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Journal of Virology, September 1998, p. 7228-7236, Vol. 72, No. 9
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Rotavirus Infection Reduces Sucrase-Isomaltase Expression in Human Intestinal Epithelial Cells by Perturbing Protein Targeting and Organization of Microvillar Cytoskeleton

Nathalie Jourdan,1 Jean Philippe Brunet,1 Catherine Sapin,2 Anne Blais,1 Jacqueline Cotte-Laffitte,1 Françoise Forestier,1 Anne-Marie Quero,1 Germain Trugnan,2 and Alain L. Servin1,*

Institut National de la Santé et de la Recherche Médicale, CJF 94 07, Pathogénie Cellulaire et Moléculaire des Microorganismes Entérovirulents, Faculté de Pharmacie, Université Paris XI, 92296 Chatenay-Malabry Cedex,1 and CJF 96 07, Signalisation Moléculaire et Physiopathologie de l'Adressage des Protéines dans les Cellules Épithéliales, Faculté de Médecine Saint Antoine, Université Paris VI, 75012 Paris,2 France

Received 17 March 1998/Accepted 29 May 1998

Rotavirus infection is the most common cause of severe infantile gastroenteritis worldwide. These viruses infect mature enterocytes of the small intestine and cause structural and functional damage, including a reduction in disaccharidase activity. It was previously hypothesized that reduced disaccharidase activity resulted from the destruction of rotavirus-infected enterocytes at the villus tips. However, this pathophysiological model cannot explain situations in which low disaccharidase activity is observed when rotavirus-infected intestine exhibits few, if any, histopathologic changes. In a previous study, we demonstrated that the simian rotavirus strain RRV replicated in and was released from human enterocyte-like Caco-2 cells without cell destruction (N. Jourdan, M. Maurice, D. Delautier, A. M. Quero, A. L. Servin, and G. Trugnan, J. Virol. 71:8268-8278, 1997). In the present study, to reinvestigate disaccharidase expression during rotavirus infection, we studied sucrase-isomaltase (SI) in RRV-infected Caco-2 cells. We showed that SI activity and apical expression were specifically and selectively decreased by RRV infection without apparent cell destruction. Using pulse-chase experiments and cell surface biotinylation, we demonstrated that RRV infection did not affect SI biosynthesis, maturation, or stability but induced the blockade of SI transport to the brush border. Using confocal laser scanning microscopy, we showed that RRV infection induces important alterations of the cytoskeleton that correlate with decreased SI apical surface expression. These results lead us to propose an alternate model to explain the pathophysiology associated with rotavirus infection.

* Corresponding author. Mailing address: CJF INSERM 94 07, Faculté de Pharmacie, 5 rue J. B. Clément, 92296 Chatenay-Malabry Cedex, France. Phone and fax: 33-1 46 83 56 61. E-mail: alain.servin{at}cep.u-psud.fr.

Journal of Virology, September 1998, p. 7228-7236, Vol. 72, No. 9
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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