CD72 is a Negative Regulator of B Cell Responses to Nuclear Lupus Self-antigens and Development of Systemic Lupus Erythematosus
1
조회
0
다운로드
0
인용
0
참고문헌
키워드
초록
Systemic lupus erythematosus (SLE) is the prototypic systemic autoimmune disease characterized by production of autoantibodies to various nuclear antigens and overexpression of genes regulated by IFN-I called IFN signature. Genetic studies on SLE patients and mutational analyses of mouse models demonstrate crucial roles of nucleic acid (NA) sensors in development of SLE. Although NA sensors are involved in induction of anti-microbial immune responses by recognizing microbial NAs, recognition of self NAs by NA sensors induces production of autoantibodies to NAs in B cells and production of IFN-I in plasmacytoid dendritic cells. Among various NA sensors, the endosomal RNA sensor TLR7 plays an essential role in development of SLE at least in mouse models. CD72 is an inhibitory B cell co-receptor containing an immunoreceptor tyrosine-based inhibition motif (ITIM) in the cytoplasmic region and a C-type lectin like-domain (CTLD) in the extracellular region. CD72 is known to regulate development of SLE because CD72 polymorphisms associate with SLE in both human and mice and CD72−/− mice develop relatively severe lupus-like disease. CD72 specifically recognizes the RNA-containing endogenous TLR7 ligand Sm/RNP by its extracellular CTLD, and inhibits B cell responses to Sm/RNP by ITIM-mediated signal inhibition. These findings indicate that CD72 inhibits development of SLE by suppressing TLR7-dependent B cell response to self NAs. CD72 is thus involved in discrimination of self-NAs from microbial NAs by specifically suppressing autoimmune responses to self-NAs.
Abstract
Systemic lupus erythematosus (SLE) is the prototypic systemic autoimmune disease characterized by production of autoantibodies to various nuclear antigens and overexpression of genes regulated by IFN-I called IFN signature. Genetic studies on SLE patients and mutational analyses of mouse models demonstrate crucial roles of nucleic acid (NA) sensors in development of SLE. Although NA sensors are involved in induction of anti-microbial immune responses by recognizing microbial NAs, recognition of self NAs by NA sensors induces production of autoantibodies to NAs in B cells and production of IFN-I in plasmacytoid dendritic cells. Among various NA sensors, the endosomal RNA sensor TLR7 plays an essential role in development of SLE at least in mouse models. CD72 is an inhibitory B cell co-receptor containing an immunoreceptor tyrosine-based inhibition motif (ITIM) in the cytoplasmic region and a C-type lectin like-domain (CTLD) in the extracellular region. CD72 is known to regulate development of SLE because CD72 polymorphisms associate with SLE in both human and mice and CD72−/− mice develop relatively severe lupus-like disease. CD72 specifically recognizes the RNA-containing endogenous TLR7 ligand Sm/RNP by its extracellular CTLD, and inhibits B cell responses to Sm/RNP by ITIM-mediated signal inhibition. These findings indicate that CD72 inhibits development of SLE by suppressing TLR7-dependent B cell response to self NAs. CD72 is thus involved in discrimination of self-NAs from microbial NAs by specifically suppressing autoimmune responses to self-NAs.
참고문헌 (67)
- Guo Y, "A genopedia of lupus genes - lessons from gene knockouts", Curr Rheumatol Rev, 9, pp.90~99 (2013)
- Mohan C, "Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis", Nat Rev Nephrol, 11, pp.329~341 (2015)
- Blasius AL, "Intracellular toll-like receptors", Immunity, 32, pp.305~315 (2010)
- Pandey S, "Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors", Cold Spring Harb Perspect Biol, 7, pp.a016246~ (2014)
- Roers A, "Recognition of endogenous nucleic acids by the innate immune system", Immunity, 44, pp.739~754 (2016)
- Miyake K, "Mechanisms controlling nucleic acid-sensing Toll-like receptors", Int Immunol, 30, pp.43~51 (2018)
- Crowl JT, "Intracellular nucleic acid detection in autoimmunity", Annu Rev Immunol, 35, pp.313~336 (2017)
- Tsubata T, "B-cell tolerance and autoimmunity", F1000 Res, 6, pp.391~ (2017)
- Tsubata T, "Ligand recognition determines the role of inhibitory B cell co-receptors in the regulation of B cell homeostasis and autoimmunity", Front Immunol, 9 (2018)
- Hitomi Y, "CD72 polymorphisms associated with alternative splicing modify susceptibility to human systemic lupus erythematosus through epistatic interaction with FCGR2B", Hum Mol Genet, 13, pp.2907~2917 (2004)
- Qu WM, "Genetic dissection of vasculitis in MRL", lpr lupus mice: a novel susceptibility locus involving the CD72c allele, 2000, pp.30, 2027~2037
- Li DH, "Modulation of peripheral B cell tolerance by CD72 in a murine model", Arthritis Rheum, 58, pp.3192~3204 (2008)
- Xu M, "CD72c is a modifier gene that regulates Faslpr-induced autoimmune disease", J Immunol, 190, pp.5436~5445 (2013)
- Akatsu C, "CD72 negatively regulates B lymphocyte responses to the lupus-related endogenous toll-like receptor 7 ligand Sm", RNP, 2016, pp.213, 2691~2706
- Funabiki M, "Autoimmune disorders associated with gain of function of the intracellular sensor MDA5", Immunity, 40, pp.199~212 (2014)
- Christensen SR, "Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus", Immunity, 25, pp.417~428 (2006)
- Savarese E, "Requirement of Toll-like receptor 7 for pristane-induced production of autoantibodies and development of murine lupus nephritis", Arthritis Rheum, 58, pp.1107~1115 (2008)
- Santiago-Raber ML, "Critical role of TLR7 in the acceleration of systemic lupus erythematosus in TLR9-deficient mice", J Autoimmun, 34, pp.339~348 (2010)
- Leadbetter EA, "Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors", Nature, 416, pp.603~607 (2002)
- Lau CM, "RNA-associated autoantigens activate B cells by combined B cell antigen receptor", Toll-like receptor 7 engagement, 2005, pp.202, 1171~1177
- Bennett L, "Interferon and granulopoiesis signatures in systemic lupus erythematosus blood", J Exp Med, 197, pp.711~723 (2003)
- Baechler EC, "Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus", Proc Natl Acad Sci U S A, 100, pp.2610~2615 (2003)
- Kadowaki N, "Natural interferon alpha", beta-producing cells link innate and adaptive immunity, 2000, pp.192, 219~226
- Savarese E, "U1 small nuclear ribonucleoprotein immune complexes induce type I interferon in plasmacytoid dendritic cells through TLR7", Blood, 107, pp.3229~3234 (2006)
- Kiefer K, "Role of type I interferons in the activation of autoreactive B cells", Immunol Cell Biol, 90, pp.498~504 (2012)
- Das A, "Follicular dendritic cell activation by TLR ligands promotes autoreactive B cell responses", Immunity, 46, pp.106~119 (2017)
- Crow YJ, "Aicardi-Goutières syndrome and the type I interferonopathies", Nat Rev Immunol, 15, pp.429~440 (2015)
- Lee-Kirsch MA, "Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus", Nat Genet, 39, pp.1065~1067 (2007)
- Namjou B, "Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort", Genes Immun, 12, pp.270~279 (2011)
- Stetson DB, "TREX1 prevents cell-intrinsic initiation of autoimmunity", Cell, 134, pp.587~598 (2008)
- Chowdhury D, "The exonuclease TREX1 is in the SET complex and acts in concert with NM23-H1 to degrade DNA during granzyme A-mediated cell death", Mol Cell, 23, pp.133~142 (2006)
- Lehtinen DA, "The TREX1 double-stranded DNA degradation activity is defective in dominant mutations associated with autoimmune disease", J Biol Chem, 283, pp.31649~31656 (2008)
- Mazur DJ, "Excision of 3′ termini by the TREX1 and TREX2 3′-->5′ exonucleases. Characterization of the recombinant proteins", J Biol Chem, 276, pp.17022~17029 (2001)
- Beck-Engeser GB, "An autoimmune disease prevented by anti-retroviral drugs", Retrovirology, 8, pp.91~ (2011)
- Gao D, "Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases", Proc Natl Acad Sci U S A, 112, pp.E5699~E5705 (2015)
- Motani K, "DNA-mediated cyclic GMP-AMP synthase-dependent and -independent regulation of innate immune responses", J Immunol, 194, pp.4914~4923 (2015)
- Kato Y, "Apoptosis-derived membrane vesicles drive the cGAS-STING pathway and enhance type I IFN production in systemic lupus erythematosus", Ann Rheum Dis, 77, pp.1507~1515 (2018)
- Teichmann LL, "Signals via the adaptor MyD88 in B cells and DCs make distinct and synergistic contributions to immune activation and tissue damage in lupus", Immunity, 38, pp.528~540 (2013)
- Hu X, "Integrating autoimmune risk loci with gene-expression data identifies specific pathogenic immune cell subsets", Am J Hum Genet, 89, pp.496~506 (2011)
- Hnisz D, "Super-enhancers in the control of cell identity and disease", Cell, 155, pp.934~947 (2013)
- Adachi T, "The B cell surface protein CD72 recruits the tyrosine phosphatase SHP-1 upon tyrosine phosphorylation", J Immunol, 160, pp.4662~4665 (1998)
- Adachi T, "CD72 negatively regulates signaling through the antigen receptor of B cells", J Immunol, 164, pp.1223~1229 (2000)
- Dustin LB, "Expression of dominant-negative src-homology domain 2-containing protein tyrosine phosphatase-1 results in increased Syk tyrosine kinase activity and B cell activation", J Immunol, 162, pp.2717~2724 (1999)
- Watanabe-Fukunaga R, "Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis", Nature, 356, pp.314~317 (1992)
- Izui S, "Induction of various autoantibodies by mutant gene lpr in several strains of mice", J Immunol, 133, pp.227~233 (1984)
- Robinson WH, "Extensive polymorphism in the extracellular domain of the mouse B cell differentiation antigen Lyb-2", CD72, 1992, pp.149, 880~886
- Tsubata T, "Negative regulation of B cell responses and self-tolerance to RNA-related lupus self-antigen", Proc Jpn Acad, Ser B, Phys Biol Sci, 94, pp.35~44 (2018)
- Pao LI, "B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity", Immunity, 27, pp.35~48 (2007)
- Sato S, "CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice", Immunity, 5, pp.551~562 (1996)
- Nitschke L, "CD22 is a negative regulator of B-cell receptor signalling", Curr Biol, 7, pp.133~143 (1997)
- Otipoby KL, "CD22 regulates thymus-independent responses and the lifespan of B cells", Nature, 384, pp.634~637 (1996)
- Lamagna C, "B cell-specific loss of Lyn kinase leads to autoimmunity", J Immunol, 192, pp.919~928 (2014)
- Hoffmann A, "Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population", Nat Immunol, 8, pp.695~704 (2007)
- Jellusova J, "CD22 x Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity", J Immunol, 184, pp.3618~3627 (2010)
- Takai T, "Role of PIR-B in autoimmune glomerulonephritis", J Biomed Biotechnol, 2011, pp.275302~ (2011)
- Wilkinson R, "Platelet endothelial cell adhesion molecule-1 (PECAM-1", CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease, 2002, pp.100, 184~193
- Brown MH, "A ligand for CD5 is CD5", J Immunol, 185, pp.6068~6074 (2010)
- Kumanogoh A, "Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling", Immunity, 13, pp.621~631 (2000)
- Crocker PR, "Siglecs and their roles in the immune system", Nat Rev Immunol, 7, pp.255~266 (2007)
- Macauley MS, "Siglec-mediated regulation of immune cell function in disease", Nat Rev Immunol, 14, pp.653~666 (2014)
- Hutzler S, "The ligand-binding domain of Siglec-G is crucial for its selective inhibitory function on B1 cells", J Immunol, 192, pp.5406~5414 (2014)
- Schlee M, "Discriminating self from non-self in nucleic acid sensing", Nat Rev Immunol, 16, pp.566~580 (2016)
- Mouchess ML, "Transmembrane mutations in Toll-like receptor 9 bypass the requirement for ectodomain proteolysis and induce fatal inflammation", Immunity, 35, pp.721~732 (2011)
- Canadian Hydroxychloroquine Study Group, "A randomized study of the effect of withdrawing hydroxychloroquine sulfate in systemic lupus erythematosus", N Engl J Med, 324, pp.150~154 (1991)
- Fava A, "Systemic lupus erythematosus: diagnosis and clinical management", J Autoimmun, 96, pp.1~13 (2019)
- Lafyatis R, "Antimalarial agents: closing the gate on Toll-like receptors", Arthritis Rheum, 54, pp.3068~3070 (2006)
- Kuznik A, "Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines", J Immunol, 186, pp.4794~4804 (2011)