Cutting edge: IL-4, IL-21, and IFN-g interact to govern T-bet and CD11c expression in TLR-activated B cells

Journal of Immunology

Volumn 197, Issue 4, 2016, Pages 1023-1028

  Naradikian, Martin S ^a   Myles, Arpita ^a   Beiting, Daniel P ^a,b   Roberts, Kenneth J ^a   Dawson, Lucas ^a,b   Herati, Ramin Sedaghat ^a,c   Bengsch, Bertram ^a   Linderman, Susanne L ^a,d   Stelekati, Erietta ^a   Spolski, Rosanne ^e   Wherry, E John ^a   Hunter, Christopher ^a,b   Hensley, Scott E ^a,d   Leonard, Warren J ^e   Cancro, Michael P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d WISTAR INSTITUTE   (United States)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 21; INTERLEUKIN 4; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR T BET; INTERLEUKIN DERIVATIVE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; HELIGMOSOMOIDES POLYGYRUS; IN VIVO STUDY; INFLUENZA; LYMPHOCYTOPOIESIS; MOUSE; NEMATODIASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD11C; B-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-4; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TOLL-LIKE RECEPTORS;

EID: 84983760966     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600522     Document Type: Article

References (31)

1. Barnett, B. E., R. P. Staupe, P. M. Odorizzi, O. Palko, V. T. Tomov, A. E. Mahan, B. Gunn, D. Chen, M. A. Paley, G. Alter, et al. 2016. Cutting edge: B cell-intrinsic T-bet expression is required to control chronic viral infection. J. Immunol. 197: 1017-1022.
2. Gerth, A. J., L. Lin, and S. L. Peng. 2003. T-bet regulates T-independent IgG2a class switching. Int. Immunol. 15: 937-944.
3. Wang, N. S., L. J. McHeyzer-Williams, S. L. Okitsu, T. P. Burris, S. L. Reiner, and M. G. McHeyzer-Williams. 2012. Divergent transcriptional programming of classspecific B cell memory by T-bet and RORa. Nat. Immunol. 13: 604-611.
4. Liu, N., N. Ohnishi, L. Ni, S. Akira, and K. B. Bacon. 2003. CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat. Immunol. 4: 687-693.
5. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
6. Peng, S. L., S. J. Szabo, and L. H. Glimcher. 2002. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. USA 99: 5545-5550.
7. Rubtsova, K., A. V. Rubtsov, L. F. van Dyk, J. W. Kappler, and P. Marrack. 2013. T-box transcription factor T-bet, a key player in a unique type of B-cell activation essential for effective viral clearance. Proc. Natl. Acad. Sci. USA 110: E3216-E3224.
8. Rubtsov, A. V., K. Rubtsova, A. Fischer, R. T. Meehan, J. Z. Gillis, J. W. Kappler, and P. Marrack. 2011. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c? B-cell population is important for the development of autoimmunity. Blood 118: 1305-1315.
9. Naradikian, M. S., Y. Hao, and M. P. Cancro. 2016. Age-associated B cells: key mediators of both protective and autoreactive humoral responses. Immunol. Rev. 269: 118-129.
10. Yates, J. L., R. Racine, K. M. McBride, and G. M. Winslow. 2013. T celldependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J. Immunol. 191: 1240-1249.
11. Molica, S., A. Dattilo, A. Mannella, and D. Levato. 1994. CD11c expression in B-cell chronic lymphocytic leukemia. A comparison of results obtained with different monoclonal antibodies. Haematologica 79: 452-455.
12. Postigo, A. A., A. L. Corbí, F. Sánchez-Madrid, and M. O. de Landázuri. 1991. Regulated expression and function of CD11c/CD18 integrin on human B lymphocytes. Relation between attachment to fibrinogen and triggering of proliferation through CD11c/CD18. J. Exp. Med. 174: 1313-1322.
13. Saadoun, D., B. Terrier, J. Bannock, T. Vazquez, C. Massad, I. Kang, F. Joly, M. Rosenzwajg, D. Sene, P. Benech, et al. 2013. Expansion of autoreactive unresponsive CD21-/low B cells in Sjögren's syndrome-associated lymphoproliferation. Arthritis Rheum. 65: 1085-1096.
14. Luthje, K., A. Kallies, Y. Shimohakamada, G. T. Belz, A. Light, D. M. Tarlinton, and S. L. Nutt. 2012. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 13: 491-498.
15. King, I. L., and M. Mohrs. 2009. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 206: 1001-1007.
16. Chtanova, T., S. G. Tangye, R. Newton, N. Frank, M. R. Hodge, M. S. Rolph, and C. R. Mackay. 2004. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J. Immunol. 173: 68-78.
17. Herbert, D. R., J. Q. Yang, S. P. Hogan, K. Groschwitz, M. Khodoun, A. Munitz, T. Orekov, C. Perkins, Q. Wang, F. Brombacher, et al. 2009. Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection. J. Exp. Med. 206: 2947-2957.
18. Hao, Y., P. O'Neill, M. S. Naradikian, J. L. Scholz, and M. P. Cancro. 2011. A Bcell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood 118: 1294-1304.
19. Huang, L., D. P. Beiting, N. G. Gebreselassie, L. F. Gagliardo, M. C. Ruyechan, N. A. Lee, J. J. Lee, and J. A. Appleton. 2015. Eosinophils and IL-4 support nematode growth coincident with an innate response to tissue injury. Plos Pathog. 11: E1005347.
20. Parrish-Novak, J., S. R. Dillon, A. Nelson, A. Hammond, C. Sprecher, J. A. Gross, J. Johnston, K. Madden, W. Xu, J. West, et al. 2000. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408: 57-63.
21. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380: 627-630.
22. Leonard, W. J. 2001. Role of Jak kinases and STATs in cytokine signal transduction. Int. J. Hematol. 73: 271-277.
23. Heinzel, F. P., M. D. Sadick, B. J. Holaday, R. L. Coffman, and R. M. Locksley. 1989. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J. Exp. Med. 169: 59-72.
24. Ozaki, K., R. Spolski, R. Ettinger, H. P. Kim, G. Wang, C. F. Qi, P. Hwu, D. J. Shaffer, S. Akilesh, D. C. Roopenian, et al. 2004. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J. Immunol. 173: 5361-5371.
25. Baumjohann, D., S. Preite, A. Reboldi, F. Ronchi, K. M. Ansel, A. Lanzavecchia, and F. Sallusto. 2013. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38: 596-605.
26. Shulman, Z., A. D. Gitlin, J. S. Weinstein, B. Lainez, E. Esplugues, R. A. Flavell, J. E. Craft, and M. C. Nussenzweig. 2014. Dynamic signaling by T follicular helper cells during germinal center B cell selection. Science 345: 1058-1062.
27. Nickerson, K. M., S. R. Christensen, J. Shupe, M. Kashgarian, D. Kim, K. Elkon, and M. J. Shlomchik. 2010. TLR9 regulates TLR7- And MyD88-dependent autoantibody production and disease in a murine model of lupus. J. Immunol. 184: 1840-1848.
28. Bubier, J. A., T. J. Sproule, O. Foreman, R. Spolski, D. J. Shaffer, H. C. Morse, III, W. J. Leonard, and D. C. Roopenian. 2009. A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc. Natl. Acad. Sci. USA 106: 1518-1523.
29. Goenka, R., J. L. Scholz, M. S. Naradikian, and M. P. Cancro. 2014. Memory B cells form in aged mice despite impaired affinity maturation and germinal center kinetics. Exp. Gerontol. 54: 109-115.
30. Stepensky, P., A. Rensing-Ehl, R. Gather, S. Revel-Vilk, U. Fischer, S. Nabhani, F. Beier, T. H. Brummendorf, S. Fuchs, S. Zenke, et al. 2015. Early-onset Evans syndrome, immunodeficiency, and premature immunosenescence associated with tripeptidyl-peptidase II deficiency. Blood 125: 753-761.
31. Ehrhardt, G. R., A. Hijikata, H. Kitamura, O. Ohara, J. Y. Wang, and M. D. Cooper. 2008. Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 205: 1807-1817.