Role of Decay-Accelerating Factor Domains and Anchorage in Internalization of Dr-Fimbriated Escherichia coli

doi:10.1128/IAI.68.3.1391-1399.2000

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Selvarangan, R.
	Articles by Nowicki, B.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Selvarangan, R.
	Articles by Nowicki, B.

Previous Article | Next Article

Infection and Immunity, March 2000, p. 1391-1399, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Role of Decay-Accelerating Factor Domains and Anchorage in Internalization of Dr-Fimbriated Escherichia coli

R. Selvarangan,¹^,² P. Goluszko,¹ V. Popov,³ J. Singhal,¹ T. Pham,¹^,² D. M. Lublin,⁴ S. Nowicki,¹^,² and B. Nowicki¹^,²^,^*

Department of Obstetrics & Gynecology,¹ Microbiology & Immunology,² and Pathology,³ The University of Texas Medical Branch, Galveston, Texas 77555-1062, and Department of Pathology, Division of Laboratory Medicine, Washington University, St. Louis, Missouri 63110⁴

Received 11 October 1999/Returned for modification 18 November 1999/Accepted 2 December 1999

Dr-fimbriated Escherichia coli capable of invading epithelial cells recognizes human decay-accelerating factor (DAF) as itscellular receptor. The role of extracellular domains and the glycosylphosphatidylinositolanchor of DAF in the process of internalization of Dr⁺ E. coli was characterized in a cell-cell interaction model. Bindingof Dr⁺ E. coli to the short consensus repeat 3 domain of DAF expressedby Chinese hamster ovary cells was critical for internalizationto occur. Deletion of short consensus repeat 3 domain or replacementof Ser¹⁶⁵ by Leu in this domain, or the use of a monoclonal antibody tothis region abolished internalization. Replacing the glycosylphosphatidylinositolanchor of DAF with the transmembrane anchor of membrane cofactorprotein or HLA-B44 resulted in abolition or reduction of internalizationrespectively. Cells expressing glycosylphosphatidylinositol-anchoredDAF but not the transmembrane-anchored DAF internalized Dr⁺ E. coli through a glycolipid pathway, since the former cellswere more sensitive to inhibition by methyl- $beta$ -cyclodextrin, asterol-chelating agent. Electron microscopic studies revealedthat the intracellular vacuoles containing the internalized Dr⁺ E. coli were morphologically distinct between the anchor variantsof DAF. The cells expressing glycosylphosphatidylinositol-anchoredDAF contained a single bacterium in tight-fitting vacuoles, whilethe cells expressing transmembrane-anchored DAF contained multiple(two or three) bacteria in spacious phagosomes. This finding suggeststhat distinct postendocytic events operate in the cells expressinganchor variants of DAF. We provide direct evidence for the DAF-mediatedinternalization of Dr⁺ E. coli and demonstrate the significance of the glycosylphosphatidylinositolanchor, which determines the ability and efficiency of the internalizationevent.

^* Corresponding author. Mailing address: Department of Obstetrics and Gynecology and Microbiology and Immunology, 301 UniversityBlvd., University of Texas Medical Branch, Galveston, TX 77555-1062.Phone: (409) 772-7599. Fax: (409) 747-0475. E-mail: bnowicki{at}utmb.edu.

Infection and Immunity, March 2000, p. 1391-1399, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

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]
O'Brien, D. P., Israel, D. A., Krishna, U., Romero-Gallo, J., Nedrud, J., Medof, M. E., Lin, F., Redline, R., Lublin, D. M., Nowicki, B. J., Franco, A. T., Ogden, S., Williams, A. D., Polk, D. B., Peek, R. M. Jr. (2006). The Role of Decay-accelerating Factor as a Receptor for Helicobacter pylori and a Mediator of Gastric Inflammation. J. Biol. Chem. 281: 13317-13323 [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]
Wroblewska-Seniuk, K., Selvarangan, R., Hart, A., Pladzyk, R., Goluszko, P., Jafari, A., du Merle, L., Nowicki, S., Yallampalli, C., Le Bouguenec, C., Nowicki, B. (2005). Dra/AfaE Adhesin of Uropathogenic Dr/Afa+ Escherichia coli Mediates Mortality in Pregnant Rats. Infect. Immun. 73: 7597-7601 [Abstract] [Full Text]
Das, M., Hart-Van Tassell, A., Urvil, P. T., Lea, S., Pettigrew, D., Anderson, K. L., Samet, A., Kur, J., Matthews, S., Nowicki, S., Popov, V., Goluszko, P., Nowicki, B. J. (2005). Hydrophilic Domain II of Escherichia coli Dr Fimbriae Facilitates Cell Invasion. Infect. Immun. 73: 6119-6126 [Abstract] [Full Text]
Servin, A. L. (2005). Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli. Clin. Microbiol. Rev. 18: 264-292 [Abstract] [Full Text]
Cohen, A. W., Hnasko, R., Schubert, W., Lisanti, M. P. (2004). Role of Caveolae and Caveolins in Health and Disease. Physiol. Rev. 84: 1341-1379 [Abstract] [Full Text]
Selvarangan, R., Goluszko, P., Singhal, J., Carnoy, C., Moseley, S., Hudson, B., Nowicki, S., Nowicki, B. (2004). Interaction of Dr Adhesin with Collagen Type IV Is a Critical Step in Escherichia coli Renal Persistence. Infect. Immun. 72: 4827-4835 [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]
Fang, L., Nowicki, B. J., Urvil, P., Goluszko, P., Nowicki, S., Young, S. L., Yallampalli, C. (2004). Epithelial Invasion by Escherichia coli Bearing Dr Fimbriae Is Controlled by Nitric Oxide-Regulated Expression of CD55. Infect. Immun. 72: 2907-2914 [Abstract] [Full Text]
Stuart, A. D., Eustace, H. E., McKee, T. A., Brown, T. D. K. (2002). A Novel Cell Entry Pathway for a DAF-Using Human Enterovirus Is Dependent on Lipid Rafts. J. Virol. 76: 9307-9322 [Abstract] [Full Text]
Goluszko, P., Niesel, D., Nowicki, B., Selvarangan, R., Nowicki, S., Hart, A., Pawelczyk, E., Das, M., Urvil, P., Hasan, R. (2001). Dr Operon-Associated Invasiveness of Escherichia coli from Pregnant Patients with Pyelonephritis. Infect. Immun. 69: 4678-4680 [Abstract] [Full Text]
Guignot, J., Bernet-Camard, M.-F., Pous, C., Plancon, L., Le Bouguenec, C., Servin, A. L. (2001). Polarized Entry of Uropathogenic Afa/Dr Diffusely Adhering Escherichia coli Strain IH11128 into Human Epithelial Cells: Evidence for {alpha}5{beta}1 Integrin Recognition and Subsequent Internalization through a Pathway Involving Caveolae and Dynamic Unstable Microtubules. Infect. Immun. 69: 1856-1868 [Abstract] [Full Text]
Guignot, J., Peiffer, I., Bernet-Camard, M.-F., Lublin, D. M., Carnoy, C., Moseley, S. L., Servin, A. L. (2000). Recruitment of CD55 and CD66e Brush Border-Associated Glycosylphosphatidylinositol-Anchored Proteins by Members of the Afa/Dr Diffusely Adhering Family of Escherichia coli That Infect the Human Polarized Intestinal Caco-2/TC7 Cells. Infect. Immun. 68: 3554-3563 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

Microbiol. Mol. Biol. Rev.	Clin. Vaccine Immunol.	All ASM Journals