Plasmacytoid dendritic cells and RNA-containing immune complexes drive expansion of peripheral B cell subsets with an SLE-like phenotype

PLoS ONE

Volumn 12, Issue 8, 2017, Pages

  Berggren, Olof ^a   Hagberg, Niklas ^a   Alexsson, Andrei ^a   Weber, Gert ^b   Rönnblom, Lars ^a   Eloranta, Maija Leena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD27 ANTIGEN; CD83 ANTIGEN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; SMALL NUCLEAR RIBONUCLEOPROTEIN; ANTIGEN ANTIBODY COMPLEX; LEUKOCYTE ANTIGEN; RNA;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE SUBPOPULATION; CCL3 GENE; CCL4 GENE; CD19+ B LYMPHOCYTE; CD27+ IGD- MEMORY B LYMPHOCYTE; CD27- IGD- B LYMPHOCYTE; CD83 GENE; CELL EXPANSION; CELL INTERACTION; CELL ISOLATION; CELL STIMULATION; CELL SURFACE; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IKAROS FAMILY ZINC FINGER 2 GENE; IL21R GENE; IL4R GENE; MEMORY CELL; PERIPHERAL LYMPHOCYTE; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PROTEIN EXPRESSION; RNA CONTAINING IMMUNE COMPLEX; SYSTEMIC LUPUS ERYTHEMATOSUS; B LYMPHOCYTE; BIOSYNTHESIS; DENDRITIC CELL; HELA CELL LINE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM;

ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, CD; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; COCULTURE TECHNIQUES; DENDRITIC CELLS; GENE EXPRESSION PROFILING; HELA CELLS; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-10; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; PHENOTYPE; RNA;

EID: 85028538972     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0183946     Document Type: Article

References (34)

1. Dörner T, Giesecke C, Lipsky PE. Mechanisms of B cell autoimmunity in SLE. Arthritis Res Ther. 2011; 13:243. https://doi.org/10.1186/ar3433 PMID: 22078750
2. Tsokos GC, Lo MS, Reis PC, Sullivan KE. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol. 2016; 12:716–730. https://doi.org/10.1038/nrrheum.2016.186 PMID: 27872476
3. Eloranta M, Rönnblom L. Cause and consequences of the activated type I interferon system in SLE. J Mol Med (Berl). 2016; 94:1103–1110. https://doi.org/10.1007/s00109-016-1421-4 PMID: 27094810
4. Anolik JH. B cell biology: implications for treatment of systemic lupus erythematosus. Lupus. 2013; 22:342–349. Epub 2013/04/05. https://doi.org/10.1177/0961203312471576 PMID: 23553777
5. Iwata S, Tanaka Y. B-cell subsets, signaling and their roles in secretion of autoantibodies. Lupus. 2016; 25:850–856. https://doi.org/10.1177/0961203316643172 PMID: 27252261
6. Anolik JH, Barnard J, Cappione A, Pugh-Bernard AE, Felgar RE, Looney RJ, et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum. 2004; 50:3580–3590. https://doi.org/10.1002/art.20592 PMID: 15529346
7. Wei C, Anolik J, Cappione A, Zheng B, Pugh-Bernard A, Brooks J, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol 2007; 178:6624–6633. PMID: 17475894
8. Dörner T, Jacobi AM, Lipsky PE. B cells in autoimmunity. Arthritis Res Ther. 2009; 11:247. https://doi.org/10.1186/ar2780 PMID: 19849820
9. Sanz I. Rationale for B cell targeting in SLE. Semin Immunopathol. 2014; 36:365–375. https://doi.org/10.1007/s00281-014-0430-z PMID: 24763533
10. Achour A, Simon Q, Mohr A, Seite JF, Youinou P, Bendaoud B, et al. Human regulatory B cells control the TFH cell response. J Allergy Clin Immunol. 2016. https://doi.org/10.1016/j.jaci.2016.09.042 PMID: 27865860
11. Mauri C, Blair PA. Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol. 2010; 6:636–643. https://doi.org/10.1038/nrrheum.2010.140 PMID: 20856268
12. Gao N, Dresel J, Eckstein V, Gellert R, Storch H, Venigalla RK, et al. Impaired suppressive capacity of activation-induced regulatory B cells in systemic lupus erythematosus. Arthritis Rheum. 2014; 66:2849–2861. https://doi.org/10.1002/art.38742 PMID: 24942956
13. Menon M, Blair PA, Isenberg DA, Mauri C. A Regulatory Feedback between Plasmacytoid Dendritic Cells and Regulatory B Cells Is Aberrant in Systemic Lupus Erythematosus. Immunity. 2016; 44:683–697. https://doi.org/10.1016/j.immuni.2016.02.012 PMID: 26968426
14. 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. PMID: 12932356
15. Fitzgerald-Bocarsly P, Dai J, Singh S. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 2008; 19:3–19. https://doi.org/10.1016/j.cytogfr.2007.10.006PMID: 18248767
16. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19(+)CD24 (hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity. 2010; 32:129–140. https://doi.org/10.1016/j.immuni.2009.11.009 PMID: 20079667
17. Berggren O, Hagberg N, Weber G, Alm GV, Rönnblom L, Eloranta ML. B lymphocytes enhance the interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum. 2012; 64:3409–3419. https://doi.org/10.1002/art.34599 PMID: 22736048
18. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of Systemic Lupus Erythematosus. Arthritis Rheum. 1982; 25:1271–1277. PMID: 7138600
19. Weber G, Trowitzsch S, Kastner B, Luhrmann R, Wahl MC. Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J. 2010; 29:4172–4184. https://doi.org/10.1038/emboj.2010.295 PMID: 21113136
20. Cederblad B, Alm GV. Interferons and the colony-stimulating factors IL-3 and GM-CSF enhance the IFN-alpha response in human blood leucocytes induced by herpes simplex virus. Scand J Immunol. 1991; 34:549–555. PMID: 1719612
21. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med. 1997; 185:1101–1111. PMID: 9091583
22. Sanz I, Wei C, Lee FE, Anolik J. Phenotypic and functional heterogeneity of human memory B cells. Semin Immunol. 2008; 20:67–82. https://doi.org/10.1016/j.smim.2007.12.006 PMID: 18258454
23. Cederblad B, Blomberg S, Vallin H, Perers A, Alm GV, Rönnblom L. Patients with systemic lupus erythematosus have reduced numbers of circulating natural interferon-a-producing cells. J Autoimmun. 1998; 11:465–470. https://doi.org/10.1006/jaut.1998.0215 PMID: 9802930
24. Jacobi AM, Reiter K, Mackay M, Aranow C, Hiepe F, Radbruch A, et al. Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum. 2008; 58:1762–1773. https://doi.org/10.1002/art.23498 PMID: 18512812
25. Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015; 42:607–612. https://doi.org/10.1016/j.immuni.2015.04.005 PMID: 25902480
26. Georg P, Bekeredjian-Ding I. Plasmacytoid dendritic cells control B cell-derived IL-10 production. Autoimmunity. 2012; 45:579–583. https://doi.org/10.3109/08916934.2012.719955 PMID: 22928676
27. Sawaf M, Dumortier H, Monneaux F. Follicular Helper T Cells in Systemic Lupus Erythematosus: Why Should They Be Considered as Interesting Therapeutic Targets? J Immunol Res. 2016; 2016:5767106. https://doi.org/10.1155/2016/5767106 PMID: 27635407
28. Krzyzak L, Seitz C, Urbat A, Hutzler S, Ostalecki C, Glasner J, et al. CD83 Modulates B Cell Activation and Germinal Center Responses. J Immunol. 2016; 196:3581–3594. https://doi.org/10.4049/jimmunol.1502163 PMID: 26983787
29. 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. https://doi.org/10.1084/jem.20110658 PMID: 21948081
30. Richardson C, Chida AS, Adlowitz D, Silver L, Fox E, Jenks SA, et al. Molecular basis of 9G4 B cell autoreactivity in human systemic lupus erythematosus. J mmunol. 2013; 191:4926–4939. https://doi.org/10.4049/jimmunol.1202263 PMID: 24108696
31. Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol. 2002; 3:822–829. https://doi.org/10.1038/ni829 PMID: 12154359.
32. Liu BS, Cao Y, Huizinga TW, Hafler DA, Toes RE. TLR-mediated STAT3 and ERK activation controls IL-10 secretion by human B cells. Eur J Immunol. 2014; 44:2121–2129. https://doi.org/10.1002/eji.201344341 PMID: 24737107
33. Nakou M, Papadimitraki ED, Fanouriakis A, Bertsias GK, Choulaki C, Goulidaki N, et al. Interleukin-21 is increased in active systemic lupus erythematosus patients and contributes to the generation of plasma B cells. Clin Exp Rheumatol. 2013; 31:172–179.
34. Silva R, Moir S, Kardava L, Debell K, Simhadri VR, Ferrando-Martinez S, et al. CD300a is expressed on human B cells, modulates BCR-mediated signaling, and its expression is down-regulated in HIV infection. Blood. 2011; 117:5870–5880. https://doi.org/10.1182/blood-2010-09-310318 PMID: 21482706