Efficient in vitro expansion of human immunodeficiency virus (HIV)-specific T-cell responses by gag mRNA-electroporated dendritic cells from treated and untreated HIV type 1-infected individuals

Journal of Virology

Volumn 82, Issue 7, 2008, Pages 3561-3573

  Van Gulck, Ellen R ^a   Vanham, Guido ^a,b   Heyndrickx, Leo ^a   Coppens, Sandra ^a   Vereecken, Katleen ^a   Atkinson, Derek ^a   Florence, Eric ^a   Kint, Ilse ^a   Berneman, Zwi Nisan ^b   Van Tendeloo, Viggo ^b  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CYTOKINE; EPITOPE; GAG PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; MESSENGER RNA; PERFORIN;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CODON; CONTROLLED STUDY; DENDRITIC CELL; ELECTROPORATION; ENZYME LINKED IMMUNOSPOT ASSAY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; IMMUNOTHERAPY; IN VITRO SELECTION; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; VIRUS IMMUNITY;

DENDRITIC CELLS; ELECTROPORATION; EPITOPE MAPPING; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON TYPE II; INTERLEUKIN-2; PERFORIN; RNA, MESSENGER; RNA, VIRAL; T-LYMPHOCYTES;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 41149180867     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02080-07     Document Type: Article

References (70)

1. + regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J. Virol. 78:2454-2459.
2. Addo, M. M., X. G. Yu, E. S. Rosenberg, B. D. Walker, and M. Altfeld. 2002. Cytotoxic T-lymphocyte (CTL) responses directed against regulatory and accessory proteins in HIV-1 infection. DNA Cell Biol. 21:671-678.
3. Allen, T. M., D. H. O'Connor, P. Jing, J. L. Dzuris, B. R. Mothe, T. U. Vogel, E. Dunphy, M. E. Liebl, C. Emerson, N. Wilson, K. J. Kunstman, X. Wang, D. B. Allison, A. L. Hughes, R. C. Desrosiers, J. D. Altman, S. M. Wolinsky, A. Sette, and D. I. Watkins. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407: 386-390.
4. Balkwill, F. R., and F. Burke. 1989. The cytokine network. Immunol. Today 10:299-304.
5. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
6. high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 108:2655-2661.
7. + T cells. Blood 107:4781-4789.
8. + T response, protein length, and sequence variability. DNA Cell Biol. 21:665-670.
9. Boczkowski, D., S. K. Nair, D. Snyder, and E. Gilboa. 1996. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J. Exp. Med. 184:465-472.
10. Bojak, A., J. Wild, L. Deml, and R. Wagner. 2002. Impact of codon usage modification on T cell immunogenicity and longevity of HIV-1 gag-specific DNA vaccines. Intervirology 45:275-286.
11. + cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
12. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
13. Brown, K., W. Gao, S. Alber, A. Trichel, M. Murphey-Corb, S. C. Watkins, A. Gambotto, and S. M. Barratt-Boyes. 2003. Adenovirus-transduced dendritic cells injected into skin or lymph node prime potent simian immunodeficiency virus-specific T cell immunity in monkeys. J. Immunol. 171:6875-6882.
14. Carbonneil, C., A. Aouba, M. Burgard, S. Cardinaud, C. Rouzioux, P. Langlade-Demoyen, and L. Weiss. 2003. Dendritic cells generated in the presence of granulocyte-macrophage colony-stimulating factor and IFN-alpha are potent inducers of HIV-specific CD8 T cells. AIDS 17:1731-1740.
15. Chassin, D., M. Andrieu, W. Cohen, B. Culmann-Penciolelli, M. Ostankovitch, D. Hanau, and J. G. Guillet. 1999. Dendritic cells transfected with the nef genes of HIV-1 primary isolates specifically activate cytotoxic T lymphocytes from seropositive subjects. Eur. J. Immunol. 29:196-202.
16. Chun, T. W., and A. S. Fauci. 1999. Latent reservoirs of HIV: obstacles to the eradication of virus. Proc. Natl. Acad. Sci. USA 96:10958-10961.
17. Day, C. L., D. E. Kaufmann, P. Kiepiela, J. A. Brown, E. S. Moodley, S. Reddy, E. W. Mackey, J. D. Miller, A. J. Leslie, C. DePierres, Z. Mncube, J. Duraiswamy, B. Zhu, Q. Eichbaum, M. Altfeld, E. J. Wherry, H. M. Coovadia, P. J. Goulder, P. Klenerman, R. Ahmed, G. J. Freeman, and B. D. Walker. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350-354.
18. Eggena, M. P., B. Barugahare, N. Jones, M. Okello, S. Mutalya, C. Kityo, P. Mugyenyi, and H. Cao. 2005. Depletion of regulatory T cells in HIV infection is associated with immune activation. J. Immunol. 174:4407-4414.
19. + T-cell responses from chronically infected individuals. J. Virol. 75:2142-2153.
20. Evans, D. T., D. H. O'Connor, P. Jing, J. L. Dzuris, J. Sidney, J. da Silva, T. M. Allen, H. Horton, J. E. Venham, R. A. Rudersdorf, T. Vogel, C. D. Pauza, R. E. Bontrop, R. DeMars, A. Sette, A. L. Hughes, and D. I. Watkins. 1999. Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat. Med. 5:1270-1276.
21. Geldmacher, C., J. R. Currier, E. Herrmann, A. Haule, E. Kuta, F. McCutchan, L. Njovu, S. Geis, O. Hoffmann, L. Maboko, C. Williamson, D. Birx, A. Meyerhans, J. Cox, and M. Hoelscher. 2007. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 81:2440-2448.
22. Gilboa, E., and J. Vieweg. 2004. Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol. Rev. 199:251-263.
23. Goulder, P. J., R. E. Phillips, R. A. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, A. J. McMichael, and S. Rowland-Jones. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
24. Gupta, S. B., C. T. Mast, N. D. Wolfe, V. Novitsky, S. A. Dubey, E. G. Kallas, M. Schechter, B. Mbewe, E. Vardas, P. Pitisuttithum, D. Burke, D. Freed, R. Mogg, P. M. Coplan, J. H. Condra, R. S. Long, K. Anderson, D. R. Casimiro, J. W. Shiver, and W. L. Straus. 2006. Cross-clade reactivity of HIV-1-specific T-cell responses in HIV-1-infected individuals from Botswana and Cameroon. J. Acquir. Immune Defic. Syndr. 42:135-139.
25. Harari, A., F. Vallelian, P. R. Meylan, and G. Pantaleo. 2005. Functional heterogeneity of memory CD4 T cell responses in different conditions of antigen exposure and persistence. J. Immunol. 174:1037-1045.
26. Hryniewicz, A., A. Boasso, Y. Edghill-Smith, M. Vaccari, D. Fuchs, D. Venzon, J. Nacsa, M. R. Betts, W. P. Tsai, J. M. Heraud, B. Beer, D. Blanset, C. Chougnet, I. Lowy, G. M. Shearer, and G. Franchini. 2006. CTLA-4 blockade decreases TGF-β, IDO, and viral RNA expression in tissues of SIVmac251-infected macaques. Blood 108:3834-3842.
27. Jacob, C. O. 1992. Tumor necrosis factor and interferon gamma: relevance for immune regulation and genetic predisposition to autoimmune disease. Semin. Immunol. 4:147-154.
28. + T cells by dendritic cells transfected with mRNA encoding cytoplasm- or lysosome-targeted Nef. Blood 107:1963-1969.
29. Keir, M. E., L. M. Francisco, and A. H. Sharpe. 2007. PD-1 and its ligands in T-cell immunity. Curr. Opin. Immunol. 19:309-314.
30. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
31. + T cells in vitro. AIDS Res. Hum. Retrovir. 23:438-450.
32. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 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.
33. Lapenta, C., S. M. Santini, M. Logozzi, M. Spada, M. Andreotti, T. Di Pucchio, S. Parlato, and F. Belardelli. 2003. Potent immune response against HIV-1 and protection from virus challenge in hu-PBL-SCID mice immunized with inactivated virus-pulsed dendritic cells generated in the presence of IFN-alpha. J. Exp. Med. 198:361-367.
34. Larsson, M., D. T. Wilkens, J. F. Fonteneau, T. J. Beadle, M. J. Merritt, R. G. Kost, P. A. Haslett, S. Cu-Uvin, N. Bhardwaj, D. F. Nixon, and B. L. Shacklett. 2002. Amplification of low-frequency antiviral CD8 T cell responses using autologous dendritic cells. AIDS 16:171-180.
35. Ling, B., R. S. Veazey, M. Hart, A. A. Lackner, M. Kuroda, B. Pahar, and P. A. Marx. 2007. Early restoration of mucosal CD4 memory CCR5 T cells in the gut of SIV-infected rhesus predicts long term non-progression. AIDS 21:2377-2385.
36. + T cells expanded with inactivated-virus-pulsed dendritic cells. J. Virol. 75:8949-8956.
37. Lu, W., L. C. Arraes, W. T. Ferreira, and J. M. Andrieu. 2004. Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat. Med. 10:1359-1365.
38. Maserati, R., A. Foli, L. Tomasoni, L. Sighinolfi, F. Maggiolo, D. Sacchini, M. Di Pietro, D. Bertelli, C. Tinelli, and F. Lori. 2007. Effects of structured treatment interruptions on metabolic, anthropometric, immunologic, and quality of life outcomes in HIV-positive adults on HAART. Curr. HIV Res. 5:337-343.
39. McMichael, A. J., and R. E. Phillips. 1997. Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15:271-296.
40. + T cell responses to SIV using mRNA-transfected DC expressing autologous viral Ag. Eur. J. Immunol. 37:2164-2173.
41. + T cell depletion on virus replication in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Exp. Med. 191:1921-1931.
42. + T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
43. Nair, M. P., R. Pottathil, E. P. Heimer, and S. A. Schwartz. 1988. Immunoregulatory activities of human immunodeficiency virus (HIV) proteins: effect of HIV recombinant and synthetic peptides on immunoglobulin synthesis and proliferative responses by normal lymphocytes. Proc. Natl. Acad. Sci. USA 85:6498-6502.
44. Pantaleo, G., and R. A. Koup. 2004. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat. Med. 10:806-810.
45. Paul, W. E. 1989. Pleiotropy and redundancy: T cell-derived lymphokines in the immune response. Cell 57:521-524.
46. Persaud, D., Y. Zhou, J. M. Siliciano, and R. F. Siliciano. 2003. Latency in human immunodeficiency virus type 1 infection: no easy answers. J. Virol. 77:1659-1665.
47. Ponsaerts, P., G. Van den Bosch, N. Cools, A. Van Driessche, G. Nijs, M. Lenjou, F. Lardon, C. Van Broeckhoven, D. R. Van Bockstaele, Z. N. Berneman, and V. F. Van Tendeloo. 2002. Messenger RNA electroporation of human monocytes, followed by rapid in vitro differentiation, leads to highly stimulatory antigen-loaded mature dendritic cells. J. Immunol. 169:1669-1675.
48. Ponsaerts, P., V. F. Van Tendeloo, N. Cools, A. Van Driessche, F. Lardon, G. Nijs, M. Lenjou, G. Mertens, C. Van Broeckhoven, D. R. Van Bockstaele, and Z. N. Berneman. 2002. mRNA-electroporated mature dendritic cells retain transgene expression, phenotypical properties and stimulatory capacity after cryopreservation. Leukemia 16:1324-1330.
49. Pope, M. 2003. Dendritic cells as a conduit to improve HIV vaccines. Curr. Mol. Med. 3:229-242.
50. Price, D. A., P. J. Goulder, P. Klenerman, A. K. Sewell, P. J. Easterbrook, M. Troop, C. R. Bangham, and R. E. Phillips. 1997. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 94:1890-1895.
51. Romani, N., S. Gruner, D. Brang, E. Kampgen, A. Lenz, B. Trockenbacher, G. Konwalinka, P. O. Fritsch, R. M. Steinman, and G. Schuler. 1994. Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180:83-93.
52. Rosignoli, G., A. Cranage, C. Burton, M. Nelson, A. Steel, B. Gazzard, F. Gotch, and N. Imami. 2007. Expression of PD-L1, a marker of disease status, is not reduced by HAART in aviraemic patients. AIDS 21:1379-1381.
53. Rowland-Jones, S., R. Tan, and A. McMichael. 1997. Role of cellular immunity in protection against HIV infection. Adv. Immunol. 65:277-346.
54. Saeboe-Larssen, S., E. Fossberg, and G. Gaudernack. 2002. mRNA-based electrotransfection of human dendritic cells and induction of cytotoxic T lymphocyte responses against the telomerase catalytic subunit (hTERT). J. Immunol. Methods 259:191-203.
55. + lymphocytes. Science 283:857-860.
56. Sempere, J. M., V. Soriano, and J. M. Benito. 2007. T regulatory cells and HIV infection. AIDS Rev. 9:54-60.
57. Strobel, I., S. Berchtold, A. Gotze, U. Schulze, G. Schuler, and A. Steinkasserer. 2000. Human dendritic cells transfected with either RNA or DNA encoding influenza matrix protein M1 differ in their ability to stimulate cytotoxic T lymphocytes. Gene Ther. 7:2028-2035.
58. + T cells leads to reversible immune dysfunction. Nat. Med. 12:1198-1202.
59. gag virus-like particles activate dendritic cells (DCs) and induce perforin expression in Gag-specific CD8+ T cells by cross-presentation of DCs. J. Virol. 77:10250-10259.
60. Van Gulck, E. R., P. Ponsaerts, L. Heyndrickx, K. Vereecken, F. Moerman, A. De Roo, R. Colebunders, G. Van den Bosch, D. R. Van Bockstaele, V. F. Van Tendeloo, S. Allard, B. Verrier, C. Maranon, G. Hoeffel, A. Hosmalin, Z. N. Berneman, and G. Vanham. 2006. Efficient Stimulation of HIV-1-specific T cells using dendritic cells electroporated with mRNA encoding autologous HIV-1 Gag and Env proteins. Blood 107:1818-1827.
61. Van Tendeloo, V. F., P. Ponsaerts, F. Lardon, G. Nijs, M. Lenjou, C. Van Broeckhoven, D. R. Van Bockstaele, and Z. N. Berneman. 2001. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 98:49-56.
62. Van Tendeloo, V. F., C. Van Broeckhoven, and Z. N. Berneman. 2001. Gene-based cancer vaccines: an ex vivo approach. Leukemia 15:545-558.
63. Villamide-Herrera, L., R. Ignatius, M. A. Eller, K. Wilkinson, C. Griffin, E. Mehlhop, J. Jones, S. Y. Han, M. G. Lewis, S. Parrish, T. C. Vancott, J. D. Lifson, S. Schlesinger, J. R. Mascola, and M. Pope. 2004. Macaque dendritic cells infected with SIV-recombinant canarypox ex vivo induce SIV-specific immune responses in vivo. AIDS Res. Hum. Retrovir. 20:871-884.
64. + regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 104:3249-3256.
65. Weissman, D., H. Ni, D. Scales, A. Dude, J. Capodici, K. McGibney, A. Abdool, S. N. Isaacs, G. Cannon, and K. Kariko. 2000. HIV gag mRNA transfection of dendritic cells (DC) delivers encoded antigen to MHC class I and II molecules, causes DC maturation, and induces a potent human in vitro primary immune response. J. Immunol. 165:4710-4717.
66. Wilson, C. C., W. C. Olson, T. Tuting, C. R. Rinaldo, M. T. Lotze, and W. J. Storkus. 1999. HIV-1-specific CTL responses primed in vitro by blood-derived dendritic cells and Th1-biasing cytokines. J. Immunol. 162:3070-3078.
67. + T-cell origin. J. Virol. 77:8719-8728.
68. + T-cell exhaustion in typical progressors but not in long-term nonprogressors. Blood 109: 4671-4678.
69. + T-cell reactivity by dendritic cells loaded with HIV-1 X4-infected apoptotic cells. J. Virol. 76: 3007-3014.
70. Zimmerli, S. C., A. Harari, C. Cellerai, F. Vallelian, P. A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. USA 102:7239-7244.