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 Kwok, T.
Right arrow Articles by Meyer, T. F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kwok, T.
Right arrow Articles by Meyer, T. F.

 Previous Article  |  Next Article 

Infection and Immunity, April 2002, p. 2108-2120, Vol. 70, No. 4
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.4.2108-2120.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Specific Entry of Helicobacter pylori into Cultured Gastric Epithelial Cells via a Zipper-Like Mechanism

Terry Kwok,1 Steffen Backert,2 Heinz Schwarz,3 Jürgen Berger,3 and Thomas F. Meyer1,2*

Abteilung Infektionsbiologie, Max-Planck-Institut für Biologie,1 Max-Planck-Institut für Entwicklungsbiologie, D-72076 Tübingen,3 Abteilung Molekulare Biologie, Max-Planck-Institut für Infektionsbiologie, D-10117 Berlin, Germany2

Received 13 August 2001/ Returned for modification 16 October 2001/ Accepted 28 December 2001

Although Helicobacter pylori has generally been considered an extracellular pathogen, a number of in vitro infection experiments and biopsy examinations have shown that it is capable of occasionally entering mammalian host cells. Here, we characterized this entry process by using AGS cells as a host cell model. In gentamicin protection-invasion assays, the number of H. pylori colonies recovered was lower than that for Salmonella enterica serovar Typhimurium X22, Escherichia coli expressing InvA, and Yersinia enterocolitica YO:9 grown at 25°C but higher than that for Neisseria gonorrhoeae VP1 and Y. enterocolitica YO:9 grown at 37°C. At the ultrastructural level, the entry process was observed to occur via a zipper-like mechanism. Internalized H. pylori was bound in tight LAMP-1-containing vacuoles in close association with condensed filamentous actin and tyrosine phosphorylation signals. Wortmannin, a potent inhibitor of phosphatidylinositol 3-kinase, and calphostin C, an inhibitor of protein kinase C, both inhibited the entry of H. pylori in a sensitive and dose-dependent manner; however, the level of entry was enhanced by sodium vanadate, an inhibitor of tyrosine phosphatases and ATPases. Furthermore, the cytokine tumor necrosis factor alpha antagonized the entry of H. pylori into AGS cells. Collectively, these results demonstrate that the entry of H. pylori into AGS cells occurs via a zipper-like mechanism which involves various host signal transduction events.


* Corresponding author. Mailing address: Max-Planck-Institut für Infektionsbiologie, Abteilung Molekulare Biologie, Schumannstr. 20/21, D-10117 Berlin, Germany. Phone: 49 30 284 69 400. Fax: 49 30 284 60 401. E-mail: meyer{at}mpiib-berlin.mpg.de.

Editor: E. I. Tuomanen


Infection and Immunity, April 2002, p. 2108-2120, Vol. 70, No. 4
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.4.2108-2120.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Zhou, P., Chandan, V., Liu, X., Chan, K., Altman, E., Li, J. (2009). Microwave-assisted sample preparation for rapid and sensitive analysis of H. pylori lipid A applicable to a single colony. J. Lipid Res. 50: 1936-1944 [Abstract] [Full Text]  
  • Agarwal, V., Hammerschmidt, S. (2009). Cdc42 and the Phosphatidylinositol 3-Kinase-Akt Pathway Are Essential for PspC-mediated Internalization of Pneumococci by Respiratory Epithelial Cells. J. Biol. Chem. 284: 19427-19436 [Abstract] [Full Text]  
  • Burnham, C.-A. D., Shokoples, S. E., Tyrrell, G. J. (2007). Invasion of HeLa cells by group B streptococcus requires the phosphoinositide-3-kinase signalling pathway and modulates phosphorylation of host-cell Akt and glycogen synthase kinase-3. Microbiology 153: 4240-4252 [Abstract] [Full Text]  
  • Bourzac, K. M., Botham, C. M., Guillemin, K. (2007). Helicobacter pylori CagA Induces AGS Cell Elongation through a Cell Retraction Defect That Is Independent of Cdc42, Rac1, and Arp2/3. Infect. Immun. 75: 1203-1213 [Abstract] [Full Text]  
  • Terebiznik, M. R., Vazquez, C. L., Torbicki, K., Banks, D., Wang, T., Hong, W., Blanke, S. R., Colombo, M. I., Jones, N. L. (2006). Helicobacter pylori VacA Toxin Promotes Bacterial Intracellular Survival in Gastric Epithelial Cells. Infect. Immun. 74: 6599-6614 [Abstract] [Full Text]  
  • Algood, H. M. S., Cover, T. L. (2006). Helicobacter pylori Persistence: an Overview of Interactions between H. pylori and Host Immune Defenses. Clin. Microbiol. Rev. 19: 597-613 [Abstract] [Full Text]  
  • Lambotin, M., Hoffmann, I., Laran-Chich, M.-P., Nassif, X., Couraud, P. O., Bourdoulous, S. (2005). Invasion of endothelial cells by Neisseria meningitidis requires cortactin recruitment by a phosphoinositide-3-kinase/Rac1 signalling pathway triggered by the lipo-oligosaccharide. J. Cell Sci. 118: 3805-3816 [Abstract] [Full Text]  
  • Peek, R. M. Jr. (2005). Events at the Host-Microbial Interface of the Gastrointestinal Tract IV. The pathogenesis of Helicobacter pylori persistence. Am. J. Physiol. Gastrointest. Liver Physiol. 289: G8-G12 [Abstract] [Full Text]  
  • Brandt, S., Kwok, T., Hartig, R., Konig, W., Backert, S. (2005). NF-{kappa}B activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl. Acad. Sci. USA 102: 9300-9305 [Abstract] [Full Text]  
  • Kierbel, A., Gassama-Diagne, A., Mostov, K., Engel, J. N. (2005). The Phosphoinositol-3-Kinase-Protein Kinase B/Akt Pathway Is Critical for Pseudomonas aeruginosa Strain PAK Internalization. Mol. Biol. Cell 16: 2577-2585 [Abstract] [Full Text]  
  • Oh, J. D., Karam, S. M., Gordon, J. I. (2005). Intracellular Helicobacter pylori in gastric epithelial progenitors. Proc. Natl. Acad. Sci. USA 102: 5186-5191 [Abstract] [Full Text]  
  • Servin, A. L. (2005). Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli. Clin. Microbiol. Rev. 18: 264-292 [Abstract] [Full Text]  
  • Enarsson, K., Brisslert, M., Backert, S., Quiding-Jarbrink, M. (2005). Helicobacter pylori Induces Transendothelial Migration of Activated Memory T Cells. Infect. Immun. 73: 761-769 [Abstract] [Full Text]  
  • Clyne, M., Drumm, B. (2004). Helicobacter pylori Infection of Human and Murine Primary Gastric Cells. Infect. Immun. 72: 5464-5469 [Abstract] [Full Text]  
  • Chen, X.-M., Splinter, P. L., Tietz, P. S., Huang, B. Q., Billadeau, D. D., LaRusso, N. F. (2004). Phosphatidylinositol 3-Kinase and Frabin Mediate Cryptosporidium parvum Cellular Invasion via Activation of Cdc42. J. Biol. Chem. 279: 31671-31678 [Abstract] [Full Text]  
  • Kansau, I., Berger, C., Hospital, M., Amsellem, R., Nicolas, V., Servin, A. L., Bernet-Camard, M.-F. (2004). Zipper-Like Internalization of Dr-Positive Escherichia coli by Epithelial Cells Is Preceded by an Adhesin-Induced Mobilization of Raft-Associated Molecules in the Initial Step of Adhesion. Infect. Immun. 72: 3733-3742 [Abstract] [Full Text]  
  • Woolsey, A. M., Sunwoo, L., Petersen, C. A., Brachmann, S. M., Cantley, L. C., Burleigh, B. A. (2003). Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J. Cell Sci. 116: 3611-3622 [Abstract] [Full Text]  
  • Kersulyte, D., Velapatino, B., Mukhopadhyay, A. K., Cahuayme, L., Bussalleu, A., Combe, J., Gilman, R. H., Berg, D. E. (2003). Cluster of Type IV Secretion Genes in Helicobacter pylori's Plasticity Zone. J. Bacteriol. 185: 3764-3772 [Abstract] [Full Text]  
  • Hynes, S. O., Teneberg, S., Roche, N., Wadstrom, T. (2003). Glycoconjugate Binding of Gastric and Enterohepatic Helicobacter spp.. Infect. Immun. 71: 2976-2980 [Abstract] [Full Text]  
  • Booth, J. W., Telio, D., Liao, E. H., McCaw, S. E., Matsuo, T., Grinstein, S., Gray-Owen, S. D. (2003). Phosphatidylinositol 3-Kinases in Carcinoembryonic Antigen-related Cellular Adhesion Molecule-mediated Internalization of Neisseria gonorrhoeae. J. Biol. Chem. 278: 14037-14045 [Abstract] [Full Text]  
  • Lundin, A., Nilsson, C., Gerhard, M., Andersson, D. I., Krabbe, M., Engstrand, L. (2003). The NudA Protein in the Gastric Pathogen Helicobacter pylori Is an Ubiquitous and Constitutively Expressed Dinucleoside Polyphosphate Hydrolase. J. Biol. Chem. 278: 12574-12578 [Abstract] [Full Text]  
  • Dubreuil, J. D., Giudice, G. D., Rappuoli, R. (2002). Helicobacter pylori Interactions with Host Serum and Extracellular Matrix Proteins: Potential Role in the Infectious Process. Microbiol. Mol. Biol. Rev. 66: 617-629 [Abstract] [Full Text]