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Influenza A Virus Infection of Intestinal Epithelial Cells Enhances the Adhesion Ability of Crohn’s Disease Associated Escherichia coli Strains

Identifieur interne : 000140 ( Main/Exploration ); précédent : 000139; suivant : 000141

Influenza A Virus Infection of Intestinal Epithelial Cells Enhances the Adhesion Ability of Crohn’s Disease Associated Escherichia coli Strains

Auteurs : Marta Aleandri [Italie] ; Maria Pia Conte [Italie] ; Giovanna Simonetti [Italie] ; Simona Panella [Italie] ; Ignacio Celestino [Italie] ; Paola Checconi [Italie] ; Massimiliano Marazzato [Italie] ; Catia Longhi [Italie] ; Paola Goldoni [Italie] ; Mauro Nicoletti [Italie] ; Nicolas Barnich [France] ; Anna Teresa Palamara [Italie] ; Serena Schippa [Italie] ; Lucia Nencioni [Italie]

Source :

RBID : PMC:4338238

Descripteurs français

English descriptors

Abstract

Modifications of intestinal glycoreceptors expression, in particular CEACAM6, typically found in ileal Crohn's disease (CD), favor, among the commensal species of microbiota, the enrichment in Escherichia coli. Removal of protein glycosidic residues by neuraminidase, a sialidase typical of influenza virus, increases adhesion ability of Escherichia coli to Caco-2 intestinal cells. In this study we investigated whether influenza virus infection of human intestinal epithelial cells could influence the adhesiveness of different Escherichia coli strains isolated from CD patients by altering surface glycoreceptors. Influenza virus infection of intestinal cells increased exposure of galactose and mannose residues on the cell surface. In particular, glycoreceptors Thomsen-Friedenreich and CEACAM6 were over-expressed in influenza virus infected cells. In the same experimental conditions, a significant increase in bacterial adhesiveness was observed, independently of their own adhesive ability. The increase was reverted by treatment with anti-TF and anti-CEACAM6 antibodies. Interestingly, influenza virus was able to efficiently replicate in human primary intestinal cells leading to TF exposure. Finally, intestinal infected cells produced high levels of pro-inflammatory cytokines compared to control. Overall these data suggest that influenza virus infection, could constitute an additional risk factor in CD patients.


Url:
DOI: 10.1371/journal.pone.0117005
PubMed: 25706391
PubMed Central: 4338238


Affiliations:


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Le document en format XML

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<title xml:lang="en" level="a" type="main">Influenza A Virus Infection of Intestinal Epithelial Cells Enhances the Adhesion Ability of Crohn’s Disease Associated
<italic>Escherichia coli</italic>
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<wicri:regionArea>IRCCS San Raffaele Pisana, Telematic University, Rome, Italy, Rome</wicri:regionArea>
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<settlement type="city">Rome</settlement>
<region nuts="2">Latium</region>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="aff004">
<addr-line>Department of Public Health and Infectious Diseases, Pasteur Institute Cenci Bolognetti Foundation, “Sapienza” University, Rome, Italy</addr-line>
</nlm:aff>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Public Health and Infectious Diseases, Pasteur Institute Cenci Bolognetti Foundation, “Sapienza” University, Rome</wicri:regionArea>
<placeName>
<settlement type="city">Rome</settlement>
<region nuts="2">Latium</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Schippa, Serena" sort="Schippa, Serena" uniqKey="Schippa S" first="Serena" last="Schippa">Serena Schippa</name>
<affiliation wicri:level="3">
<nlm:aff id="aff001">
<addr-line>Department of Public Health and Infectious Diseases, “Sapienza” University, Rome, Italy</addr-line>
</nlm:aff>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Public Health and Infectious Diseases, “Sapienza” University, Rome</wicri:regionArea>
<placeName>
<settlement type="city">Rome</settlement>
<region nuts="2">Latium</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Nencioni, Lucia" sort="Nencioni, Lucia" uniqKey="Nencioni L" first="Lucia" last="Nencioni">Lucia Nencioni</name>
<affiliation wicri:level="3">
<nlm:aff id="aff001">
<addr-line>Department of Public Health and Infectious Diseases, “Sapienza” University, Rome, Italy</addr-line>
</nlm:aff>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Department of Public Health and Infectious Diseases, “Sapienza” University, Rome</wicri:regionArea>
<placeName>
<settlement type="city">Rome</settlement>
<region nuts="2">Latium</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Antibodies (immunology)</term>
<term>Antigens, CD (immunology)</term>
<term>Antigens, Tumor-Associated, Carbohydrate (immunology)</term>
<term>Bacterial Adhesion</term>
<term>Caco-2 Cells</term>
<term>Cell Adhesion Molecules (immunology)</term>
<term>Crohn Disease (microbiology)</term>
<term>Escherichia coli (physiology)</term>
<term>GPI-Linked Proteins (immunology)</term>
<term>Galactose (metabolism)</term>
<term>Humans</term>
<term>Influenza A Virus, H1N1 Subtype (pathogenicity)</term>
<term>Intestinal Mucosa (microbiology)</term>
<term>Intestinal Mucosa (virology)</term>
<term>Mannose (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Adhérence bactérienne</term>
<term>Anticorps (immunologie)</term>
<term>Antigènes CD (immunologie)</term>
<term>Antigènes glycanniques associés aux tumeurs (immunologie)</term>
<term>Cellules Caco-2</term>
<term>Escherichia coli (physiologie)</term>
<term>Galactose (métabolisme)</term>
<term>Humains</term>
<term>Maladie de Crohn (microbiologie)</term>
<term>Mannose (métabolisme)</term>
<term>Molécules d'adhérence cellulaire (immunologie)</term>
<term>Muqueuse intestinale (microbiologie)</term>
<term>Muqueuse intestinale (virologie)</term>
<term>Protéines liées au GPI (immunologie)</term>
<term>Sous-type H1N1 du virus de la grippe A (pathogénicité)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en">
<term>Antibodies</term>
<term>Antigens, CD</term>
<term>Antigens, Tumor-Associated, Carbohydrate</term>
<term>Cell Adhesion Molecules</term>
<term>GPI-Linked Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Galactose</term>
<term>Mannose</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Anticorps</term>
<term>Antigènes CD</term>
<term>Antigènes glycanniques associés aux tumeurs</term>
<term>Molécules d'adhérence cellulaire</term>
<term>Protéines liées au GPI</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladie de Crohn</term>
<term>Muqueuse intestinale</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Crohn Disease</term>
<term>Intestinal Mucosa</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Galactose</term>
<term>Mannose</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Influenza A Virus, H1N1 Subtype</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Sous-type H1N1 du virus de la grippe A</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Escherichia coli</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Escherichia coli</term>
</keywords>
<keywords scheme="MESH" qualifier="virologie" xml:lang="fr">
<term>Muqueuse intestinale</term>
</keywords>
<keywords scheme="MESH" qualifier="virology" xml:lang="en">
<term>Intestinal Mucosa</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Bacterial Adhesion</term>
<term>Caco-2 Cells</term>
<term>Humans</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Adhérence bactérienne</term>
<term>Cellules Caco-2</term>
<term>Humains</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>Modifications of intestinal glycoreceptors expression, in particular CEACAM6, typically found in ileal Crohn's disease (CD), favor, among the commensal species of microbiota, the enrichment in
<italic>Escherichia coli</italic>
. Removal of protein glycosidic residues by neuraminidase, a sialidase typical of influenza virus, increases adhesion ability of
<italic>Escherichia coli</italic>
to Caco-2 intestinal cells. In this study we investigated whether influenza virus infection of human intestinal epithelial cells could influence the adhesiveness of different
<italic>Escherichia coli</italic>
strains isolated from CD patients by altering surface glycoreceptors. Influenza virus infection of intestinal cells increased exposure of galactose and mannose residues on the cell surface. In particular, glycoreceptors Thomsen-Friedenreich and CEACAM6 were over-expressed in influenza virus infected cells. In the same experimental conditions, a significant increase in bacterial adhesiveness was observed, independently of their own adhesive ability. The increase was reverted by treatment with anti-TF and anti-CEACAM6 antibodies. Interestingly, influenza virus was able to efficiently replicate in human primary intestinal cells leading to TF exposure. Finally, intestinal infected cells produced high levels of pro-inflammatory cytokines compared to control. Overall these data suggest that influenza virus infection, could constitute an additional risk factor in CD patients.</p>
</div>
</front>
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<name sortKey="To, Kk" uniqKey="To K">KK To</name>
</author>
<author>
<name sortKey="Chan, Kh" uniqKey="Chan K">KH Chan</name>
</author>
<author>
<name sortKey="Li, Iw" uniqKey="Li I">IW Li</name>
</author>
<author>
<name sortKey="Tsang, Ty" uniqKey="Tsang T">TY Tsang</name>
</author>
<author>
<name sortKey="Tse, H" uniqKey="Tse H">H Tse</name>
</author>
</analytic>
</biblStruct>
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<analytic>
<author>
<name sortKey="Wootton, Sh" uniqKey="Wootton S">SH Wootton</name>
</author>
<author>
<name sortKey="Scheifele, Dw" uniqKey="Scheifele D">DW Scheifele</name>
</author>
<author>
<name sortKey="Mak, A" uniqKey="Mak A">A Mak</name>
</author>
<author>
<name sortKey="Petric, M" uniqKey="Petric M">M Petric</name>
</author>
<author>
<name sortKey="Skowronski, Dm" uniqKey="Skowronski D">DM Skowronski</name>
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</analytic>
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<author>
<name sortKey="Hu, Y" uniqKey="Hu Y">Y Hu</name>
</author>
<author>
<name sortKey="Lu, S" uniqKey="Lu S">S Lu</name>
</author>
<author>
<name sortKey="Song, Z" uniqKey="Song Z">Z Song</name>
</author>
<author>
<name sortKey="Wang, W" uniqKey="Wang W">W Wang</name>
</author>
<author>
<name sortKey="Hao, P" uniqKey="Hao P">P Hao</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Okayama, S" uniqKey="Okayama S">S Okayama</name>
</author>
<author>
<name sortKey="Arakawa, S" uniqKey="Arakawa S">S Arakawa</name>
</author>
<author>
<name sortKey="Ogawa, K" uniqKey="Ogawa K">K Ogawa</name>
</author>
<author>
<name sortKey="Makino, T" uniqKey="Makino T">T Makino</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Boudeau, J" uniqKey="Boudeau J">J Boudeau</name>
</author>
<author>
<name sortKey="Barnich, N" uniqKey="Barnich N">N Barnich</name>
</author>
<author>
<name sortKey="Darfeuille Michaud, A" uniqKey="Darfeuille Michaud A">A Darfeuille-Michaud</name>
</author>
</analytic>
</biblStruct>
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<analytic>
<author>
<name sortKey="Iebba, V" uniqKey="Iebba V">V Iebba</name>
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</author>
<author>
<name sortKey="Lepanto, Ms" uniqKey="Lepanto M">MS Lepanto</name>
</author>
<author>
<name sortKey="Di Nardo, G" uniqKey="Di Nardo G">G Di Nardo</name>
</author>
<author>
<name sortKey="Santangelo, F" uniqKey="Santangelo F">F Santangelo</name>
</author>
</analytic>
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<analytic>
<author>
<name sortKey="Schippa, S" uniqKey="Schippa S">S Schippa</name>
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<author>
<name sortKey="Iebba, V" uniqKey="Iebba V">V Iebba</name>
</author>
<author>
<name sortKey="Totino, V" uniqKey="Totino V">V Totino</name>
</author>
<author>
<name sortKey="Santangelo, F" uniqKey="Santangelo F">F Santangelo</name>
</author>
<author>
<name sortKey="Lepanto, M" uniqKey="Lepanto M">M Lepanto</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Rolhion, N" uniqKey="Rolhion N">N Rolhion</name>
</author>
<author>
<name sortKey="Hofman, P" uniqKey="Hofman P">P Hofman</name>
</author>
<author>
<name sortKey="Darfeuille Michaud, A" uniqKey="Darfeuille Michaud A">A Darfeuille-Michaud</name>
</author>
</analytic>
</biblStruct>
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<analytic>
<author>
<name sortKey="Nencioni, L" uniqKey="Nencioni L">L Nencioni</name>
</author>
<author>
<name sortKey="Iuvara, A" uniqKey="Iuvara A">A Iuvara</name>
</author>
<author>
<name sortKey="Aquilano, K" uniqKey="Aquilano K">K Aquilano</name>
</author>
<author>
<name sortKey="Ciriolo, Mr" uniqKey="Ciriolo M">MR Ciriolo</name>
</author>
<author>
<name sortKey="Cozzolino, F" uniqKey="Cozzolino F">F Cozzolino</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
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<author>
<name sortKey="Nencioni, L" uniqKey="Nencioni L">L Nencioni</name>
</author>
<author>
<name sortKey="De Chiara, G" uniqKey="De Chiara G">G De Chiara</name>
</author>
<author>
<name sortKey="Sgarbanti, R" uniqKey="Sgarbanti R">R Sgarbanti</name>
</author>
<author>
<name sortKey="Amatore, D" uniqKey="Amatore D">D Amatore</name>
</author>
<author>
<name sortKey="Aquilano, K" uniqKey="Aquilano K">K Aquilano</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Sgarbanti, R" uniqKey="Sgarbanti R">R Sgarbanti</name>
</author>
<author>
<name sortKey="Nencioni, L" uniqKey="Nencioni L">L Nencioni</name>
</author>
<author>
<name sortKey="Amatore, D" uniqKey="Amatore D">D Amatore</name>
</author>
<author>
<name sortKey="Coluccio, P" uniqKey="Coluccio P">P Coluccio</name>
</author>
<author>
<name sortKey="Fraternale, A" uniqKey="Fraternale A">A Fraternale</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Checconi, P" uniqKey="Checconi P">P Checconi</name>
</author>
<author>
<name sortKey="Sgarbanti, R" uniqKey="Sgarbanti R">R Sgarbanti</name>
</author>
<author>
<name sortKey="Celestino, I" uniqKey="Celestino I">I Celestino</name>
</author>
<author>
<name sortKey="Limongi, D" uniqKey="Limongi D">D Limongi</name>
</author>
<author>
<name sortKey="Amatore, D" uniqKey="Amatore D">D Amatore</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Hu, Y" uniqKey="Hu Y">Y Hu</name>
</author>
<author>
<name sortKey="Lu, S" uniqKey="Lu S">S Lu</name>
</author>
<author>
<name sortKey="Song, Z" uniqKey="Song Z">Z Song</name>
</author>
<author>
<name sortKey="Wang, W" uniqKey="Wang W">W Wang</name>
</author>
<author>
<name sortKey="Hao, P" uniqKey="Hao P">P Hao</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Pang, Ik" uniqKey="Pang I">IK Pang</name>
</author>
<author>
<name sortKey="Pillai, Ps" uniqKey="Pillai P">PS Pillai</name>
</author>
<author>
<name sortKey="Iwasaki, A" uniqKey="Iwasaki A">A Iwasaki</name>
</author>
</analytic>
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<biblStruct></biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<affiliations>
<list>
<country>
<li>France</li>
<li>Italie</li>
</country>
<region>
<li>Auvergne (région administrative)</li>
<li>Auvergne-Rhône-Alpes</li>
<li>Latium</li>
</region>
<settlement>
<li>Clermont-Ferrand</li>
<li>Rome</li>
</settlement>
</list>
<tree>
<country name="Italie">
<region name="Latium">
<name sortKey="Aleandri, Marta" sort="Aleandri, Marta" uniqKey="Aleandri M" first="Marta" last="Aleandri">Marta Aleandri</name>
</region>
<name sortKey="Celestino, Ignacio" sort="Celestino, Ignacio" uniqKey="Celestino I" first="Ignacio" last="Celestino">Ignacio Celestino</name>
<name sortKey="Celestino, Ignacio" sort="Celestino, Ignacio" uniqKey="Celestino I" first="Ignacio" last="Celestino">Ignacio Celestino</name>
<name sortKey="Checconi, Paola" sort="Checconi, Paola" uniqKey="Checconi P" first="Paola" last="Checconi">Paola Checconi</name>
<name sortKey="Conte, Maria Pia" sort="Conte, Maria Pia" uniqKey="Conte M" first="Maria Pia" last="Conte">Maria Pia Conte</name>
<name sortKey="Goldoni, Paola" sort="Goldoni, Paola" uniqKey="Goldoni P" first="Paola" last="Goldoni">Paola Goldoni</name>
<name sortKey="Longhi, Catia" sort="Longhi, Catia" uniqKey="Longhi C" first="Catia" last="Longhi">Catia Longhi</name>
<name sortKey="Marazzato, Massimiliano" sort="Marazzato, Massimiliano" uniqKey="Marazzato M" first="Massimiliano" last="Marazzato">Massimiliano Marazzato</name>
<name sortKey="Nencioni, Lucia" sort="Nencioni, Lucia" uniqKey="Nencioni L" first="Lucia" last="Nencioni">Lucia Nencioni</name>
<name sortKey="Nicoletti, Mauro" sort="Nicoletti, Mauro" uniqKey="Nicoletti M" first="Mauro" last="Nicoletti">Mauro Nicoletti</name>
<name sortKey="Palamara, Anna Teresa" sort="Palamara, Anna Teresa" uniqKey="Palamara A" first="Anna Teresa" last="Palamara">Anna Teresa Palamara</name>
<name sortKey="Palamara, Anna Teresa" sort="Palamara, Anna Teresa" uniqKey="Palamara A" first="Anna Teresa" last="Palamara">Anna Teresa Palamara</name>
<name sortKey="Panella, Simona" sort="Panella, Simona" uniqKey="Panella S" first="Simona" last="Panella">Simona Panella</name>
<name sortKey="Panella, Simona" sort="Panella, Simona" uniqKey="Panella S" first="Simona" last="Panella">Simona Panella</name>
<name sortKey="Schippa, Serena" sort="Schippa, Serena" uniqKey="Schippa S" first="Serena" last="Schippa">Serena Schippa</name>
<name sortKey="Simonetti, Giovanna" sort="Simonetti, Giovanna" uniqKey="Simonetti G" first="Giovanna" last="Simonetti">Giovanna Simonetti</name>
</country>
<country name="France">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Barnich, Nicolas" sort="Barnich, Nicolas" uniqKey="Barnich N" first="Nicolas" last="Barnich">Nicolas Barnich</name>
</region>
</country>
</tree>
</affiliations>
</record>

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