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PMID: 9573069 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genetic control of immune response to recombinant antigens carried by an attenuated Salmonella typhimurium vaccine strain: Nramp1 influences T-helper subset responses and protection against leishmanial challenge.

Infection and immunity ·Vol. 66 ·No. 5 ·1998-05-00 ·Pages 1910-7

Soo SS, Villarreal-Ramos B, Anjam Khan CM, Hormaeche CE, Blackwell JM

Abstract

Attenuated strains of Salmonella typhimurium have been widely used as vehicles for delivery and expression of vaccine antigens in murine models of infectious disease. In mice, early bacterial replication following infection with S. typhimurium is controlled by the gene (Nramp1, formerly Ity/Lsh/Bcg) encoding the natural-resistance-associated macrophage protein (Nramp1). Nramp1 regulates macrophage activation and has multiple pleiotropic effects, including regulation of tumor necrosis factor alpha, interleukin 1beta (IL-1beta), and major histocompatibility complex class II molecules, all of which influence antigen processing and presentation. Nramp1 also has a direct effect on antigen processing, possibly by regulating the activity of proteases in the late endosomal compartment. Hence, there are multiple ways (regulation of bacterial load or recombinant antigen dose, class II molecule expression, costimulatory or adjuvant activity, and antigen processing) that Nramp1 might influence responses to recombinant salmonella vaccines. To test the hypothesis that Nramp1 influences responses to vaccination, congenic mouse strains have been used to analyze immune responses to recombinant antigens (tetanus toxoid antigen and leishmanial gp63) carried by live attenuated S. typhimurium aroA aroD mutants. Results show that congenic mice carrying the wild-type (S. typhimurium resistance) Nramp1 allele mount a predominantly T-helper-1 (IL-2 and gamma interferon) response to vaccination and show enhanced resolution of lesions following challenge infection with Leishmania major. In contrast, mice carrying mutant (S. typhimurium susceptibility) Nramp1 mount a T-helper-2 (immunoglobulin E and IL-4) response and show exacerbated lesion growth upon challenge.

MeSH Terms
Animals Antibodies, Bacterial/blood Bacterial Vaccines/immunology Carrier Proteins/genetics Cation Transport Proteins Cytokines/biosynthesis Female Leishmaniasis/prevention & control Membrane Proteins/genetics Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Inbred CBA Salmonella typhimurium/immunology Th1 Cells/immunology Th2 Cells/immunology Vaccines, Attenuated/immunology Vaccines, Synthetic/immunology
Chemicals
Antibodies, Bacterial Bacterial Vaccines Carrier Proteins Cation Transport Proteins Cytokines Membrane Proteins Vaccines, Attenuated Vaccines, Synthetic natural resistance-associated macrophage protein 1
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Soo S S
Department of Pathology, University of Cambridge, United Kingdom.
Villarreal-Ramos B
Anjam Khan C M
Hormaeche C E
Blackwell J M
References (44)
44 references, click to expand
  1. Genetics of resistance to infection with Salmonella typhimurium in mice.
    J Infect Dis. 1976 Jan;133(1):72-8 PMID: 1107437
  2. Cloning and characterization of a mammalian proton-coupled metal-ion transporter.
    Nature. 1997 Jul 31;388(6641):482-8 PMID: 9242408
  3. Immunological regulation of experimental cutaneous leishmaniasis. 1. Immunogenetic aspects of susceptibility to Leishmania tropica in mice.
    Parasite Immunol. 1980 Winter;2(4):303-14 PMID: 7220075
  4. Regulation of I-A expression by murine peritoneal macrophages: differences linked to the Bcg gene.
    J Immunol. 1987 Mar 1;138(5):1372-6 PMID: 3543128
  5. Oral Salmonella typhimurium vaccine expressing circumsporozoite protein protects against malaria.
    Science. 1988 Apr 15;240(4850):336-8 PMID: 3281260
  6. Protective immunity evoked by oral administration of attenuated aroA Salmonella typhimurium expressing cloned streptococcal M protein.
    J Exp Med. 1988 Jul 1;168(1):25-32 PMID: 3294331
  7. Analysis of Lsh gene expression in congenic B10.L-Lshr mice.
    Curr Top Microbiol Immunol. 1988;137:301-9 PMID: 3138075
  8. Acquisition of cell-mediated immunity to Leishmania. II. LSH gene regulation of accessory cell function.
    Immunology. 1988 Sep;65(1):17-22 PMID: 3141269
  9. 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
  10. 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
  11. Lsh, antigen presentation and the development of CMI.
    Res Immunol. 1989 Oct;140(8):810-5; discussion 815-22 PMID: 2696054
  12. Anti-viral immunity induced by recombinant nucleoprotein of influenza A virus. III. Delivery of recombinant nucleoprotein to the immune system using attenuated Salmonella typhimurium as a live carrier.
    Immunology. 1990 Aug;70(4):540-6 PMID: 2168340
  13. Oral Salmonella typhimurium (AroA-) vaccine expressing a major leishmanial surface protein (gp63) preferentially induces T helper 1 cells and protective immunity against leishmaniasis.
    J Immunol. 1990 Oct 1;145(7):2281-5 PMID: 2144549
  14. Molecular genetics of inherited susceptibility to intracellular parasites.
    Behring Inst Mitt. 1991 Feb;(88):1-12 PMID: 1675564
  15. Immunization of mice with an attenuated Salmonella typhimurium strain expressing a membrane protein of Francisella tularensis. A model for identification of bacterial determinants relevant to the host defence against tularemia.
    Res Microbiol. 1990 Sep-Oct;141(7-8):887-91 PMID: 2101478
  16. Live attenuated Salmonella vaccines and their potential as oral combined vaccines carrying heterologous antigens.
    J Immunol Methods. 1991 Aug 28;142(1):113-20 PMID: 1919015
  17. Role of inorganic nitrogen oxides and tumor necrosis factor alpha in killing Leishmania donovani amastigotes in gamma interferon-lipopolysaccharide-activated macrophages from Lshs and Lshr congenic mouse strains.
    Infect Immun. 1991 Nov;59(11):3935-44 PMID: 1937752
  18. Construction of genetically defined double aro mutants of Salmonella typhi.
    Vaccine. 1991 Nov;9(11):810-6 PMID: 1759503
  19. Clinical acceptability and immunogenicity of CVD 908 Salmonella typhi vaccine strain.
    Vaccine. 1992;10(7):443-6 PMID: 1609547
  20. Establishment of stable, cell-mediated immunity that makes "susceptible" mice resistant to Leishmania major.
    Science. 1992 Jul 24;257(5069):539-42 PMID: 1636090
  21. Two related genes encoding extremely hydrophobic proteins suppress a lethal mutation in the yeast mitochondrial processing enhancing protein.
    J Biol Chem. 1992 Dec 5;267(34):24625-33 PMID: 1447206
  22. Use of the nirB promoter to direct the stable expression of heterologous antigens in Salmonella oral vaccine strains: development of a single-dose oral tetanus vaccine.
    Biotechnology (N Y). 1992 Aug;10(8):888-92 PMID: 1368983
  23. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg.
    Cell. 1993 May 7;73(3):469-85 PMID: 8490962
  24. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes.
    J Exp Med. 1994 Feb 1;179(2):601-8 PMID: 8294870
  25. NH2-terminal sequence of macrophage-expressed natural resistance-associated macrophage protein (Nramp) encodes a proline/serine-rich putative Src homology 3-binding domain.
    J Exp Med. 1994 May 1;179(5):1683-7 PMID: 7513015
  26. Linkage analysis of IL4 and other chromosome 5q31.1 markers and total serum immunoglobulin E concentrations.
    Science. 1994 May 20;264(5162):1152-6 PMID: 8178175
  27. T-helper 1-like subset selection in Mycobacterium bovis bacillus Calmette-Guérin-infected resistant and susceptible mice.
    Immunology. 1994 Apr;81(4):618-25 PMID: 8039813
  28. Interaction with extracellular matrix proteins influences Lsh/Ity/Bcg (candidate Nramp) gene regulation of macrophage priming/activation for tumour necrosis factor-alpha and nitrite release.
    Immunology. 1994 May;82(1):42-50 PMID: 8045593
  29. Genetic control of antibody responses induced against an antigen delivered by recombinant attenuated Salmonella typhimurium.
    Infect Immun. 1994 Oct;62(10):4310-9 PMID: 7927689
  30. Construction, expression, and immunogenicity of the Schistosoma mansoni P28 glutathione S-transferase as a genetic fusion to tetanus toxin fragment C in a live Aro attenuated vaccine strain of Salmonella.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11261-5 PMID: 7972044
  31. Leishmania donovani-infected macrophages: characterization of the parasitophorous vacuole and potential role of this organelle in antigen presentation.
    J Cell Sci. 1994 Aug;107 ( Pt 8):2137-50 PMID: 7983173
  32. Construction, expression, and immunogenicity of multiple tandem copies of the Schistosoma mansoni peptide 115-131 of the P28 glutathione S-transferase expressed as C-terminal fusions to tetanus toxin fragment C in a live aro-attenuated vaccine strain of Salmonella.
    J Immunol. 1994 Dec 15;153(12):5634-42 PMID: 7527446
  33. The Bcg gene story.
    Immunobiology. 1994 Oct;191(4-5):451-60 PMID: 7713559
  34. Genetic regulation of leishmanial and mycobacterial infections: the Lsh/Ity/Bcg gene story continues.
    Immunol Lett. 1994 Dec;43(1-2):99-107 PMID: 7737696
  35. Protection against Leishmania major infection in genetically susceptible BALB/c mice by gp63 delivered orally in attenuated Salmonella typhimurium (AroA- AroD-).
    Immunology. 1995 May;85(1):1-7 PMID: 7635511
  36. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene.
    J Exp Med. 1995 Sep 1;182(3):655-66 PMID: 7650477
  37. Gamma interferon and interleukin-10 gene expression in innately susceptible and resistant mice during the early phase of Salmonella typhimurium infection.
    Infect Immun. 1996 Mar;64(3):849-54 PMID: 8641791
  38. Allelic association of gene markers on chromosomes 5q and 11q with atopy and bronchial hyperresponsiveness.
    Am J Respir Crit Care Med. 1996 Apr;153(4 Pt 1):1280-4 PMID: 8616554
  39. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):5105-10 PMID: 8643535
  40. Structure and function of the natural-resistance-associated macrophage protein (Nramp1), a candidate protein for infectious and autoimmune disease susceptibility.
    Mol Med Today. 1996 May;2(5):205-11 PMID: 8796889
  41. Resistance to intracellular infections: comparative genomic analysis of Nramp.
    Trends Genet. 1996 Jun;12(6):201-4 PMID: 8928221
  42. Nramp1 transfection transfers Ity/Lsh/Bcg-related pleiotropic effects on macrophage activation: influence on antigen processing and presentation.
    Infect Immun. 1997 Feb;65(2):380-6 PMID: 9009286
  43. Nramp1 locus encodes a 65 kDa interferon-gamma-inducible protein in murine macrophages.
    Biochem J. 1997 Aug 1;325 ( Pt 3):779-86 PMID: 9271100
  44. Natural resistance to Salmonella typhimurium in different inbred mouse strains.
    Immunology. 1979 Jun;37(2):311-8 PMID: 381178
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1998-05-00
Pages
1910-7
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC108143
Subset
IM
Grants
Wellcome Trust · United Kingdom
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