Home LiteratureArticle Details
PMID: 16520379 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Epithelial cells are sensitive detectors of bacterial pore-forming toxins.

The Journal of biological chemistry ·Vol. 281 ·No. 18 ·2006-05-05 ·Pages 12994-8

Ratner AJ, Hippe KR, Aguilar JL, Bender MH, Nelson AL, Weiser JN

Abstract

Epithelial cells act as an interface between human mucosal surfaces and the surrounding environment. As a result, they are responsible for the initiation of local immune responses, which may be crucial for prevention of invasive infection. Here we show that epithelial cells detect the presence of bacterial pore-forming toxins (including pneumolysin from Streptococcus pneumoniae, alpha-hemolysin from Staphylococcus aureus, streptolysin O from Streptococcus pyogenes, and anthrolysin O from Bacillus anthracis) at nanomolar concentrations, far below those required to cause cytolysis. Phosphorylation of p38 MAPK appears to be a conserved response of epithelial cells to subcytolytic concentrations of bacterial poreforming toxins, and this activity is inhibited by the addition of high molecular weight osmolytes to the extracellular medium. By sensing osmotic stress caused by the insertion of a sublethal number of pores into their membranes, epithelial cells may act as an early warning system to commence an immune response, while the local density of toxin-producing bacteria remains low. Osmosensing may thus represent a novel innate immune response to a common bacterial virulence strategy.

MeSH Terms
Bacillus anthracis/metabolism Bacterial Proteins/chemistry Bacterial Toxins/chemistry Cell Line, Tumor Epithelial Cells/metabolism,microbiology Hemolysin Proteins/chemistry Humans Interleukin-8/metabolism Membrane Glycoproteins/chemistry Osmosis Staphylococcus aureus/metabolism Streptococcus pneumoniae/metabolism Streptolysins/chemistry p38 Mitogen-Activated Protein Kinases/metabolism
Chemicals
Bacterial Proteins Bacterial Toxins Hemolysin Proteins Interleukin-8 Membrane Glycoproteins Streptolysins anthrolysin O, Bacillus anthracis streptolysin O p38 Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ratner Adam J
Department of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104, USA. ratner@mail.med.upenn.edu
Hippe Karen R
Aguilar Jorge L
Bender Matthew H
Nelson Aaron L
Weiser Jeffrey N
References (31)
31 references, click to expand
  1. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1966-71 PMID: 12569171
  2. Differential sensitivity of pneumolysin-induced channels to gating by divalent cations.
    J Membr Biol. 1992 May;127(3):195-203 PMID: 1379644
  3. Pneumolysin-mediated activation of NFkappaB in human neutrophils is antagonized by docosahexaenoic acid.
    Clin Exp Immunol. 2005 May;140(2):274-81 PMID: 15807851
  4. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins.
    Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):10995-1000 PMID: 15256590
  5. Resealing of large transmembrane pores produced by streptolysin O in nucleated cells is accompanied by NF-kappaB activation and downstream events.
    FASEB J. 2002 Feb;16(2):237-9 PMID: 11744625
  6. Anthrolysin O and other gram-positive cytolysins are toll-like receptor 4 agonists.
    J Exp Med. 2004 Dec 20;200(12):1647-55 PMID: 15611291
  7. STUDIES ON THE CHEMICAL NATURE OF THE SUBSTANCE INDUCING TRANSFORMATION OF PNEUMOCOCCAL TYPES : INDUCTION OF TRANSFORMATION BY A DESOXYRIBONUCLEIC ACID FRACTION ISOLATED FROM PNEUMOCOCCUS TYPE III.
    J Exp Med. 1944 Feb 1;79(2):137-58 PMID: 19871359
  8. Differential effects of p38- and extracellular signal-regulated kinase mitogen-activated protein kinase inhibitors on inducible nitric oxide synthase and tumor necrosis factor production in murine macrophages stimulated with Streptococcus pneumoniae.
    J Infect Dis. 2002 Apr 1;185(7):921-6 PMID: 11920316
  9. Alpha-haemolysin of uropathogenic E. coli induces Ca2+ oscillations in renal epithelial cells.
    Nature. 2000 Jun 8;405(6787):694-7 PMID: 10864327
  10. DNA from periodontopathogenic bacteria is immunostimulatory for mouse and human immune cells.
    Infect Immun. 2003 Feb;71(2):850-6 PMID: 12540566
  11. Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae.
    Infect Immun. 1989 Jul;57(7):2037-42 PMID: 2731982
  12. Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock.
    Nat Cell Biol. 2003 Dec;5(12):1104-10 PMID: 14634666
  13. Expression of an antisense hla fragment in Staphylococcus aureus reduces alpha-toxin production in vitro and attenuates lethal activity in a murine model.
    Infect Immun. 1997 Jan;65(1):179-84 PMID: 8975909
  14. Streptococcus pneumoniae-induced p38 MAPK-dependent phosphorylation of RelA at the interleukin-8 promotor.
    J Biol Chem. 2004 Dec 17;279(51):53241-7 PMID: 15485852
  15. Pneumolysin activates the synthesis and release of interleukin-8 by human neutrophils in vitro.
    J Infect Dis. 2002 Aug 15;186(4):562-5 PMID: 12195386
  16. Proinflammatory interactions of pneumolysin with human neutrophils.
    J Infect Dis. 2001 Feb 15;183(4):604-11 PMID: 11170986
  17. p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages in vitro and during infection in vivo.
    J Immunol. 2001 Jan 1;166(1):582-7 PMID: 11123340
  18. A conserved tryptophan in pneumolysin is a determinant of the characteristics of channels formed by pneumolysin in cells and planar lipid bilayers.
    Biochem J. 1998 Feb 1;329 ( Pt 3):571-7 PMID: 9445384
  19. Synergistic proinflammatory responses induced by polymicrobial colonization of epithelial surfaces.
    Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3429-34 PMID: 15728393
  20. Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model.
    Infect Immun. 2005 Nov;73(11):7718-26 PMID: 16239576
  21. Neurotoxicity of pneumolysin, a major pneumococcal virulence factor, involves calcium influx and depends on activation of p38 mitogen-activated protein kinase.
    Neurobiol Dis. 2002 Dec;11(3):355-68 PMID: 12586546
  22. Infection by Streptococcus pyogenes induces the receptor activator of NF-kappaB ligand expression in mouse osteoblastic cells.
    Infect Immun. 2003 Feb;71(2):948-55 PMID: 12540577
  23. Pneumolysin potentiates production of prostaglandin E(2) and leukotriene B(4) by human neutrophils.
    Infect Immun. 2001 May;69(5):3494-6 PMID: 11292782
  24. Innate immune response of oral and foreskin keratinocytes: utilization of different signaling pathways by various bacterial species.
    Infect Immun. 2004 Jan;72(1):352-8 PMID: 14688115
  25. Pneumococcal pneumolysin and H(2)O(2) mediate brain cell apoptosis during meningitis.
    J Clin Invest. 2002 Jan;109(1):19-27 PMID: 11781347
  26. Structure of alpha-latrotoxin oligomers reveals that divalent cation-dependent tetramers form membrane pores.
    Nat Struct Biol. 2000 Jan;7(1):48-53 PMID: 10625427
  27. Activation of ERK by Ca2+ store depletion in rat liver epithelial cells.
    Am J Physiol. 1999 Jan;276(1 Pt 1):C221-30 PMID: 9886938
  28. The apoptotic response to pneumolysin is Toll-like receptor 4 dependent and protects against pneumococcal disease.
    Infect Immun. 2005 Oct;73(10):6479-87 PMID: 16177320
  29. Characterization of anthrolysin O, the Bacillus anthracis cholesterol-dependent cytolysin.
    Infect Immun. 2003 Jun;71(6):3183-9 PMID: 12761097
  30. Role of streptolysin O in a mouse model of invasive group A streptococcal disease.
    Infect Immun. 2000 Nov;68(11):6384-90 PMID: 11035749
  31. Cystic fibrosis pathogens activate Ca2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells.
    J Biol Chem. 2001 Jun 1;276(22):19267-75 PMID: 11278360
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2006-05-05
Epub
2006-00-06
Pages
12994-8
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC1586115
Subset
IM
Grants
NIAID NIH HHS · R01 AI044231 · United States
NIAID NIH HHS · AI065450 · United States
NIAID NIH HHS · AI044231 · United States
NIAID NIH HHS · R21 AI054647 · United States
NIAID NIH HHS · R21 AI044231 · United States
NIAID NIH HHS · AI054647 · United States
NIAID NIH HHS · K08 AI065450 · United States
NIAID NIH HHS · AI038446 · United States
NIAID NIH HHS · R01 AI038446 · 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