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Journal of Virology, December 2001, p. 11834-11850, Vol. 75, No. 23
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.23.11834-11850.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Differential Infection of Polarized Epithelial Cell
Lines by Sialic Acid-Dependent and Sialic Acid-Independent
Rotavirus Strains
Max
Ciarlet,
Sue E.
Crawford, and
Mary K.
Estes*
Department of Molecular Virology and
Microbiology, Baylor College of Medicine, Houston, Texas 77030
Received 18 July 2001/Accepted 30 August 2001
Infection of epithelial cells by some animal rotaviruses, but not
human or most animal rotaviruses, requires the presence of
N-acetylneuraminic (sialic) acid (SA) on the cell
surface for efficient infectivity. To further understand how
rotaviruses enter susceptible cells, six different polarized epithelial
cell lines, grown on permeable filter membrane supports containing
0.4-µm pores, were infected apically or basolaterally with
SA-independent or SA-dependent rotaviruses. SA-independent rotaviruses
applied apically or basolaterally were capable of efficiently infecting both sides of the epithelium of all six polarized cell lines tested, while SA-dependent rotaviruses only infected efficiently through the apical surface of five of the polarized cell lines tested. Regardless of the route of virus entry, SA-dependent and SA-independent rotaviruses were released almost exclusively from the apical domain of
the plasma membrane of polarized cells before monolayer disruption or
cell lysis. The transepithelial electrical resistance (TER) of cells
decreased at the same time, irrespective of whether infection with
SA-independent rotaviruses occurred apically or basolaterally. The TER
of cells infected apically with SA-dependent rotaviruses decreased
earlier than that of cells infected basolaterally. Rotavirus infection
decreased TER before the appearance of cytopathic effect and cell death
and resulted in an increase in the paracellular permeability to
[3H]inulin as a function of loss of TER. The presence of
SA residues on either the apical or basolateral side was determined
using a Texas Red-conjugated lectin, wheat germ agglutinin (WGA), which binds SA residues. WGA bound exclusively to SA residues on the apical
surface of the cells, confirming the requirement for SA residues on the
apical cell membrane for efficient infectivity of SA-dependent
rotaviruses. These results indicate that the rotavirus SA-independent
cellular receptor is present on both sides of the epithelium, but
SA-dependent and SA-independent rotavirus strains infect polarized
epithelial cells by different mechanisms, which may be relevant for
pathogenesis and selection of vaccine strains. Finally,
rotavirus-induced alterations of the epithelial barrier and
paracellular permeability suggest that common mechanisms of pathogenesis may exist between viral and bacterial pathogens of the
intestinal tract.
*
Corresponding author. Mailing address: Department of
Molecular Virology & Microbiology, Baylor College of Medicine, One
Baylor Plaza, Mailstop BCM-385, Houston, TX 77030. Phone: (713)
798-3585. Fax: (713) 798-3586. E-mail:
mestes{at}bcm.tmc.edu.
Journal of Virology, December 2001, p. 11834-11850, Vol. 75, No. 23
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.23.11834-11850.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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