Home LiteratureArticle Details
PMID: 12819096 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa.

Infection and immunity ·Vol. 71 ·No. 7 ·2003-07-00 ·Pages 4059-66

Lau GW, Goumnerov BC, Walendziewicz CL, Hewitson J, Xiao W, Mahajan-Miklos S, Tompkins RG, Perkins LA, Rahme LG

Abstract

Pseudomonas aeruginosa is a gram-negative pathogen that infects immunocompromised and cystic fibrosis patients. The molecular basis of the host-P. aeruginosa interaction and the effect of specific P. aeruginosa virulence factors on various components of the innate immunity pathways are largely unknown. We examine interactions between P. aeruginosa virulence factors and components of innate immunity response in the Drosophila melanogaster model system to reveal the importance of the Toll signaling pathway in resistance to infection by the P. aeruginosa human isolate PA14. Using the two PA14-isogenic mutants plcS and dsbA, we show that Drosophila loss-of-function mutants of Spatzle, the extracellular ligand of Toll, and Dorsal and Dif, two NF-kappa B-like transcription factors, allow increased P. aeruginosa infectivity within fly tissues. In contrast, a constitutively active Toll mutant and a loss-of-function mutant of Cactus, an I kappa B-like factor that inhibits the Toll signaling, reduce infectivity. Our finding that Dorsal activity is required to restrict P. aeruginosa infectivity in Drosophila provides direct in vivo evidence for Dorsal function in adult fly immunity. Additionally, our results provide the basis for future studies into interactions between P. aeruginosa virulence factors and components of the Toll signaling pathway, which is functionally conserved between flies and humans.

MeSH Terms
Animals Disease Susceptibility Drosophila Proteins/physiology Drosophila melanogaster/microbiology Humans Pseudomonas Infections/immunology Pseudomonas aeruginosa/pathogenicity Receptors, Cell Surface/physiology Toll-Like Receptors Virulence Factors
Chemicals
Drosophila Proteins Receptors, Cell Surface Tl protein, Drosophila Toll-Like Receptors Virulence Factors
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Lau Gee W
Department of Surgery, Harvard Medical School and Massachusetts General Hospital and Shriners Burns Institute, Boston, Massachusetts 02114, USA.
Goumnerov Boyan C
Walendziewicz Cynthia L
Hewitson Jennifer
Xiao Wenzhong
Mahajan-Miklos Shalina
Tompkins Ronald G
Perkins Lizabeth A
Rahme Laurence G
References (41)
41 references, click to expand
  1. Pseudomonas aeruginosa septicaemia in burns.
    Burns. 1999 Nov;25(7):611-6 PMID: 10563687
  2. Role and activation of type III secretion system genes in Pseudomonas aeruginosa-induced Drosophila killing.
    Microb Pathog. 2002 Jun;32(6):287-95 PMID: 12137756
  3. DsbA: a protein-folding catalyst contributing to bacterial virulence.
    Microbes Infect. 1999 Dec;1(14):1221-8 PMID: 10580278
  4. Toll signaling pathways in the innate immune response.
    Curr Opin Immunol. 2000 Feb;12(1):13-9 PMID: 10679407
  5. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3376-81 PMID: 10725405
  6. The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila.
    Immunity. 2000 May;12(5):569-80 PMID: 10843389
  7. Inducible antibacterial defence system in Drosophila.
    Nature. 1972 May 26;237(5352):232-5 PMID: 4625204
  8. Pseudomonas: the compromised host.
    Hosp Pract. 1976 Aug;11(8):91-100 PMID: 829230
  9. Mutations in the hemolytic-phospholipase C operon result in decreased virulence of Pseudomonas aeruginosa PAO1 grown under phosphate-limiting conditions.
    Infect Immun. 1989 May;57(5):1369-73 PMID: 2496027
  10. Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo.
    Genes Dev. 1991 May;5(5):797-807 PMID: 1827421
  11. Dif, a dorsal-related gene that mediates an immune response in Drosophila.
    Cell. 1993 Nov 19;75(4):753-63 PMID: 8242747
  12. Expression and nuclear translocation of the rel/NF-kappa B-related morphogen dorsal during the immune response of Drosophila.
    C R Acad Sci III. 1993 Oct;316(10):1218-24 PMID: 8062131
  13. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila.
    EMBO J. 1995 Feb 1;14(3):536-45 PMID: 7859742
  14. Signals from the IL-1 receptor homolog, Toll, can activate an immune response in a Drosophila hemocyte cell line.
    Biochem Biophys Res Commun. 1995 Apr 6;209(1):111-6 PMID: 7726823
  15. Common virulence factors for bacterial pathogenicity in plants and animals.
    Science. 1995 Jun 30;268(5219):1899-902 PMID: 7604262
  16. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9465-9 PMID: 7568155
  17. Role of Pseudomonas aeruginosa lipase in inflammatory mediator release from human inflammatory effector cells (platelets, granulocytes, and monocytes.
    Infect Immun. 1996 Aug;64(8):3252-8 PMID: 8757861
  18. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults.
    Cell. 1996 Sep 20;86(6):973-83 PMID: 8808632
  19. 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
  20. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14614-9 PMID: 9405661
  21. A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway.
    EMBO J. 1998 Aug 10;17(5):1217-27 PMID: 9482719
  22. Regulated nuclear import of Rel proteins in the Drosophila immune response.
    Nature. 1998 Mar 5;392(6671):93-7 PMID: 9510254
  23. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis.
    Development. 1998 May;125(10):1909-20 PMID: 9550723
  24. In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila.
    J Biol Chem. 1998 Apr 24;273(17):10463-9 PMID: 9553105
  25. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model.
    Cell. 1999 Jan 8;96(1):47-56 PMID: 9989496
  26. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2408-13 PMID: 10051655
  27. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor.
    Genes Dev. 1999 Apr 1;13(7):792-7 PMID: 10197979
  28. Pseudomonas aeruginosa hemolytic phospholipase C suppresses neutrophil respiratory burst activity.
    Infect Immun. 1999 May;67(5):2371-6 PMID: 10225897
  29. Phylogenetic perspectives in innate immunity.
    Science. 1999 May 21;284(5418):1313-8 PMID: 10334979
  30. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF.
    EMBO J. 1999 Jun 15;18(12):3380-91 PMID: 10369678
  31. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects.
    J Bacteriol. 2000 Jul;182(13):3843-5 PMID: 10851003
  32. Plants and animals share functionally common bacterial virulence factors.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8815-21 PMID: 10922040
  33. Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts.
    Mol Microbiol. 2000 Sep;37(5):981-8 PMID: 10972817
  34. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia.
    Immunity. 2000 Nov;13(5):737-48 PMID: 11114385
  35. Drosophila as a model host for Pseudomonas aeruginosa infection.
    J Bacteriol. 2001 Feb;183(4):1466-71 PMID: 11157963
  36. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein.
    Nature. 2001 Dec 13;414(6865):756-9 PMID: 11742401
  37. A genome-wide analysis of immune responses in Drosophila.
    Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15119-24 PMID: 11742098
  38. Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila.
    J Immunol. 2002 Feb 15;168(4):1542-6 PMID: 11823479
  39. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants.
    Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2152-7 PMID: 11854512
  40. The Toll and Imd pathways are the major regulators of the immune response in Drosophila.
    EMBO J. 2002 Jun 3;21(11):2568-79 PMID: 12032070
  41. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila.
    Mol Cell. 1999 Nov;4(5):827-37 PMID: 10619029
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2003-07-00
Pages
4059-66
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC162001
Subset
IM
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]