Home LiteratureArticle Details
PMID: 10225878 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Functional expression of Nramp1 in vitro in the murine macrophage line RAW264.7.

Infection and immunity ·Vol. 67 ·No. 5 ·1999-05-00 ·Pages 2225-32

Govoni G, Canonne-Hergaux F, Pfeifer CG, Marcus SL, Mills SD, Hackam DJ, Grinstein S, Malo D, Finlay BB, Gros P

Abstract

Mutations at the Nramp1 locus in vivo cause susceptibility to infection by unrelated intracellular microbes. Nramp1 encodes an integral membrane protein abundantly expressed in the endosomal-lysosomal compartment of macrophages and is recruited to the phagosomal membrane following phagocytosis. The mechanism by which Nramp1 affects the biochemical properties of the phagosome to control microbial replication is unknown. To devise an in vitro assay for Nramp1 function, we introduced a wild-type Nramp1(G169) cDNA into RAW 264.7 macrophages (which bear a homozygous mutant Nramp1(D169) allele and thus are permissive to replication of specific intracellular parasites). Recombinant Nramp1 was expressed in a membranous compartment in RAW264.7 cells and was recruited to the membrane of Salmonella typhimurium and Yersinia enterocolitica containing phagosomes. Evaluation of the antibacterial activity of RAW264.7 transfectants showed that expression of the recombinant Nramp1 protein abrogated intracellular replication of S. typhimurium. Studies with a replication-defective S. typhimurium mutant suggest that this occurs through an enhanced bacteriostatic activity. The effect of Nramp1 expression was specific, since (i) it was not seen in RAW264.7 transfectants overexpressing the closely related Nramp2 protein, and (ii) control RAW264.7 cells, Nramp1, and Nramp2 transfectants could all efficiently kill a temperature-sensitive, replication-defective mutant of S. typhimurium. Finally, increased antibacterial activity of the Nramp1 RAW264.7 transfectants was linked to increased phagosomal acidification, a distinguishing feature of primary macrophages expressing a wild-type Nramp1 allele. Together, these results indicate that transfection of Nramp1 cDNAs in the RAW264.7 macrophage cell line can be used as a direct assay to study both Nramp1 function and mechanism of action as well as to identify structure-function relationships in this protein.

MeSH Terms
Alleles Animals Carrier Proteins/genetics,immunology,metabolism Cation Transport Proteins Cell Line DNA, Complementary/genetics Gene Expression Genes, myc Hydrogen-Ion Concentration Macrophages/immunology,metabolism,microbiology Membrane Proteins/genetics,immunology,metabolism Mice Mutation Mycobacterium bovis/immunology,pathogenicity Phagosomes/immunology,metabolism,microbiology Recombinant Fusion Proteins/genetics,immunology,metabolism Salmonella typhimurium/genetics,immunology,pathogenicity Transfection Yersinia enterocolitica/genetics,immunology,pathogenicity
Chemicals
Carrier Proteins Cation Transport Proteins DNA, Complementary Membrane Proteins Recombinant Fusion Proteins natural resistance-associated macrophage protein 1
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Govoni G
Department of Biochemistry, McGill University, Montreal, Quebec.
Canonne-Hergaux F
Pfeifer C G
Marcus S L
Mills S D
Hackam D J
Grinstein S
Malo D
Finlay B B
Gros P
References (39)
39 references, click to expand
  1. Structural conservation of ion conduction pathways in K channels and glutamate receptors.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):4882-6 PMID: 7761417
  2. Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites.
    Genomics. 1994 Sep 1;23(1):51-61 PMID: 7829102
  3. 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
  4. Nramp defines a family of membrane proteins.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10089-93 PMID: 7479731
  5. 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
  6. Functional macrophage cell lines transformed by Abelson leukemia virus.
    Cell. 1978 Sep;15(1):261-7 PMID: 212198
  7. Differences in response among inbred mouse strains to infection with small doses of Mycobacterium bovis BCG.
    Infect Immun. 1981 Apr;32(1):42-7 PMID: 7012036
  8. Genetic control of natural resistance to Mycobacterium bovis (BCG) in mice.
    J Immunol. 1981 Dec;127(6):2417-21 PMID: 6795274
  9. Cellular mechanisms of genetically controlled host resistance to Mycobacterium bovis (BCG).
    J Immunol. 1983 Oct;131(4):1966-72 PMID: 6311901
  10. The Bcg/Ity/Lsh locus: genetic transfer of resistance to infections in C57BL/6J mice transgenic for the Nramp1 Gly169 allele.
    Infect Immun. 1996 Aug;64(8):2923-9 PMID: 8757814
  11. Resistance to intracellular infections: comparative genomic analysis of Nramp.
    Trends Genet. 1996 Jun;12(6):201-4 PMID: 8928221
  12. Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains.
    J Immunol. 1996 Oct 15;157(8):3559-68 PMID: 8871656
  13. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome.
    J Exp Med. 1997 Feb 17;185(4):717-30 PMID: 9034150
  14. Cloning and characterization of a mammalian proton-coupled metal-ion transporter.
    Nature. 1997 Jul 31;388(6641):482-8 PMID: 9242408
  15. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene.
    Nat Genet. 1997 Aug;16(4):383-6 PMID: 9241278
  16. Cell-specific and inducible Nramp1 gene expression in mouse macrophages in vitro and in vivo.
    J Leukoc Biol. 1997 Aug;62(2):277-86 PMID: 9261342
  17. Functional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family.
    J Biol Chem. 1997 Nov 14;272(46):28933-8 PMID: 9360964
  18. Susceptibility to leprosy is linked to the human NRAMP1 gene.
    J Infect Dis. 1998 Jan;177(1):133-45 PMID: 9419180
  19. Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans.
    N Engl J Med. 1998 Mar 5;338(10):640-4 PMID: 9486992
  20. Trafficking of porin-deficient Salmonella typhimurium mutants inside HeLa cells: ompR and envZ mutants are defective for the formation of Salmonella-induced filaments.
    Infect Immun. 1998 Apr;66(4):1806-11 PMID: 9529120
  21. Evidence that genetic susceptibility to Mycobacterium tuberculosis in a Brazilian population is under oligogenic control: linkage study of the candidate genes NRAMP1 and TNFA.
    Tuber Lung Dis. 1997;78(1):35-45 PMID: 9666961
  22. Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification.
    J Exp Med. 1998 Jul 20;188(2):351-64 PMID: 9670047
  23. Genetic control of the innate resistance of mice to Salmonella typhimurium: expression of the Ity gene in peritoneal and splenic macrophages isolated in vitro.
    J Immunol. 1983 Dec;131(6):3006-13 PMID: 6358358
  24. Genetic control of the innate resistance of mice to Salmonella typhimurium: Ity gene is expressed in vivo by 24 hours after infection.
    J Immunol. 1983 Dec;131(6):3014-20 PMID: 6315821
  25. Phenotypic expression of genetically-controlled natural resistance to Mycobacterium bovis (BCG).
    J Immunol. 1984 Feb;132(2):888-92 PMID: 6361135
  26. Expression of the natural resistance gene Lsh in resident liver macrophages.
    Infect Immun. 1984 Mar;43(3):1033-40 PMID: 6698599
  27. Sequence of gene malG in E. coli K12: homologies between integral membrane components from binding protein-dependent transport systems.
    EMBO J. 1985 Sep;4(9):2287-93 PMID: 3000770
  28. Role of mononuclear phagocytes in expression of resistance and susceptibility to Mycobacterium avium infections in mice.
    Infect Immun. 1986 Dec;54(3):811-9 PMID: 3023238
  29. Regulation of host resistance to Mycobacterium intracellulare in vivo and in vitro by the Bcg gene.
    Immunogenetics. 1989;30(3):218-21 PMID: 2673999
  30. Killing of Mycobacterium smegmatis by macrophages from genetically susceptible and resistant mice.
    J Leukoc Biol. 1990 Jan;47(1):25-30 PMID: 2294152
  31. Functional expression of the Bcg gene in macrophages.
    Res Immunol. 1989 Oct;140(8):793-7 PMID: 2696052
  32. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities.
    Mol Cell Biol. 1990 Apr;10(4):1652-63 PMID: 1969610
  33. Genetic regulation of macrophage priming/activation: the Lsh gene story.
    Immunol Lett. 1991 Oct;30(2):241-8 PMID: 1757110
  34. Topology of the hydrophobic membrane-bound components of the histidine periplasmic permease. Comparison with other members of the family.
    J Biol Chem. 1992 Feb 5;267(4):2329-36 PMID: 1733937
  35. Influence of H-2 genes on growth of Mycobacterium tuberculosis in the lungs of chronically infected mice.
    Immunology. 1992 May;76(1):129-32 PMID: 1628890
  36. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg.
    Cell. 1993 May 7;73(3):469-85 PMID: 8490962
  37. Implication of phagosome-lysosome fusion in restriction of Mycobacterium avium growth in bone marrow macrophages from genetically resistant mice.
    Infect Immun. 1993 Sep;61(9):3775-84 PMID: 8359899
  38. Cloning of Entamoeba genes encoding proteolipids of putative vacuolar proton-translocating ATPases.
    Infect Immun. 1994 Aug;62(8):3572-5 PMID: 8039932
  39. Identification and characterization of a second mouse Nramp gene.
    Genomics. 1995 Jan 20;25(2):514-25 PMID: 7789986
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1999-05-00
Pages
2225-32
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC115961
Subset
IM
Grants
NIAID NIH HHS · R01 AI035237 · United States
NIAID NIH HHS · R21 AI035237 · United States
NIAID NIH HHS · AI35237 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com