Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with Leishmania major

Journal of Experimental Medicine

Volumn 186, Issue 7, 1997, Pages 1137-1147

  Gurunathan, Sanjay ^a   Sacks, David L ^a   Brown, Daniel R ^b   Reiner, Steven L ^b   Charest, Hughes ^a   Glaichenhaus, Nicolas ^c   Seder, Robert A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; PARASITE ANTIGEN; RECOMBINANT INTERLEUKIN 12; RECOMBINANT PROTEIN;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; IMMUNIZATION; INFECTION CONTROL; LEISHMANIA MAJOR; LEISHMANIASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTOZOAL INFECTION; VACCINATION;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GENES, PROTOZOAN; IMMUNODOMINANT EPITOPES; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-4; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; PROTOZOAN PROTEINS; PROTOZOAN VACCINES; RECOMBINANT PROTEINS; VACCINATION; VACCINES, DNA; VACCINES, SYNTHETIC;

EID: 0030822043     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.7.1137     Document Type: Article

References (54)

1. Ulmer, J.B., J.J. Donnelly, S.E. Parker, G.H. Rhodes, P.L. Felgner, V.J. Dwarki, S.H. Gromkowski, R.R. Deck, C.M. De Witt, A. Friedman et al. 1993. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science (Wash. DC). 259:1745-1749.
2. Wang, B., K.E. Ugen, V. Srikantan, M.G. Agadjanyan, K. Dang, Y. Refaeli, A.I. Sato, J. Boyer, W.V. Williams, and D.B. Weiner. 1993. Gene inoculation generates immune responses against human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA. 90:4156-4160.
3. Xiang, Z.Q., S. Spitalnik, M. Tran, W.H. Wunner, J. Cheng, and H.C. Ertl. 1994. Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus. Virology. 199:132-140.
4. Michel, M.L., H.L. Davis, M. Schleef, M. Mancini, P. Tiollais, and R.G. Whalen. 1995. DNA-mediated immunization to the hepatitis B surface antigen in mice: aspects of the humoral response mimic hepatitis B viral infection in humans. Proc. Natl. Acad. Sci. USA. 92:5307-5311.
5. Lagging, L.M., K. Meyer, D. Hoft, M. Houghton, R.B. Belshe, and R. Ray. 1995. Immune responses to plasmid DNA encoding the hepatitis C virus core protein. J. Virol. 69:5859-5863.
6. Luke, CJ., K. Carner, X. Liang, and A.G. Barbour. 1997. An OspA-based DNA vaccine protects mice against infection with Borrelia burgdorferi. J. Infect. Dis. 175:91-97.
7. Sedegah, M., R. Hedstrom, P. Hobart, and S.L. Hoffman. 1994. Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. Proc. Natl. Acad. Sci. USA. 91:9866-9870.
8. Tascon, R.E., M.J. Colston, S. Ragno, E. Stavropoulos, D. Gregory, and D.B. Lowrie. 1996. Vaccination against tuberculosis by DNA injection. Nat. Med. 2:888-892.
9. Huygen, K., J. Content, O. Denis, D.L. Montgomery, A.M. Yawman, R.R. Deck, C.M. De Witt, I.M. Orme, S. Baldwin, C. D'Souza et al. 1996. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine. Nat. Med. 2:893-898.
10. Lopez-Macias, C., M.A. Lopez-Hernandez, C.R. Gonzalez, A. Isibasi, and V. Ortiz-Navarrete. 1995. Induction of antibodies against Salmonella typhi OmpC porin by naked DNA immunization. Ann. NY Acad. Sci. 772:285-288.
11. Gonzalez Armas, J.C., C.S. Morello, L.D. Cranmer, and D.H. Spector. 1996. DNA immunization confers protection against murine cytomegalovirus infection. J. Virol. 70:7921-7928.
12. Yokoyama, M., J. Zhang, and J.L. Whitton. 1995. DNA immunization confers protection against lethal lymphocytic choriomeningitis virus infection. J. Virol. 69:2684-2688.
13. Allsopp, C.E., M. Plebanski, S. Gilbert, R.E. Sinden, S. Harris, G. Frankel, G. Dougan, C. Hioe, D. Nixon, E. Paoletti, G. Layton, and A.V. Hill. 1996. Comparison of numerous delivery systems for the induction of cytotoxic T lymphocytes by immunization. Eur. J. Immunol. 26:1951-1959.
14. Corr, M., D.J. Lee, D.A. Carson, and H. Tighe. 1996. Gene vaccination with naked plasmid DNA: mechanism of CTL priming. J. Exp. Med. 184:1555-1560.
15. Doe, B., M. Selby, S. Barnett, J. Baenzinger, and C.M. Walker. 1996. Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone marrow-derived cells. Proc. Natl. Acad. Sci. USA. 93: 8578-8583.
16. Raz, E., H. Tighe, Y. Sato, M. Corr, J.A. Dudler, M. Roman, S.L. Swain, H.L. Spiegelberg, and D.A. Carson. 1996. Preferential induction of a Th1 immune response and inhibition of specific IgE antibody formation by plasmid DNA immunization. Proc. Natl. Acad. Sci. USA. 93:5141-5145.
17. Sato, Y., M. Roman, H. Tighe, D. Lee, M. Corr, M.D. Nguyen, G.J. Silverman, M. Lotz, D.A. Carson, and E. Raz. 1996. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science (Wash. DC). 273:352-354.
18. Pertmer, T.M., T.R. Roberts, andJ.R. Haynes. 1996. Influenza virus nucleoprotein-specific immunoglobulin G subclass and cytokine responses elicited by DNA vaccination are dependent on the route of vector DNA delivery. J .Virol. 70: 6119-6125.
19. Feltquate, D.M., S. Heaney, R.G. Webster, and H.L. Robinson. 1997. Different T helper cell types and antibody isotypes generated by saline and gene gun DNA immunization. J. Immunol. 158:2278-2284.
20. Scott, P., P. Natovitz, R.L. Coffman, E. Pearce, and A. Sher. 1988. Immunoregulation of cutaneous leishmaniasis. T cell lines that transfer protective immunity or exacerbation belong to different T helper subsets and respond to distinct parasite antigens. J. Exp. Med. 168:1675-1684.
21. Heinzel, F.P., M.D. Sadick, B.J. Holaday, R.L. Coffman, and R.M. Locksley. 1989. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J. Exp. Med. 169:59-72.
22. Heinzel, F.P., M.D. Sadick, S.S. Mutha, and R.M. Locksley. 1991. Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc. Natl. Acad. Sci. USA. 88:7011-7015.
23. Boom, W.H., L. Liebster, A.K. Abbas, and R.G. Titus. 1990. Patterns of cytokine secretion in murine leishmaniasis: correlation with disease progression or resolution. Infect. Immunol. 58:3863-3870.
24. Heinzel, F.P., D.S. Schoenhaut, R.M. Rerko, L.E. Rosser, and M.K. Gately. 1993. Recombinant interleukin 12 cures mice infected with Leishmania major. J. Exp. Med. 177: 1505-1509.
25. Sypek, J.P., C.L. Chung, S.E. Mayor, J.M. Subramanyam, S.J. Goldman, D.S. Sieburth, S.F. Wolf, and R.G. Schaub. 1993. Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response. J. Exp. Med. 177:1797-1802.
26. Sadick, M.D., F.P. Heinzel, B.J. Holaday, R.T. Pu, R.S. Dawkins, and R.M. Locksley. 1990. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon γ-independent mechanism. J. Exp. Med. 171:115-127.
27. Wakil, A.E., Z.E. Wang, and R.M. Locksley. 1996. Leishmania major: targeting IL-4 in successful immunomodulation of murine infection. Exp. Parasitol. 84:214-222.
28. Afonso, L.C., T.M. Scharton, L.Q. Vieira, M. Wysocka, G. Trinchieri, and P. Scott. 1994. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science (Wash. DC). 263:235-237.
29. Mougneau, E., F. Altare, A.E. Wakil, S. Zheng, T. Coppola, Z.E. Wang, R. Waldmann, R.M. Locksley, and N. Glaichenhaus. 1995. Expression cloning of a protective Leishmania antigen. Science (Wash. DC). 268:563-566.
30. Julia, V., M. Rassoulzadegan, and N. Glaichenhaus. 1996. Resistance to Leishmania major induced by tolerance to a single antigen. Science (Wash. DC). 274:421-423.
31. +T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity. 6:541-549.
32. Seder, R.A., R. Gazzinelli, A. Sher, and W.E. Paul. 1993. Interleukin 12 acts directly on CD4+ T cells to enhance priming for interferon γ production and diminishes interleukin 4 inhibition of such priming. Proc. Natl. Acad. Sci. USA. 90:10188-10192.
33. + T cells during initiation of infection. J. Exp. Med. 179:447-456.
34. Scott, P., A. Eaton, W.C. Gause, X. di Zhou, and B. Hondowicz. 1996. Early IL-4 production does not predict susceptibility to Leishmania major. Exp. Parasitol. 84:178-187.
35. Launois, P., K.G. Swihart, G. Milon, and J.A. Louis. 1997. Early production of IL-4 in susceptible mice infected with Leishmania major rapidly induces IL-12 unresponsiveness. J. Immunol. 158:3317-3324.
36. + T lymphocytes to mediate protective immunity against Leishmania. J. Exp. Med. 169:1819-1827.
37. Muller, I., T. Pedrazzini, P. Kropf, J. Louis, and G. Milon. 1991. Establishment of resistance to Leishmania major infection in susceptible BALB/c mice requires parasite-specific CD8+ T cells. Int. Immunol. 3:587-597.
38. Muller, I., P. Kropf, R.J. Etges and J.A. Louis. 1993. Gamma interferon response in secondary Leishmania major infection: role of CD8+ T cells. Infect. Immunol. 61:3730-3738.
39. da Conceicao-Silva, F., B.L. Perlaza, J.A. Louis, and P. Romero. 1994. Leishmania major infection in mice primes for specific major histocompatibility complex class I-restricted CD8+ cytotoxic T cell responses. Eur. J. Immunol. 24:2813-2817.
40. Stefani, M.M., I. Muller, and J.A. Louis. 1994. Leishmania major-specific CD8+ T cells are inducers and targets of nitric oxide produced by parasitized macrophages. Eur. J. Immunol. 24:746-752.
41. Xu, D., and F.Y. Liew. 1995. Protection against leishmaniasis by injection of DNA encoding a major surface glycoprotein, gp63, of L. major. Immunology. 84:173-176.
42. Wolff, J.A., J.J. Ludtke, G. Acsadi, P. Williams, and A. Jani. 1992. Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Human Mol. Genet. 1:363-369.
43. Deck, R.R., C.M. DeWitt, J.J. Donnelly, M.A. Liu, and J.B. Ulmer. 1997. Characterization of humoral immune responses induced by an influenza hemagglutin DNA vaccine. Vaccine. 15:71-78.
44. Krieg, A.M., A.K. Yi, S. Matson, T.J. Waldschmidt, G.A. Bishop, R. Teasdale, G.A. Koretzky, and D.M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature (Lond.). 374:546-549.
45. Klinman, D.M., A.K. Yi, S.L. Beaucage, J. Conover, and A.M. Krieg. 1996. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc. Natl. Acad. Sci. USA. 93: 2879-2883.
46. Halpern, M.D., R.J. Kurlander, and D.S. Pisetsky. 1996. Bacterial DNA induces murine interferon-gamma production by stimulation of interleukin-12 and tumor necrosis factor-α. Cell. Immunol. 167:72-78.
47. Sonehara, K., H. Saito, E. Kuramoto, S. Yamamoto, T. Yamamoto, and T. Tokunaga. 1996. Hexamer palindromic oligonucleotides with 5′-CG-3′ motif(s) induce production of interferon. J. Interferon Cytokine Res. 16:799-803.
48. Stacey, K.J., M.J. Sweet, and D.A. Hume. 1996. Macrophages ingest and are activated by bacterial DNA. J. Immunol. 157: 2116-2122.
49. Bliss, J., V. Van Cleave, K. Murray, A. Wiencis, M. Ketchum, R. Maylor, T. Haire, C. Resmini, A.K. Abbas, and S.F. Wolf. 1996. IL-12, as an adjuvant, promotes a T helper 1 cell, but does not suppress a T helper 2 cell recall response. J. Immunol. 156:887-894.
50. Morris, L., A.B. Troutt, E. Handman, and A. Kelso. 1992. Changes in the precursor frequencies of IL-4 and IFN-γ secreting CD4+ cells correlate with resolution of lesions in murine cutaneous leishmaniasis. J. Immunol. 149:2715-2721.
51. Morris, L., A.B. Troutt, K.S. McLeod, A. Kelso, E. Handman, and T. Aebischer. 1993. Interleukin-4 but not γ interferon production correlates with the severity of murine cutaneous leishmaniasis. Infect. Immunol. 61:3459-3465.
52. Doherty, T.M., and R.L. Coffman. 1996. Leishmania major. effect of infectious dose on T cell subset development in BALB/c mice. Exp. Parasitol. 84:124-135.
53. Reiner, S.L., Z.E. Wang, F. Hatam, P. Scott, and R.M. Locksley. 1993. TH1 and TH2 cell antigen receptors in experimental leishmaniasis. Science (Wash. DC). 259:1457-1460.
54. Locksley, R.M., S.L. Reiner, F. Hatam, D.R. Littman, and N. Killeen. 1993. Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice. Science (Wash. DC). 261:1448-1451.