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Infection and Immunity, July 2004, p. 3733-3742, Vol. 72, No. 7
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.7.3733-3742.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

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

Imad Kansau,1 Cédric Berger,1 Maxime Hospital,1 Raymonde Amsellem,1 Valérie Nicolas,2 Alain L. Servin,1* and Marie-Françoise Bernet-Camard1

Institut National de la Santé et de la Recherche Médicale (INSERM), Unité 510,1 Imagerie Cellulaire, IFR75-ISIT, Faculté de Pharmacie Paris XI, F-92296 Châtenay-Malabry, France2

Received 25 September 2003/ Returned for modification 18 December 2003/ Accepted 26 February 2004

We undertook a study of the mechanism by which Dr-positive bacteria invade epithelial cells. Our findings show that Dr-positive bacteria enter via a zipper-like mechanism that is independent of the Dr-induced mobilization of F-actin and of the signaling molecules that control Dr-induced F-actin rearrangements. We also observed that Dr-positive IH11128 bacteria entered cells that were positive for the caveola marker VIP21/caveolin (HeLa and Caco-2/Cav-1 cells) to the same extent as those that were not (parental Caco-2 cells). Using fluorescence labeling and confocal laser scanning microscopy, we provide evidence that during the adhesion step, the {alpha}5ß1 integrin, which plays a pivotal role in Afa/Dr diffusely adhering Escherichia coli bacterial entry, is mobilized around adhering Dr-positive bacteria. We show that the receptor for Afa/Dr adhesins, glycosylphosphatidylinositol-anchored CD55; the raft marker, ganglioside GM1; and VIP21/caveolin are all recruited around adhering Dr-positive bacteria. We also observed that extracting membrane cholesterol with methyl-ß-cyclodextrin (MBCD) did not affect the recruitment of CD55, GM1, or ß1 integrin to adhering Dr-positive bacteria. In contrast, extracting or changing membrane-bound cholesterol by means of drugs that modify lipid rafts (MBCD, filipin III, or mevalonate plus lovastatin plus MBCD) inhibited the entry of Dr-positive IH11128 both into cells that expressed VIP21/caveolin (HeLa and Caco-2/Cav-1 cells) and into those that did not (parental Caco-2 cells). Finally, restoring cholesterol within the cell membrane of MBCD-treated cells restored Dr-positive IH11128 internalization.

* Corresponding author. Mailing address: Unité 510 INSERM, Faculté de Pharmacie, Paris XI, F-92296 Châtenay-Malabry, France. Phone: 33-1-46-83-56-61. Fax: 33-1-46-83-58-44. E-mail: alain.servin{at}cep.u-psud.fr.

Editor: V. J. DiRita

Infection and Immunity, July 2004, p. 3733-3742, Vol. 72, No. 7
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.7.3733-3742.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Guignot, J., Hudault, S., Kansau, I., Chau, I., Servin, A. L. (2009). Human Decay-Accelerating Factor and CEACAM Receptor-Mediated Internalization and Intracellular Lifestyle of Afa/Dr Diffusely Adhering Escherichia coli in Epithelial Cells. Infect. Immun. 77: 517-531 [Abstract] [Full Text]  
  • Korotkova, N., Yarova-Yarovaya, Y., Tchesnokova, V., Yazvenko, N., Carl, M. A., Stapleton, A. E., Moseley, S. L. (2008). Escherichia coli DraE Adhesin-Associated Bacterial Internalization by Epithelial Cells Is Promoted Independently by Decay-Accelerating Factor and Carcinoembryonic Antigen-Related Cell Adhesion Molecule Binding and Does Not Require the DraD Invasin. Infect. Immun. 76: 3869-3880 [Abstract] [Full Text]  
  • Korotkova, N., Cota, E., Lebedin, Y., Monpouet, S., Guignot, J., Servin, A. L., Matthews, S., Moseley, S. L. (2006). A Subfamily of Dr Adhesins of Escherichia coli Bind Independently to Decay-accelerating Factor and the N-domain of Carcinoembryonic Antigen. J. Biol. Chem. 281: 29120-29130 [Abstract] [Full Text]  
  • Goluszko, P., Nowicki, B. (2005). Membrane Cholesterol: a Crucial Molecule Affecting Interactions of Microbial Pathogens with Mammalian Cells. Infect. Immun. 73: 7791-7796 [Full Text]  
  • Servin, A. L. (2005). Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli. Clin. Microbiol. Rev. 18: 264-292 [Abstract] [Full Text]  


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