Evidence that Yaa-induced loss of marginal zone B cells is a result of dendritic cell-mediated enhanced activation

Journal of Autoimmunity

Volumn 34, Issue 4, 2010, Pages 349-355

  Santiago Raber, Marie Laure ^a   Amano, Hirofumi ^b   Amano, Eri ^b   Fossati Jimack, Liliane ^c   Swee, Lee Kim ^d   Rolink, Antonio ^d   Izui, Shozo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Dendritic cell; Marginal zone B cell; Systemic lupus erythematosus; The Yaa mutation

Indexed keywords

B CELL ACTIVATING FACTOR; CHROMOSOME PROTEIN; IMMUNOGLOBULIN M ANTIBODY; LIGAND; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; Y LINKED AUTOIMMUNE ACCELERATION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL LOSS; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; DEVELOPMENTAL DISORDER; ENZYME DEFICIENCY; GENE EXPRESSION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENE;

ANIMALS; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; DENDRITIC CELLS; GENES, Y-LINKED; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUTATION; TOLL-LIKE RECEPTOR 7; TRANSLOCATION, GENETIC;

EID: 77952241013     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.01.001     Document Type: Article

References (46)

1. Murphy E.D., Roths Jb A Y chromosome associated factor in strain BXSB producing accelerated autoimmunity and lymphoproliferation. Arthritis Rheum 1979, 22:1188-1194.
2. Izui S., Iwamoto M., Fossati L., Merino R., Takahashi S., Ibnou-Zekri N. The Yaa gene model of systemic lupus erythematosus. Immunol Rev 1995, 144:137-156.
3. - bone marrow chimeric mice. J Exp Med 1991, 174:1023-1029.
4. + B cells to produce lupus autoantibodies in vivo. Eur J Immunol 1995, 25:3412-3417.
5. Pisitkun P., Deane J.A., Difilippantonio M.J., Tarasenko T., Satterthwaite A.B., Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006, 312:1669-1672.
6. Subramanian S., Tus K., Li Q.Z., Wang A., Tian X.H., Zhou J., et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci USA 2006, 103:9970-9975.
7. Lau C.M., Broughton C., Tabor A.S., Akira S., Flavell R.A., Mamula M.J., et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med 2005, 202:1171-1177.
8. Berland R., Fernandez L., Kari E., Han J.H., Lomakin I., Akira S., et al. Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity 2006, 25:429-440.
9. Deane J.A., Pisitkun P., Barrett R.S., Feigenbaum L., Town T., Ward J.M., et al. Control of Toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immunity 2007, 27:801-810.
10. Fairhurst A.M., Hwang S.H., Wang A., Tian X.H., Boudreaux C., Zhou X.J., et al. Yaa autoimmune phenotypes are conferred by overexpression of TLR7. Eur J Immunol 2008, 38:1971-1978.
11. Amano M., Baumgarth N., Dick M.D., Brossay L., Kronenberg M., Herzenberg L.A., et al. CD1 expression defines subsets of follicular and marginal zone B cells in the spleen: β2-microglobulin-dependent and independent forms. J Immunol 1998, 161:1710-1717.
12. high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol 1999, 162:7198-7207.
13. Won W.-J., Kearney J.F. CD9 is a unique marker for marginal zone B cells, B1 cells, and plasma cells in mice. J Immunol 2002, 168:5605-5611.
14. Martin F., Oliver A.M., Kearney J.F. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001, 14:617-629.
15. Tanigaki K., Han H., Yamamoto N., Tashiro K., Ikegawa M., Kuroda K., et al. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat Immunol 2002, 3:443-450.
16. Amano H., Amano E., Moll T., Marinkovic D., Ibnou-Zekri N., Martínez-Soria E., et al. The Yaa mutation promoting murine lupus causes defective development of marginal zone B cells. J Immunol 2003, 170:2293-2301.
17. Santiago-Raber M.L., Kikuchi S., Borel P., Uematsu S., Akira S., Kotzin B.L., et al. Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus. J Immunol 2008, 181:1556-1562.
18. Martin F., Kearney J.F. Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity 2000, 12:39-49.
19. Cariappa A., Tang M., Parng C., Nebelitskiy E., Carroll M., Georgopoulos K., et al. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 2001, 14:603-615.
20. Seo S.-J., Buckler J., Erikson J. Novel roles of Lyn in B cell migration and lipopolysaccharide responsiveness revealed using anti-double-stranded DNA Ig transgenic mice. J Immunol 2001, 166:3710-3723.
21. Samardzic T., Marinkovic D., Danzer C.-P., Gerlach J., Nitschke L., Wirth T. Reduction of marginal zone B cells in CD22-deficient mice. Eur J Immunol 2002, 32:561-567.
22. Pillai S., Cariappa A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat Rev Immunol 2009, 9:767-777.
23. Balázs M., Martin F., Zhou T., Kearney J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 2002, 17:341-352.
24. Vinuesa C.G., Sunners Y., Pongracz J., Ball J., Toellner K.M., Taylor D., et al. Tracking the response of Xid B cells in vivo: TI-2 antigen induces migration and proliferation but Btk is essential for terminal differentiation. Eur J Immunol 2001, 31:1340-1350.
25. Karlsson M.C.I., Guinamard R., Bolland S., Sankala M., Steinman R.M., Ravetch J.V. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J Exp Med 2003, 198:333-340.
26. Song H., Cerny J. Functional heterogeneity of marginal zone B cells revealed by their ability to generate both early antibody-forming cells and germinal centers with hypermutation and memory in response to a T-dependent antigen. J Exp Med 2003, 198:1923-1935.
27. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S., Brink R.A., et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 1988, 334:676-682.
28. Wessels M.R., Butko P., Ma M., Warren H.B., Lage A.L., Carroll M.C. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci USA 1995, 92:11490-11494.
29. McKenna H.J., Stocking K.L., Miller R.E., Brasel K., De Smedt T., Maraskovsky E., et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 2000, 95:3489-3497.
30. Izui S., Higaki M., Morrow D., Merino R. The Y chromosome from autoimmune BXSB/MpJ mice induces a lupus-like syndrome in (NZW×C57BL/6)F1 male mice, but not in C57BL/6 male mice. Eur J Immunol 1988, 18:911-915.
31. Rauch M., Tussiwand R., Bosco N., Rolink A.G. Crucial role for BAFF-BAFF-R signaling in the survival and maintenance of mature B cells. PLoS One 2009, 4:e5456.
32. Kamath A.T., Sheasby C.E., Tough D.F. Dendritic cells and NK cells stimulate bystander T cell activation in response to TLR agonists through secretion of IFN-αβ and IFN-γ. J Immunol 2005, 174:767-776.
33. Grimaldi C.M., Michael D.J., Diamond B. Expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J Immunol 2001, 167:1886-1890.
34. Li Y., Li H., Weigert M. Autoreactive B cells in the marginal zone that express dual receptors. J Exp Med 2002, 195:181-188.
35. Guinamard R., Okigaki M., Schlessinger J., Ravetch J.V. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat Immunol 2000, 1:31-36.
36. Haas K.M., Hasegawa M., Steeber D.A., Poe J.C., Zabel M.D., Bock C.B., et al. Complement receptors CD21/35 link innate and protective immunity during Streptococcus pneumoniae infection by regulating IgG3 antibody responses. Immunity 2002, 17:713-723.
37. Maraskovsky E., Brasel K., Teepe M., Roux E.R., Lyman S.D., Shortman K., et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996, 184:1953-1962.
38. Batten M., Groom J., Cachero T.G., Qian F., Schnieder P., Tschopp J., et al. BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med 2000, 192:1453-1465.
39. Rolink A.G., Tschopp J., Schneider P., Meclchers F. BAFF is a survival and maturation factor for mouse B cells. Eur J Immunol 2002, 32:2004-2010.
40. Martin F., Kearney J.F. Marginal-zone B cells. Nat Rev Immunol 2002, 2:323-335.
41. Fossati L., Iwamoto M., Merino R., Izui S. Selective enhancing effect of the Yaa gene on immune responses against self and foreign antigens. Eur J Immunol 1995, 25:166-173.
42. Bubier J.A., Sproule T.J., Foreman O., Spolski R., Shaffer D.J., Morse H.C., et al. A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc Natl Acad Sci USA 2009, 106:1518-1523.
43. Gorden K.K., Qiu X.X., Binsfeld C.C., Vasilakos J.P., Alkan S.S. Cutting edge: Activation of murine TLR8 by a combination of imidazoquinoline immune response modifiers and polyT oligodeoxynucleotides. J Immunol 2006, 177:6584-6587.
44. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002, 3:196-200.
45. Jurk M., Heil F., Vollmer J., Schetter C., Krieg A.M., Wagner H., et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol 2002, 3:499.
46. Lan T., Kandimalla E.R., Yu D., Bhagat L., Li Y., Wang D., et al. Stabilized immune modulatory RNA compounds as agonists of Toll-like receptors 7 and 8. Proc Natl Acad Sci USA 2007, 104:13750-13755.