Induction of HIV-specific T and B cell responses with a replicating and conditionally infectious lentiviral vaccine

European Journal of Immunology

Volumn 38, Issue 5, 2008, Pages 1310-1320

  Wingard, Jeremy B ^a,c   Anderson, Bart ^b   Weissman, Drew ^b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Dendritic cell; HIV; Immune response; Lentiviral vector

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; LENTIVIRUS VACCINE; LENTIVIRUS VECTOR; UNCLASSIFIED DRUG; DNA VACCINE; GAG PROTEIN; GAMMA INTERFERON; P55 GAG PRECURSOR PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN PRECURSOR;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNIZATION; IN VITRO STUDY; LENTIVIRINAE; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SUPERNATANT; T LYMPHOCYTE; VACCINATION; VIRUS CORE; VIRUS REPLICATION; ANIMAL; ANTIBODY PRODUCTION; BAGG ALBINO MOUSE; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; IMMUNOLOGY; METABOLISM; METHODOLOGY; TRANSPLANTATION; ULTRASTRUCTURE; VIROLOGY; VIRUS NUCLEOCAPSID;

AIDS VACCINES; ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; FEMALE; FUSION PROTEINS, GAG-POL; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENETIC VECTORS; HIV; HIV CORE PROTEIN P24; INTERFERON TYPE II; LENTIVIRUS; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON; NUCLEOCAPSID; PROTEIN PRECURSORS; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; VACCINATION; VACCINES, DNA;

EID: 47049088108     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200738069     Document Type: Article

References (75)

1. Banchereau, J. and Palucka, A. K., Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 2005. 5: 296-306.
2. Ashley, D. M., Faiola, B., Nair, S., Hale, L. P., Bigner, D. D. and Gilboa, E., Bone marrow-generated dendritic cells pulsed with tumor extracts or tumor RNA induce antitumor immunity against central nervous system tumors. J. Exp. Med. 1997. 186: 1177-1182.
3. Nestle, F. O., Alijagic, S., Gilliet, M., Sun, Y., Grabbe, S., Dummer, R., Burg, G. and Schadendorf, D., Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 1998. 4: 328-332.
4. Mayordomo, J. I., Loftus, D. J., Sakamoto, H., De Cesare, C. M., Appasamy, P. M., Lotze, M. T., Storkus, W. J. et al., Therapy of murine tumors with p53 wild-type and mutant sequence peptide-based vaccines. J. Exp. Med. 1996. 183: 1357-1365.
5. Celluzzi, C. M., Mayordomo, J. I., Storkus,W. J., Lotze, M. T. and Falo, L. D., Jr., Peptide-pulsed dendritic cells induce antigen-specific CTL-mediated protective tumor immunity. J. Exp. Med. 1996. 183: 283-287.
6. Lundstrom, K., Latest development in viral vectors for gene therapy. Trends Biotechnol. 2003. 21: 117-122.
7. Breckpot, K., Dullaers, M., Bonehill, A., van Meirvenne, S., Heirman, C., de Greef, C., van der Bruggen, P. and Thielemans, K., Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J. Gene Med. 2003. 5: 654-667.
8. He, Y., Zhang, J., Mi, Z., Robbins, P. and Falo, L. D., Jr., Immunization with lentiviral vector-transduced dendritic cells induces strong and long-lasting T cell responses and therapeutic immunity. J. Immunol. 2005. 174: 3808-3817.
9. Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature 1998. 392: 245-252.
10. Zarei, S., Leuba, F., Arrighi, J. F., Hauser, C. and Piguet, V., Transduction of dendritic cells by antigen-encoding lentiviral vectors permits antigen processing and MHC class I-dependent presentation. J. Allergy Clin. Immunol. 2002. 109: 988-994.
11. Metharom, P., Ellem, K. A., Schmidt, C. and Wei, M. Q., Lentiviral vector-mediated tyrosinase-related protein 2 gene transfer to dendritic cells for the therapy of melanoma. Hum. Gene Ther. 2001. 12: 2203-2213.
12. De Smedt, T., Pajak, B., Klaus, G. G., Noelle, R. J., Urbain, J., Leo, O. and Moser, M., Antigen-specific T lymphocytes regulate lipopolysaccharide-induced apoptosis of dendritic cells in vivo. J. Immunol. 1998. 161: 4476-4479.
13. Brent, L., Cohen, I. R., Doherty, P. C., Feldmann, M., Matzinger, P., Ghost, L., Holgate, S. T. et al., Crystal-ball gazing - the future of immunological research viewed from the cutting edge. Clin. Exp. Immunol. 2007. 147: 1-10.
14. Finzi, A., Orthwein, A., Mercier, J. and Cohen, E. A., Productive HIV-1 assembly takes place at the plasma membrane. J. Virol. 2007. 81: 7476-7490.
15. Gottlinger, H. G., The HIV-1 assembly machine. Aids 2001. 15 Suppl 5: S13-S20.
16. Allan, R. S., Waithman, J., Bedoui, S., Jones, C. M., Villadangos, J. A., Zhan, Y., Lew, A. M. et al., Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006. 25: 153-162.
17. den Haan, J. M., Lehar, S. M. and Bevan, M. J., CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 2000. 192: 1685-1696.
18. + T cell cross-priming with exogenous antigens. J. Immunol. 2001. 166: 7268-7275.
19. Maurer, T., Heit, A., Hochrein, H., Ampenberger, F., O'Keeffe, M., Bauer, S., Lipford, G. B. et al., CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 2002. 32: 2356-2364.
20. Shen, H., Ackerman, A. L., Cody, V., Giodini, A., Hinson, E. R., Cresswell, P., Edelson, R. L. et al., Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology 2006. 117: 78-88.
21. Fonteneau, J. F., Kavanagh, D. G., Lirvall, M., Sanders, C., Cover, T. L., Bhardwaj, N. and Larsson, M., Characterization of the MHC class I cross-presentation pathway for cell-associated antigens by human dendritic cells. Blood 2003. 102: 4448-4455.
22. Palliser, D., Guillen, E., Ju, M. and Eisen, H. N., Multiple intracellular routes in the cross-presentation of a soluble protein by murine dendritic cells. J. Immunol. 2005. 174: 1879-1887.
23. Butler, S. L., Hansen, M. S. and Bushman, F. D., A quantitative assay for HIV DNA integration in vivo. Nat. Med. 2001. 7: 631-634.
24. Kramer, B., Pelchen-Matthews, A., Deneka, M., Garcia, E., Piguet, V. and Marsh, M., HIV interaction with endosomes in macrophages and dendritic cells. Blood Cells Mol. Dis. 2005. 35: 136-142.
25. Delcayre, A., Shu, H. and Le Pecq, J. B., Dendritic cell-derived exosomes in cancer immunotherapy: Exploiting nature's antigen delivery pathway. Expert Rev. Anticancer Ther. 2005. 5: 537-547.
26. Turville, S. G., Santos, J. J., Frank, I., Cameron, P. U., Wilkinson, J., Miranda-Saksena, M., Dable, J. et al., Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 2004. 103: 2170-2179.
27. Nermut, M. V., Zhang, W. H., Francis, G., Ciampor, F., Morikawa, Y. and Jones, I. M., Time course of Gag protein assembly in HIV-1-infected cells: A study by immunoelectron microscopy. Virology 2003. 305: 219-227.
28. Morikawa, Y., Shibuya, M., Goto, T. and Sano, K., In vitro processing of human immunodeficiency virus type 1 Gag virus-like particles. Virology 2000. 272: 366-374.
29. Smith, A. J., Srinivasakumar, N., Hammarskjold, M. L. and Rekosh, D., Requirements for incorporation of Pr160gag-pol from human immunodeficiency virus type 1 into virus-like particles. J. Virol. 1993. 67: 2266-2275.
30. Palmowski, M. J., Lopes, L., Ikeda, Y., Salio, M., Cerundolo, V. and Collins, M. K., Intravenous injection of a lentiviral vector encoding NYESO-1 induces an effective CTL response. J. Immunol. 2004. 172: 1582-1587.
31. Zarei, S., Abraham, S., Arrighi, J. F., Haller, O., Calzascia, T., Walker, P. R., Kundig, T. M. et al., Lentiviral transduction of dendritic cells confers protective antiviral immunity in vivo. J. Virol. 2004. 78: 7843-7845.
32. Coskun, A. K., van Maanen, M., Janka, D., Stockton, D., Stankiewicz, P., Yatsenko, S. and Sutton, R. E., Isolation and characterization of mouse-human microcell hybrid cell clones permissive for infectious HIV particle release. Virology 2007. 362: 283-293.
33. Randolph, G. J., Angeli, V. and Swartz, M. A., Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 2005. 5: 617-628.
34. Gilboa, E., Nair, S. K. and Lyerly, H. K., Immunotherapy of cancer with dendritic-cell-based vaccines. Cancer Immunol. Immunother. 1998. 46: 82-87.
35. Gilboa, E. and Vieweg, J., Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol. Rev. 2004. 199: 251-263.
36. Esslinger, C., Chapatte, L., Finke, D., Miconnet, I., Guillaume, P., Levy, F. and MacDonald, H. R., In vivo administration of a lentiviral vaccine targets DCs and induces efficient CD8(+) Tcell responses. J. Clin. Invest. 2003. 111: 1673-1681.
37. Daecke, J., Fackler, O. T., Dittmar, M. T. and Krausslich, H. G., Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J. Virol. 2005. 79: 1581-1594.
38. Vidricaire, G., Imbeault, M. and Tremblay, M. J., Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J. Virol. 2004. 78: 11904-11915.
39. Hao, H. N. and Lyman, W. D., HIV infection of fetal human astrocytes: The potential role of a receptor-mediated endocytic pathway. Brain Res. 1999. 823: 24-32.
40. Filice, G., Cereda, P. M., Orsolini, P., Soldini, L., Razzini, E., Campisi, D. and Gulminetti, R., Endocytosis constitute the infectious route of HIV-1 entry in human and rabbit monocytes lacking the CD4 receptor. Microbiologica 1991. 14: 77-93.
41. Pauza, C. D., The endocytic pathway for human immunodeficiency virus infection. Adv. Exp. Med. Biol. 1991. 300: 111-138.
42. Hladik, F., Sakchalathorn, P., Ballweber, L., Lentz, G., Fialkow, M., Eschenbach, D. and McElrath, M. J., Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007. 26: 257-270.
43. Diaz-Griffero, F., Taube, R., Muehlbauer, S.M. and Brojatsch, J., Efficient production of HIV-1 viral-like particles in mouse cells. Biochem. Biophys. Res. Commun. 2008.368: 463-469.
44. Carbone, F. R., Belz, G. T. and Heath, W. R., Transfer of antigen between migrating and lymph node-resident DCs in peripheral T-cell tolerance and immunity. Trends Immunol. 2004. 25: 655-658.
45. Belz, G. T., Smith, C. M., Kleinert, L., Reading, P., Brooks, A., Shortman, K., Carbone, F. R. and Heath, W. R., Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci USA 2004. 101: 8670-8675.
46. Datta, S. K., Redecke, V., Prilliman, K. R., Takabayashi, K., Corr, M., Tallant, T., DiDonato, J. et al., A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J. Immunol. 2003. 170: 4102-4110.
47. Schulz, O., Diebold, S. S., Chen, M., Naslund, T. I., Nolte, M. A., Alexopoulou, L., Azuma, Y. T. et al., Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005. 433: 887-892.
48. Gatti, E. and Pierre, P., Understanding the cell biology of antigen presentation: The dendritic cell contribution. Curr. Opin. Cell Biol. 2003. 15: 468-473.
49. Delamarre, L., Holcombe, H. and Mellman, I., Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation. J. Exp. Med. 2003. 198: 111-122.
50. Nair, S. K., Immunotherapy of cancer with dendritic cell-based vaccines. Gene Ther. 1998. 5: 1445-1446.
51. Weissman, D., Ni, H., Scales, D., Dude, A., Capodici, J., McGibney, K., Abdool, A. et al., 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. 2000. 165: 4710-4717.
52. Derby, N. R., Gray, S.,Wayner, E., Campogan, D., Vlahogiannis, G., Kraft, Z., Barnett, S. W. et al., Isolation and characterization of monoclonal antibodies elicited by trimeric HIV-1 Env gp140 protein immunogens. Virology 2007. 366: 433-545.
53. Franke, R., Hirsch, T. and Eichler, J., A rationally designed synthetic mimic of the discontinuous CD4-binding site of HIV-1 gp120. J. Recept. Signal Transduct. Res. 2006. 26: 453-460.
54. Hunke, C., Hirsch, T. and Eichler, J., Structure-based synthetic mimicry of discontinuous protein binding sites: Inhibitors of the interaction of Mena EVH1 domain with proline-rich ligands. Chembiochem. 2006. 7: 1258-1264.
55. Kim, M., Qiao, Z., Yu, J., Montefiori, D. and Reinherz, E. L., Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 2007. 25: 5102-5114.
56. Zolla-Pazner, S., Improving on nature: Focusing the immune response on the V3 loop. Hum. Antibodies 2005. 14: 69-72.
57. Mata, M., Yao, Z. J., Zubair, A., Syres, K. and Paterson, Y., Evaluation of a recombinant Listeria monocytogenes expressing an HIV protein that protects mice against viral challenge. Vaccine 2001. 19: 1435-1445.
58. Letvin, N. L., Correlates of immune protection and the development of a human immunodeficiency virus vaccine. Immunity 2007. 27: 366-369.
59. Lu, X., Humeau, L., Slepushkin, V., Binder, G., Yu, Q., Slepushkina, T., Chen, Z. et al., Safe two-plasmid production for the first clinical lentivirus vector that achieves >99% transduction in primary cells using a one-step protocol. J. Gene Med. 2004. 6: 963-973.
60. Baltathakis, I., Alcantara, O. and Boldt, D. H., Expression of different NF-kappaB pathway genes in dendritic cells (DCs) or macrophages assessed by gene expression profiling. J. Cell. Biochem. 2001. 83: 281-290.
61. Hacein-Bey-Abina, S., von Kalle, C., Schmidt, M., Le Deist, F., Wulffraat, N., McIntyre, E., Radford, I. et al., A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Eng. J. Med. 2003. 348: 255-256.
62. + infected patients grouped according to CD4 count and viral load. Mol. Ther. 2004. 9: 902-913.
63. Manilla, P., Rebello, T., Afable, C., Lu, X., Slepushkin, V., Humeau, L. M., Schonely, K. et al., Regulatory considerations for novel gene therapy products: A review of the process leading to the first clinical lentiviral vector. Hum. Gene Ther. 2005. 16: 17-25.
64. Sinn, P. L., Sauter, S. L. and McCray, P. B., Jr., Gene therapy progress and prospects: Development of improved lentiviral and retroviral vectors - design, biosafety, and production. Gene Ther. 2005. 12: 1089-1098.
65. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S. and Steinman, R. M., Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1992. 176: 1693-1702.
66. Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N. and Schuler, G., An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 1999. 223: 77-92.
67. O'Doherty, U., Swiggard, W. J. and Malim, M. H., Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 2000. 74: 10074-10080.
68. Clouse, K. A., Powell, D., Washington, I., Poli, G., Strebel, K., Farrar, W., Barstad, P. et al., Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J. Immunol. 1989. 142: 431-438.
69. Folks, T. M., Clouse, K. A., Justement, J., Rabson, A., Duh, E., Kehrl, J. H. and Fauci, A. S., Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc. Natl. Acad. Sci. USA 1989. 86: 2365-2368.
70. Ferns, R. B., Tedder, R. S. and Weiss, R. A., Characterization of monoclonal antibodies against the human immunodeficiency virus (HIV) gag products and their use in monitoring HIV isolate variation. J. Gen. Virol. 1987. 68: 1543-1551.
71. Ferns, R. B., Partridge, J. C., Spence, R. P., Hunt, N. and Tedder, R. S., Epitope location of 13 anti-gag HIV-1 monoclonal antibodies using oligopeptides and their cross reactivity with HIV-2. AIDS 1989. 3: 829-834.
72. Mata, M., Travers, P. J., Liu, Q., Frankel, F. R. and Paterson, Y., The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J. Immunol. 1998. 161: 2985-2993.
73. + T cells in the spleen and gut-associated lymphoid tissue by parenteral or mucosal immunization with recombinant Listeria monocytogenes HIV Gag. J. Immunol. 2003. 170: 5176-5187.
74. Chesebro, B., Wehrly, K., Nishio, J. and Perryman, S., Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: Definition of critical amino acids involved in cell tropism. J. Virol. 1992. 66: 6547-6554.
75. Toohey, K., Wehrly, K., Nishio, J., Perryman, S. and Chesebro, B., Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread. Virology 1995. 213: 70-79.