Previous Article | Next Article 
Infection and Immunity, May 2000, p. 2916-2924, Vol. 68, No. 5
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Pseudomonas aeruginosa Cystic Fibrosis
Isolates Induce Rapid, Type III Secretion-Dependent, but
ExoU-Independent, Oncosis of Macrophages and Polymorphonuclear
Neutrophils
Denis
Dacheux,1
Bertrand
Toussaint,1
Marceline
Richard,2
Guy
Brochier,2
Jacques
Croize,3 and
Ina
Attree1,*
Département de Biologie
Moléculaire et Structurale, BBSI, UMR-314 CNRS,
CEA-Grenoble,1 and Service de
Bactériologie et Virologie, CHU,3
Grenoble, and Service d'Imagerie et de Microscopie
Electronique, CRSSA, La Tronche,2 France
Received 18 November 1999/Returned for modification 27 December
1999/Accepted 25 January 2000
Pseudomonas aeruginosa, an opportunistic pathogen
responsible most notably for severe infections in cystic fibrosis (CF)
patients, utilizes the type III secretion system for eukaryotic cell
intoxication. The CF clinical isolate CHA shows toxicity towards human
polymorphonuclear neutrophils (PMNs) which is dependent on the type III
secretion system but independent of the cytotoxin ExoU. In the present
study, the cytotoxicity of this strain toward human and murine
macrophages was demonstrated. In low-multiplicity infections
(multiplicity of infection, 10), approximately 40% of the cells die
within 60 min. Analysis of CHA-infected cells by transmission electron
microscopy, DNA fragmentation assay, and Hoechst staining revealed the
hallmarks of oncosis: cellular and nuclear swelling, disintegration of
the plasma membrane, and absence of DNA fragmentation. A panel of 29 P. aeruginosa CF isolates was screened for type III system genotype, protein secretion profile, and cytotoxicity toward PMNs and
macrophages. This study showed that six CF isolates were able to induce
rapid ExoU-independent oncosis on phagocyte cells.
*
Corresponding author. Mailing address: DBMS/BBSI,
CEA-Grenoble, 17 rue des Martyrs, 38054 Grenoble cedex 09, France.
Phone: 33.4.76.88.34.83. Fax: 33.4.76.88.44.99. E-mail:
iattreedelic{at}cea.fr.
Infection and Immunity, May 2000, p. 2916-2924, Vol. 68, No. 5
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
El Solh, A. A., Alhajhusain, A.
(2009). Update on the treatment of Pseudomonas aeruginosa pneumonia. J Antimicrob Chemother
64: 229-238
[Abstract]
[Full Text]
-
Baer, M., Sawa, T., Flynn, P., Luehrsen, K., Martinez, D., Wiener-Kronish, J. P., Yarranton, G., Bebbington, C.
(2009). An Engineered Human Antibody Fab Fragment Specific for Pseudomonas aeruginosa PcrV Antigen Has Potent Antibacterial Activity. Infect. Immun.
77: 1083-1090
[Abstract]
[Full Text]
-
Zhang, Y., Li, X., Carpinteiro, A., Gulbins, E.
(2008). Acid Sphingomyelinase Amplifies Redox Signaling in Pseudomonas aeruginosa-Induced Macrophage Apoptosis. J. Immunol.
181: 4247-4254
[Abstract]
[Full Text]
-
El Solh, A. A., Akinnusi, M. E., Wiener-Kronish, J. P., Lynch, S. V., Pineda, L. A., Szarpa, K.
(2008). Persistent Infection with Pseudomonas aeruginosa in Ventilator-associated Pneumonia. Am. J. Respir. Crit. Care Med.
178: 513-519
[Abstract]
[Full Text]
-
Caroline, G., Eric, F., Bohn, Y.-S. T., Sylvie, E., Attree, I.
(2008). Oligomerization of PcrV and LcrV, Protective Antigens of Pseudomonas aeruginosa and Yersinia pestis. J. Biol. Chem.
283: 23940-23949
[Abstract]
[Full Text]
-
Shen, D.-K., Filopon, D., Chaker, H., Boullanger, S., Derouazi, M., Polack, B., Toussaint, B.
(2008). High-cell-density regulation of the Pseudomonas aeruginosa type III secretion system: implications for tryptophan catabolites. Microbiology
154: 2195-2208
[Abstract]
[Full Text]
-
Miao, E. A., Ernst, R. K., Dors, M., Mao, D. P., Aderem, A.
(2008). Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. USA
105: 2562-2567
[Abstract]
[Full Text]
-
Sano, G.-i., Takada, Y., Goto, S., Maruyama, K., Shindo, Y., Oka, K., Matsui, H., Matsuo, K.
(2007). Flagella Facilitate Escape of Salmonella from Oncotic Macrophages. J. Bacteriol.
189: 8224-8232
[Abstract]
[Full Text]
-
Bashaw, J., Norris, S., Weeks, S., Trevino, S., Adamovicz, J. J., Welkos, S.
(2007). Development of In Vitro Correlate Assays of Immunity to Infection with Yersinia pestis. CVI
14: 605-616
[Abstract]
[Full Text]
-
Gregory, A. D., Hogue, L. A., Ferkol, T. W., Link, D. C.
(2007). Regulation of systemic and local neutrophil responses by G-CSF during pulmonary Pseudomonas aeruginosa infection. Blood
109: 3235-3243
[Abstract]
[Full Text]
-
Zolfaghar, I., Evans, D. J., Ronaghi, R., Fleiszig, S. M. J.
(2006). Type III Secretion-Dependent Modulation of Innate Immunity as One of Multiple Factors Regulated by Pseudomonas aeruginosa RetS. Infect. Immun.
74: 3880-3889
[Abstract]
[Full Text]
-
Zulianello, L., Canard, C., Kohler, T., Caille, D., Lacroix, J.-S., Meda, P.
(2006). Rhamnolipids Are Virulence Factors That Promote Early Infiltration of Primary Human Airway Epithelia by Pseudomonas aeruginosa.. Infect. Immun.
74: 3134-3147
[Abstract]
[Full Text]
-
Dockrell, D. H., Whyte, M. K. B.
(2006). Regulation of phagocyte lifespan in the lung during bacterial infection. J. Leukoc. Biol.
79: 904-908
[Abstract]
[Full Text]
-
Rocha, C. L., Rucks, E. A., Vincent, D. M., Olson, J. C.
(2005). Examination of the Coordinate Effects of Pseudomonas aeruginosa ExoS on Rac1. Infect. Immun.
73: 5458-5467
[Abstract]
[Full Text]
-
Worgall, S., Heguy, A., Luettich, K., O'Connor, T. P., Harvey, B.-G., Quadri, L. E. N., Crystal, R. G.
(2005). Similarity of Gene Expression Patterns in Human Alveolar Macrophages in Response to Pseudomonas aeruginosa and Burkholderia cepacia. Infect. Immun.
73: 5262-5268
[Abstract]
[Full Text]
-
Corech, R., Rao, A., Laxova, A., Moss, J., Rock, M. J., Li, Z., Kosorok, M. R., Splaingard, M. L., Farrell, P. M., Barbieri, J. T.
(2005). Early Immune Response to the Components of the Type III System of Pseudomonas aeruginosa in Children with Cystic Fibrosis. J. Clin. Microbiol.
43: 3956-3962
[Abstract]
[Full Text]
-
Watt, A P, Courtney, J, Moore, J, Ennis, M, Elborn, J S
(2005). Neutrophil cell death, activation and bacterial infection in cystic fibrosis. Thorax
60: 659-664
[Abstract]
[Full Text]
-
Ader, F., Le Berre, R., Faure, K., Gosset, P., Epaulard, O., Toussaint, B., Polack, B., Nowak, E., Viget, N. B., Kipnis, E., Guery, B. P.
(2005). Alveolar Response to Pseudomonas aeruginosa: Role of the Type III Secretion System. Infect. Immun.
73: 4263-4271
[Abstract]
[Full Text]
-
Winstanley, C., Kaye, S. B, Neal, T. J, Chilton, H. J, Miksch, S., Hart, C A., and the Microbiology Ophthalmic Group,
(2005). Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis. J Med Microbiol
54: 519-526
[Abstract]
[Full Text]
-
Fink, S. L., Cookson, B. T.
(2005). Apoptosis, Pyroptosis, and Necrosis: Mechanistic Description of Dead and Dying Eukaryotic Cells. Infect. Immun.
73: 1907-1916
[Full Text]
-
Allen, L., Dockrell, D. H., Pattery, T., Lee, D. G., Cornelis, P., Hellewell, P. G., Whyte, M. K. B.
(2005). Pyocyanin Production by Pseudomonas aeruginosa Induces Neutrophil Apoptosis and Impairs Neutrophil-Mediated Host Defenses In Vivo. J. Immunol.
174: 3643-3649
[Abstract]
[Full Text]
-
Linares, J. F., Lopez, J. A., Camafeita, E., Albar, J. P., Rojo, F., Martinez, J. L.
(2005). Overexpression of the Multidrug Efflux Pumps MexCD-OprJ and MexEF-OprN Is Associated with a Reduction of Type III Secretion in Pseudomonas aeruginosa. J. Bacteriol.
187: 1384-1391
[Abstract]
[Full Text]
-
Shaver, C. M., Hauser, A. R.
(2004). Relative Contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to Virulence in the Lung. Infect. Immun.
72: 6969-6977
[Abstract]
[Full Text]
-
Jain, M., Ramirez, D., Seshadri, R., Cullina, J. F., Powers, C. A., Schulert, G. S., Bar-Meir, M., Sullivan, C. L., McColley, S. A., Hauser, A. R.
(2004). Type III Secretion Phenotypes of Pseudomonas aeruginosa Strains Change during Infection of Individuals with Cystic Fibrosis. J. Clin. Microbiol.
42: 5229-5237
[Abstract]
[Full Text]
-
Lanotte, P., Watt, S., Mereghetti, L., Dartiguelongue, N., Rastegar-Lari, A., Goudeau, A., Quentin, R.
(2004). Genetic features of Pseudomonas aeruginosa isolates from cystic fibrosis patients compared with those of isolates from other origins. J Med Microbiol
53: 73-81
[Abstract]
[Full Text]
-
Miyata, S., Casey, M., Frank, D. W., Ausubel, F. M., Drenkard, E.
(2003). Use of the Galleria mellonella Caterpillar as a Model Host To Study the Role of the Type III Secretion System in Pseudomonas aeruginosa Pathogenesis. Infect. Immun.
71: 2404-2413
[Abstract]
[Full Text]
-
Jendrossek, V., Fillon, S., Belka, C., Muller, I., Puttkammer, B., Lang, F.
(2003). Apoptotic Response of Chang Cells to Infection with Pseudomonas aeruginosa Strains PAK and PAO-I: Molecular Ordering of the Apoptosis Signaling Cascade and Role of Type IV Pili. Infect. Immun.
71: 2665-2673
[Abstract]
[Full Text]
-
Esco, M. A., Hazlett, L. D., Kurpakus-Wheater, M.
(2002). Pseudomonas aeruginosa Binds to Extracellular Matrix Deposited by Human Corneal Epithelial Cells. IOVS
43: 3654-3659
[Abstract]
[Full Text]
-
Jacob, T., Lee, R. J., Engel, J. N., Machen, T. E.
(2002). Modulation of Cytosolic Ca2+ Concentration in Airway Epithelial Cells by Pseudomonas aeruginosa. Infect. Immun.
70: 6399-6408
[Abstract]
[Full Text]
-
Dacheux, D., Epaulard, O., de Groot, A., Guery, B., Leberre, R., Attree, I., Polack, B., Toussaint, B.
(2002). Activation of the Pseudomonas aeruginosa Type III Secretion System Requires an Intact Pyruvate Dehydrogenase aceAB Operon. Infect. Immun.
70: 3973-3977
[Abstract]
[Full Text]
-
Hirakata, Y., Srikumar, R., Poole, K., Gotoh, N., Suematsu, T., Kohno, S., Kamihira, S., Hancock, R. E. W., Speert, D. P.
(2002). Multidrug Efflux Systems Play an Important Role in the Invasiveness of Pseudomonas aeruginosa. JEM
196: 109-118
[Abstract]
[Full Text]
-
Lyczak, J. B., Cannon, C. L., Pier, G. B.
(2002). Lung Infections Associated with Cystic Fibrosis. Clin. Microbiol. Rev.
15: 194-222
[Abstract]
[Full Text]
-
Pukatzki, S., Kessin, R. H., Mekalanos, J. J.
(2002). The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA
10.1073/pnas.052704399v1
[Abstract]
[Full Text]
-
Usher, L. R., Lawson, R. A., Geary, I., Taylor, C. J., Bingle, C. D., Taylor, G. W., Whyte, M. K. B.
(2002). Induction of Neutrophil Apoptosis by the Pseudomonas aeruginosa Exotoxin Pyocyanin: A Potential Mechanism of Persistent Infection. J. Immunol.
168: 1861-1868
[Abstract]
[Full Text]
-
Feltman, H., Schulert, G., Khan, S., Jain, M., Peterson, L., Hauser, A. R.
(2001). Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology
147: 2659-2669
[Abstract]
[Full Text]
-
Finck-Barbancon, V., Frank, D. W.
(2001). Multiple Domains Are Required for the Toxic Activity of Pseudomonas aeruginosa ExoU. J. Bacteriol.
183: 4330-4344
[Abstract]
[Full Text]
-
Ha, U., Jin, S.
(2001). Growth Phase-Dependent Invasion of Pseudomonas aeruginosa and Its Survival within HeLa Cells. Infect. Immun.
69: 4398-4406
[Abstract]
[Full Text]
-
Ferguson, M. W., Maxwell, J. A., Vincent, T. S., da Silva, J., Olson, J. C.
(2001). Comparison of the exoS Gene and Protein Expression in Soil and Clinical Isolates of Pseudomonas aeruginosa. Infect. Immun.
69: 2198-2210
[Abstract]
[Full Text]
-
Moss, J., Ehrmantraut, M. E., Banwart, B. D., Frank, D. W., Barbieri, J. T.
(2001). Sera from Adult Patients with Cystic Fibrosis Contain Antibodies to Pseudomonas aeruginosa Type III Apparatus. Infect. Immun.
69: 1185-1188
[Abstract]
[Full Text]
-
Dacheux, D., Attree, I., Toussaint, B.
(2001). Expression of ExsA in trans Confers Type III Secretion System-Dependent Cytotoxicity on Noncytotoxic Pseudomonas aeruginosa Cystic Fibrosis Isolates. Infect. Immun.
69: 538-542
[Abstract]
[Full Text]
-
Pukatzki, S., Kessin, R. H., Mekalanos, J. J.
(2002). The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA
99: 3159-3164
[Abstract]
[Full Text]