SLE-associated risk factors affect DC function

Immunological Reviews

Volumn 269, Issue 1, 2016, Pages 100-117

  Son, Myoungsun ^a   Kim, Sun Jung ^a   Diamond, Betty ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Dendritic cells; Immune tolerance; Risk alleles; Systemic lupus

Indexed keywords

AUTOANTIBODY; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; COLECALCIFEROL; COMPLEMENT COMPONENT C1Q; DIHYDROXYCOLECALCIFEROL; FC RECEPTOR; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; TRANSCRIPTION FACTOR;

ALLELE; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL SUBPOPULATION; DENDRITIC CELL; DISEASE PREDISPOSITION; GENETIC RISK; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; ADAPTIVE IMMUNITY; B LYMPHOCYTE; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; RISK FACTOR;

ADAPTIVE IMMUNITY; ALLELES; AUTOANTIBODIES; B-LYMPHOCYTES; DENDRITIC CELLS; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; IMMUNE TOLERANCE; IMMUNITY, INNATE; LUPUS ERYTHEMATOSUS, SYSTEMIC; POLYMORPHISM, GENETIC; RISK FACTORS;

EID: 84950160580     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12348     Document Type: Article

References (208)

1. Mildner A, Jung S. Development and function of dendritic cell subsets. Immunity 2014;40:642-656.
2. Schulz O, et al. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 2000;13:453-462.
3. Hochrein H, et al. Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J Exp Med 2000;192:823-833.
4. - subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999;189:587-592.
5. Pulendran B, et al. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc Natl Acad Sci USA 1999;96:1036-1041.
6. Coombes JL, Maloy KJ. Control of intestinal homeostasis by regulatory T cells and dendritic cells. Semin Immunol 2007;19:116-126.
7. + regulatory T cells. J Dermatol Sci 2009;54:69-75.
8. + dendritic cells. Eur J Immunol 2010;40:1877-1883.
9. + regulatory T cells. J Immunol 2008;181:6923-6933.
10. O'Doherty U, et al. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 1994;82:487-493.
11. Tezuka H, et al. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 2011;34:247-257.
12. Young LJ, et al. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat Immunol 2008;9:1244-1252.
13. + dendritic cells to produce type I IFN. J Immunol 2001;166:2291-2295.
14. Proietto AI, et al. Differential production of inflammatory chemokines by murine dendritic cell subsets. Immunobiology 2004;209:163-172.
15. + cytotoxic regulatory T cells. Blood 2006;107:1031-1038.
16. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003;19:225-234.
17. + subset of human blood dendritic cells is a direct precursor of Langerhans cells. J Immunol 1999;163:1409-1419.
18. Dzionek A, et al. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000;165:6037-6046.
19. + nonlymphoid dendritic cells. Immunity 2012;37:60-73.
20. Watchmaker PB, et al. Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat Immunol 2014;15:98-108.
21. Segura E, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 2013;38:336-348.
22. Greter M, et al. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 2012;36:1031-1046.
23. Segura E, Amigorena S. Inflammatory dendritic cells in mice and humans. Trends Immunol 2013;34:440-445.
24. Munn DH, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2, 3-dioxygenase. Science 2002;297:1867-1870.
25. Mellor AL, et al. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2, 3 dioxygenase. Int Immunol 2004;16:1391-1401.
26. Holtschke T, et al. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 1996;87:307-317.
27. Tailor P, Tamura T, Morse HC 3rd, Ozato K. The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood 2008;111:1942-1945.
28. - dendritic cell development. Proc Natl Acad Sci USA 2004;101:8981-8986.
29. + dendritic cells in cytotoxic T cell immunity. Science 2008;322:1097-1100.
30. Edelson BT, et al. CD8alpha(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 2011;35:236-248.
31. Lewis KL, et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 2011;35:780-791.
32. Hacker C, et al. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 2003;4:380-386.
33. + dendritic cell subset in Id2-deficient mice. J Allergy Clin Immunol 2003;111:136-142.
34. Ghosh HS, Cisse B, Bunin A, Lewis KL, Reizis B. Continuous expression of the transcription factor e2-2 maintains the cell fate of mature plasmacytoid dendritic cells. Immunity 2010;33:905-916.
35. Cisse B, et al. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 2008;135:37-48.
36. Schotte R, Nagasawa M, Weijer K, Spits H, Blom B. The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J Exp Med 2004;200:1503-1509.
37. Sasaki I, et al. Spi-B is critical for plasmacytoid dendritic cell function and development. Blood 2012;120:4733-4743.
38. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003;21:685-711.
39. Dhodapkar MV, Steinman RM, Krasovsky J, Munz C, Bhardwaj N. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 2001;193:233-238.
40. Nakagawa T, et al. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 1998;280:450-453.
41. Bamboat ZM, et al. Human liver dendritic cells promote T cell hyporesponsiveness. J Immunol 2009;182:1901-1911.
42. Round JL, O'Connell RM, Mazmanian SK. Coordination of tolerogenic immune responses by the commensal microbiota. J Autoimmun 2010;34:J220-J225.
43. Huang YM, Yang JS, Xu LY, Link H, Xiao BG. Autoantigen-pulsed dendritic cells induce tolerance to experimental allergic encephalomyelitis (EAE) in Lewis rats. Clin Exp Immunol 2000;122:437-444.
44. Fleeton M, et al. Involvement of dendritic cell subsets in the induction of oral tolerance and immunity. Ann N Y Acad Sci 2004;1029:60-65.
45. Alvarez D, Vollmann EH, von Andrian UH. Mechanisms and consequences of dendritic cell migration. Immunity 2008;29:325-342.
46. Manicassamy S, Pulendran B. Dendritic cell control of tolerogenic responses. Immunol Rev 2011;241:206-227.
47. Medzhitov R, Janeway CA Jr. Innate immunity: the virtues of a nonclonal system of recognition. Cell 1997;91:295-298.
48. Tian J, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007;8:487-496.
49. Bowie A, O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J Leukoc Biol 2000;67:508-514.
50. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science 2003;300:1524-1525.
51. Agrawal S, et al. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J Immunol 2003;171:4984-4989.
52. Dillon S, et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest 2006;116:916-928.
53. Hidmark A, von Saint Paul A, Dalpke AH. Cutting edge: TLR13 is a receptor for bacterial RNA. J Immunol 2012;189:2717-2721.
54. Signorino G, et al. Role of Toll-like receptor 13 in innate immune recognition of group B streptococci. Infect Immun 2014;82:5013-5022.
55. Akashi S, et al. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J Exp Med 2003;198:1035-1042.
56. Miyake K. Innate recognition of lipopolysaccharide by CD14 and toll-like receptor 4-MD-2: unique roles for MD-2. Int Immunopharmacol 2003;3:119-128.
57. Hoene V, Peiser M, Wanner R. Human monocyte-derived dendritic cells express TLR9 and react directly to the CpG-A oligonucleotide D19. J Leukoc Biol 2006;80:1328-1336.
58. Honda K, et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005;434:772-777.
59. Takaoka A, et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 2005;434:243-249.
60. Steinhagen F, et al. IRF-5 and NF-kappaB p50 co-regulate IFN-beta and IL-6 expression in TLR9-stimulated human plasmacytoid dendritic cells. Eur J Immunol 2013;43:1896-1906.
61. Kawasaki A, et al. Association of IRF5 polymorphisms with systemic lupus erythematosus in a Japanese population: support for a crucial role of intron 1 polymorphisms. Arthritis Rheum 2008;58:826-834.
62. Akahoshi M, et al. Promoter polymorphisms in the IRF3 gene confer protection against systemic lupus erythematosus. Lupus 2008;17:568-574.
63. Fu Q, et al. Association of a functional IRF7 variant with systemic lupus erythematosus. Arthritis Rheum 2011;63:749-754.
64. Stone RC, et al. Interferon regulatory factor 5 activation in monocytes of systemic lupus erythematosus patients is triggered by circulating autoantigens independent of type I interferons. Arthritis Rheum 2012;64:788-798.
65. Liossis SN, Vassilopoulos D, Kovacs B, Tsokos GC. Immune cell biochemical abnormalities in systemic lupus erythematosus. Clin Exp Rheumatol 1997;15:677-684.
66. Scheinecker C, Zwolfer B, Koller M, Manner G, Smolen JS. Alterations of dendritic cells in systemic lupus erythematosus: phenotypic and functional deficiencies. Arthritis Rheum 2001;44:856-865.
67. Koller M, Zwolfer B, Steiner G, Smolen JS, Scheinecker C. Phenotypic and functional deficiencies of monocyte-derived dendritic cells in systemic lupus erythematosus (SLE) patients. Int Immunol 2004;16:1595-1604.
68. Gajewski TF, Qian D, Fields P, Fitch FW. Anergic T-lymphocyte clones have altered inositol phosphate, calcium, and tyrosine kinase signaling pathways. Proc Natl Acad Sci USA 1994;91:38-42.
69. Merrell KT, et al. Identification of anergic B cells within a wild-type repertoire. Immunity 2006;25:953-962.
70. Ding D, Mehta H, McCune WJ, Kaplan MJ. Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus. J Immunol 2006;177:5878-5889.
71. Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL. Plasmacytoid dendritic cells (natural interferon- alpha/beta-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 2001;159:237-243.
72. Fukuyama S, Kajiwara E, Suzuki N, Miyazaki N, Sadoshima S, Onoyama K. Systemic lupus erythematosus after alpha-interferon therapy for chronic hepatitis C: a case report and review of the literature. Am J Gastroenterol 2000;95:310-312.
73. Tolaymat A, Leventhal B, Sakarcan A, Kashima H, Monteiro C. Systemic lupus erythematosus in a child receiving long-term interferon therapy. J Pediatr 1992;120:429-432.
74. Niewold TB, Swedler WI. Systemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis C. Clin Rheumatol 2005;24:178-181.
75. Kariuki SN, Crow MK, Niewold TB. The PTPN22 C1858T polymorphism is associated with skewing of cytokine profiles toward high interferon-alpha activity and low tumor necrosis factor alpha levels in patients with lupus. Arthritis Rheum 2008;58:2818-2823.
76. Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK. Association of the IRF5 risk haplotype with high serum interferon-alpha activity in systemic lupus erythematosus patients. Arthritis Rheum 2008;58:2481-2487.
77. Kariuki SN, Kirou KA, MacDermott EJ, Barillas-Arias L, Crow MK, Niewold TB. Cutting edge: autoimmune disease risk variant of STAT4 confers increased sensitivity to IFN-alpha in lupus patients in vivo. J Immunol 2009;182:34-38.
78. Santiago-Raber ML, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med 2003;197:777-788.
79. Wu X, Peng SL. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum 2006;54:336-342.
80. Hron JD, Peng SL. Type I IFN protects against murine lupus. J Immunol 2004;173:2134-2142.
81. Wang Y, et al. PTPN22 variant R620W associates with reduced TLR7-induced type 1 Interferon in SLE. Arthritis Rheum 2015;67:2403-2414.
82. Thomas R, Davis LS, Lipsky PE. Rheumatoid synovium is enriched in mature antigen-presenting dendritic cells. J Immunol 1994;152:2613-2623.
83. De Palma G, et al. The possible role of ChemR23/Chemerin axis in the recruitment of dendritic cells in lupus nephritis. Kidney Int 2011;79:1228-1235.
84. Fiore N, et al. Immature myeloid and plasmacytoid dendritic cells infiltrate renal tubulointerstitium in patients with lupus nephritis. Mol Immunol 2008;45:259-265.
85. Keller AD, Maniatis T. Identification and characterization of a novel repressor of beta-interferon gene expression. Genes Dev 1991;5:868-879.
86. Turner CA Jr, Mack DH, Davis MM. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 1994;77:297-306.
87. Keller AD, Maniatis T. Only two of the five zinc fingers of the eukaryotic transcriptional repressor PRDI-BF1 are required for sequence-specific DNA binding. Mol Cell Biol 1992;12:1940-1949.
88. Kuo TC, Calame KL. B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites. J Immunol 2004;173:5556-5563.
89. Dillon SC, Zhang X, Trievel RC, Cheng X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 2005;6:227.
90. Gyory I, Wu J, Fejer G, Seto E, Wright KL. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol 2004;5:299-308.
91. Ancelin K, et al. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 2006;8:623-630.
92. Martins G, Calame K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu Rev Immunol 2008;26:133-169.
93. Kallies A, et al. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J Exp Med 2004;200:967-977.
94. Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 2003;19:607-620.
95. Lin KI, et al. Reishi polysaccharides induce immunoglobulin production through the TLR4/TLR2-mediated induction of transcription factor Blimp-1. J Biol Chem 2006;281:24111-24123.
96. Doody GM, Stephenson S, Tooze RM. BLIMP-1 is a target of cellular stress and downstream of the unfolded protein response. Eur J Immunol 2006;36:1572-1582.
97. Cattoretti G, Shaknovich R, Smith PM, Jack HM, Murty VV, Alobeid B. Stages of germinal center transit are defined by B cell transcription factor coexpression and relative abundance. J Immunol 2006;177:6930-6939.
98. Cattoretti G, Angelin-Duclos C, Shaknovich R, Zhou H, Wang D, Alobeid B. PRDM1/Blimp-1 is expressed in human B-lymphocytes committed to the plasma cell lineage. J Pathol 2005;206:76-86.
99. Shaffer AL, et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004;21:81-93.
100. Martins GA, et al. Transcriptional repressor Blimp-1 regulates T cell homeostasis and function. Nat Immunol 2006;7:457-465.
101. Gong D, Malek TR. Cytokine-dependent Blimp-1 expression in activated T cells inhibits IL-2 production. J Immunol 2007;178:242-252.
102. Cimmino L, et al. Blimp-1 attenuates Th1 differentiation by repression of ifng, tbx21, and bcl6 gene expression. J Immunol 2008;181:2338-2347.
103. Kallies A, et al. Transcriptional repressor Blimp-1 is essential for T cell homeostasis and self-tolerance. Nat Immunol 2006;7:466-474.
104. Rutishauser RL, et al. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 2009;31:296-308.
105. Kallies A, Xin A, Belz GT, Nutt SL. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 2009;31:283-295.
106. Shin H, et al. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 2009;31:309-320.
107. Iwakoshi NN, Pypaert M, Glimcher LH. The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J Exp Med 2007;204:2267-2275.
108. Shaffer AL, et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002;17:51-62.
109. Kim SJ, Zou YR, Goldstein J, Reizis B, Diamond B. Tolerogenic function of Blimp-1 in dendritic cells. J Exp Med 2011;208:2193-2199.
110. Kim SJ, Gregersen PK, Diamond B. Regulation of dendritic cell activation by microRNA let-7c and BLIMP1. J Clin Invest 2013;123:823-833.
111. Gateva V, et al. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 2009;41:1228-1233.
112. Han JW, et al. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet 2009;41:1234-1237.
113. Zhou XJ, et al. Genetic association of PRDM1-ATG5 intergenic region and autophagy with systemic lupus erythematosus in a Chinese population. Ann Rheum Dis 2011;70:1330-1337.
114. Piskurich JF, Lin KI, Lin Y, Wang Y, Ting JP, Calame K. BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat Immunol 2000;1:526-532.
115. Smith MA, et al. Positive regulatory domain I (PRDM1) and IRF8/PU.1 counter-regulate MHC class II transactivator (CIITA) expression during dendritic cell maturation. J Biol Chem 2011;286:7893-7904.
116. Vander Lugt B, et al. Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat Immunol 2014;15:161-167.
117. Nakagawa TY, Rudensky AY. The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol Rev 1999;172:121-129.
118. Hsieh CS, deRoos P, Honey K, Beers C, Rudensky AY. A role for cathepsin L and cathepsin S in peptide generation for MHC class II presentation. J Immunol 2002;168:2618-2625.
119. Yang H, Kala M, Scott BG, Goluszko E, Chapman HA, Christadoss P. Cathepsin S is required for murine autoimmune myasthenia gravis pathogenesis. J Immunol 2005;174:1729-1737.
120. Saegusa K, et al. Cathepsin S inhibitor prevents autoantigen presentation and autoimmunity. J Clin Invest 2002;110:361-369.
121. Rupanagudi KV, et al. Cathepsin S inhibition suppresses systemic lupus erythematosus and lupus nephritis because cathepsin S is essential for MHC class II-mediated CD4 T cell and B cell priming. Ann Rheum Dis 2015;74:452-463.
122. Ellinghaus D, et al. Association between variants of PRDM1 and NDP52 and Crohn's disease, based on exome sequencing and functional studies. Gastroenterology 2013;145:339-347.
123. + T cells. J Immunol 2012;189:5682-5693.
124. Jostins L, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012;491:119-124.
125. Kim SJ, et al. Expression of Blimp-1 in dendritic cells modulates the innate inflammatory response in dextran sodium sulfate-induced colitis. Mol Med 2014;20:707-719.
126. Chang DH, Angelin-Duclos C, Calame K. BLIMP-1: trigger for differentiation of myeloid lineage. Nat Immunol 2000;1:169-176.
127. Severa M, et al. The transcriptional repressor BLIMP1 curbs host defenses by suppressing expression of the chemokine CCL8. J Immunol 2014;192:2291-2304.
128. Kallies A, et al. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 2011;117:1869-1879.
129. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008;8:34-47.
130. + dendritic cells. Blood 2012;120:5163-5172.
131. Dobel T, et al. FcgammaRIII (CD16) equips immature 6-sulfo LacNAc-expressing dendritic cells (slanDCs) with a unique capacity to handle IgG-complexed antigens. Blood 2013;121:3609-3618.
132. Tamoutounour S, et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 2013;39:925-938.
133. Regnault A, et al. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med 1999;189:371-380.
134. Heijnen IA, et al. Antigen targeting to myeloid-specific human Fc gamma RI/CD64 triggers enhanced antibody responses in transgenic mice. J Clin Invest 1996;97:331-338.
135. Kima PE, et al. Internalization of Leishmania mexicana complex amastigotes via the Fc receptor is required to sustain infection in murine cutaneous leishmaniasis. J Exp Med 2000;191:1063-1068.
136. Sutterwala FS, Noel GJ, Clynes R, Mosser DM. Selective suppression of interleukin-12 induction after macrophage receptor ligation. J Exp Med 1997;185:1977-1985.
137. Grazia Cappiello M, Sutterwala FS, Trinchieri G, Mosser DM, Ma X. Suppression of Il-12 transcription in macrophages following Fc gamma receptor ligation. J Immunol 2001;166:4498-4506.
138. Kim S, Elkon KB, Ma X. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 2004;21:643-653.
139. Kim SJ, et al. Increased IL-12 inhibits B cells' differentiation to germinal center cells and promotes differentiation to short-lived plasmablasts. J Exp Med 2008;205:2437-2448.
140. Tanaka M, Krutzik SR, Sieling PA, Lee DJ, Rea TH, Modlin RL. Activation of Fc gamma RI on monocytes triggers differentiation into immature dendritic cells that induce autoreactive T cell responses. J Immunol 2009;183:2349-2355.
141. Laborde EA, et al. Immune complexes inhibit differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol 2007;179:673-681.
142. Kim SJ, Diamond B. Generation and maturation of bone marrow-derived DCs under serum-free conditions. J Immunol Methods 2007;323:101-108.
143. Karassa FB, Trikalinos TA, Ioannidis JP. Fcgamma R-SLEM-AI. Role of the Fcgamma receptor IIa polymorphism in susceptibility to systemic lupus erythematosus and lupus nephritis: a meta-analysis. Arthritis Rheum 2002;46:1563-1571.
144. Binstadt BA, Geha RS, Bonilla FA. IgG Fc receptor polymorphisms in human disease: implications for intravenous immunoglobulin therapy. J Allergy Clin Immunol 2003;111:697-703.
145. White JH. Vitamin D metabolism and signaling in the immune system. Rev Endocr Metab Disord 2012;13:21-29.
146. Karthaus N, et al. Vitamin D controls murine and human plasmacytoid dendritic cell function. J Invest Dermatol 2014;134:1255-1264.
147. Pedersen AW, Claesson MH, Zocca MB. Dendritic cells modified by vitamin D: future immunotherapy for autoimmune diseases. Vitam Horm 2011;86:63-82.
148. Di Rosa M, Malaguarnera M, Nicoletti F, Malaguarnera L. Vitamin D3: a helpful immuno-modulator. Immunology 2011;134:123-139.
149. Piemonti L, et al. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol 2000;164:4443-4451.
150. Sigmundsdottir H, et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat Immunol 2007;8:285-293.
151. Unger WW, Laban S, Kleijwegt FS, van der Slik AR, Roep BO. Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur J Immunol 2009;39:3147-3159.
152. Brosbol-Ravnborg A, Bundgaard B, Hollsberg P. Synergy between vitamin D(3) and Toll-like receptor agonists regulates human dendritic cell response during maturation. Clin Dev Immunol 2013;2013:807971.
153. Sato T, et al. Human CD1c(+) myeloid dendritic cells acquire a high level of retinoic acid-producing capacity in response to vitamin D(3). J Immunol 2013;191:3152-3160.
154. Dickie LJ, Church LD, Coulthard LR, Mathews RJ, Emery P, McDermott MF. Vitamin D3 down-regulates intracellular Toll-like receptor 9 expression and Toll-like receptor 9-induced IL-6 production in human monocytes. Rheumatology 2010;49:1466-1471.
155. Sadeghi K, et al. Vitamin D3 down-regulates monocyte TLR expression and triggers hyporesponsiveness to pathogen-associated molecular patterns. Eur J Immunol 2006;36:361-370.
156. Griffin MD, Lutz W, Phan VA, Bachman LA, McKean DJ, Kumar R. Dendritic cell modulation by 1alpha, 25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. Proc Natl Acad Sci USA 2001;98:6800-6805.
157. + tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther 2013;19:269-277.
158. Ben-Zvi I, et al. The impact of vitamin D on dendritic cell function in patients with systemic lupus erythematosus. PLoS ONE 2010;5:e9193.
159. Mok CC, Birmingham DJ, Ho LY, Hebert LA, Song H, Rovin BH. Vitamin D deficiency as marker for disease activity and damage in systemic lupus erythematosus: a comparison with anti-dsDNA and anti-C1q. Lupus 2012;21:36-42.
160. Yamada M, et al. Complement C1q regulates LPS-induced cytokine production in bone marrow-derived dendritic cells. Eur J Immunol 2004;34:221-230.
161. Castellano G, et al. Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood 2004;103:3813-3820.
162. Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology 1998;199:265-285.
163. Ghebrehiwet B, Hosszu KK, Valentino A, Peerschke EI. The C1q family of proteins: insights into the emerging non-traditional functions. Front Immunol 2012;3:52-61.
164. Castellano G, Trouw LA, Fiore N, Daha MR, Schena FP, van Kooten C. Infiltrating dendritic cells contribute to local synthesis of C1q in murine and human lupus nephritis. Mol Immunol 2010;47:2129-2137.
165. Vegh Z, Kew RR, Gruber BL, Ghebrehiwet B. Chemotaxis of human monocyte-derived dendritic cells to complement component C1q is mediated by the receptors gC1qR and cC1qR. Mol Immunol 2006;43:1402-1407.
166. Brencicova E, Diebold SS. Nucleic acids and endosomal pattern recognition: how to tell friendfrom foe? Front Cell Infect Microbiol 2013;3:37.
167. Leffler J, Bengtsson AA, Blom AM. The complement system in systemic lupus erythematosus: an update. Ann Rheum Dis 2014;73:1601-1606.
168. Eggleton P, Tenner AJ, Reid KB. C1q receptors. Clin Exp Immunol 2000;120:406-412.
169. Son M, Santiago-Schwarz F, Al-Abed Y, Diamond B. C1q limits dendritic cell differentiation and activation by engaging LAIR-1. Proc Natl Acad Sci USA 2012;109:E3160-E3167.
170. Hosszu KK, et al. DC-SIGN, C1q, and gC1qR form a trimolecular receptor complex on the surface of monocyte-derived immature dendritic cells. Blood 2012;120:1228-1236.
171. Zutter MM, Edelson BT. The alpha2beta1 integrin: a novel collectin/C1q receptor. Immunobiology 2007;212:343-353.
172. Olde Nordkamp MJ, van Eijk M, Urbanus RT, Bont L, Haagsman HP, Meyaard L. Leukocyte-associated Ig-like receptor-1 is a novel inhibitory receptor for surfactant protein D. J Leukoc Biol 2014;96:105-111.
173. Lebbink RJ, et al. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 2006;203:1419-1425.
174. Meyaard L. The inhibitory collagen receptor LAIR-1 (CD305). J Leukoc Biol 2008;83:799-803.
175. Meyaard L, et al. LAIR-1, a novel inhibitory receptor expressed on human mononuclear leukocytes. Immunity 1997;7:283-290.
176. Xu M, Zhao R, Zhao ZJ. Identification and characterization of leukocyte-associated Ig-like receptor-1 as a major anchor protein of tyrosine phosphatase SHP-1 in hematopoietic cells. J Biol Chem 2000;275:17440-17446.
177. Son M, Diamond B. C1q-mediated repression of human monocytes is regulated by leukocyte-associated Ig-like receptor 1 (LAIR-1). Mol Med 2015;20:559-568.
178. Verbrugge A, Rijkers ES, de Ruiter T, Meyaard L. Leukocyte-associated Ig-like receptor-1 has SH2 domain-containing phosphatase-independent function and recruits C-terminal Src kinase. Eur J Immunol 2006;36:190-198.
179. Lebbink RJ, et al. The soluble leukocyte-associated Ig-like receptor (LAIR)-2 antagonizes the collagen/LAIR-1 inhibitory immune interaction. J Immunol 2008;180:1662-1669.
180. Tang X, et al. Leukocyte-associated Ig-like receptor-1-deficient mice have an altered immune cell phenotype. J Immunol 2012;188:548-558.
181. Kaveri SV, Silverman GJ, Bayry J. Natural IgM in immune equilibrium and harnessing their therapeutic potential. J Immunol 2012;188:939-945.
182. Gronwall C, Silverman GJ. Natural IgM: beneficial autoantibodies for the control of inflammatory and autoimmune disease. J Clin Immunol 2014;34(Suppl):S12-S21.
183. Scott D, Botto M. The paradoxical roles of C1q and C3 in autoimmunity. Immunobiology 2015. doi: 10.10161/j.imbio.2015.05.001. [Epub ahead of print].
184. Korb LC, Ahearn JM. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol 1997;158:4525-4528.
185. Ogden CA, et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001;194:781-795.
186. 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.
187. Kim SJ, Gershov D, Ma X, Brot N, Elkon KB. I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med 2002;196:655-665.
188. Kim SJ, Gershov D, Ma X, Brot N, Elkon KB. Opsonization of apoptotic cells and its effect on macrophage and T cell immune responses. Ann N Y Acad Sci 2003;987:68-78.
189. Hoffmann PR, et al. Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J Immunol 2005;174:1393-1404.
190. Ramirez-Ortiz ZG, et al. The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat Immunol 2013;14:917-926.
191. Galvan MD, Foreman DB, Zeng E, Tan JC, Bohlson SS. Complement component C1q regulates macrophage expression of Mer tyrosine kinase to promote clearance of apoptotic cells. J Immunol 2012;188:3716-3723.
192. Vandivier RW, et al. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J Immunol 2002;169:3978-3986.
193. Stegert M, Bock M, Trendelenburg M. Clinical presentation of human C1q deficiency: how much of a lupus? Mol Immunol 2015;67:3-11.
194. Botto M, et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 1998;19:56-59.
195. Racila E, et al. A polymorphism in the complement component C1qA correlates with prolonged response following rituximab therapy of follicular lymphoma. Clin Cancer Res 2008;14:6697-6703.
196. Martens HA, et al. Analysis of C1q polymorphisms suggests association with systemic lupus erythematosus, serum C1q and CH50 levels and disease severity. Ann Rheum Dis 2009;68:715-720.
197. Trouw LA, et al. Genetic variants in the region of the C1q genes are associated with rheumatoid arthritis. Clin Exp Immunol 2013;173:76-83.
198. Radanova M, Vasilev V, Dimitrov T, Deliyska B, Ikonomov V, Ivanova D. Association of rs172378 C1q gene cluster polymorphism with lupus nephritis in Bulgarian patients. Lupus 2015;24:280-289.
199. Kanakoudi-Tsakalidou F, et al. Simultaneous changes in serum HMGB1 and IFN-alpha levels and in LAIR-1 expression on plasmatoid dendritic cells of patients with juvenile SLE. New therapeutic options? Lupus 2014;23:305-312.
200. Seelen MA, Trouw LA, Daha MR. Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens 2003;12:619-624.
201. Marto N, Bertolaccini ML, Calabuig E, Hughes GR, Khamashta MA. Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis 2005;64:444-448.
202. Franchin G, Son M, Kim SJ, Ben-Zvi I, Zhang J, Diamond B. Anti-DNA antibodies cross-react with C1q. J Autoimmun 2013;44:34-39.
203. Lood C, et al. C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 2009;60:3081-3090.
204. Santer DM, et al. C1q deficiency leads to the defective suppression of IFN-alpha in response to nucleoprotein containing immune complexes. J Immunol 2010;185:4738-4749.
205. Teh BK, Yeo JG, Chern LM, Lu J. C1q regulation of dendritic cell development from monocytes with distinct cytokine production and T cell stimulation. Mol Immunol 2011;48:1128-1138.
206. Baruah P, et al. Mice lacking C1q or C3 show accelerated rejection of minor H disparate skin grafts and resistance to induction of tolerance. Eur J Immunol 2010;40:1758-1767.
207. Baumann I, et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 2002;46:191-201.
208. Gaipl US, et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 2007;28:114-121.