During the digestive-tract phase of infection, poliovirus (PV) is found in the oropharynx and the intestine. It has been proposed that PV enters the organism by crossing M cells, which are scattered in the epithelial sheet covering lymphoid follicles of Peyer’s patches. However, PV translocation through M cells has never been demonstrated. A model of M-like cells has been previously developed using monolayers of polarized Caco-2 enterocytes cocultured with lymphocytes isolated from Peyer’s patches. In this model, lymphoepithelial interactions trigger the appearance of epithelial cells having morphological and functional characteristics of M cells. We have demonstrated efficient, temperature-dependent PV transcytosis in Caco-2 cell monolayers containing M-like cells. This experimental evidence is consistent with M cells serving as gateways allowing PV access to the basal face of enterocytes, the underlying immune follicle cells, and PV transport toward mesenteric lymph nodes.
AmerongenH. M.,
WilsonG. A.,
FieldsB. N.,
NeutraM. R.1994; Proteolytic processing of reovirus is required for adherence to intestinal M cells. Journal of Virology 68:8428–8432
BassD. M.,
TrierJ. S.,
DambrauskasR.,
WolfJ. L.1988; Reovirus type I infection of small intestinal epithelium in suckling mice and its effect on M cells. Laboratory Investigation 58:226–235
BlondelB.,
DuncanG.,
CoudercT.,
DelpeyrouxF.,
PavioN.,
Colbère-GarapinF.1998; Molecular aspects of poliovirus biology with a special focus on the interactions with nerve cells. Journal of Neurovirology 4:1–26
Costa de BeauregardM. A.,
PringaultE.,
RobineS.,
LouvardD.1995; Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO Journal 14:409–421
DickinsonB. L.,
BadizadeganK.,
WuZ.,
AhouseJ. C.,
ZhuX.,
SimisterN. E.,
BlumbergR. S.,
LencerW. I.1999; Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. Journal of Clinical Investigation 104:903–911
El BahiS.,
CaliotE.,
BensM.,
BogdanovaA.,
KerneisS.,
KahnA.,
VandewalleA.,
PringaultE.2002; Lympho-epithelial interactions trigger specific regulation of gene expression in the M-cell containing follicle-associated epithelium of Peyer’s patches. Journal of Immunology 168:3713–3720
EmmanuelA. V.,
MasonH. J.,
KammM. A.2001; Relationship between psychological state and level of activity of extrinsic gut innervation in patients with a functional gut disorder. Gut 49:209–213
GebertA.1996; M-cells in the rabbit tonsil exhibit distinctive glycoconjugates in their apical membranes. Journal of Histochemistry and Cytochemistry 44:1033–1042
GullbergE. M.,
LeonardM.,
KarlssonJ.,
HopkinsA. M.,
BraydenD.,
BairdA. W.,
ArturssonP.2000; Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochemical and Biophysical Research Communications 279:803–813
HeppnerF. L.,
ChristA. D.,
KleinM. A.,
PrinzM.,
FriedM.,
KraehenbuhlJ. P.,
AguzziA.2001; Transepithelial prion transport by M cells. Nature Medicine 7:976–977
KerneisS.,
BogdanovaA.,
KraehenbuhlJ. P.,
PringaultE.1997; Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277:949–952
KerneisS.,
CaliotE.,
StubbeH.,
BogdanovaA.,
KraehenbuhlJ.,
PringaultE.2000; Molecular studies of the intestinal mucosal barrier physiopathology using cocultures of epithelial and immune cells: a technical update. Microbes and Infection 2:1119–1124
LopezM.,
JordierF.,
BardinF.,
CoulombelL.,
ChabannonC.,
DubreuilP.1999; Identification of a new class of Ig superfamily antigens expressed in hemopoiesis. In Leucocyte Typing VI . White Cell Differentiation Antigens pp 1081 Edited by
KishimotoT. K.,
KikutaniH.,
von dem BorneA. E. G.,
GoyertS. M.,
MasonD. Y.,
MiyasakaM.,
MorettaM.,
OkumuraK.,
ShawS.,
SpringerT. A.,
SugamuraK.,
ZolaH.
New York: Garland Publishing;
MadaraJ. L.,
TrierJ. S.1994; The functional morphology of the mucosa of the small intestine. In Physiology of the Gastrointestinal Tract pp 1577 Edited by
JohnsonL. R.
New York: Raven Press;
MadaraJ. L.,
ByeW. A.,
TrierJ. S.1984; Structural features of and cholesterol distribution in M-cell membranes in guinea pig, rat and mouse Peyer’s patches. Gastroenterology 87:1091–1103
NeutraM. R.,
PringaultE.,
KraehenbuhlJ. P.1996b; Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annual Review of Immunology 14:275–300
OwenR. L.1977; Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer’s patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 72:440–451
OwenR. L.,
JonesA. L.1974; Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203
PintoM.,
Robine-LeonS.,
AppayM.,
KedingerM.,
TriadouN.,
DussaulxE.,
LacroixB.,
Simon-AssmannP.,
HaffenK.,
FoghJ.,
ZweibaumA.1983; Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biology of the Cell 47:323–330
SicinskiP.,
RowinskiJ.,
WarcholJ. B.,
JarzabekZ.,
GutW.,
SzczygielB.,
BieleckiK.,
KochG.1990; Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58
WolfJ. L.,
RubinD. H.,
FinbergR.,
KauffmanR. S.,
SharpeA. H.,
TrierJ. S.,
FieldsB. N.1981; Intestinal M cells: a pathway for entry of reovirus into the host. Science 212:471–472
WolfJ. L.,
DambrauskasR.,
SharpeA. H.,
TrierJ. S.1987; Adherence to and penetration of the intestinal epithelium by reovirus type 1 in neonatal mice. Gastroenterology 92:82–91