CD19 controls Toll-like receptor 9 responses in human B cells

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 3, 2016, Pages 889-898.e6

  Morbach, Henner ^a   Schickel, Jean Nicolas ^a   Cunningham Rundles, Charlotte ^b   Conley, Mary Ellen ^c   Reisli, Ismail ^d   Franco, Jose Luis ^e   Meffre, Eric ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^d SELCUK UNIVERSITY   (Turkey)

^e UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

AKT; B cells; Bruton tyrosine kinase; CD19; common variable immunodeficiency; phosphoinositide 3 kinase; Toll like receptor 9

Indexed keywords

BRUTON TYROSINE KINASE; CD19 ANTIGEN; CD23 ANTIGEN; FOCAL ADHESION KINASE 2; IMMUNOGLOBULIN M ANTIBODY; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE LYN; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR; AGAMMAGLOBULINAEMIA TYROSINE KINASE; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN TYROSINE KINASE;

ALLELE; ARTICLE; B LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; AGONISTS; ANTAGONISTS AND INHIBITORS; CASE CONTROL STUDY; GENE SILENCING; GENETICS; HETEROZYGOTE; HOMOZYGOTE; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MUTATION; PHOSPHORYLATION;

ANTIGENS, CD19; B-LYMPHOCYTES; CASE-CONTROL STUDIES; FOCAL ADHESION KINASE 2; GENE KNOCKDOWN TECHNIQUES; HETEROZYGOTE; HOMOZYGOTE; HUMANS; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ANTIGEN, B-CELL; TOLL-LIKE RECEPTOR 9;

EID: 84951838660     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.08.040     Document Type: Article

References (48)

1. R.H. Carter, and D.T. Fearon CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes Science 256 1992 105 107
2. T.F. Tedder, M. Inaoki, and S. Sato The CD19-CD21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity Immunity 6 1997 107 118
3. A.N. Anzelon, H. Wu, and R.C. Rickert Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function Nat Immunol 4 2003 287 294
4. A.M. Buhl, and J.C. Cambier Phosphorylation of CD19 Y484 and Y515, and linked activation of phosphatidylinositol 3-kinase, are required for B cell antigen receptor-mediated activation of Bruton's tyrosine kinase J Immunol 162 1999 4438 4446
5. M. Fujimoto, Y. Fujimoto, J.C. Poe, P.J. Jansen, C.A. Lowell, A.L. DeFranco, and et al. CD19 regulates Src family protein tyrosine kinase activation in B lymphocytes through processive amplification Immunity 13 2000 47 57
6. M. Fujimoto, J.C. Poe, A.B. Satterthwaite, M.I. Wahl, O.N. Witte, and T.F. Tedder Complementary roles for CD19 and Bruton's tyrosine kinase in B lymphocyte signal transduction J Immunol 168 2002 5465 5476
7. P. Engel, L.J. Zhou, D.C. Ord, S. Sato, B. Koller, and T.F. Tedder Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule Immunity 3 1995 39 50
8. R.C. Rickert, K. Rajewsky, and J. Roes Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice Nature 376 1995 352 355
9. M.C. van Zelm, I. Reisli, M. van der Burg, D. Castano, C.J. van Noesel, M.J. van Tol, and et al. An antibody-deficiency syndrome due to mutations in the CD19 gene N Engl J Med 354 2006 1901 1912
10. M.C. van Zelm, J. Smet, M. van der Burg, A. Ferster, P.Q. Le, L. Schandene, and et al. Antibody deficiency due to a missense mutation in CD19 demonstrates the importance of the conserved tryptophan 41 in immunoglobulin superfamily domain formation Hum Mol Genet 20 2011 1854 1863
11. N. Vince, D. Boutboul, G. Mouillot, N. Just, M. Peralta, J.L. Casanova, and et al. Defects in the CD19 complex predispose to glomerulonephritis, as well as IgG1 subclass deficiency J Allergy Clin Immunol 127 2011 538 541 e1-5
12. C. Cunningham-Rundles, L. Radigan, A.K. Knight, L. Zhang, L. Bauer, and A. Nakazawa TLR9 activation is defective in common variable immune deficiency J Immunol 176 2006 1978 1987
13. N. Romberg, N. Chamberlain, D. Saadoun, M. Gentile, T. Kinnunen, Y.S. Ng, and et al. CVID-associated TACI mutations affect autoreactive B cell selection and activation J Clin Invest 123 2013 4283 4293
14. J.E. Yu, A.K. Knight, L. Radigan, T.U. Marron, L. Zhang, S. Sanchez-Ramon, and et al. Toll-like receptor 7 and 9 defects in common variable immunodeficiency J Allergy Clin Immunol 124 2009 349 356 e1-3
15. A. Denz, H. Eibel, H. Illges, G. Kienzle, M. Schlesier, and H.H. Peter Impaired up-regulation of CD86 in B cells of "type A" common variable immunodeficiency patients Eur J Immunol 30 2000 1069 1077
16. S. Weller, M. Bonnet, H. Delagreverie, L. Israel, M. Chrabieh, L. Marodi, and et al. IgM+IgD+CD27+ B cells are markedly reduced in IRAK-4-, MyD88-, and TIRAP- but not UNC-93B-deficient patients Blood 120 2012 4992 5001
17. V. Hornung, S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdorfer, T. Giese, and et al. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides J Immunol 168 2002 4531 4537
18. D.J. Rawlings, M.A. Schwartz, S.W. Jackson, and A. Meyer-Bahlburg Integration of B cell responses through Toll-like receptors and antigen receptors Nat Rev Immunol 12 2012 282 294
19. J. Huggins, T. Pellegrin, R.E. Felgar, C. Wei, M. Brown, B. Zheng, and et al. CpG DNA activation and plasma-cell differentiation of CD27-naive human B cells Blood 109 2007 1611 1619
20. I. Isnardi, Y.S. Ng, I. Srdanovic, R. Motaghedi, S. Rudchenko, H. von Bernuth, and et al. IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans Immunity 29 2008 746 757
21. K.M. Nickerson, S.R. Christensen, J.L. Cullen, and W. Meng Luning Prak ET, Shlomchik MJ. TLR9 promotes tolerance by restricting survival of anergic anti-DNA B cells, yet is also required for their activation J Immunol 190 2013 1447 1456
22. S.R. Christensen, J. Shupe, K. Nickerson, M. Kashgarian, R.A. Flavell, and M.J. Shlomchik Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus Immunity 25 2006 417 428
23. H. Artac, I. Reisli, R. Kara, I. Pico-Knijnenburg, S. Adin-Cinar, S. Pekcan, and et al. B-cell maturation and antibody responses in individuals carrying a mutated CD19 allele Genes Immun 11 2010 523 530
24. M.E. Conley, M.E. Fitch-Hilgenberg, J.L. Cleveland, O. Parolini, and J. Rohrer Screening of genomic DNA to identify mutations in the gene for Bruton's tyrosine kinase Hum Mol Genet 3 1994 1751 1756
25. M.E. Conley, A. Broides, V. Hernandez-Trujillo, V. Howard, H. Kanegane, T. Miyawaki, and et al. Genetic analysis of patients with defects in early B-cell development Immunol Rev 203 2005 216 234
26. A.V. Sauer, H. Morbach, I. Brigida, Y.S. Ng, A. Aiuti, and E. Meffre Defective B cell tolerance in adenosine deaminase deficiency is corrected by gene therapy J Clin Invest 122 2012 2141 2152
27. J.N. Schickel, J.L. Pasquali, A. Soley, A.M. Knapp, M. Decossas, A. Kern, and et al. Carabin deficiency in B cells increases BCR-TLR9 costimulation-induced autoimmunity EMBO Mol Med 4 2012 1261 1275
28. V. Zennou, C. Petit, D. Guetard, U. Nerhbass, L. Montagnier, and P. Charneau HIV-1 genome nuclear import is mediated by a central DNA flap Cell 101 2000 173 185
29. M. Fujimoto, J.C. Poe, M. Inaoki, and T.F. Tedder CD19 regulates B lymphocyte responses to transmembrane signals Semin Immunol 10 1998 267 277
30. K. Okkenhaug, and B. Vanhaesebroeck PI3K in lymphocyte development, differentiation and activation Nat Rev Immunol 3 2003 317 330
31. Y. Aiba, M. Kameyama, T. Yamazaki, T.F. Tedder, and T. Kurosaki Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase Blood 111 2008 1497 1503
32. H.H. Jabara, D.R. McDonald, E. Janssen, M.J. Massaad, N. Ramesh, A. Borzutzky, and et al. DOCK8 functions as an adaptor that links TLR-MyD88 signaling to B cell activation Nat Immunol 13 2012 612 620
33. S.L. Doyle, C.A. Jefferies, C. Feighery, and L.A. O'Neill Signaling by Toll-like receptors 8 and 9 requires Bruton's tyrosine kinase J Biol Chem 282 2007 36953 36960
34. G. Yang, Y. Zhou, X. Liu, L. Xu, Y. Cao, R.J. Manning, and et al. A mutation in MYD88 (L265P) supports the survival of lymphoplasmacytic cells by activation of Bruton tyrosine kinase in Waldenstrom macroglobulinemia Blood 122 2013 1222 1232
35. M.E. Conley, A.K. Dobbs, D.M. Farmer, S. Kilic, K. Paris, S. Grigoriadou, and et al. Primary B cell immunodeficiencies: comparisons and contrasts Annu Rev Immunol 27 2009 199 227
36. A. Marshak-Rothstein Toll-like receptors in systemic autoimmune disease Nat Rev Immunol 6 2006 823 835
37. A.M. Buhl, C.M. Pleiman, R.C. Rickert, and J.C. Cambier Qualitative regulation of B cell antigen receptor signaling by CD19: selective requirement for PI3-kinase activation, inositol-1,4,5-trisphosphate production and Ca2+ mobilization J Exp Med 186 1997 1897 1910
38. M. Hasegawa, M. Fujimoto, J.C. Poe, D.A. Steeber, C.A. Lowell, and T.F. Tedder A CD19-dependent signaling pathway regulates autoimmunity in Lyn-deficient mice J Immunol 167 2001 2469 2478
39. H. Suzuki, S. Matsuda, Y. Terauchi, M. Fujiwara, T. Ohteki, T. Asano, and et al. PI3K and Btk differentially regulate B cell antigen receptor-mediated signal transduction Nat Immunol 4 2003 280 286
40. A. Castello, M. Gaya, J. Tucholski, T. Oellerich, K.H. Lu, A. Tafuri, and et al. Nck-mediated recruitment of BCAP to the BCR regulates the PI(3)K-Akt pathway in B cells Nat Immunol 14 2013 966 975
41. M. Ni, AWt MacFarlane, M. Toft, C.A. Lowell, K.S. Campbell, and J.A. Hamerman B-cell adaptor for PI3K (BCAP) negatively regulates Toll-like receptor signaling through activation of PI3K Proc Natl Acad Sci U S A 109 2012 267 272
42. T.D. Troutman, W. Hu, S. Fulenchek, T. Yamazaki, T. Kurosaki, J.F. Bazan, and et al. Role for B-cell adapter for PI3K (BCAP) as a signaling adapter linking Toll-like receptors (TLRs) to serine/threonine kinases PI3K/Akt Proc Natl Acad Sci U S A 109 2012 273 278
43. C.L. Baumann, I.M. Aspalter, O. Sharif, A. Pichlmair, S. Bluml, F. Grebien, and et al. CD14 is a coreceptor of Toll-like receptors 7 and 9 J Exp Med 207 2010 2689 2701
44. C. Han, J. Jin, S. Xu, H. Liu, N. Li, and X. Cao Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b Nat Immunol 11 2010 734 742
45. N. Yazawa, M. Fujimoto, S. Sato, K. Miyake, N. Asano, Y. Nagai, and et al. CD19 regulates innate immunity by the toll-like receptor RP105 signaling in B lymphocytes Blood 102 2003 1374 1380
46. T. Kubo, Y. Uchida, Y. Watanabe, M. Abe, A. Nakamura, M. Ono, and et al. Augmented TLR9-induced Btk activation in PIR-B-deficient B-1 cells provokes excessive autoantibody production and autoimmunity J Exp Med 206 2009 1971 1982
47. E. Janssen, H. Morbach, S. Ullas, J.M. Bannock, C. Massad, L. Menard, and et al. Dedicator of cytokinesis 8-deficient patients have a breakdown in peripheral B-cell tolerance and defective regulatory T cells J Allergy Clin Immunol 134 2014 1365 1374
48. B. He, R. Santamaria, W. Xu, M. Cols, K. Chen, I. Puga, and et al. The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88 Nat Immunol 11 2010 836 845