Self DNA from lymphocytes that have undergone activation-induced cell death enhances murine B cell proliferation and antibody production

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Lu, Qing ^a   Wang, Ji Yang ^a   Wang, Luman ^a   Jiang, Xuechao ^a   Chu, Yiwei ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD86 ANTIGEN; DNA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; SYNDECAN 1; X BOX BINDING PROTEIN 1; DEOXYRIBONUCLEASE I; PRDM1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1 GENE; CELL COUNT; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PLASMA CELL; PROTEIN EXPRESSION; SYSTEMIC LUPUS ERYTHEMATOSUS; X BOX BINDING PROTEIN 1 GENE; ANIMAL; BAGG ALBINO MOUSE; GENETICS; LYMPHOCYTE; LYMPHOCYTE ACTIVATION; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PHYSIOLOGY;

MURINAE;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; DEOXYRIBONUCLEASE I; DNA; FEMALE; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED MRL LPR; TRANSCRIPTION FACTORS;

EID: 84907841905     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109095     Document Type: Article

References (62)

1. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG, et al. (2000) Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet 25: 177-181.
2. Yasutomo K, Horiuchi T, Kagami S, Tsukamoto H, Hashimura C, et al. (2001) Mutation of DNASE1 in people with systemic lupus erythematosus. Nat Genet 28: 313-314.
3. Emlen W, Niebur J, Kadera R (1994) Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol 152: 3685-3692.
4. Qian Y, Conway KL, Lu X, Seitz HM, Matsushima GK, et al. (2006) Autoreactive MZ and B-1 B-cell activation by Faslpr is coincident with an increased frequency of apoptotic lymphocytes and a defect in macrophage clearance. Blood 108: 974-982.
5. Finke D, Randers K, Hoerster R, Hennig H, Zawatzky R, et al. (2007) Elevated levels of endogenous apoptotic DNA and IFN-alpha in complement C4-deficient mice: implications for induction of systemic lupus erythematosus. Eur J Immunol 37: 1702-1709.
6. Su KY, Pisetsky DS (2009) The role of extracellular DNA in autoimmunity in SLE. Scand J Immunol 70: 175-183.
7. Means TK, Latz E, Hayashi F, Murali MR, Golenbock DT, et al. (2005) Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J Clin Invest 115: 407-417.
8. Dall'era MC, Cardarelli PM, Preston BT, Witte A, Davis JC Jr (2005) Type I interferon correlates with serological and clinical manifestations of SLE. Ann Rheum Dis 64: 1692-1697.
9. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, et al. (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
10. Barton GM, Kagan JC, Medzhitov R (2006) Intracellular localization of Tolllike receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol 7: 49-56.
11. Yasuda K, Yu P, Kirschning CJ, Schlatter B, Schmitz F, et al. (2005) Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J Immunol 174: 6129-6136.
12. Kono DH, Haraldsson MK, Lawson BR, Pollard KM, Koh YT, et al. (2009) Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc Natl Acad Sci USA 106: 12061-12066.
13. Anolik JH, Barnard J, Cappione A, Pugh-Bernard AE, Felgar RE, et al. (2004) Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 50: 3580-3590.
14. Jacob N, Stohl W (2010) Autoantibody-dependent and autoantibody-independent roles for B cells in systemic lupus erythematosus: past, present, and future. Autoimmunity 43: 84-97.
15. Vinuesa CG, Chang PP (2013) Innate B cell helpers reveal novel types of antibody responses. Nat Immunol 14: 119-126.
16. Bernasconi NL, Onai N, Lanzavecchia A (2003) A role for Toll-like receptors in acquired immunity: upregulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101: 4500-4504.
17. Bernasconi NL, Traggiai E, Lanzavecchia A (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199- 2202.
18. Phan TG, Amesbury M, Gardam S, Crosbie J, Hasbold J, et al. (2003) B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J Exp Med 197: 845-860.
19. Zhang W, Xu W, Xiong S (2011) Macrophage differentiation and polarization via phosphatidylinositol 3-kinase/Akt-ERK signaling pathway conferred by serum amyloid P component. J Immunol 187: 1764-1777.
20. Cai Y, Zhang W, Xiong S (2013) Mannose-binding lectin blunts macrophage polarization and ameliorates lupus nephritis. PLoS One 8: e62465.
21. Sano H, Takai O, Harata N, Yoshinaga K, Kodama-Kamada I, et al. (1989) Binding properties of human anti-DNA antibodies to cloned human DNA fragments. Scand J Immunol 30: 51-63.
22. Sano H, Morimoto C (1982) DNA isolated from DNA/anti-DNA antibody immune complexes in systemic lupus Erythematosus is rich in guanine-cytosine content. J Immunol 128: 1341-1345.
23. Santiago-Raber ML, Laporte C, Reininger L, Izui S (2004) Genetic basis of murine lupus. Autoimmun Rev 3: 33-39.
24. Oracki SA, Walker JA, Hibbs ML, Corcoran LM, Tarlinton DM (2010) Plasma cell development and survival. Immunol Rev 237: 140-159.
25. Nordan RP, Potter M (1986) A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro. Science 233: 566-569.
26. Suematsu S, Matsuda T, Aozasa K, Akira S, Nakano N, et al. (1989) IgG1 plasmacytosis in interleukin 6 transgenic mice. Proc Natl Acad Sci USA 86: 7547-7551.
27. Kawano Y, Noma T, Kou K, Yoshizawa I, Yata J (1995) Regulation of human IgG subclass production by cytokines: human IgG subclass production enhanced differentially by interleukin-6. Immunology 84: 278-284.
28. Eisner MD, Amory J, Mullaney B, Tierney L Jr, Browner WS (1996) Necrotizing lymphadenitis associated with systemic lupus erythematosus. Semin Arthritis Rheum 26: 477-482.
29. Gergely P Jr, Grossman C, Niland B, Puskas F, Neupane H, et al. (2002) Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum 46: 175-190.
30. Jiang N, Pisetsky DS (2005) The effect of inflammation on the generation of plasma DNA from dead and dying cells in the peritoneum. J Leukoc Biol 77: 296-302.
31. Pisetsky DS (2013) Immune activation by histones: Plusses and minuses in inflammation. Eur J Immunol 43: 3163-3166.
32. Karikó K, Ni H, Capodici J, Lamphier M, Weissman D (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550.
33. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
34. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, et al. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107.
35. Ishii KJ, Suzuki K, Coban C, Takeshita F, Itoh Y, et al. (2001) Genomic DNA released by dying cells induces the maturation of APCs. J Immunol 167: 2602- 2607.
36. Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, et al. (1995) CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
37. Dil N, Marshall AJ (2009) Role of phosphoinositide 3-kinase p110 delta in TLR4- And TLR9-mediated B cell cytokine production and differentiation. Mol Immunol 46: 1970-1978.
38. Marcelletti JF (1996) IL-10 inhibits lipopolysaccharide-induced murine B cell proliferation and cross-linking of surface antigen receptors or ligation of CD40 restores the response. J Immunol 157: 3323-3333.
39. Liu J, Karypis G, Hippen KL, Vegoe AL, Ruiz P, et al. (2006) Genomic view of systemic autoimmunity in MRLlpr mice. Genes Immun 7: 156-168.
40. Brummel R, Lenert P (2005) Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 174: 2429-2434.
41. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, et al. (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190: 1697-1710.
42. Genestier L, Taillardet M, Mondiere P, Gheit H, Bella C, et al. (2007) TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J Immunol 178: 7779-7786.
43. Gunn KE, Brewer JW (2006) Evidence that marginal zone B cells possess an enhanced secretory apparatus and exhibit superior secretory activity. J Immunol 177: 3791-3798.
44. Martin F, Kearney JF (2002) Marginal-zone B cells. Nat Rev Immunol 2: 323- 335.
45. William J, Euler C, Shlomchik MJ (2005) Short-lived plasmablasts dominate the early spontaneous rheumatoid factor response: differentiation pathways, hypermutating cell types, and affinity maturation outside the germinal center. J Immunol 174: 6879-6887.
46. Martin F, Kearney JF (2000) B-cell subsets and the mature preimmune repertoire: marginal zone and B1 B cells as part of a "natural immune memory". Immunol Rev 175: 70-79.
47. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, et al. (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8: 487-496.
48. Ouchida R, Mori H, Hase K, Takatsu H, Kurosaki T, et al. (2012) Critical role of the IgM Fc receptor in IgM homeostasis, B-cell survival, and humoral immune responses. Proc Natl Acad Sci USA 109: E2699-E2706.
49. Klinman DM (1990) Polyclonal B cell activation in lupus-prone mice precedes and predicts the development of autoimmune disease. J Clin Invest 86: 1249- 1254.
50. Arce E, Jackson DG, Gill MA, Bennett LB, Banchereau J, et al. (2001) Increased frequency of pre-germinal center B cells and plasma cell precursors in the blood of children with systemic lupus erythematosus. J Immunol 167: 2361-2369.
51. Hoyer BF, Moser K, Hauser AE, Peddinghaus A, Voigt C, et al. (2004) Short lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J Exp Med 199: 1577-1584.
52. Cassese G, Lindenau S, de Boer B, Arce S, Hauser A, et al. (2001) Inflamed kidneys of NZB/W mice are a major site for the homeostasis of plasma cells. Eur J Immunol 31: 2726-2732.
53. Dorner M, Brandt S, Tinguely M, Zucol F, Bourquin JP, et al. (2009) Plasma cell toll-like receptor (TLR) expression differs from that of B cells, and plasma cell TLR triggering enhances immunoglobulin production. Immunology 128: 573- 579.
54. Tuvim MJ, Gilbert BE, Dickey BF, Evans SE (2012) Synergistic TLR2/6 and TLR9 activation protects mice against lethal influenza pneumonia. PLoS One 7: e30596.
55. Petterson T, Jendholm J, Ma°nsson A, Bjartell A, Riesbeck K, et al. (2011) Effects of NOD-like receptors in human B lymphocytes and crosstalk between NOD1/NOD2 and Toll-like receptors. J Leukoc Biol 89: 177-187.
56. Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, et al. (2002) Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 46: 191-201.
57. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, et al. (2007) Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 28: 114-121.
58. Grammer AC, Slota R, Fischer R, Gur H, Girschick H, et al. (2003) Abnormal germinal center reactions in systemic lupus erythematosus demonstrated by blockade of CD154-CD40 interactions. J Clin Invest 112: 1506-1520.
59. Higuchi T, Aiba Y, Nomura T, Matsuda J, Mochida K, et al. (2002) Cutting Edge: Ectopic expression of CD40 ligand on B cells induces lupus-like autoimmune disease. J Immunol 168: 9-12.
60. Schroeder K, Herrmann M, Winkler TH (2013) The role of somatic hypermutation in the generation of pathogenic antibodies in SLE. Autoimmunity 46: 121-127.
61. Puga I, Cols M, Barra CM, He B, Cassis L, et al. (2012) B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 13: 170-180.
62. Dörner T, Giesecke C, Lipsky PE (2011) Mechanisms of B cell autoimmunity in SLE. Arthritis Res Ther 13: 243-255.