This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kahl, B. C.
Right arrow Articles by Cheung, A. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kahl, B. C.
Right arrow Articles by Cheung, A. L.

 Previous Article  |  Next Article 

Infection and Immunity, September 2000, p. 5385-5392, Vol. 68, No. 9
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Staphylococcus aureus RN6390 Replicates and Induces Apoptosis in a Pulmonary Epithelial Cell Line

Barbara C. Kahl,1 Mark Goulian,2 Willem van Wamel,3 Mathias Herrmann,4 Sanford M. Simon,2 Gilla Kaplan,5 Georg Peters,4 and Ambrose L. Cheung3,*

Laboratory of Bacterial Pathogenesis and Immunology,1 Laboratory of Cellular Biophysics,2 and Laboratory of Cellular Physiology and Immunology,5 Rockfeller University, New York, New York 10021; Department of Microbiology, Dartmouth Medical School, Hanover, New Hampshire 032553; and Medical Microbiology, Westfälische Wilhelms Universität Münster, D-48149 Münster, Germany4

Received 20 March 2000/Returned for modification 10 May 2000/Accepted 26 May 2000

Staphylococcus aureus frequently colonizes the airways of patients with compromised airway defenses (e.g., cystic fibrosis [CF] patients) for extended periods. Persistent and relapsing infections may be related to live S. aureus bacteria actively residing inside epithelial cells. In this study, we infected a respiratory epithelial cell line, which was derived from a CF patient, with S. aureus RN6390. Internalization of S. aureus was found to be time and dose dependent and could be blocked by cytochalasin D. Transmission electron microscopy revealed that internalized bacteria resided within endocytic vacuoles without any evidence of lysosomal fusion in a 24-h period. The results of internalization experiments and time-lapse fluorescence microscopy of epithelial cells infected with green fluorescent S. aureus indicate that, after an initial lag period of 7 to 9 h, intracellular bacteria began to replicate, with three to five divisions in a 24-h period, leading to apoptosis of infected cells. Induction of apoptosis required bacterial internalization and is associated with intracellular replication. The slow and gradual replication of S. aureus inside epithelial cells hints at the role of host factors or signals in bacterial growth and further suggests possible cross talk between host cells and S. aureus.

* Corresponding author. Mailing address: Department of Microbiology, Dartmouth Medical School, Hanover, NH 03255. Phone: (603) 650-1340. Fax: (603) 650-1318. E-mail: Ambrose.Cheung{at}Dartmouth.edu.

Infection and Immunity, September 2000, p. 5385-5392, Vol. 68, No. 9
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Tamber, S., Cheung, A. L. (2009). SarZ Promotes the Expression of Virulence Factors and Represses Biofilm Formation by Modulating SarA and agr in Staphylococcus aureus. Infect. Immun. 77: 419-428 [Abstract] [Full Text]  
  • Trotonda, M. P., Tamber, S., Memmi, G., Cheung, A. L. (2008). MgrA Represses Biofilm Formation in Staphylococcus aureus. Infect. Immun. 76: 5645-5654 [Abstract] [Full Text]  
  • Memmi, G., Filipe, S. R., Pinho, M. G., Fu, Z., Cheung, A. (2008). Staphylococcus aureus PBP4 Is Essential for {beta}-Lactam Resistance in Community-Acquired Methicillin-Resistant Strains. Antimicrob. Agents Chemother. 52: 3955-3966 [Abstract] [Full Text]  
  • Whiston, E. A., Sugi, N., Kamradt, M. C., Sack, C., Heimer, S. R., Engelbert, M., Wawrousek, E. F., Gilmore, M. S., Ksander, B. R., Gregory, M. S. (2008). {alpha}B-Crystallin Protects Retinal Tissue during Staphylococcus aureus- Induced Endophthalmitis. Infect. Immun. 76: 1781-1790 [Abstract] [Full Text]  
  • Li, D., Cheung, A. (2008). Repression of hla by rot Is Dependent on sae in Staphylococcus aureus. Infect. Immun. 76: 1068-1075 [Abstract] [Full Text]  
  • Rani, S. A., Pitts, B., Beyenal, H., Veluchamy, R. A., Lewandowski, Z., Davison, W. M., Buckingham-Meyer, K., Stewart, P. S. (2007). Spatial Patterns of DNA Replication, Protein Synthesis, and Oxygen Concentration within Bacterial Biofilms Reveal Diverse Physiological States. J. Bacteriol. 189: 4223-4233 [Abstract] [Full Text]  
  • Manna, A. C., Ray, B. (2007). Regulation and characterization of rot transcription in Staphylococcus aureus. Microbiology 153: 1538-1545 [Abstract] [Full Text]  
  • Matsumoto, Y., Kaito, C., Morishita, D., Kurokawa, K., Sekimizu, K. (2007). Regulation of Exoprotein Gene Expression by the Staphylococcus aureus cvfB Gene. Infect. Immun. 75: 1964-1972 [Abstract] [Full Text]  
  • Schnaith, A., Kashkar, H., Leggio, S. A., Addicks, K., Kronke, M., Krut, O. (2007). Staphylococcus aureus Subvert Autophagy for Induction of Caspase-independent Host Cell Death. J. Biol. Chem. 282: 2695-2706 [Abstract] [Full Text]  
  • Peerschke, E. I. B., Bayer, A. S., Ghebrehiwet, B., Xiong, Y. Q. (2006). gC1qR/p33 Blockade Reduces Staphylococcus aureus Colonization of Target Tissues in an Animal Model of Infective Endocarditis.. Infect. Immun. 74: 4418-4423 [Abstract] [Full Text]  
  • Palma, M., Bayer, A., Kupferwasser, L. I., Joska, T., Yeaman, M. R., Cheung, A. (2006). Salicylic Acid Activates Sigma Factor B by rsbU-Dependent and -Independent Mechanisms.. J. Bacteriol. 188: 5896-5903 [Abstract] [Full Text]  
  • Buzzola, F. R., Barbagelata, M. S., Caccuri, R. L., Sordelli, D. O. (2006). Attenuation and Persistence of and Ability To Induce Protective Immunity to a Staphylococcus aureus aroA Mutant in Mice.. Infect. Immun. 74: 3498-3506 [Abstract] [Full Text]  
  • Manna, A. C., Cheung, A. L. (2006). Expression of SarX, a Negative Regulator of agr and Exoprotein Synthesis, Is Activated by MgrA in Staphylococcus aureus.. J. Bacteriol. 188: 4288-4299 [Abstract] [Full Text]  
  • Jarry, T. M., Cheung, A. L. (2006). Staphylococcus aureus Escapes More Efficiently from the Phagosome of a Cystic Fibrosis Bronchial Epithelial Cell Line than from Its Normal Counterpart.. Infect. Immun. 74: 2568-2577 [Abstract] [Full Text]  
  • Escotte, S., Al Alam, D., Le Naour, R., Puchelle, E., Guenounou, M., Gangloff, S. C. (2006). T Cell Chemotaxis and Chemokine Release after Staphylococcus aureus Interaction with Polarized Airway Epithelium. Am. J. Respir. Cell Mol. Bio. 34: 348-354 [Abstract] [Full Text]  
  • Garver, L. S., Wu, J., Wu, L. P. (2006). The peptidoglycan recognition protein PGRP-SC1a is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila. Proc. Natl. Acad. Sci. USA 103: 660-665 [Abstract] [Full Text]  
  • Fournier, B., Philpott, D. J. (2005). Recognition of Staphylococcus aureus by the Innate Immune System. Clin. Microbiol. Rev. 18: 521-540 [Abstract] [Full Text]  
  • Ingavale, S., van Wamel, W., Luong, T. T., Lee, C. Y., Cheung, A. L. (2005). Rat/MgrA, a Regulator of Autolysis, Is a Regulator of Virulence Genes in Staphylococcus aureus. Infect. Immun. 73: 1423-1431 [Abstract] [Full Text]  
  • Francolini, I., Norris, P., Piozzi, A., Donelli, G., Stoodley, P. (2004). Usnic Acid, a Natural Antimicrobial Agent Able To Inhibit Bacterial Biofilm Formation on Polymer Surfaces. Antimicrob. Agents Chemother. 48: 4360-4365 [Abstract] [Full Text]  
  • da Silva, M. C. A., Zahm, J.-M., Gras, D., Bajolet, O., Abely, M., Hinnrasky, J., Milliot, M., de Assis, M. C., Hologne, C., Bonnet, N., Merten, M., Plotkowski, M. C., Puchelle, E. (2004). Dynamic interaction between airway epithelial cells and Staphylococcus aureus. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L543-L551 [Abstract] [Full Text]  
  • Manna, A. C., Ingavale, S. S., Maloney, M., van Wamel, W., Cheung, A. L. (2004). Identification of sarV (SA2062), a New Transcriptional Regulator, Is Repressed by SarA and MgrA (SA0641) and Involved in the Regulation of Autolysis in Staphylococcus aureus. J. Bacteriol. 186: 5267-5280 [Abstract] [Full Text]  
  • Yilmaz, O., Jungas, T., Verbeke, P., Ojcius, D. M. (2004). Activation of the Phosphatidylinositol 3-Kinase/Akt Pathway Contributes to Survival of Primary Epithelial Cells Infected with the Periodontal Pathogen Porphyromonas gingivalis. Infect. Immun. 72: 3743-3751 [Abstract] [Full Text]  
  • Krut, O., Sommer, H., Kronke, M. (2004). Antibiotic-induced persistence of cytotoxic Staphylococcus aureus in non-phagocytic cells. J Antimicrob Chemother 53: 167-173 [Abstract] [Full Text]  
  • Marouni, M. J., Sela, S. (2004). Fate of Streptococcus pyogenes and epithelial cells following internalization. J Med Microbiol 53: 1-7 [Abstract] [Full Text]  
  • Rothfork, J. M., Dessus-Babus, S., Van Wamel, W. J. B., Cheung, A. L., Gresham, H. D. (2003). Fibrinogen Depletion Attenuates Staphyloccocus aureus Infection by Preventing Density-Dependent Virulence Gene Up-Regulation. J. Immunol. 171: 5389-5395 [Abstract] [Full Text]  
  • Kahl, B. C., Duebbers, A., Lubritz, G., Haeberle, J., Koch, H. G., Ritzerfeld, B., Reilly, M., Harms, E., Proctor, R. A., Herrmann, M., Peters, G. (2003). Population Dynamics of Persistent Staphylococcus aureus Isolated from the Airways of Cystic Fibrosis Patients during a 6-Year Prospective Study. J. Clin. Microbiol. 41: 4424-4427 [Abstract] [Full Text]  
  • Seral, C., Van Bambeke, F., Tulkens, P. M. (2003). Quantitative Analysis of Gentamicin, Azithromycin, Telithromycin, Ciprofloxacin, Moxifloxacin, and Oritavancin (LY333328) Activities against Intracellular Staphylococcus aureus in Mouse J774 Macrophages. Antimicrob. Agents Chemother. 47: 2283-2292 [Abstract] [Full Text]  
  • Krut, O., Utermohlen, O., Schlossherr, X., Kronke, M. (2003). Strain-Specific Association of Cytotoxic Activity and Virulence of Clinical Staphylococcus aureus Isolates. Infect. Immun. 71: 2716-2723 [Abstract] [Full Text]  
  • Manna, A. C., Cheung, A. L. (2003). sarU, a sarA Homolog, Is Repressed by SarT and Regulates Virulence Genes in Staphylococcus aureus. Infect. Immun. 71: 343-353 [Abstract] [Full Text]  
  • Leid, J. G., Shirtliff, M. E., Costerton, J. W., Stoodley, a. P. (2002). Human Leukocytes Adhere to, Penetrate, and Respond to Staphylococcus aureus Biofilms. Infect. Immun. 70: 6339-6345 [Abstract] [Full Text]  
  • Shirtliff, M. E., Mader, J. T. (2002). Acute Septic Arthritis. Clin. Microbiol. Rev. 15: 527-544 [Abstract] [Full Text]  
  • Gomez, M. I., Sordelli, D. O., Buzzola, F. R., Garcia, V. E. (2002). Induction of Cell-Mediated Immunity to Staphylococcus aureus in the Mouse Mammary Gland by Local Immunization with a Live Attenuated Mutant. Infect. Immun. 70: 4254-4260 [Abstract] [Full Text]  
  • Jett, B. D., Gilmore, M. S. (2002). Internalization of Staphylococcus aureus by Human Corneal Epithelial Cells: Role of Bacterial Fibronectin-Binding Protein and Host Cell Factors. Infect. Immun. 70: 4697-4700 [Abstract] [Full Text]  
  • Somerville, G. A., Beres, S. B., Fitzgerald, J. R., DeLeo, F. R., Cole, R. L., Hoff, J. S., Musser, J. M. (2002). In Vitro Serial Passage of Staphylococcus aureus: Changes in Physiology, Virulence Factor Production, and agr Nucleotide Sequence. J. Bacteriol. 184: 1430-1437 [Abstract] [Full Text]  
  • Bateman, B. T., Donegan, N. P., Jarry, T. M., Palma, M., Cheung, A. L. (2001). Evaluation of a Tetracycline-Inducible Promoter in Staphylococcus aureus In Vitro and In Vivo and Its Application in Demonstrating the Role of sigB in Microcolony Formation. Infect. Immun. 69: 7851-7857 [Abstract] [Full Text]  
  • Bantel, H., Sinha, B., Domschke, W., Peters, G., Schulze-Osthoff, K., Janicke, R. U. (2001). {alpha}-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. JCB 155: 637-648 [Abstract] [Full Text]  
  • Kielian, T., Cheung, A., Hickey, W. F. (2001). Diminished Virulence of an Alpha-Toxin Mutant of Staphylococcus aureus in Experimental Brain Abscesses. Infect. Immun. 69: 6902-6911 [Abstract] [Full Text]  
  • Qazi, S. N. A., Counil, E., Morrissey, J., Rees, C. E. D., Cockayne, A., Winzer, K., Chan, W. C., Williams, P., Hill, P. J. (2001). agr Expression Precedes Escape of Internalized Staphylococcus aureus from the Host Endosome. Infect. Immun. 69: 7074-7082 [Abstract] [Full Text]  
  • Jones, C. H., Bolken, T. C., Jones, K. F., Zeller, G. O., Hruby, D. E. (2001). Conserved DegP Protease in Gram-Positive Bacteria Is Essential for Thermal and Oxidative Tolerance and Full Virulence in Streptococcus pyogenes. Infect. Immun. 69: 5538-5545 [Abstract] [Full Text]  
  • Schmidt, K. A., Manna, A. C., Gill, S., Cheung, A. L. (2001). SarT, a Repressor of {alpha}-Hemolysin in Staphylococcus aureus. Infect. Immun. 69: 4749-4758 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»