Home LiteratureArticle Details
PMID: 17337571 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal.

Journal of bacteriology ·Vol. 189 ·No. 9 ·2007-05-00 ·Pages 3425-33

Farrow JM, Pesci EC

Abstract

Pseudomonas aeruginosa is an opportunistic pathogen that causes serious infections in immunocompromised patients and those with cystic fibrosis (CF). This gram-negative bacterium uses multiple cell-to-cell signals to control numerous cellular functions and virulence. One of these signals is 2-heptyl-3-hydroxy-4-quinolone, which is referred to as the Pseudomonas quinolone signal (PQS). This signal functions as a coinducer for a transcriptional regulator (PqsR) to positively control multiple virulence genes and its own synthesis. PQS production is required for virulence in multiple models of infection, and it has been shown to be produced in the lungs of CF patients infected by P. aeruginosa. One of the precursor compounds from which PQS is synthesized is the metabolite anthranilate. This compound can be derived from the conversion of chorismate to anthranilate by an anthranilate synthase or through the degradation of tryptophan via the anthranilate branch of the kynurenine pathway. In this study, we present data which help to define the kynurenine pathway in P. aeruginosa and show that the kynurenine pathway serves as a critical source of anthranilate for PQS synthesis. We also show that the kyn pathway genes are induced during growth with tryptophan and that they are autoregulated by kynurenine. This study provides solid foundations for the understanding of how P. aeruginosa produces the anthranilate that serves as a precursor to PQS and other 4-quinolones.

MeSH Terms
Antibiosis Artificial Gene Fusion Chorismic Acid/metabolism Gene Deletion Gene Expression Regulation, Bacterial Genetic Complementation Test Kynurenine/metabolism Metabolic Networks and Pathways/genetics Microbial Viability Models, Biological Pseudomonas aeruginosa/genetics,metabolism Quinolones/metabolism Staphylococcus aureus/drug effects Tryptophan/metabolism beta-Galactosidase/biosynthesis,genetics ortho-Aminobenzoates/metabolism
Chemicals
2-heptyl-3-hydroxy-4-quinolone Quinolones ortho-Aminobenzoates anthranilic acid Kynurenine Tryptophan beta-Galactosidase Chorismic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Farrow John M
Department of Microbiology and Immunology, East Carolina University School of Medicine, BT 132, 600 Moye Blvd., Greenville, NC 27834, USA.
Pesci Everett C
References (50)
50 references, click to expand
  1. Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology.
    J Bacteriol. 2005 Aug;187(15):5267-77 PMID: 16030221
  2. DNA sequences and characterization of four early genes of the tryptophan pathway in Pseudomonas aeruginosa.
    J Bacteriol. 1990 Feb;172(2):853-66 PMID: 2105306
  3. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants.
    Gene. 1998 May 28;212(1):77-86 PMID: 9661666
  4. A bacterial cell to cell signal in the lungs of cystic fibrosis patients.
    FEMS Microbiol Lett. 2002 Sep 24;215(1):41-6 PMID: 12393198
  5. Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase.
    J Bacteriol. 1980 Jun;142(3):836-42 PMID: 6769912
  6. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants.
    J Bacteriol. 2002 Dec;184(23):6481-9 PMID: 12426335
  7. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa.
    Gene. 1994 Oct 11;148(1):81-6 PMID: 7926843
  8. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):197-201 PMID: 8278364
  9. Endogenous kynurenines as targets for drug discovery and development.
    Nat Rev Drug Discov. 2002 Aug;1(8):609-20 PMID: 12402501
  10. Aerobic tryptophan degradation pathway in bacteria: novel kynurenine formamidase.
    FEMS Microbiol Lett. 2003 Oct 24;227(2):219-27 PMID: 14592712
  11. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications.
    J Bacteriol. 1990 Feb;172(2):884-900 PMID: 2153661
  12. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa.
    J Bacteriol. 2005 Jul;187(13):4372-80 PMID: 15968046
  13. Bacterial quorum sensing in pathogenic relationships.
    Infect Immun. 2000 Sep;68(9):4839-49 PMID: 10948095
  14. [Biosynthesis of 2-n-alkyl-4-hydroxyquinoline derivates (pseudane) in Pseudomonas aeruginosa].
    Eur J Biochem. 1971 Feb 1;18(3):391-400 PMID: 5542949
  15. Pathogenesis of cystic fibrosis.
    Lancet. 1993 Apr 24;341(8852):1065-9 PMID: 7682274
  16. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa.
    J Bacteriol. 2002 Dec;184(23):6472-80 PMID: 12426334
  17. NAD biosynthesis: identification of the tryptophan to quinolinate pathway in bacteria.
    Chem Biol. 2003 Dec;10(12):1195-204 PMID: 14700627
  18. The Pseudomonas siderophore quinolobactin is synthesized from xanthurenic acid, an intermediate of the kynurenine pathway.
    Mol Microbiol. 2004 Apr;52(2):371-84 PMID: 15066027
  19. Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa.
    J Am Soc Mass Spectrom. 2004 Jun;15(6):862-9 PMID: 15144975
  20. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture.
    J Bacteriol. 2005 Jan;187(2):554-66 PMID: 15629927
  21. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands.
    Mol Microbiol. 2006 Dec;62(6):1689-99 PMID: 17083468
  22. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR.
    Mol Microbiol. 2003 Oct;50(1):29-43 PMID: 14507361
  23. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication.
    Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1339-44 PMID: 14739337
  24. Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines.
    J Bacteriol. 2005 Jun;187(11):3630-5 PMID: 15901684
  25. Common virulence factors for bacterial pathogenicity in plants and animals.
    Science. 1995 Jun 30;268(5219):1899-902 PMID: 7604262
  26. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment.
    J Bacteriol. 2003 Apr;185(7):2080-95 PMID: 12644477
  27. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11229-34 PMID: 10500159
  28. 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa.
    J Antimicrob Chemother. 1992 Nov;30(5):615-23 PMID: 1493979
  29. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension.
    Gene. 1989 Apr 15;77(1):61-8 PMID: 2744488
  30. Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11633-7 PMID: 11573001
  31. Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice.
    Infect Immun. 2004 Jul;72(7):4275-8 PMID: 15213173
  32. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa.
    J Bacteriol. 2000 May;182(10):2702-8 PMID: 10781536
  33. Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning.
    J Bacteriol. 2001 Nov;183(21):6207-14 PMID: 11591663
  34. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones.
    Mol Microbiol. 2005 Feb;55(4):998-1014 PMID: 15686549
  35. A quorum sensing-associated virulence gene of Pseudomonas aeruginosa encodes a LysR-like transcription regulator with a unique self-regulatory mechanism.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14613-8 PMID: 11724939
  36. Utilization of human respiratory secretions by mucoid Pseudomonas aeruginosa of cystic fibrosis origin.
    Infect Immun. 1982 Aug;37(2):662-9 PMID: 6811437
  37. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1490-4 PMID: 7878006
  38. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model.
    Cell. 1999 Jan 8;96(1):47-56 PMID: 9989496
  39. Structure of a naturally occurring antagonist of dihydrostreptomycin.
    Biochem J. 1956 May;63(1):124-30 PMID: 13315257
  40. Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections.
    Infect Immun. 1997 Aug;65(8):3086-90 PMID: 9234758
  41. Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13245-50 PMID: 9371831
  42. Electroporation of freshly plated Escherichia coli and Pseudomonas aeruginosa cells.
    Biotechniques. 1998 Dec;25(6):954-6, 958 PMID: 9863047
  43. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis.
    J Bacteriol. 2003 Apr;185(7):2066-79 PMID: 12644476
  44. A minimal tiling path cosmid library for functional analysis of the Pseudomonas aeruginosa PAO1 genome.
    Microb Comp Genomics. 2000;5(4):189-203 PMID: 11471833
  45. Chromosomal genetics of Pseudomonas.
    Microbiol Rev. 1979 Mar;43(1):73-102 PMID: 111024
  46. The high amino-acid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa.
    J Med Microbiol. 1996 Aug;45(2):110-9 PMID: 8683546
  47. Secondary metabolites of the fluorescent pseudomonads.
    Microbiol Rev. 1979 Sep;43(3):422-42 PMID: 120492
  48. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants.
    Nucleic Acids Res. 1989 May 11;17(9):3469-78 PMID: 2657660
  49. Conserved virulence factors of Pseudomonas aeruginosa are required for killing Bacillus subtilis.
    J Microbiol. 2005 Oct;43(5):443-50 PMID: 16273037
  50. Cell-to-cell signaling and Pseudomonas aeruginosa infections.
    Emerg Infect Dis. 1998 Oct-Dec;4(4):551-60 PMID: 9866731
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2007-05-00
Epub
2007-00-02
Pages
3425-33
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1855905
Subset
IM
Grants
NIAID NIH HHS · R01 AI046682 · United States
NIAID NIH HHS · R01-AI46682 · 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]