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Journal of Virology, March 2000, p. 2323-2332, Vol. 74, No. 5
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Rotavirus Infection Induces an Increase in Intracellular Calcium Concentration in Human Intestinal Epithelial Cells: Role in Microvillar Actin Alteration

Jean-Philippe Brunet, Jacqueline Cotte-Laffitte, Catherine Linxe, Anne-Marie Quero, Monique Géniteau-Legendre, and Alain Servin*

Institut National de la Santé et de la Recherche Médicale, Unité 510, Pathogènes et Fonctions des Cellules Épithéliales Polarisées, Faculté de Pharmacie, Université Paris XI, 92296 Châtenay-Malabry cedex, France

Received 14 September 1999/Accepted 6 December 1999

Rotaviruses, which infect mature enterocytes of the small intestine, are recognized as the most important cause of viral gastroenteritis in young children. We have previously reported that rotavirus infection induces microvillar F-actin disassembly in human intestinal epithelial Caco-2 cells (N. Jourdan, J. P. Brunet, C. Sapin, A. Blais, J. Cotte-Laffitte, F. Forestier, A. M. Quero, G. Trugnan, and A. L. Servin, J. Virol. 72:7228-7236, 1998). In this study, to determine the mechanism responsible for rotavirus-induced F-actin alteration, we investigated the effect of infection on intracellular calcium concentration ([Ca2+]i) in Caco-2 cells, since Ca2+ is known to be a determinant factor for actin cytoskeleton regulation. As measured by quin2 fluorescence, viral replication induced a progressive increase in [Ca2+]i from 7 h postinfection, which was shown to be necessary and sufficient for microvillar F-actin disassembly. During the first hours of infection, the increase in [Ca2+]i was related only to an increase in Ca2+ permeability of plasmalemma. At a late stage of infection, [Ca2+]i elevation was due to both extracellular Ca2+ influx and Ca2+ release from the intracellular organelles, mainly the endoplasmic reticulum (ER). We noted that at this time the [Ca2+]i increase was partially related to a phospholipase C (PLC)-dependent mechanism, which probably explains the Ca2+ release from the ER. We also demonstrated for the first time that viral proteins or peptides, released into culture supernatants of rotavirus-infected Caco-2 cells, induced a transient increase in [Ca2+]i of uninfected Caco-2 cells, by a PLC-dependent efflux of Ca2+ from the ER and by extracellular Ca2+ influx. These supernatants induced a Ca2+-dependent microvillar F-actin alteration in uninfected Caco-2 cells, thus participating in rotavirus pathogenesis.

* Corresponding author. Mailing address: INSERM U-510, Faculté de Pharmacie, 5 rue J. B. Clément, 92296 Châtenay-Malabry cedex, France. Phone and fax: 33-1 46 83 56 61. E-mail: alain.servin{at}cep.u-psud.fr.

Journal of Virology, March 2000, p. 2323-2332, Vol. 74, No. 5
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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