Efficient stimulation of HIV-1-specific T cells using dendritic cells electroporated with mRNA encoding autologous HIV-1 Gag and Env proteins

Blood

Volumn 107, Issue 5, 2006, Pages 1818-1827

  Van Gulck, Ellen R A ^a   Ponsaerts, Peter ^b   Heyndrickx, Leo ^b   Vereecken, Katleen ^b   Moerman, Filip ^b   De Roo, Ann ^b   Colebunders, Robert ^b   Van Den Bosch, Glenn ^b   Van Bockstaele, Dirk R ^b   Van Tendeloo, Viggo F I ^b   Allard, Sabine ^b   Verrier, Bernard ^b   Marañón, Concepción ^b   Hoeffel, Guillaume ^b   Hosmalin, Anne ^b   Berneman, Zwi N ^b   Vanham, Guido ^b  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GAG PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ADULT; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CELLULAR IMMUNITY; CLINICAL ARTICLE; CODON; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ELECTROPORATION; FEMALE; GENE AMPLIFICATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS GENE;

EID: 33344461737     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-01-0339     Document Type: Article

References (56)

1. Sleasman JW, Goodenow MM. HIV-1 infection. J Allergy Clin Immunol. 2003;111:582-592.
2. Rowland-Jones S, Tan R, McMichael A. Role of cellular immunity in protection against HIV infection. Adv Immunol. 1997;65:277-346.
3. Persaud D, Zhou Y, Siliciano JM, Siliciano RF. Latency in human immunodeficiency virus type 1 infection: no easy answers. J Virol. 2003;77:1659-1665.
4. + T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med. 1999;5:512-517.
5. McMichael AJ, Phillips RE. Escape of human immunodeficiency virus from immune control. Annu Rev Immunol. 1997;15:271-296.
6. Chun TW, Stuyver L, Mizell SB, et al. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci U S A. 1997;94:13193-13197.
7. Chun TW, Fauci AS. Latent reservoirs of HIV: obstacles to the eradication of virus. Proc Natl Acad Sci U S A. 1999;96:10958-10961.
8. Finzi D, Hermankova M, Pierson T, et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science. 1997; 278:1295-1300.
9. Wong JK, Hezareh M, Gunthard HF, et al. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science. 1997;278:1291-1295.
10. Pope M. Dendritic cells as a conduit to improve HIV vaccines. Curr Mol Med. 2003;3:229-242.
11. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245-252.
12. Boczkowski D, Nair SK, Snyder D, Gilboa E. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med. 1996;184:465-472.
13. Van Tendeloo VFI, Van Broeckhoven C, Berneman ZN. Gene-based cancer vaccines: an ex vivo approach. Leukemia. 2001;15:545-558.
14. Larsson M, Wilkens DT, Fonteneau J, et al. Amplification of low-frequency antiviral CD8 T cell responses using autologous dendritic cells. AIDS. 2002;16:171-180.
15. Engelmayer J, Larsson M, Lee A, Cox WI, Steinman RM, Bhardwaj N. Mature dendritic cells infected with canarypox virus elicit strong anti-human immunodeficiency virus CD8+ and CD4+ T-cell responses from chronically infected individuals. J Virol. 2001;75:2142-2153.
16. Zhao X, Huang X, Gupta P, et al. Induction of anti-human immunodeficiency virus type 1 (HIV-1) CD8+ and CD4+ T-cell reactivity by dendritic cells loaded with HIV-1 X4-infected apoptotic cells. J Virol. 2002;76:3007-3014.
17. Tsunetsugu-Yokota Y, Morikawa Y, Isogai M, et al. Yeast-derived human immunodeficiency virus type 1 p55gag virus like particles activate dendritic cells (DCs) and induce perforin expression in gag-specific CD8+ T cells by cross-presentation of DCs. J Virol. 2003;77:10250-10259.
18. Marañón C, Desoutter J, Hoeffel G, Cohen W, Hanau D, Hosmalin A. Dendritic cells cross-present HIV antigens from live as well as apoptotic infected CD4+ T lymphocytes. Proc Natl Acad Sci U S A. 2004;101:6092-6097.
19. Wilson CC, Olson WC, Tuting T, Rinaldo CR, Lotze MT, Storkus WJ. HIV-1-specific CTL responses primed in vitro by blood-derived dendritic cells and Th1-biasing cytokines. J Immunol. 1999;162:3070-3078.
20. Carbonneil C, Aouba A, Burgard M, et al. 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. 2003;17:1731-1740.
21. Brown K, Gao W, Alber S, et al. Adenovirus-transduced dendritic cells injected into skin or lymph node prime potent simian immunodeficiency virus-specific T cell immunity in monkeys. J Immunol. 2003;171:6875-6882.
22. Villamide-Herrera L, Ignatius R, Eller MA, et al. Macaque dendritic cells infected with SIV-recombinant canarypox ex vivo induce SIV-specific immune responses in vivo. AIDS Res Hum Retroviruses. 2004;20:871-884.
23. Lapenta C, Santini SM, Logozzi M, et al. Potent immune response against HIV-1 and protection from virus challenge in hu-PBL-SCID mice immunized with inactivated virus-pulsed DC generated in the presence of IFN-alpha. J Exp Med. 2003;198:361-367.
24. Yoshida A, Tanaka R, Murakami T, et al. Induction of protective immune responses against R5 human immunodeficiency virus type 1 (HIV-1) infection in hu-PBL-SCID mice by intrasplenic immunization with HIV-1-pulsed dendritic cells: possible involvement of a novel factor of human CD4+ T-cell origin. J Virol. 2003;77:8719-8728.
25. Lu W, Andrieu JM. In vitro human immunodeficiency virus eradication by autologous CD8(+) T cells expanded with inactivated-virus-pulsed DC. J Virol. 2001;75:8949-8956.
26. Lu W, Arreas LC, Ferreira WT, Andrieu JM. Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat Med. 2004;10:1359-1365.
27. Van Tendeloo V, Ponsaerts P, Lardon F, et al. 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. 2001;98:49-56.
28. Ponsaerts P, Van Tendeloo VFI, Cools N, et al. mRNA-electroporated mature dendritic cells retain transgene expression, phenotypical properties and stimulatory capacity after cryopreservation. Leukemia. 2002;16:1324-1330.
29. Ponsaerts P, Van den Bosch G, Cools N, et al. Messenger RNA electroporation of human monocytes, followed by rapid in vitro differentiation, leads to highly stimulatory antigen-loaded mature dendritic cells. J Immunol. 2002;169:1669-1675.
30. Gilboa E, Vieweg J. Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol Rev. 2004;199:251-263.
31. Strobel I, Berchtold S, Gotze A, Schulze U, Schuler G, Steinkasserer A. 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. 2000;7:2028-2035.
32. Saeboe-Larssen S, Fossberg E, Gaudernack G. mRNA-based electrotransfection of human dendritic cells and induction of cytotoxic T lymphocyte responses against the telomerase catalytic subunit (hTERT). J Immunol Methods. 2002;259:191-203.
33. Sullenger BA, Gilboa E. Emerging clinical applications of RNA. Nature. 2002;418:252-258.
34. Ponsaerts P, Van Tendeloo VFI, Berneman ZN. Cancer immunotherapy using RNA-loaded dendritic cells. Clin Exp Immunol. 2003;134:378-384.
35. Romani N, Gruner S, Brang D, et al. Proliferating dendritic cell progenitors in human blood. J Exp Med. 1994;180:83-93.
36. Ponsaerts P, Van Tendeloo VFI, Cools N, et al. mRNA-electroporated mature dendritic cells retain transgene expression, phenotypical properties and stimulatory capacity after cryopreservation. Leukemia. 2002;16:1324-1330.
37. Romani N, Lenz A, Glassel H, et al. Cultured human Langerhans cells resemble lymphoid dendritic cells in phenotype and function. J Invest Dermatol. 1989;93:600-609.
38. Bojak A, Wild J, Deml L, Wagner R. Impact of codon usage modification on T cell immunogenicity and longevity of HIV-1 gag-specific DNA vaccines. Intervirology. 2002;45:275-286.
39. Beirnaert E, Willems B, Peeters M, et al. Design and evaluation of an in-house HIV-1 (group M and O), SIVmnd and SIVcpz antigen capture assay. J Virol Methods. 1998;73:65-70.
40. Delwart EL, Busch MP, Kalish ML, Mosley JW, Mullins JI. Rapid molecular epidemiology of human immunodeficiency virus transmission. AIDS Res Hum Retroviruses. 1995;11:1081-1093.
41. Heyndrickx L, Janssens W, Zekeng L, et al. Simplified strategy for detection of recombinant human immunodeficiency virus type 1 group M isolates by gag/env heteroduplex mobility assay. J Virol. 2000;74:363-370.
42. Technelysium. Chromas. http://www.technelysium.com.au\chromas.html. Accessed July 4, 2005.
43. GenomeNet service. CLUSTALW. http://align.genome.jp/. Accessed July 4, 2005.
44. Ibis therapeutics. BioEdit v.7.0.5. http://www.mbio.ncsu.edu/BioEdit/ page2.html. Accessed July 4, 2005.
45. Pantaleo G, Koup RA. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat Med. 2004;10:806-810.
46. Betts M, Yusim K, Koup RA. Optimal antigens for HIV vaccines based on CD8+ T response, protein length, and sequence variability. DNA Cell Biol. 2002;21:665-670.
47. Monie D, Simmonsz RP, Nettles RE, et al. A novel assay allows genotyping of the latent reservoir for human immunodeficiency virus type 1 in the resting CD4+ T cells of viremic patients. J Virol. 2005;79:5185-5202.
48. Chun TW, Justement JS, Lempicki RA, Yang J, et al. Gene expression and viral production in latently infected, resting CD4+ T cells in viremic versus aviremic HIV-infected individuals. Proc Natl Acad Sci U S A. 2003;100:1908-1913.
49. Zack JA, Salvatore AJ, Stacy R, et al. HIV-1 entry into quiescent primary lymphocytes: Molecular analysis reveals a labile, latent viral structure. Cell. 1990;61:213-222.
50. Harari A, Petitpierre S, Vallelian F, Pantaleo G. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood. 2004; 103:966-972.
51. Younes SA, Yassine-Diab B, Dumont AR, et al. HIV-1 viremia prevents the establishment of interleukin 2-producing HIV-specific memory CD4+ T cells endowed with proliferative capacity. J Exp Med. 2003;198:1909-1922.
52. + T cells is associated with diminished interleukin-2 (IL-2) production and is recovered by exogenous IL-2. J Virol. 2003;77:10900-10909.
53. Zimmerli SC, Harari A, Cellerai C, Vallelian F, Bart PA, Pantaleo G. HIV-1-specific IFN-γ/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc Natl Acad Sci U S A. 2005;102:7239-7244.
54. Harari A, Vallelian F, Meylan PR, Pantaleo G. Functional heterogeneity of memory CD4 T cell responses in different conditions of antigen exposure and persistence. J Immunol 2005;174:1037-1045.
55. Addo MM, Yu XG, Rosenberg ES, Walker BD, Altfeld M. Cytotoxic T-lymphocyte (CTL) responses directed against regulatory and accessory proteins in HIV-1 infection. DNA Cell Biol. 2002;21:671-678.
56. Larsson M, Messmer D, Somersan JF, et al. Requirement of mature dendritic cells for efficient activation of influenza A-specific memory CD8+ T cells. J Immunol. 2000;165:1182-1190.