The combination of 4-1BBL and CD40L strongly enhances the capacity of dendritic cells to stimulate HIV-specific T cell responses

Journal of Leukocyte Biology

Volumn 89, Issue 6, 2011, Pages 989-999

  de Keersmaecker, Brenda ^a   Heirman, Carlo ^a   Corthals, Jurgen ^a   Empsen, Christophe ^b   van Grunsven, Leo A ^b   Allard, Sabine D ^a,c   Pen, Joeri ^a   Lacor, Patrick ^c   Thielemans, Kris ^a   Aerts, Joeri L ^a  

^a FACULTY OF MEDICINE AND PHARMACY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

Costimulatory molecules; Regulatory t cells; T cell proliferation; T cell survival

Indexed keywords

CD137 LIGAND; CD40 LIGAND; MESSENGER RNA;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CYTOKINE PRODUCTION; DENDRITIC CELL; ELECTROPORATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

4-1BB LIGAND; ANTIGENS, CD40; BLOTTING, WESTERN; CD40 LIGAND; CELL PROLIFERATION; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HIV; HIV INFECTIONS; HIV SEROPOSITIVITY; HUMANS; LYMPHOCYTE ACTIVATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 79957868214     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0810466     Document Type: Article

References (69)

1. Betts, M. R., Nason, M., West, S., De Rosa, S., Migueles, S., Abraham, J., Lederman, M., Benito, J., Goepfert, P., Connors, M., Roederer, M., Koup, R (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107, 4781-4789.
2. Lieberman, J., Skolnik, P., Parkerson, G. R., Fabry, J., Landry, B., Bethel, J., Kagan, J. (1997) Safety of autologous, ex vivo-expanded human immunodeficiency virus (HIV)-specific cytotoxic T-lymphocyte infusion in HIV-infected patients. Blood 90, 2196-2206.
3. Lu, W., Arraes, L., Ferreira, W., Andrieu, J. (2004) Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat. Med. 10, 1359-1365.
4. De Keersmaecker, B., Thielemans, K, Aerts, J. L. (2011) Fighting with the enemy's weapons? The role of costimulatory molecules in HIV. Curr. Mol. Med., in press.
5. Broll, K, Richter, G., Pauly, S., Hofstaedter, F., Schwarz, H. (2001) CD137 expression in tumor vessel walls. High correlation with malignant tumors. Am. J. Clin. Pathol. 115, 543-549.
6. Heinisch, I. V., Daigle, I., Knopfli, B., Simon, H. (2000) CD137 activation abrogates granulocyte-macrophage colony-stimulating factor-mediated anti-apoptosis in neutrophils. Eur. J. Immunol. 30, 3441-3446.
7. Kim, D. H., Chang, W., Lee, Y., Lee, K, Kim, Y., Kwon, B., Kang, C. (2008) 4-1BB engagement costimulates NKT cell activation and exacerbates NKT cell ligand-induced airway hyperresponsiveness and inflammation. J. Immunol. 180, 2062-2068.
8. Nishimoto, H., Lee, S., Hong, H., Potter, K, Maeda-Yamamoto, M., Ki-noshita, T., Kawakami, Y, Mittler, R, Kwon, B., Ware, C, Croft, M., Kawakami, T. (2005) Costimulation of mast cells by 4-1BB, a member of the tumor necrosis factor receptor superfamily, with the high-affinity IgE receptor. Blood 106, 4241-4248.
9. Wilcox, R. A, Chapoval, A, Gorski, K, Otsuji, M., Shin, T., Flies, D., Tamada, K, Mittler, R, Tsuchiya, H., Pardoll, D., Chen, L. (2002) Cutting edge: expression of functional CD137 receptor by dendritic cells. J. Immunol. 168, 4262-4267.
10. Wilcox, R A, Tamada, K, Strome, S., Chen, L. (2002) Signaling through NK cell-associated CD137 promotes both helper function for CD8+ cytolytic T cells and responsiveness to IL-2 but not cytolytic activity. J. Immunol. 169, 4230-4236.
11. Zhang, X., Voskens, C, Sallin, M., Maniar, A, Montes, C, Zhang, Y, Lin, W., Li, G., Burch, E., Tan, M., Hertzano, R, Chapoval, A, Tamada, K, Gastman, B., Schulze, D., Strome, S. (2010) CD137 promotes proliferation and survival of human B cells. J. Immunol. 184, 787-795.
12. Zheng, G., Wang, B., Chen, A. (2004) The 4-1BB costimulation augments the proliferation of CD4 + CD25+ regulatory T cells. J. Immunol. 173, 2428-2434.
13. Won, E., Cha, K, Byun, J., Kim, D., Shin, S., Ahn, B., Kim, Y, Rice, A, Walz, T., Kwon, B., Cho, H. (2010) The structure of the trimer of human 4-1BB ligand is unique among members of the TNF superfamily. J. Biol. Chem. 285, 9202-9210.
14. Laderach, D., Wesa, A, Galy, A. (2003) 4-1BB-ligand is regulated on human dendritic cells and induces the production of IL-12. Cell. Immunol. 226, 37-44.
15. Watts, T. H. (2005) TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23-68.
16. Bukczynski, J., Wen, T., Ellefsen, K, Gauldie, J., Watts, T. (2004) Co-stimulatory ligand 4-1BBL (CD137L) as an efficient adjuvant for human antiviral cytotoxic T cell responses. Proc. Natl. Acad. Sci. USA 101, 1291-1296.
17. Lee, H. W., Park, S., Choi, B., Kim, H., Nam, K, Kwon, B. (2002) 4-1BB promotes the survival of CD8+ T lymphocytes by increasing expression of Bcl-xL and Bfl-1. J. Immunol. 169, 4882-4888.
18. Wang, C, Wen, T., Routy, J., Bernard, N., Sekaly, R, Watts, T. (2007) 4-1BBL induces TNF receptor-associated factor 1-dependent Bim modulation in human T cells and is a critical component in the costimulation-dependent rescue of functionally impaired HIV-specific CD8 T cells. J. Immunol. 179, 8252-8263.
19. Calarota, S. A, Hokey, D., Dai, A, Jure-Kunkel, M., Balimane, P., Weiner, D. (2008) Augmentation of SIV DNA vaccine-induced cellular immunity by targeting the 4-1BB costimulatory molecule. Vaccine 26, 3121-3134.
20. Van Kooten, C, Banchereau, J. (2000) CD40-CD40 ligand. J. Leukoc. Biol. 67, 2-17.
21. Caux, C, Massacrier, C, Vanbervliet, B., Dubois, B., Van Kooten, C, Du-rand, I., Banchereau, J. (1994) Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 180, 1263-1272.
22. Cella, M., Scheidegger, D., Palmer-Lehmann, K, Lane, P., Lanzavecchia, A, Alber, G. (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184, 747-752.
23. Serra, P., Amrani, A, Yamanouchi, J., Han, B., Thiessen, S., Utsugi, T., Verdaguer, J., Santamaria, P. (2003) CD40 ligation releases immature dendritic cells from the control of regulatory CD4 + CD25+ T cells. Immunity 19, 877-889.
24. Hanig, J., Lutz, M. B. (2008) Suppression of mature dendritic cell function by regulatory T cells in vivo is abrogated by CD40 licensing. J. Immunol. 180, 1405-1413.
25. Misra, N., Bayry, J., Lacroix-Desmazes, S., Kazatchkine, M. D., Kaveri, S. V. (2004) Cutting edge: human CD4 + CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J. Immunol. 172, 4676-4680.
26. Huang, X. L., Fan, Z., Zheng, L., Borowski, L., Li, H., Thomas, E. K, Hil- debrand, W. H., Zhao, X. Q., Rinaldo, C. R (2003) Priming of human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T cell responses by dendritic cells loaded with HIV-1 proteins. J. Infect. Dis. 187, 315-319.
27. Huang, X. L., Fan, Z., Borowski, L., Rinaldo, C. R. (2008) Maturation of dendritic cells for enhanced activation of anti-HIV-1 CD8(+) T cell immunity. J. Leukoc. Biol. 83, 1530-1540.
28. Routy, J. P., Boulassel, M. R, Yassine-Diab, B., Nicolette, C, Healey, D., Jain, R., Landry, C, Yegorov, O., Tcherepanova, I., Monesmith, T., Finke, L., Sekaly, R P. (2010) Immunologic activity and safety of autologous HIV RNA-electroporated dendritic cells in HIV-1 infected patients receiving antiretroviral therapy. Clin. Immunol. 134, 140-147.
29. Allard, S. D., Pletinckx, K, Breckpot, K, Heirman, C, Bonehill, A., Michiels, A., van Baalen, C, Gruters, R, Osterhaus, A, Lacor, P., Thiele-mans, K, Aerts, J. (2008) Functional T-cell responses generated by dendritic cells expressing the early HIV-1 proteins Tat, Rev and Nef. Vaccine 26, 3735-3741.
30. De Keersmaecker, B., Heirman, C, Allard, S., Bonehill, A., Corthals, J., Thielemans, K, Aerts, J. (2010) Lumenal part of the DC-LAMP protein is not required for induction of antigen-specific T cell responses by means of antigen-DC-LAMP messenger RNA-electroporated dendritic cells. Hum. Gene Ther. 21, 479-485.
31. Bonehill, A, Tuyaerts, S., Van Nuffel, A, Heirman, C, Bos, T., Fostier, K., Neyns, B., Thielemans, K (2008) Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA Mol. Ther. 16, 1170-1180.
32. Tuyaerts, S., Van Meirvenne, S., Bonehill, A, Heirman, C, Corthals, J., Waldmann, H., Breckpot, K, Thielemans, K, Aerts, J. (2007) Expression of human GITRL on myeloid dendritic cells enhances their immunos-timulatory function but does not abrogate the suppressive effect of CD4 + CD25+ regulatory T cells. J. Leukoc. Biol. 82, 93-105.
33. Michiels, A, Tuyaerts, S., Bonehill, A, Corthals, J., Breckpot, K, Heirman, C, Van Meirvenne, S., Dullaers, M., Allard, S., Brasseur, F., van der Bruggen, P., Thielemans, K (2005) Electroporation of immature and mature dendritic cells: implications for dendritic cell-based vaccines. Gene Ther. 12, 772-782.
34. Ahmadzadeh, M., Rosenberg, S. (2006) IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood 107, 2409-2414.
35. Betts, M. R, Brenchley, J., Price, D., De Rosa, S., Douek, D., Roederer, M., Koup, R (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281, 65-78.
36. Wolfl, M., Kuball, J., Ho, W., Nguyen, H., Manley, T., Bleakley, M., Greenberg, P. (2007) Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 110, 201-210.
37. Bukczynski, J., Wen, T., Wang, C, Christie, N, Routy, J., Boulassel, M., Kovacs, C, Macdonald, K, Ostrowski, M., Sekaly, R, Bernard, N, Watts, T. (2005) Enhancement of HIV-specific CD8 T cell responses by dual co-stimulation with CD80 and CD137L. J. Immunol. 175, 6378-6389.
38. Borrow, P., Lewicki, H., Hahn, B., Shaw, G., Oldstone, M. (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68, 6103-6110.
39. Koup, R A, Safrit, J., Cao, Y., Andrews, C, McLeod, G., Borkowsky, W., Farthing, C, Ho, D. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68, 4650-4655.
40. Bevan, M.J. (2004) Helping the CD8(+) T-cell response. Nat. Rev. Immunol. 4, 595-602.
41. Rosenberg, E. S., Billingsley, J., Caliendo, A, Boswell, S., Sax, P., Kalams, S., Walker, B. (1997) Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278, 1447-1450.
42. Gramaglia, I., Cooper, D., Miner, K, Kwon, B., Croft, M. (2000) Co-stimulation of antigen-specific CD4 T cells by 4-1BB ligand. Eur. J. Immunol. 30, 392-402.
43. Houtenbos, I., Westers, T., Dijkhuis, A, de Gruijl, T., Ossenkoppele, G., van de Loosdrecht, A. (2007) Leukemia-specific T-cell reactivity induced by leukemic dendritic cells is augmented by 4-1BB targeting. Clin. Cancer Res. 13, 307-315.
44. Habib-Agahi, M., Jaberipour, M., Searle, P. (2009) 4-1BBL costimulation retrieves CD28 expression in activated T cells. Cell. Immunol. 256, 39-46.
45. Waller, E. C, McKinney, N, Hicks, R, Carmichael, A, Sissons, J., Wills, M. (2007) Differential costimulation through CD137 (4-1BB) restores proliferation of human virus-specific "effector memory" (CD28(-) CD45RA(HI)) CD8(+) T cells. Blood 110, 4360-4366.
46. Bertram, E. M., Dawicki, W., Watts, T. (2004) Role of T cell costimulation in anti-viral immunity. Semin. Immunol. 16, 185-196.
47. Wen, T., Bukczynski, J., Watts, T. (2002) 4-1BB ligand-mediated costimulation of human T cells induces CD4 and CD8 T cell expansion, cytokine production, and the development of cytolytic effector function. J. Immunol. 168, 4897-4906.
48. Cannons, J. L., Lau, P., Ghumman, B., DeBenedette, M., Yagita, H., Oku-mura, K, Watts, T. (2001) 4-1BB ligand induces cell division, sustains survival, and enhances effector function of CD4 and CD8 T cells with similar efficacy. J. Immunol. 167, 1313-1324.
49. Takahashi, C, Mittler, R, Vella, A. (1999) Cutting edge: 4-1BB is a bona fide CD8 T cell survival signal. J. Immunol. 162, 5037-5040.
50. Melero, I., Shuford, W., Newby, S., Aruffo, A, Ledbetter, J., Hellstrom, K, Mittler, R, Chen, L. (1997) Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat. Med 3, 682-685.
51. Zhu, Y, Zhu, G., Luo, L., Flies, A, Chen, L. (2007) CD137 stimulation delivers an antigen-independent growth signal for T lymphocytes with memory phenotype. Blood 109, 4882-4889.
52. Serghides, L., Bukczynski, J., Wen, T, Wang, C, Routy, J., Boulassel, M., Sekaly, R., Ostrowski, M., Bernard, N, Watts, T (2005) Evaluation of OX40 ligand as a costimulator of human antiviral memory CD8 T cell responses: comparison with B7.1 and 4-1BBL. J. Immunol 175, 6368-6377.
53. Kober, J., Leitner, J., Klauser, C, Woitek, R, Majdic, O., Stockl, J., Hern-dler-Brandstetter, D., Grubeck-Loebenstein, B., Reipert, B., Pickl, W., Pfis-tershammer, K, Steinberger, P. (2008) The capacity of the TNF family members 4-1BBL, OX40L, CD70, GITRL, CD30L and LIGHT to costimu-late human T cells. Eur. J. Immunol. 38, 2678-2688.
54. Lahey, T. P., Loisel, S., Wieland-Alter, W. (2007) Glucocorticoid-induced tumor necrosis factor receptor family-related protein triggering enhances HIV-specific CD4+ T cell cytokine secretion and protects HIV-specific CD4+ T cells from apoptosis. J. Infect. Dis. 196, 43-49.
55. Bishop, G. A, Xie, P. (2007) Multiple roles of TRAF3 signaling in lymphocyte function. Immunol. Res. 39, 22-32.
56. Chase, A. J., Yang, H., Zhang, H., Blankson, J., Siliciano, R (2008) Preservation of FoxP3+ regulatory T cells in the peripheral blood of human immunodeficiency virus type 1-infected elite suppressors correlates with low CD4+ T-cell activation. J. Virol. 82, 8307-8315.
57. Nilsson, J., Boasso, A., Velilla, P., Zhang, R, Vaccari, M., Franchini, G., Shearer, G., Andersson, J., Chougnet, C. (2006) HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 108, 3808-3817.
58. Kinter, A, McNally, J., Riggin, L., Jackson, R, Roby, G., Fauci, A. (2007) Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals. Proc. Natl. Acad. Sci. USA 104, 3390-3395.
59. Macatangay, B. J., Szajnik, M., Whiteside, T., Riddler, S., Rinaldo, C. (2010) Regulatory T cell suppression of Gag-specific CD8 T cell polyfunc-tional response after therapeutic vaccination of HIV-1-infected patients on ART. PLoS ONE 5, e9852.
60. Choi, B. K, Bae, J., Choi, E., Kang, W., Sakaguchi, S., Vinay, D., Kwon, B. (2004) 4-1BB-dependent inhibition of immunosuppression by activated CD4 + CD25+ T cells. J. Leukoc. Biol. 75, 785-791.
61. Robertson, S. J., Messer, R, Carmody, A, Mittler, R, Burlak, C, Hasenkrug, K (2008) CD137 costimulation of CD8+ T cells confers resistance to suppression by virus-induced regulatory T cells. J. Immunol. 180, 5267-5274.
62. Shimizu, J., Yamazaki, S., Takahashi, T., Ishida, Y, Sakaguchi, S. (2002) Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3, 135-142.
63. Nagar, M., Jacob-Hirsch, J., Vernitsky, H., Berkun, Y, Ben-Horin, S., Amariglio, N., Bank, I., Kloog, Y, Rechavi, G, Goldstein, I. (2010) TNF activates a NF-kB-regulated cellular program in human CD45RA- regulatory T cells that modulates their suppressive function. J. Immunol 184, 3570-3581.
64. Elpek, K G., Yolcu, E., Franke, D., Lacelle, C, Schabowsky, R, Shirwan, H. (2007) Ex vivo expansion of CD4+CD25+FoxP3+ T regulatory cells based on synergy between IL-2 and 4-1BB signaling.J. Immunol. 179, 7295-7304.
65. Kang, Y J., Kim, S., Shimada, S., Otsuka, M., Seit-Nebi, A, Kwon, B., Watts, T., Han, J. (2007) Cell surface 4-1BBL mediates sequential signaling pathways "downstream" of TLR and is required for sustained TNF production in macrophages. Nat. Immunol. 8, 601-609.
66. Banerjee, D. K, Dhodapkar, M., Matayeva, E., Steinman, R, Dhodapkar, K (2006) Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 108, 2655-2661.
67. Speiser, D. E., Valmori, D., Rimoldi, D., Pittet, M., Lienard, D., Cerun-dolo, V., MacDonald, H., Cerottini, J., Romero, P. (1999) CD28-negative cytolytic effector T cells frequently express NK receptors and are present at variable proportions in circulating lymphocytes from healthy donors and melanoma patients. Eur. J. Immunol. 29, 1990-1999.
68. Petrovas, C, Mueller, Y, Dimitriou, I., Altork, S., Banerjee, A, Sklar, P., Mounzer, K, Altman, J., Katsikis, P. (2007) Increased mitochondrial mass characterizes the survival defect of HIV-specific CD8(+) T cells. Blood 109, 2505-2513.
69. Day, C. L., Kaufmann, D., Kiepiela, P., Brown, J., Moodley, E., Reddy, S., Mackey, E., Miller, J., Leslie, A, DePierres, C, Mncube, Z., Duraiswamy, J., Zhu, B., Eichbaum, Q., Altfeld, M., Wherry, E., Coovadia, H., Goulder, P., Klenerman, P., Ahmed, R, Freeman, G., Walker, B. (2006) PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443, 350-354.