Selective effects of NF-κB1 deficiency in CD4+ T cells on Th2 and TFh induction by alum-precipitated protein vaccines

European Journal of Immunology

Volumn 41, Issue 6, 2011, Pages 1573-1582

  Serre, Karine ^a   Mohr, Elodie ^a,b   Bénézech, Cécile ^a   Bird, Roger ^a   Khan, Mahmood ^a   Caamaño, Jorge H ^a   Cunningham, Adam F ^a   Maclennan, Ian C M ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Alum; CXCR5; Follicular helper T cells; IL 4; NF kB1

Indexed keywords

ALUM PRECIPITATED OVA VACCINE; CHEMOKINE RECEPTOR CXCR5; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN 13; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 5; NUCLEAR FACTOR KAPPA B1; NUCLEIC ACID BINDING PROTEIN; OX40 LIGAND; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL 6; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL COUNT; CONTROLLED STUDY; FOLLICULAR HELPER T LYMPHOCYTE; HELPER CELL; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; TH2 CELL;

ADOPTIVE TRANSFER; ALUM COMPOUNDS; ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GERMINAL CENTER; IMMUNIZATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NF-KAPPA B; OVALBUMIN; RECEPTORS, CXCR5; TH2 CELLS; UP-REGULATION;

EID: 79957557930     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041126     Document Type: Article

References (45)

1. Cunningham, A. F., Serre, K., Mohr, E., Khan, M. and Toellner, K. M., Loss of CD154 impairs the Th2 extrafollicular plasma cell response but not early T cell proliferation and interleukin-4 induction. Immunology 2004. 113: 187-193.
2. Cunningham, A. F., Fallon, P. G., Khan, M., Vacheron, S., Acha-Orbea, H., MacLennan, I. C., McKenzie, A. N. and Toellner, K. M., Th2 activities induced during virgin T cell priming in the absence of IL-4, IL-13, and B cells. J. Immunol. 2002. 169: 2900-2906.
3. Mohr, E., Serre, K., Manz, R. A., Cunningham, A. F., Khan, M., Hardie, D. L., Bird, R. and MacLennan, I. C., Dendritic cells and monocyte/macrophages that create the IL-6/APRIL-rich lymph node microenvironments where plasmablasts mature. J. Immunol. 2009. 182: 2113-2123.
4. Vinuesa, C. G., Tangye, S. G., Moser, B. and Mackay, C. R., Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 2005. 5: 853-865.
5. Paul, W. E. and Zhu, J., How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 2010. 10: 225-235.
6. Brewer, J. M., Conacher, M., Hunter, C. A., Mohrs, M., Brombacher, F. and Alexander, J., Aluminium hydroxide adjuvant initiates strong antigen-specific Th2 responses in the absence of IL-4- or IL-13-mediated signaling. J. Immunol. 1999. 163: 6448-6454.
7. Cunningham, A. F., Serre, K., Toellner, K. M., Khan, M., Alexander, J., Brombacher, F. and MacLennan, I. C., Pinpointing IL-4-independent and IL-4-influenced acquisition and maintenance of Th2 activity by CD4 T cells. Eur. J. Immunol. 2004. 34: 686-694.
8. van Panhuys, N., Tang, S. C., Prout, M., Camberis, M., Scarlett, D., Roberts, J., Hu-Li, J. et al., In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc. Natl. Acad. Sci. USA 2008. 105: 12423-12428.
9. Li, Q. and Verma, I. M., NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2002. 2: 725-734.
10. Artis, D., Shapira, S., Mason, N., Speirs, K. M., Goldschmidt, M., Caamano, J., Liou, H. C. et al., Differential requirement for NF-kappa B family members in control of helminth infection and intestinal inflammation. J. Immunol. 2002. 169: 4481-4487.
11. Das, J., Chen, C. H., Yang, L., Cohn, L., Ray, P. and Ray, A., A critical role for NF-kappa B in GATA3 expression and TH2 differentiation in allergic airway inflammation. Nat. Immunol. 2001. 2: 45-50.
12. Donovan, C. E., Mark, D. A., He, H. Z., Liou, H. C., Kobzik, L., Wang, Y., De Sanctis, G. T. et al., NF-kappa B/Rel transcription factors: c-Rel promotes airway hyperresponsiveness and allergic pulmonary inflammation. J. Immunol. 1999. 163: 6827-6833.
13. Yang, L., Cohn, L., Zhang, D. H., Homer, R., Ray, A. and Ray, P., Essential role of nuclear factor kappaB in the induction of eosinophilia in allergic airway inflammation. J. Exp. Med. 1998. 188: 1739-1750.
14. Artis, D., Kane, C. M., Fiore, J., Zaph, C., Shapira, S., Joyce, K., Macdonald, A. et al., Dendritic cell-intrinsic expression of NF-kappa B1 is required to promote optimal Th2 cell differentiation. J. Immunol. 2005. 174: 7154-7159.
15. Artis, D., Speirs, K., Joyce, K., Goldschmidt, M., Caamano, J., Hunter, C. A. and Scott, P., NF-kappa B1 is required for optimal CD4+ Th1 cell development and resistance to Leishmania major. J. Immunol. 2003. 170: 1995-2003.
16. Sriskantharajah, S., Belich, M. P., Papoutsopoulou, S., Janzen, J., Tybulewicz, V., Seddon, B. and Ley, S. C., Proteolysis of NF-kappaB1 p105 is essential for T cell antigen receptor-induced proliferation. Nat. Immunol. 2009. 10: 38-47.
17. Song, J., So, T. and Croft, M., Activation of NF-kappaB1 by OX40 contributes to antigen-driven T cell expansion and survival. J. Immunol. 2008. 180: 7240-7248.
18. + T cells to alum-precipitated ovalbumin compared to ovalbumin expressed by Salmonella. Mol. Immunol. 2008. 45: 3558-3566.
19. + T cells produce these cytokines in response to alum-precipitated protein in vivo. Mol. Immunol. 2010. 47: 1914-1922.
20. + T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 1999. 190: 1123-1134.
21. Haynes, N. M., Allen, C. D., Lesley, R., Ansel, K. M., Killeen, N. and Cyster, J. G., Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol. 2007. 179: 5099-5108.
22. + T cells. Eur. J. Immunol. 2009. 39: 1573-1586.
23. Pai, S. Y., Truitt, M. L. and Ho, I. C., GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc. Natl. Acad. Sci. USA 2004. 101: 1993-1998.
24. Kim, J. I., Ho, I. C., Grusby, M. J. and Glimcher, L. H., The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity 1999. 10: 745-751.
25. Quirion, M. R., Gregory, G. D., Umetsu, S. E., Winandy, S. and Brown, M. A., Cutting edge: Ikaros is a regulator of Th2 cell differentiation. J. Immunol. 2009. 182: 741-745.
26. Yu, D., Rao, S., Tsai, L. M., Lee, S. K., He, Y., Sutcliffe, E. L., Srivastava, M. et al., The Transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009. 31: 457-468.
27. Johnston, R. J., Poholek, A. C., Ditoro, D., Yusuf, I., Eto, D., Barnett, B., Dent, A. L. et al., Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009. 325: 1006-1010.
28. Nurieva, R. I., Chung, Y., Martinez, G. J., Yang, X. O., Tanaka, S., Matskevitch, T. D., Wang, Y. H. and Dong, C., Bcl6 mediates the development of T follicular helper cells. Science 2009. 325: 1001-1005.
29. Zheng, Y., Ouaaz, F., Bruzzo, P., Singh, V., Gerondakis, S. and Beg, A. A., NF-kappa B RelA (p65) is essential for TNF-alpha-induced fas expression but dispensable for both TCR-induced expression and activation-induced cell death. J. Immunol. 2001. 166: 4949-4957.
30. Schmitz, M. L. and Krappmann, D., Controlling NF-kappaB activation in T cells by costimulatory receptors. Cell Death Differ. 2006. 13: 834-842.
31. Akiba, H., Miyahira, Y., Atsuta, M., Takeda, K., Nohara, C., Futagawa, T., Matsuda, H. et al., Critical contribution of OX40 ligand to T helper cell type 2 differentiation in experimental leishmaniasis. J. Exp. Med. 2000. 191: 375-380.
32. Linton, P. J., Bautista, B., Biederman, E., Bradley, E. S., Harbertson, J., Kondrack, R. M., Padrick, R. C. and Bradley, L. M., Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J. Exp. Med. 2003. 197: 875-883.
33. Salek-Ardakani, S., Song, J., Halteman, B. S., Jember, A. G., Akiba, H., Yagita, H. and Croft, M., OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J. Exp. Med. 2003. 198: 315-324.
34. Ishii, N., Ndhlovu, L. C., Murata, K., Sato, T., Kamanaka, M. and Sugamura, K., OX40 (CD134) and OX40 ligand interaction plays an adjuvant role during in vivo Th2 responses. Eur. J. Immunol. 2003. 33: 2372-2381.
35. + T cells to express interleukin 4 and upregulates expression of the chemokine receptor, Blr-1. J. Exp. Med. 1998. 188: 297-304.
36. Ito, T., Wang, Y. H., Duramad, O., Hori, T., Delespesse, G. J., Watanabe, N., Qin, F. X. et al., TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 2005. 202: 1213-1223.
37. + T cells in B follicles. Eur. J. Immunol. 1999. 29: 1610-1616.
38. Walker, L. S., Gulbranson-Judge, A., Flynn, S., Brocker, T., Raykundalia, C., Goodall, M., Forster, R. et al., Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J. Exp. Med. 1999. 190: 1115-1122.
39. Li-Weber, M., Giasi, M. and Krammer, P. H., Involvement of Jun and Rel proteins in up-regulation of interleukin-4 gene activity by the T cell accessory molecule CD28. J. Biol. Chem. 1998. 273: 32460-32466.
40. Reinhardt, R. L., Liang, H. E. and Locksley, R. M., Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 2009. 10: 385-393.
41. King, I. L. and Mohrs, M., IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 2009. 206: 1001-1007.
42. Zaretsky, A. G., Taylor, J. J., King, I. L., Marshall, F. A., Mohrs, M. and Pearce, E. J., T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med. 2009. 206: 991-999.
43. Yusuf, I., Kageyama, R., Monticelli, L., Johnston, R. J., Ditoro, D., Hansen, K., Barnett, B. and Crotty, S., Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 2010. 185: 190-202.
44. Cannons, J. L., Yu, L. J., Hill, B., Mijares, L. A., Dombroski, D., Nichols, K. E., Antonellis, A. et al., SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity 2004. 21: 693-706.
45. Sha, W. C., Liou, H. C., Tuomanen, E. I. and Baltimore, D., Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 1995. 80: 321-330.