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PMID: 9314562 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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

The Journal of experimental medicine ·Vol. 186 ·No. 7 ·1997-10-06 ·Pages 1137-47

Gurunathan S, Sacks DL, Brown DR, Reiner SL, Charest H, Glaichenhaus N, Seder RA

Abstract

To determine whether DNA immunization could elicit protective immunity to Leishmania major in susceptible BALB/c mice, cDNA for the cloned Leishmania antigen LACK was inserted into a euykaryotic expression vector downstream to the cytomegalovirus promoter. Susceptible BALB/c mice were then vaccinated subcutaneously with LACK DNA and challenged with L. major promastigotes. We compared the protective efficacy of LACK DNA vaccination with that of recombinant LACK protein in the presence or absence of recombinant interleukin (rIL)-12 protein. Protection induced by LACK DNA was similar to that achieved by LACK protein and rIL-12, but superior to LACK protein without rIL-12. The immunity conferred by LACK DNA was durable insofar as mice challenged 5 wk after vaccination were still protected, and the infection was controlled for at least 20 wk after challenge. In addition, the ability of mice to control infection at sites distant to the site of vaccination suggests that systemic protection was achieved by LACK DNA vaccination. The control of disease progression and parasitic burden in mice vaccinated with LACK DNA was associated with enhancement of antigen-specific interferon-gamma (IFN-gamma) production. Moreover, both the enhancement of IFN-gamma production and the protective immune response induced by LACK DNA vaccination was IL-12 dependent. Unexpectedly, depletion of CD8(+) T cells at the time of vaccination or infection also abolished the protective response induced by LACK DNA vaccination, suggesting a role for CD8(+) T cells in DNA vaccine induced protection to L. major. Thus, DNA immunization may offer an attractive alternative vaccination strategy against intracellular pathogens, as compared with conventional vaccination with antigens combined with adjuvants.

MeSH Terms
Animals Antibodies, Protozoan/biosynthesis Antigens, Protozoan/genetics,immunology CD8-Positive T-Lymphocytes/immunology Female Genes, Protozoan Immunodominant Epitopes/genetics,immunology Interferon-gamma/biosynthesis Interleukin-12/genetics,immunology Interleukin-4/biosynthesis Leishmania major/immunology Leishmaniasis, Cutaneous/immunology,prevention & control Mice Mice, Inbred BALB C Protozoan Proteins/genetics,immunology Protozoan Vaccines/immunology Recombinant Proteins/immunology Vaccination Vaccines, DNA/immunology Vaccines, Synthetic/immunology
Chemicals
Antibodies, Protozoan Antigens, Protozoan Immunodominant Epitopes Protozoan Proteins Protozoan Vaccines Recombinant Proteins Vaccines, DNA Vaccines, Synthetic LACK antigen, Leishmania Interleukin-12 Interleukin-4 Interferon-gamma
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Gurunathan S
Lymphokine Regulation Unit, Laboratory of Clinical Investigation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
Sacks D L
Brown D R
Reiner S L
Charest H
Glaichenhaus N
Seder R A
References (54)
54 references, click to expand
  1. Patterns of cytokine secretion in murine leishmaniasis: correlation with disease progression or resolution.
    Infect Immun. 1990 Dec;58(12):3863-70 PMID: 2123823
  2. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon gamma-independent mechanism.
    J Exp Med. 1990 Jan 1;171(1):115-27 PMID: 2104918
  3. Establishment of resistance to Leishmania major infection in susceptible BALB/c mice requires parasite-specific CD8+ T cells.
    Int Immunol. 1991 Jun;3(6):587-97 PMID: 1909563
  4. Changes in the precursor frequencies of IL-4 and IFN-gamma secreting CD4+ cells correlate with resolution of lesions in murine cutaneous leishmaniasis.
    J Immunol. 1992 Oct 15;149(8):2715-21 PMID: 1357029
  5. TH1 and TH2 cell antigen receptors in experimental leishmaniasis.
    Science. 1993 Mar 5;259(5100):1457-60 PMID: 8451641
  6. Heterologous protection against influenza by injection of DNA encoding a viral protein.
    Science. 1993 Mar 19;259(5102):1745-9 PMID: 8456302
  7. Recombinant interleukin 12 cures mice infected with Leishmania major.
    J Exp Med. 1993 May 1;177(5):1505-9 PMID: 8097524
  8. Gene inoculation generates immune responses against human immunodeficiency virus type 1.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4156-60 PMID: 8483929
  9. Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle.
    Hum Mol Genet. 1992 Sep;1(6):363-9 PMID: 1301910
  10. Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response.
    J Exp Med. 1993 Jun 1;177(6):1797-802 PMID: 8098733
  11. Interleukin-4 but not gamma interferon production correlates with the severity of murine cutaneous leishmaniasis.
    Infect Immun. 1993 Aug;61(8):3459-65 PMID: 8335376
  12. Gamma interferon response in secondary Leishmania major infection: role of CD8+ T cells.
    Infect Immun. 1993 Sep;61(9):3730-8 PMID: 8359894
  13. Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice.
    Science. 1993 Sep 10;261(5127):1448-51 PMID: 8367726
  14. Interleukin 12 acts directly on CD4+ T cells to enhance priming for interferon gamma production and diminishes interleukin 4 inhibition of such priming.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10188-92 PMID: 7901851
  15. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major.
    Science. 1994 Jan 14;263(5144):235-7 PMID: 7904381
  16. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection.
    J Exp Med. 1994 Feb 1;179(2):447-56 PMID: 7905017
  17. Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus.
    Virology. 1994 Feb 15;199(1):132-40 PMID: 8116236
  18. Leishmania major-specific CD8+ T cells are inducers and targets of nitric oxide produced by parasitized macrophages.
    Eur J Immunol. 1994 Mar;24(3):746-52 PMID: 7510243
  19. Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein.
    Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9866-70 PMID: 7937907
  20. Leishmania major infection in mice primes for specific major histocompatibility complex class I-restricted CD8+ cytotoxic T cell responses.
    Eur J Immunol. 1994 Nov;24(11):2813-7 PMID: 7957573
  21. DNA immunization confers protection against lethal lymphocytic choriomeningitis virus infection.
    J Virol. 1995 Apr;69(4):2684-8 PMID: 7884923
  22. CpG motifs in bacterial DNA trigger direct B-cell activation.
    Nature. 1995 Apr 6;374(6522):546-9 PMID: 7700380
  23. Expression cloning of a protective Leishmania antigen.
    Science. 1995 Apr 28;268(5210):563-6 PMID: 7725103
  24. Protection against leishmaniasis by injection of DNA encoding a major surface glycoprotein, gp63, of L. major.
    Immunology. 1995 Feb;84(2):173-6 PMID: 7750991
  25. 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 U S A. 1995 Jun 6;92(12):5307-11 PMID: 7777503
  26. Immune responses to plasmid DNA encoding the hepatitis C virus core protein.
    J Virol. 1995 Sep;69(9):5859-63 PMID: 7637033
  27. Induction of antibodies against Salmonella typhi OmpC porin by naked DNA immunization.
    Ann N Y Acad Sci. 1995 Nov 27;772:285-8 PMID: 8546410
  28. Bacterial DNA induces murine interferon-gamma production by stimulation of interleukin-12 and tumor necrosis factor-alpha.
    Cell Immunol. 1996 Jan 10;167(1):72-8 PMID: 8548847
  29. IL-12, as an adjuvant, promotes a T helper 1 cell, but does not suppress a T helper 2 cell recall response.
    J Immunol. 1996 Feb 1;156(3):887-94 PMID: 8558014
  30. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2879-83 PMID: 8610135
  31. Preferential induction of a Th1 immune response and inhibition of specific IgE antibody formation by plasmid DNA immunization.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):5141-5 PMID: 8643542
  32. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization.
    Science. 1996 Jul 19;273(5273):352-4 PMID: 8662521
  33. Vaccination against tuberculosis by DNA injection.
    Nat Med. 1996 Aug;2(8):888-92 PMID: 8705858
  34. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine.
    Nat Med. 1996 Aug;2(8):893-8 PMID: 8705859
  35. 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. 1996 Sep;70(9):6119-25 PMID: 8709236
  36. Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone marrow-derived cells.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8578-83 PMID: 8710913
  37. Comparison of numerous delivery systems for the induction of cytotoxic T lymphocytes by immunization.
    Eur J Immunol. 1996 Aug;26(8):1951-9 PMID: 8765044
  38. Macrophages ingest and are activated by bacterial DNA.
    J Immunol. 1996 Sep 1;157(5):2116-22 PMID: 8757335
  39. Resistance to Leishmania major induced by tolerance to a single antigen.
    Science. 1996 Oct 18;274(5286):421-3 PMID: 8832890
  40. Gene vaccination with naked plasmid DNA: mechanism of CTL priming.
    J Exp Med. 1996 Oct 1;184(4):1555-60 PMID: 8879229
  41. DNA immunization confers protection against murine cytomegalovirus infection.
    J Virol. 1996 Nov;70(11):7921-8 PMID: 8892915
  42. Hexamer palindromic oligonucleotides with 5'-CG-3' motif(s) induce production of interferon.
    J Interferon Cytokine Res. 1996 Oct;16(10):799-803 PMID: 8910764
  43. Leishmania major: effect of infectious dose on T cell subset development in BALB/c mice.
    Exp Parasitol. 1996 Nov;84(2):124-35 PMID: 8932762
  44. Early IL-4 production does not predict susceptibility to Leishmania major.
    Exp Parasitol. 1996 Nov;84(2):178-87 PMID: 8932767
  45. Leishmania major: targeting IL-4 in successful immunomodulation of murine infection.
    Exp Parasitol. 1996 Nov;84(2):214-22 PMID: 8932771
  46. An OspA-based DNA vaccine protects mice against infection with Borrelia burgdorferi.
    J Infect Dis. 1997 Jan;175(1):91-7 PMID: 8985201
  47. Different T helper cell types and antibody isotypes generated by saline and gene gun DNA immunization.
    J Immunol. 1997 Mar 1;158(5):2278-84 PMID: 9036975
  48. Characterization of humoral immune responses induced by an influenza hemagglutinin DNA vaccine.
    Vaccine. 1997 Jan;15(1):71-8 PMID: 9041669
  49. Early production of IL-4 in susceptible mice infected with Leishmania major rapidly induces IL-12 unresponsiveness.
    J Immunol. 1997 Apr 1;158(7):3317-24 PMID: 9120289
  50. IL-4 rapidly produced by V beta 4 V alpha 8 CD4+ T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice.
    Immunity. 1997 May;6(5):541-9 PMID: 9175832
  51. 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. 1988 Nov 1;168(5):1675-84 PMID: 2903212
  52. 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. 1989 Jan 1;169(1):59-72 PMID: 2521244
  53. Elimination of CD4+ suppressor T cells from susceptible BALB/c mice releases CD8+ T lymphocytes to mediate protective immunity against Leishmania.
    J Exp Med. 1989 May 1;169(5):1819-27 PMID: 2523955
  54. 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 U S A. 1991 Aug 15;88(16):7011-5 PMID: 1908085
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1997-10-06
Pages
1137-47
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2199076
Subset
IM
Grants
NIAID NIH HHS · AI-01309 · United States
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