymorphism and association with systemic lupus erythematosus. Hum Genet 2005;117:220-227.
39. Zhou XJ, et al. FCGR2B and FCRLB gene polymorphisms associated with IgA nephropathy. PLoS ONE 2013;8:e61208.
40. Duan ZH, et al. The FCGR2B rs10917661 polymorphism may confer susceptibility to ankylosing spondylitis in Han Chinese: a case-control study. Scand J Rheumatol 2012;41:219-222.
41. Luan JJ, et al. Defective Fc gamma RII gene expression in macrophages of NOD mice: genetic linkage with up-regulation of IgG1 and IgG2b in serum. J Immunol 1996;157:4707-4716.
42. Jiang Y, et al. Genetically determined aberrant down-regulation of FcgammaRIIB1 in germinal center B cells associated with hyper-IgG and IgG autoantibodies in murine systemic lupus erythematosus. Int Immunol 1999;11:1685-1691.
43. Pritchard NR, Cutler AJ, Uribe S, Chadban SJ, Morley BJ, Smith KGC. Autoimmune-prone mice share a promoter haplotype associated with reduced expression and function of the Fc receptor FcgammaRII. Curr Biol 2000;10:227-230.
44. Jiang Y, et al. Polymorphisms in IgG Fc receptor IIB regulatory regions associated with autoimmune susceptibility. Immunogenetics 2000;51:429-435.
45. Li X, et al. Allelic-dependent expression of an activating Fc receptor on B cells enhances humoral immune responses. Sci Transl Med 2013;5:216ra175.
46. Zhang Y, et al. Immune complex/Ig negatively regulate TLR4-triggered inflammatory response in macrophages through Fc gamma RIIb-dependent PGE2 production. J Immunol 2009;182:554-562.
47. Wenink MH, et al. The inhibitory Fc gamma IIb receptor dampens TLR4-mediated immune responses and is selectively up-regulated on dendritic cells from rheumatoid arthritis patients with quiescent disease. J Immunol 2009;183:4509-4520.
48. Karsten CM, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat Med 2012;18:1401-1406.
49. Amigorena S, et al. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 1992;256:1808-1812.
50. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature 1994;369:340.
51. Malbec O, et al. Fc epsilon receptor I-associated lyn-dependent phosphorylation of Fc gamma receptor IIB during negative regulation of mast cell activation. J Immunol 1998;160:1647-1658.
52. Katsumata O, et al. Association of FcgammaRII with low-density detergent-resistant membranes is important for cross-linking-dependent initiation of the tyrosine phosphorylation pathway and superoxide generation. J Immunol 2001;167:5814-5823.
53. Kwiatkowska K, Sobota A. The clustered Fcgamma receptor II is recruited to Lyn-containing membrane domains and undergoes phosphorylation in a cholesterol-dependent manner. Eur J Immunol 2001;31:989-998.
54. Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature 1996;383:263-266.
55. Ono M, Okada H, Bolland S, Yanagi S, Kurosaki T, Ravetch JV. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 1997;90:293-301.
56. Bogers WM, Stad RK, Van Es LA, Daha MR. Both Kupffer cells and liver endothelial cells play an important role in the clearance of IgA and IgG immune complexes. Res Immunol 1992;143:219-224.
57. Ganesan LP, et al. FcgammaRIIb on liver sinusoidal endothelium clears small immune complexes. J Immunol 2012;189:4981-4988.
58. van Lent P, et al. 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 2003;163:1839-1848.
59. Qin D, et al. Fc gamma receptor IIB on follicular dendritic cells regulates the B cell recall response. J Immunol 2000;164:6268-6275.
60. Barrington RA, Pozdnyakova O, Zafari MR, Benjamin CD, Carroll MC. B lymphocyte memory: role of stromal cell complement and FcgammaRIIB receptors. J Exp Med 2002;196:1189-1199.
61. Bergtold A, Desai DD, Gavhane A, Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 2005;23:503-514.
62. Li X, et al. A novel polymorphism in the Fcgamma receptor IIB (CD32B) transmembrane region alters receptor signaling. Arthritis Rheum 2003;48:3242-3252.
63. Willcocks LC, et al. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc Natl Acad Sci USA 2010;107:7881-7885.
64. Harley IT, Kaufman KM, Langefeld CD, Harley JB, Kelly JA. Genetic susceptibility to SLE: new insights from fine mapping and genome-wide association studies. Nat Rev Genet 2009;10:285-290.
65. Lau CS, Yin G, Mok MY. Ethnic and geographical differences in systemic lupus erythematosus: an overview. Lupus 2006;15:715-719.
66. Mackay M, et al. Selective dysregulation of the FcgammaIIB receptor on memory B cells in SLE. J Exp Med 2006;203:2157-2164.
67. van Venrooij WJ, van Beers JJ, Pruijn GJ. Anti-CCP antibody, a marker for the early detection of rheumatoid arthritis. Ann N Y Acad Sci 2008;1143:268-285.
68. Radstake TR, et al. The functional variant of the inhibitory Fcgamma receptor IIb (CD32B) is associated with the rate of radiologic joint damage and dendritic cell function in rheumatoid arthritis. Arthritis Rheum 2006;54:3828-3837.
69. Zhou XJ, et al. Copy number variation of FCGR3A rather than FCGR3B and FCGR2B is associated with susceptibility to anti-GBM disease. Int Immunol 2010;22:45-51.
70. Tackenberg B, et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci USA 2009;106:4788-4792.
71. Bruin M, et al. Platelet count, previous infection and FCGR2B genotype predict development of chronic disease in newly diagnosed idiopathic thrombocytopenia in childhood: results of a prospective study. Br J Haematol 2004;127:561-567.
72. Asahi A, et al. Helicobacter pylori eradication shifts monocyte Fcgamma receptor balance toward inhibitory FcgammaRIIB in immune thrombocytopenic purpura patients. J Clin Invest 2008;118:2939-2949.
73. Wu Z, Zhou J, Prsoon P, Wei X, Liu X, Peng B. Low expression of FCGRIIB in macrophages of immune thrombocytopenia-affected individuals. Int J Hematol 2012;96:588-593.
74. Satoh T, et al. Fcgamma receptor IIB gene polymorphism in adult Japanese patients with primary immune thrombocytopenia. Blood 2013;122:1991-1992.
75. Wu J, et al. Functional Fcgamma receptor polymorphisms are associated with human allergy. PLoS ONE 2014;9:e89196.
76. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 1996;379:346-349.
77. Clynes R, Maizes JS, Guinamard R, Ono M, Takai T, Ravetch JV. Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J Exp Med 1999;189:179-185.
78. Yuasa T, et al. Deletion of fcgamma receptor IIB renders H-2(b) mice susceptible to collagen-induced arthritis. J Exp Med 1999;189:187-194.
79. Suzuki Y, et al. Distinct contribution of Fc receptors and angiotensin II-dependent pathways in anti-GBM glomerulonephritis. Kidney Int 1998;54:1166-1174.
80. Nakamura A, et al. Fcgamma receptor IIB-deficient mice develop Goodpasture's syndrome upon immunization with type IV collagen: a novel murine model for autoimmune glomerular basement membrane disease. J Exp Med 2000;191:899-906.
81. Blom AB, van Lent PL, Holthuysen AE, Jacobs C, van den Berg WB. Skewed balance in basal expression and regulation of activating v inhibitory Fcgamma receptors in macrophages of collagen induced arthritis sensitive mice. Ann Rheum Dis 2003;62:465-471.
82. Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 2000;13:277-285.
83. Boross P, et al. The inhibiting Fc receptor for IgG, FcgammaRIIB, is a modifier of autoimmune susceptibility. J Immunol 2011;187:1304-1313.
84. Vanden Berghe T, et al. Passenger mutations confound interpretation of all genetically modified congenic mice. Immunity 2015;43:200-209.
85. McGaha TL, Sorrentino B, Ravetch JV. Restoration of tolerance in lupus by targeted inhibitory receptor expression. Science 2005;307:590-593.
86. Brownlie RJ, et al. Distinct cell-specific control of autoimmunity and infection by FcgammaRIIb. J Exp Med 2008;205:883-895.
87. Sharp PE, et al. FcgammaRIIb on myeloid cells and intrinsic renal cells rather than B cells protects from nephrotoxic nephritis. J Immunol 2013;190:340-348.
88. Yilmaz-Elis AS, et al. FcgammaRIIb on myeloid cells rather than on B cells protects from collagen-induced arthritis. J Immunol 2014;192:5540-5547.
89. Wakeland EK, Liu K, Graham RR, Behrens TW. Delineating the genetic basis of systemic lupus erythematosus. Immunity 2001;15:397-408.
90. Xiu Y, et al. Transcriptional regulation of Fcgr2b gene by polymorphic promoter region and its contribution to humoral immune responses. J Immunol 2002;169:4340-4346.
91. Rahman ZS, Niu H, Perry D, Wakeland E, Manser T, Morel L. Expression of the autoimmune Fcgr2b NZW allele fails to be upregulated in germinal center B cells and is associated with increased IgG production. Genes Immun 2007;8:604-612.
92. Espeli M, et al. Analysis of a wild mouse promoter variant reveals a novel role for FcgammaRIIb in the control of the germinal center and autoimmunity. J Exp Med 2012;209:2307-2319.
93. Li F, Smith P, Ravetch JV. Inhibitory Fcgamma receptor is required for the maintenance of tolerance through distinct mechanisms. J Immunol 2014;192:3021-3028.
94. Guo F, Velu CS, Grimes HL, Zheng Y. Rho GTPase Cdc42 is essential for B-lymphocyte development and activation. Blood 2009;114:2909-2916.
95. Burbage M, et al. Cdc42 is a key regulator of B cell differentiation and is required for antiviral humoral immunity. J Exp Med 2015;212:53-72.
96. + anti-DNA plasma cells. Nat Immunol 2005;6:99-106.
97. Xiang Z, et al. FcgammaRIIb controls bone marrow plasma cell persistence and apoptosis. Nat Immunol 2007;8:419-429.
98. Shlomchik MJ, Marshak-Rothstein A, Wolfowicz CB, Rothstein TL, Weigert MG. The role of clonal selection and somatic mutation in autoimmunity. Nature 1987;328:805-811.
99. Chan TD, et al. Elimination of germinal-center-derived self-reactive B cells is governed by the location and concentration of self-antigen. Immunity 2012;37:893-904.
100. William J, Euler C, Primarolo N, Shlomchik MJ. B cell tolerance checkpoints that restrict pathways of antigen-driven differentiation. J Immunol 2006;176:2142-2151.
101. Tiller T, et al. Development of self-reactive germinal center B cells and plasma cells in autoimmune Fc gammaRIIB-deficient mice. J Exp Med 2010;207:2767-2778.
102. Rahman ZS, Manser T. Failed up-regulation of the inhibitory IgG Fc receptor Fc gamma RIIB on germinal center B cells in autoimmune-prone mice is not associated with deletion polymorphisms in the promoter region of the Fc gamma RIIB gene. J Immunol 2005;175:1440-1449.
103. Jorgensen TN, et al. Development of murine lupus involves the combined genetic contribution of the SLAM and FcgammaR intervals within the Nba2 autoimmune susceptibility locus. J Immunol 2010;184:775-786.
104. Lin Q, et al. Genetic dissection of the effects of stimulatory and inhibitory IgG Fc receptors on murine lupus. J Immunol 2006;177:1646-1654.
105. Vuyyuru R, Mohan C, Manser T, Rahman ZS. The lupus susceptibility locus Sle1 breaches peripheral B cell tolerance at the antibody-forming cell and germinal center checkpoints. J Immunol 2009;183:5716-5727.
106. Schroeder K, Herrmann M, Winkler TH. The role of somatic hypermutation in the generation of pathogenic antibodies in SLE. Autoimmunity 2013;46:121-127.
107. Detanico T, St Clair JB, Aviszus K, Kirchenbaum G, Guo W, Wysocki LJ. Somatic mutagenesis in autoimmunity. Autoimmunity 2013;46:102-114.
108. Sabouri Z, et al. Redemption of autoantibodies on anergic B cells by variable-region glycosylation and mutation away from self-reactivity. Proc Natl Acad Sci USA 2014;111:E2567-E2575.
109. Schwickert TA, et al. A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J Exp Med 2011;208:1243-1252.
110. Gitlin AD, Shulman Z, Nussenzweig MC. Clonal selection in the germinal centre by regulated proliferation and hypermutation. Nature 2014;509:637-640.
111. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-252.
112. Heath WR, Carbone FR. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol 2009;10:1237-1244.
113. Dudziak D, et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007;315:107-111.
114. Joffre OP, Segura E, Savina A, Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol 2012;12:557-569.
115. Steinman RM. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012;30:1-22.
116. Itano AA, et al. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003;19:47-57.
117. Hawiger D, et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 2001;194:769-779.
118. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003;21:685-711.
119. Roake JA, Rao AS, Morris PJ, Larsen CP, Hankins DF, Austyn JM. Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J Exp Med 1995;181:2237-2247.
120. Reis e Sousa C. Dendritic cells in a mature age. Nat Rev Immunol 2006;6:476-483.
121. Miller JC, et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 2012;13:888-899.
122. Yada A, et al. Accelerated antigen presentation and elicitation of humoral response in vivo by FcgammaRIIB- and FcgammaRI/III-mediated immune complex uptake. Cell Immunol 2003;225:21-32.
123. Kalergis AM, Ravetch JV. Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells. J Exp Med 2002;195:1653-1659.
124. 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.
125. Dhodapkar KM, et al. Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc Natl Acad Sci USA 2005;102:2910-2915.
126. Dhodapkar KM, et al. Selective blockade of the inhibitory Fcgamma receptor (FcgammaRIIB) in human dendritic cells and monocytes induces a type I interferon response program. J Exp Med 2007;204:1359-1369.
127. Laborde EA, et al. Immune complexes inhibit differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol 2007;179:673-681.
128. Pricop L, et al. Differential modulation of stimulatory and inhibitory Fc gamma receptors on human monocytes by Th1 and Th2 cytokines. J Immunol 2001;166:531-537.
129. Tridandapani S, Siefker K, Teillaud JL, Carter JE, Wewers MD, Anderson CL. Regulated expression and inhibitory function of Fcgamma RIIb in human monocytic cells. J Biol Chem 2002;277:5082-5089.
130. + CTL responses in vivo. J Immunol 2002;168:2240-2246.
131. Desai DD, et al. Fc gamma receptor IIB on dendritic cells enforces peripheral tolerance by inhibiting effector T cell responses. J Immunol 2007;178:6217-6226.
132. van Montfoort N, et al. Fcgamma receptor IIb strongly regulates fcgamma receptor-facilitated T cell activation by dendritic cells. J Immunol 2012;189:92-101.
133. Liu Y, Gao X, Masuda E, Redecha PB, Blank MC, Pricop L. Regulated expression of FcgammaR in human dendritic cells controls cross-presentation of antigen-antibody complexes. J Immunol 2006;177:8440-8447.
134. + dendritic cells. Blood 2012;120:5163-5172.
135. Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 2005;5:617-628.
136. Cyster JG. Chemokines and the homing of dendritic cells to the T cell areas of lymphoid organs. J Exp Med 1999;189:447-450.
137. Forster R, et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999;99:23-33.
138. Sallusto F, et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 1998;28:2760-2769.
139. Clatworthy MR, Aronin CE, Mathews RJ, Morgan NY, Smith KG, Germain RN. Immune complexes stimulate CCR7-dependent dendritic cell migration to lymph nodes. Nat Med 2014;20:1458-1463.
140. Bharadwaj D, Stein MP, Volzer M, Mold C, Du Clos TW. The major receptor for C-reactive protein on leukocytes is fcgamma receptor II. J Exp Med 1999;190:585-590.
141. Bharadwaj D, Mold C, Markham E, Du Clos TW. Serum amyloid P component binds to Fc gamma receptors and opsonizes particles for phagocytosis. J Immunol 2001;166:6735-6741.
142. Vermeire S, Van Assche G, Rutgeerts P. The role of C-reactive protein as an inflammatory marker in gastrointestinal diseases. Nat Clin Pract Gastroenterol Hepatol 2005;2:580-586.
143. Grad E, Danenberg HD. C-reactive protein and atherothrombosis: cause or effect? Blood Rev 2013;27:23-29.
144. Du Clos TW, Zlock LT, Rubin RL. Analysis of the binding of C-reactive protein to histones and chromatin. J Immunol 1988;141:4266-4270.
145. Pepys MB, Booth SE, Tennent GA, Butler PJ, Williams DG. Binding of pentraxins to different nuclear structures: C-reactive protein binds to small nuclear ribonucleoprotein particles, serum amyloid P component binds to chromatin and nucleoli. Clin Exp Immunol 1994;97:152-157.
146. Gershov D, Kim S, Brot N, Elkon KB. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J Exp Med 2000;192:1353-1364.
147. Lu J, Marnell LL, Marjon KD, Mold C, Du Clos TW, Sun PD. Structural recognition and functional activation of FcgammaR by innate pentraxins. Nature 2008;456:989-992.
148. Du Clos TW, Mold C. Pentraxins (CRP, SAP) in the process of complement activation and clearance of apoptotic bodies through Fcgamma receptors. Curr Opin Organ Transplant 2011;16:15-20.
149. van Mirre E, et al. Neutrophil responsiveness to IgG, as determined by fixed ratios of mRNA levels for activating and inhibitory FcgammaRII (CD32), is stable over time and unaffected by cytokines. Blood 2006;108:584-590.
150. Willcocks LC, et al. 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.
151. Ericson JA, et al. Gene expression during the generation and activation of mouse neutrophils: implication of novel functional and regulatory pathways. PLoS ONE 2014;9:e108553.
152. Rosales C, Brown EJ. Signal transduction by neutrophil immunoglobulin G Fc receptors. Dissociation of intracytoplasmic calcium concentration rise from inositol 1, 4, 5-trisphosphate. J Biol Chem 1992;267:5265-5271.
153. Zhou MJ, Brown EJ. CR3 (Mac-1, alpha M beta 2, CD11b/CD18) and Fc gamma RIII cooperate in generation of a neutrophil respiratory burst: requirement for Fc gamma RIII and tyrosine phosphorylation. J Cell Biol 1994;125:1407-1416.
154. Coxon A, et al. Fc gamma RIII mediates neutrophil recruitment to immune complexes. a mechanism for neutrophil accumulation in immune-mediated inflammation. Immunity 2001;14:693-704.
155. Ooi JD, et al. FcgammaRIIB regulates T-cell autoreactivity, ANCA production, and neutrophil activation to suppress anti-myeloperoxidase glomerulonephritis. Kidney Int 2014;86:1140-1149.
156. Stein MP, et al. C-reactive protein binding to FcgammaRIIa on human monocytes and neutrophils is allele-specific. J Clin Invest 2000;105:369-376.
157. Aas V, Sand KL, Asheim HC, Benestad HB, Iversen JG. C-reactive protein triggers calcium signalling in human neutrophilic granulocytes via FcgammaRIIa in an allele-specific way. Scand J Immunol 2013;77:442-451.
158. Cox N, Pilling D, Gomer RH. Distinct Fcgamma receptors mediate the effect of serum amyloid p on neutrophil adhesion and fibrocyte differentiation. J Immunol 2014;193:1701-1708.
159. Maharjan AS, Roife D, Brazill D, Gomer RH. Serum amyloid P inhibits granulocyte adhesion. Fibrogenesis Tissue Repair 2013;6:2.
160. Gautier EL, et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 2012;13:1118-1128.
161. Clatworthy MR, Smith KG. FcgammaRIIb balances efficient pathogen clearance and the cytokine-mediated consequences of sepsis. J Exp Med 2004;199:717-723.
162. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008;8:279-289.
163. Asea A, et al. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 2002;277:15028-15034.
164. Chen T, Guo J, Han C, Yang M, Cao X. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol 2009;182:1449-1459.
165. Schulz C, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012;336:86-90.
166. Hashimoto D, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013;38:792-804.
167. Angeli V, et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 2006;24:203-215.
168. Halin C, Tobler NE, Vigl B, Brown LF, Detmar M. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 2007;110:3158-3167.
169. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005;201:1089-1099.
170. Shrestha B, et al. B cell-derived vascular endothelial growth factor A promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes. J Immunol 2010;184:4819-4826.
171. Haneda Y, Hasegawa S, Hirano R, Hashimoto K, Ohsaki A, Ichiyama T. Leukotriene D4 enhances tumor necrosis factor-alpha-induced vascular endothelial growth factor production in human monocytes/macrophages. Cytokine 2011;55:24-28.
172. Clatworthy MR, Harford SK, Mathews RJ, Smith KG. FcgammaRIIb inhibits immune complex-induced VEGF-A production and intranodal lymphangiogenesis. Proc Natl Acad Sci USA 2014;111:17971-17976.
173. Junt T, et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007;450:110-114.
174. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 2009;10:786-793.
175. Kurosaka D, et al. Clinical significance of serum levels of vascular endothelial growth factor, angiopoietin-1, and angiopoietin-2 in patients with rheumatoid arthritis. J Rheumatol 2010;37:1121-1128.
176. Navarro C, et al. Vascular endothelial growth factor plasma levels in patients with systemic lupus erythematosus and primary antiphospholipid syndrome. Lupus 2002;11:21-24.