Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine

Journal of Experimental Medicine

Volumn 203, Issue 3, 2006, Pages 607-617

  Trumpfheller, Christine ^a   Finke, Jennifer S ^a   López, Carolina B ^b   Moran, Thomas M ^b   Moltedo, Bruno ^b   Soares, Helena ^a   Huang, Yaoxing ^c   Schlesinger, Sarah J ^a,c   Chae, Gyu Park ^a   Nussenzweig, Michel C ^a   Granelli Piperno, Angela ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c AARON DIAMOND AIDS RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTIGEN; ANTIGEN P24; CD40 LIGAND MONOCLONAL ANTIBODY; DENDRITIC CELL VACCINE; GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 2; PEPTIDE; PLASMID DNA; PROTEIN P41; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOSE RESPONSE; DRUG EFFICACY; HAPLOTYPE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOID TISSUE; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN ENGINEERING; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VACCINATION; VACCINIA;

ADENOVIRIDAE; AIDS VACCINES; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN PRESENTATION; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; GENE PRODUCTS, GAG; GENETIC VECTORS; HAPLOTYPES; HIV-1; HUMANS; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; INJECTIONS, SUBCUTANEOUS; LECTINS, C-TYPE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; VACCINIA VIRUS;

EID: 33645048192     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052005     Document Type: Article

References (55)

1. Seder, R.A., and J.R. Mascola. 2003. Basic immunology of vaccine development. In The Vaccine Book. B.R. Bloom and P.-H. Lambert, editors. Academic Press, Boston. 51-72 pp.
2. Berzofsky, J.A., J.D. Ahlers, J. Janik, J. Morris, S. Oh, M. Terabe, and I.M. Belyakov. 2004. Progress on new vaccine strategies against chronic viral infections. J. Clin. Invest. 114:450-462.
3. 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.
4. Saul, A., V. Nussenzweig, and R.S. Nussenzweig. 2004. Rationale for malaria vaccine development. In Novel Vaccination Strategies. S.H.E. Kaufmann, editor. Wiley-Vch Verlag GmbH & Co. 479-503.
5. Frazer, I.H. 2004. Prevention of cervical cancer through papillomavirus vaccination. Nat. Rev. Immunol. 4:46-54.
6. + T-cell response. Nat. Rev. Immunol. 4:595-602.
7. Rosenberg, E.S., J.M. Billingsley, A.M. Caliendo, S.L. Boswell, P. Sax, S.A. Kalams, and B.D. Walker. 1997. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science. 278:1447-1450.
8. Martinez, V., D. Costagliola, O. Bonduelle, N. N'Go, A. Schruriger, I. Theodorou, J.-P. Clauvel, D. Sicard, H. Agut, P. Debre, et al. 2005. Combination of HIV-1-specific CD4 Th1 cell responses and IgG2 anitbodies is the best predictor for persistence of long-term nonprogression. J. Infect. Dis. 191:2053-2063.
9. + T cells. J. Exp. Med. 200:701-712.
10. Kaech, S.M., E.J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2:251-262.
11. Levine, M.M., and M.B. Sztein. 2004. Vaccine development strategies for improving immunization: the role of modern immunology. Nat. Immunol. 5:460-464.
12. Steinman, R.M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271-296.
13. Hart, D.N.J. 1997. Dendritic cells: unique leukocyte populations which control the primary immune response. Blood. 90:3245-3287.
14. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y.-J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
15. Lanzavecchia, A., and F. Sallusto. 2001. Regulation of T cell immunity by dendritic cells. Cell. 106:263-266.
16. Moser, M. 2003. Dendritic cells in immunity and tolerance - do they display opposite functions? Immunity. 19:5-8.
17. Pulendran, B. 2004. Modulating vaccine reponses with dendritic cells and toll-like receptors. Immunol. Rev. 199:227-250.
18. Inaba, K., and R.M. Steinman. 1985. Protein-specific helper T lymphocyte formation initiated by dendritic cells. Science. 229:475-479.
19. Inaba, K., J.P. Metlay, M.T. Crowley, and R.M. Steinman. 1990. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J. Exp. Med. 172:631-640.
20. Schuler-Thurner, B., E.S. Schultz, T.G. Berger, G. Weinlich, S. Ebner, P. Woerl, A. Bender, B. Feuerstein, P.O. Fritsch, N. Romani, and G. Schuler. 2002. Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J. Exp. Med. 195:1279-1288.
21. -. subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189:587-592.
22. Jiang, W., W.J. Swiggard, C. Heufler, M. Peng, A. Mirza, R.M. Steinman, and M.C. Nussenzweig. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature. 375:151-155.
23. Mahnke, K., M. Guo, S. Lee, H. Sepulveda, S.L. Swain, M. Nussenzweig, and R.M. Steinman. 2000. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell Biol. 151:673-683.
24. Kraal, G., M. Breel, M. Janse, and G. Bruin. 1986. Langerhans cells, veiled cells, and interdigitating cells in the mouse recognized by a monoclonal antibody. J. Exp. Med. 163:981-997.
25. Vremec, D., and K. Shortman. 1997. Dendritic cell subtypes in mouse lymphoid organs. Cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J. Immunol. 159:565-573.
26. Inaba, K., W.J. Swiggard, M. Inaba, J. Meltzer, A. Mirza, T. Sasagawa, M.C. Nussenzweig, and R.M. Steinman. 1995. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. I. Expression on dendritic cells and other subsets of mouse leukocytes. Cell. Immunol. 163:148-156.
27. Witmer-Pack, M.D., W.J. Swiggard, A. Mirza, K. Inaba, and R.M. Steinman. 1995. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues. Cell. Immunol. 163:157-162.
28. Hawiger, D., K. Inaba, Y. Dorsett, K. Guo, K. Mahnke, M. Rivera, J.V. Ravetch, R.M. Steinman, and M.C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194:769-780.
29. + T cell tolerance. J. Exp. Med. 196:1627-1638.
30. Bonifaz, L.C., D.P. Bonnyay, A. Charalambous, D.I. Darguste, S. Fujii, H. Soares, M.K. Brimnes, B. Moltedo, T.M. Moran, and R.M. Steinman. 2004. In vivo targeting of antigens to the DEC-205 receptor on maturing dendritic cells improves T cell vaccination. J. Exp. Med. 199:815-824.
31. Hawiger, D., R.F. Masilamani, E. Bettelli, V.K. Kuchroo, and M.C. Nussenzweig. 2004. Immunological unresponsiveness characterized by increased expression of CD5 on peripheral T cells induced by dendritic cells in vivo. Immunity. 20:695-705.
32. Trombetta, E.S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23:975-1028.
33. + T cell expansion with variable dependence on type I IFN. J. Exp. Med. 199:775-784.
34. Kern, F., N. Faulhaber, C. Frommel, E. Khatamzas, S. Prosch, C. Schonemann, I. Kretzschmar, R. Volkmer-Engert, H.D. Volk, and P. Reinke. 2000. Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur. J. Immunol. 30:1676-1682.
35. Maecker, H.T., H.S. Dunn, M.A. Suni, E. Khatamzas, C.J. Pitcher, T. Bunde, N. Persaud, W. Trigona, T.-M. Fu, E. Sinclair, et al. 2001. Use of overlapping peptide mixtures as antigens for cytokine flow cytometry. J. Immunol. Methods. 255:27-40.
36. Mata, M., P.J. Travers, Q. Liu, F.R. Frankel, and Y. Paterson. 1998. 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. 161:2985-2993.
37. McMichael, A.J., and T. Hanke. 2003. HIV vaccines 1983-2003. Nat. Med. 9:874-880.
38. Emini, E.A., and W.C. Koff. 2004. AIDS/HIV. Developing an AIDS vaccine: need, uncertainty, hope. Science. 304:1913-1914.
39. Donnelly, J.J., B. Wahren, and M.A. Liu. 2005. DNA vaccines: progress and challenges. J. Immunol. 175:633-639.
40. Nussenzweig, M.C., and R.M. Steinman. 1980. Contributions of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J. Exp. Med. 151:1196-1212.
41. Xu, R., A.J. Johnson, D. Liggitt, and M.J. Bevan. 2004. Cellular and humoral immunity against vaccinia virus infection of mice. J. Immunol. 172:6265-6271.
42. Dubos, R. 1988. Pasteur and Modern Science. Science Tech Publishers, Madison, WI. 168 pp.
43. Boscardin, S.B., J.C.R. Hafalla, R.F. Masilamani, A.O. Kamphorst, H.A. Zebroski, U. Rai, A. Morrot, F. Zavala, R.M. Steinman, R.S. Nussenzweig, and M.C. Nussenzweig. 2005. Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses. J. Exp. Med. 203:599-600.
44. McConkey, S.J., W.H. Reece, V.S. Moorthy, D. Webster, S. Dunachie, G. Butcher, J.M. Vuola, T.J. Blanchard, P. Gothard, K. Watkins, et al. 2003. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med. 9:729-735.
45. Mora, J.R., G. Cheng, D. Picarella, M. Briskin, N. Buchanan, and U.H. von Andrian. 2005. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201:303-316.
46. Bachmann, M.F., P. Wolint, K. Schwarz, and A. Oxenius. 2005. Recall proliferation potential of memory CD8+ T cells and antiviral protection. J. Immunol. 175:4677-4685.
47. Fang, M., and L.J. Sigal. 2005. Antibodies and CD8+ T cells are complementary and essential for natural resistance to a highly lethal cytopathic virus. J. Immunol. 175:6829-6836.
48. + T cell tolerance. Immunity. 18:713-720.
49. + T cell tolerance through PD-1 and CTLA-4. Nat. Immunol. 6:280-286.
50. Schulz, O., S.S. Diebold, M. Chen, T.I. Naslund, M.A. Nolte, L. Alexopoulou, Y.T. Azuma, R.A. Flavell, P. Liljestrom, and C. Reis e Sousa. 2005. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature. 433:887-892.
51. Fujii, S., K. Liu, C. Smith, A.J. Bonito, and R.M. Steinman. 2004. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199:1607-1618.
52. Liu, K., J. Idoyaga, A. Charalambous, S. Fujii, A. Bonito, J. Mordoh, R. Wainstok, X.F. Bai, Y. Liu, and R.M. Steinman. 2005. Innate NKT lymphocytes confer superior adaptive immunity via tumor-capturing dendritic cells. J. Exp. Med. 202:1507-1516.
53. Moser, M., and K.M. Murphy. 2000. Dendritic cell regulation of Th1-Th2 development. Nat. Immunol. 1:199-205.
54. Heath, A.W., W.W. Wu, and M.C. Howard. 1994. Monoclonal antibodies to murine CD40 define two distinct functional epitopes. Eur. J. Immunol. 24:1828-1834.
55. Brimnes, M.K., L. Bonifaz, R.M. Steinman, and T.M. Moran. 2003. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally non-immunogenic protein. J. Exp. Med. 198:133-144.