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Science 20 November 1998: Vol. 282. no. 5393, pp. 1494 - 1497 DOI: 10.1126/science.282.5393.1494
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Reports
Induction and Evasion of Host Defenses by Type 1-Piliated Uropathogenic Escherichia coli
Matthew A. Mulvey,
Yolanda S. Lopez-Boado,
Carole L. Wilson,
Robyn Roth,
William C. Parks,
John Heuser,
Scott J. Hultgren
*
Virtually all uropathogenic strains of Escherichia coli
encode filamentous surface adhesive organelles called type 1 pili. High-resolution electron microscopy of infected mouse bladders revealed
that type 1 pilus tips interacted directly with the lumenal surface of
the bladder, which is embedded with hexagonal arrays of integral
membrane glycoproteins known as uroplakins. Attached pili were
shortened and facilitated intimate contact of the bacteria with the
uroplakin-coated host cells. Bacterial attachment resulted in
exfoliation of host bladder epithelial cells as part of an innate host
defense system. Exfoliation occurred through a rapid apoptosis-like
mechanism involving caspase activation and host DNA fragmentation.
Bacteria resisted clearance in the face of host defenses within the
bladder by invading into the epithelium.
M. A. Mulvey and S. J. Hultgren, Department of Molecular
Microbiology and Microbial Pathogenesis, Box 8230, Washington
University School of Medicine, 660 S. Euclid Avenue, St. Louis, MO
63110, USA. Y. S. Lopez-Boado, C. L. Wilson, W. C. Parks, Department of Medicine, Box 8032, Washington University School
of Medicine, 660 S. Euclid Avenue, St. Louis, MO 63110, USA. R. Roth
and J. Heuser, Department of Cell Biology and Physiology, Box
8228, Washington University School of Medicine, 660 S. Euclid Avenue,
St. Louis, MO 63110, USA.
*
To whom correspondence should be addressed. E-mail:
hultgren{at}borcim.wustl.edu
Read the Full Text
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- A Salmonella fim Homologue in Citrobacter freundii Mediates Invasion In Vitro and Crossing of the Blood-Brain Barrier in the Rat Pup Model.
- P. Hess, A. Altenhofer, A. S. Khan, N. Daryab, K. S. Kim, J. Hacker, and T. A. Oelschlaeger (2004)
Infect. Immun.
72, 5298-5307
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- The Usher N Terminus Is the Initial Targeting Site for Chaperone-Subunit Complexes and Participates in Subsequent Pilus Biogenesis Events.
- T. W. Ng, L. Akman, M. Osisami, and D. G. Thanassi (2004)
J. Bacteriol.
186, 5321-5331
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- Uropathogenic Escherichia coli Triggers Oxygen-Dependent Apoptosis in Human Neutrophils through the Cooperative Effect of Type 1 Fimbriae and Lipopolysaccharide.
- R. Blomgran, L. Zheng, and O. Stendahl (2004)
Infect. Immun.
72, 4570-4578
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- Interaction of Dr Adhesin with Collagen Type IV Is a Critical Step in Escherichia coli Renal Persistence.
- R. Selvarangan, P. Goluszko, J. Singhal, C. Carnoy, S. Moseley, B. Hudson, S. Nowicki, and B. Nowicki (2004)
Infect. Immun.
72, 4827-4835
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- Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium.
- P. Acharya, J. Beckel, W. G. Ruiz, E. Wang, R. Rojas, L. Birder, and G. Apodaca (2004)
Am J Physiol Renal Physiol
287, F305-F318
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- Identification of Acyloxyacyl Hydrolase, a Lipopolysaccharide- Detoxifying Enzyme, in the Murine Urinary Tract.
- J. A. Feulner, M. Lu, JohnM. Shelton, M. Zhang, J. A. Richardson, and R. S. Munford (2004)
Infect. Immun.
72, 3171-3178
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- Bacterial Penetration of Bladder Epithelium through Lipid Rafts.
- M. J. Duncan, G. Li, J.-S. Shin, J. L. Carson, and S. N. Abraham (2004)
J. Biol. Chem.
279, 18944-18951
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- Ablation of the Tamm-Horsfall protein gene increases susceptibility of mice to bladder colonization by type 1-fimbriated Escherichia coli.
- L. Mo, X.-H. Zhu, H.-Y. Huang, E. Shapiro, D. L. Hasty, and X.-R. Wu (2004)
Am J Physiol Renal Physiol
286, F795-F802
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- From the Cover: Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis.
- S. S. Justice, C. Hung, J. A. Theriot, D. A. Fletcher, G. G. Anderson, M. J. Footer, and S. J. Hultgren (2004)
PNAS
101, 1333-1338
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- Variation of High Mannose Chains of Tamm-Horsfall Glycoprotein Confers Differential Binding to Type 1-fimbriated Escherichia coli.
- D. Cavallone, N. Malagolini, A. Monti, X.-R. Wu, and F. Serafini-Cessi (2004)
J. Biol. Chem.
279, 216-222
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- Inactivation of ompX Causes Increased Interactions of Type 1 Fimbriated Escherichia coli with Abiotic Surfaces.
- K. Otto and M. Hermansson (2004)
J. Bacteriol.
186, 226-234
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- Localization of Cystic Fibrosis Transmembrane Conductance Regulator to Lipid Rafts of Epithelial Cells Is Required for Pseudomonas aeruginosa-Induced Cellular Activation.
- M. P. Kowalski and G. B. Pier (2004)
J. Immunol.
172, 418-425
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- Highly Resistant Metabolically Deficient Dwarf Mutant of Escherichia coli Is the Cause of a Chronic Urinary Tract Infection.
- K. Trulzsch, H. Hoffmann, C. Keller, S. Schubert, L. Bader, J. Heesemann, and A. Roggenkamp (2003)
J. Clin. Microbiol.
41, 5689-5694
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- Structural basis of urothelial permeability barrier function as revealed by Cryo-EM studies of the 16 nm uroplakin particle.
- G. Min, G. Zhou, M. Schapira, T.-T. Sun, and X.-P. Kong (2003)
J. Cell Sci.
116, 4087-4094
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- Pseudomonas aeruginosa-Induced Apoptosis Is Defective in Respiratory Epithelial Cells Expressing Mutant Cystic Fibrosis Transmembrane Conductance Regulator.
- C. L. Cannon, M. P. Kowalski, K. S. Stopak, and G. B. Pier (2003)
Am. J. Respir. Cell Mol. Biol.
29, 188-197
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- Intracellular Bacterial Biofilm-Like Pods in Urinary Tract Infections.
- G. G. Anderson, J. J. Palermo, J. D. Schilling, R. Roth, J. Heuser, and S. J. Hultgren (2003)
Science
301, 105-107
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- Chaperone-Subunit-Usher Interactions Required for Donor Strand Exchange during Bacterial Pilus Assembly.
- M. M. Barnhart, F. G. Sauer, J. S. Pinkner, and S. J. Hultgren (2003)
J. Bacteriol.
185, 2723-2730
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- Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichiacoli.
- J. D. Schilling, S. M. Martin, C. S. Hung, R. G. Lorenz, and S. J. Hultgren (2003)
PNAS
100, 4203-4208
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- CD14- and Toll-Like Receptor-Dependent Activation of Bladder Epithelial Cells by Lipopolysaccharide and Type 1 Piliated Escherichia coli.
- J. D. Schilling, S. M. Martin, D. A. Hunstad, K. P. Patel, M. A. Mulvey, S. S. Justice, R. G. Lorenz, and S. J. Hultgren (2003)
Infect. Immun.
71, 1470-1480
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- Urinary tract infection in iNOS-deficient mice with focus on bacterial sensitivity to nitric oxide.
- M. Poljakovic and K. Persson (2003)
Am J Physiol Renal Physiol
284, F22-F31
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- Effect of Trimethoprim-Sulfamethoxazole on Recurrent Bacteriuria and Bacterial Persistence in Mice Infected with Uropathogenic Escherichia coli.
- J. D. Schilling, R. G. Lorenz, and S. J. Hultgren (2002)
Infect. Immun.
70, 7042-7049
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- Host-Pathogen Interactions: Subversion and Utilization of the NF-{kappa}B Pathway during Infection.
- C. M. Tato and C. A. Hunter (2002)
Infect. Immun.
70, 3311-3317
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- Assessment of Virulence of Uropathogenic Escherichia coli Type 1 Fimbrial Mutants in Which the Invertible Element Is Phase-Locked On or Off.
- N. W. Gunther IV, J. A. Snyder, V. Lockatell, I. Blomfield, D. E. Johnson, and H. L. T. Mobley (2002)
Infect. Immun.
70, 3344-3354
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- Identification of Target Tissue Glycosphingolipid Receptors for Uropathogenic, F1C-fimbriated Escherichia coli and Its Role in Mucosal Inflammation.
- F. Backhed, B. Alsen, N. Roche, J. Angstrom, A. von Euler, M. E. Breimer, B. Westerlund-Wikstrom, S. Teneberg, and A. Richter-Dahlfors (2002)
J. Biol. Chem.
277, 18198-18205
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- Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding.
- G. Zhou, W.-J. Mo, P. Sebbel, G. Min, T. A. Neubert, R. Glockshuber, X.-R. Wu, T.-T. Sun, and X.-P. Kong (2002)
J. Cell Sci.
114, 4095-4103
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- Molecular Regulation of Urothelial Renewal and Host Defenses during Infection with Uropathogenic Escherichia coli.
- I. U. Mysorekar, M. A. Mulvey, S. J. Hultgren, and J. I. Gordon (2002)
J. Biol. Chem.
277, 7412-7419
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