Home LiteratureArticle Details
PMID: 12595455 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Isolation of acid-inducible genes of Mycobacterium tuberculosis with the use of recombinase-based in vivo expression technology.

Infection and immunity ·Vol. 71 ·No. 3 ·2003-03-00 ·Pages 1379-88

Saviola B, Woolwine SC, Bishai WR

Abstract

A better understanding of mycobacterial gene regulation under certain stress conditions (e.g., low pH) may provide insight into mechanisms of adaptation during infection. To identify mycobacterial promoters induced at low pH, we adapted the recombinase-based in vivo expression technology (RIVET) promoter trap system for use with mycobacteria. Our results show that the TnpR recombinase of transposon gammadelta is active in Mycobacterium smegmatis and Mycobacterium tuberculosis. We developed a method to perform sequential double selection with mycobacteria by using RIVET, with a kanamycin preselection and a sucrose postselection. A library of M. tuberculosis DNA inserted upstream of tnpR was created, and using the double selection, we identified two promoters which are upregulated at low pH. The promoter regions drive the expression of a gene encoding a putative lipase, lipF (Rv3487c), as well as a PE-PGRS gene, Rv0834c, in a pH-dependent manner in both M. smegmatis and M. tuberculosis. The acid inducibility of lipF and Rv0834c was independent of the stress response sigma factor, SigF, as acid induction of the two genes in an M. tuberculosis sigF mutant strain was similar to that in the wild-type strain. No induction of lipF or Rv0834c was observed during infection of J774 murine macrophages, an observation which is in agreement with previous reports on the failure of phagosomes containing M. tuberculosis to acidify.

MeSH Terms
Animals Cell Line DNA Nucleotidyltransferases/metabolism Gene Expression Regulation, Bacterial Gene Library Green Fluorescent Proteins Hydrogen-Ion Concentration Luminescent Proteins/genetics Macrophages/immunology Mice Mycobacterium tuberculosis/genetics Promoter Regions, Genetic Recombinases
Chemicals
Luminescent Proteins Recombinases Green Fluorescent Proteins DNA Nucleotidyltransferases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Saviola Beatrice
Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA.
Woolwine Samuel C
Bishai William R
References (29)
29 references, click to expand
  1. Mycobacterium tuberculosis phagosome.
    Mol Microbiol. 1999 Mar;31(6):1603-9 PMID: 10209735
  2. Use of genetic recombination as a reporter of gene expression.
    Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2634-8 PMID: 8146167
  3. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence.
    Nature. 1998 Jun 11;393(6685):537-44 PMID: 9634230
  4. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guérin.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3111-5 PMID: 1901654
  5. Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic.
    Infect Immun. 1991 May;59(5):1823-31 PMID: 1902198
  6. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase.
    Science. 1994 Feb 4;263(5147):678-81 PMID: 8303277
  7. A stationary-phase stress-response sigma factor from Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2790-4 PMID: 8610119
  8. Regulation of the inducible acetamidase gene of Mycobacterium smegmatis.
    Microbiology. 1997 Jul;143 ( Pt 7):2267-76 PMID: 9245815
  9. Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection.
    Mol Microbiol. 1995 Nov;18(4):671-83 PMID: 8817490
  10. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence.
    J Bacteriol. 2002 Nov;184(21):5826-32 PMID: 12374814
  11. Expression of the Bacillus subtilis sacB gene confers sucrose sensitivity on mycobacteria.
    J Bacteriol. 1996 Feb;178(4):1197-9 PMID: 8576057
  12. Identification of novel staphylococcal virulence genes by in vivo expression technology.
    Mol Microbiol. 1998 Mar;27(5):967-76 PMID: 9535086
  13. Regulation of heat-shock response in bacteria.
    Ann N Y Acad Sci. 1998 Jun 30;851:147-51 PMID: 9668617
  14. FACS-optimized mutants of the green fluorescent protein (GFP).
    Gene. 1996;173(1 Spec No):33-8 PMID: 8707053
  15. Construction and characterization of a Mycobacterium tuberculosis mutant lacking the alternate sigma factor gene, sigF.
    Infect Immun. 2000 Oct;68(10):5575-80 PMID: 10992456
  16. A study of mycobacterial transcriptional apparatus: identification of novel features in promoter elements.
    J Bacteriol. 1996 Aug;178(16):4847-53 PMID: 8759847
  17. Expression of the green fluorescent protein (GFP) in mycobacterium avium as a tool to study the interaction between Mycobacteria and host cells.
    Microb Pathog. 1997 Apr;22(4):193-8 PMID: 9140914
  18. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family.
    Science. 2000 May 26;288(5470):1436-9 PMID: 10827956
  19. Protein-DNA recognition.
    Annu Rev Biochem. 1984;53:293-321 PMID: 6236744
  20. Positions of strand exchange in mycobacteriophage L5 integration and characterization of the attB site.
    J Bacteriol. 1996 Sep;178(18):5533-6 PMID: 8808947
  21. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages.
    J Immunol. 1994 Sep 15;153(6):2568-78 PMID: 8077667
  22. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited.
    J Exp Med. 1995 Jan 1;181(1):257-70 PMID: 7807006
  23. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes.
    J Bacteriol. 2002 Jul;184(14):4025-32 PMID: 12081975
  24. Exposure to antibiotics induces expression of the Mycobacterium tuberculosis sigF gene: implications for chemotherapy against mycobacterial persistors.
    Antimicrob Agents Chemother. 1999 Feb;43(2):218-25 PMID: 9925509
  25. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project.
    JAMA. 1999 Aug 18;282(7):677-86 PMID: 10517722
  26. The Persistence of Tuberculous Infections.
    Am J Pathol. 1933;9(Suppl):711-718.1 PMID: 19970106
  27. The identification of Mycobacterium marinum genes differentially expressed in macrophage phagosomes using promoter fusions to green fluorescent protein.
    Mol Microbiol. 1998 Sep;29(5):1167-77 PMID: 9767585
  28. Immunopathogenesis of pulmonary tuberculosis.
    Hosp Pract (Off Ed). 1993 Jan 15;28(1):51-8 PMID: 8419415
  29. Color selection with a hygromycin-resistance-based Escherichia coli-mycobacterial shuttle vector.
    Gene. 1995 Dec 1;166(1):181-2 PMID: 8529888
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2003-03-00
Pages
1379-88
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC148880
Subset
IM
Grants
NIAID NIH HHS · R01 AI043846 · United States
NIAID NIH HHS · AI50360 · United States
NIAID NIH HHS · AI37856 · United States
NIAID NIH HHS · R01 AI037856 · United States
NIAID NIH HHS · R01 AI036973 · United States
NIAID NIH HHS · AI43846 · United States
NIAID NIH HHS · AI36973 · United States
NIAID NIH HHS · F32 AI050360 · 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: [email protected]