Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase
Staphylococcus aureus is an important nosocomial and community-acquired facultative intracellular pathogen. Many studies have reported that S. aureus infections are associated with intestinal symptoms, but little is known about the molecular mechanisms implicated in S. aureus-induced alterations of...
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2021-08-01
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doaj-6714e1f532614475a594fb4d830ae0282021-08-13T10:49:41ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-08-01910.3389/fcell.2021.699970699970Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–IsomaltaseAhmedElmontaser Mergani0AhmedElmontaser Mergani1Dalanda Wanes2Natalie Schecker3Katja Branitzki-Heinemann4Katja Branitzki-Heinemann5Hassan Y. Naim6Maren von Köckritz-Blickwede7Maren von Köckritz-Blickwede8Department of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hanover, GermanyDepartment of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyDepartment of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyDepartment of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hanover, GermanyDepartment of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyDepartment of Biochemistry, University of Veterinary Medicine Hannover, Hanover, GermanyResearch Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hanover, GermanyStaphylococcus aureus is an important nosocomial and community-acquired facultative intracellular pathogen. Many studies have reported that S. aureus infections are associated with intestinal symptoms, but little is known about the molecular mechanisms implicated in S. aureus-induced alterations of intestinal functions. In this study, we investigated the implication of lipid rafts in the interaction of S. aureus with Caco-2 cells. To assess potential alterations in the lipid raft structure and effects on the hydrolytic function, we utilized sucrase–isomaltase (SI) as the major intestinal α-glucosidase that is associated with and sorted to the apical membrane via lipid rafts. Seven days post-confluent, Caco-2 cells were infected with S. aureus Newman and further incubated for an additional 2 days. After 48 h, the levels of SI expression as well as the enzymatic function of this protein were assessed in the infected versus non-infected cells. Analysis of the sorting behavior of SI to the apical membrane constituted another crucial aspect in studying the effects of S. aureus on Caco-2 cells. For this purpose, the apical membranes or brush border membranes (BBMs; referred to as P2 fraction) were separated in both infected and non-infected cells from the basolateral and intracellular membranes (referred to as P1 fraction) by employing a cationic-based procedure using CaCl2. The data show that there is no significant change in the overall expression levels of SI in the infected versus non-infected cells as assessed by Western blotting analysis using monoclonal anti-SI antibodies. By contrast, a significant decrease in the localization as well as the specific hydrolytic activities of SI toward sucrose and isomaltose (Palatinose) was observed in the BBM (P2 fraction) in Caco-2 cells 48 h post-infection. Concomitantly, the specific SI activities increased in the basolateral membrane/intracellular fraction (P1). Noteworthy, the specific activity of SI in the BBM of infected cells was markedly reduced as compared with that of the non-infected counterparts. The data accumulated from this study strongly suggest that infections with S. aureus influence the final step in the lipid raft-associated trafficking of human SI and thereby may trigger secondary functional gastrointestinal disorders.https://www.frontiersin.org/articles/10.3389/fcell.2021.699970/fullS. aureushuman sucrase–isomaltasebrush border membraneslipid raftssucrase–isomaltase |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
AhmedElmontaser Mergani AhmedElmontaser Mergani Dalanda Wanes Natalie Schecker Katja Branitzki-Heinemann Katja Branitzki-Heinemann Hassan Y. Naim Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede |
spellingShingle |
AhmedElmontaser Mergani AhmedElmontaser Mergani Dalanda Wanes Natalie Schecker Katja Branitzki-Heinemann Katja Branitzki-Heinemann Hassan Y. Naim Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase Frontiers in Cell and Developmental Biology S. aureus human sucrase–isomaltase brush border membranes lipid rafts sucrase–isomaltase |
author_facet |
AhmedElmontaser Mergani AhmedElmontaser Mergani Dalanda Wanes Natalie Schecker Katja Branitzki-Heinemann Katja Branitzki-Heinemann Hassan Y. Naim Maren von Köckritz-Blickwede Maren von Köckritz-Blickwede |
author_sort |
AhmedElmontaser Mergani |
title |
Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase |
title_short |
Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase |
title_full |
Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase |
title_fullStr |
Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase |
title_full_unstemmed |
Staphylococcus aureus Infection Influences the Function of Intestinal Cells by Altering the Lipid Raft-Dependent Sorting of Sucrase–Isomaltase |
title_sort |
staphylococcus aureus infection influences the function of intestinal cells by altering the lipid raft-dependent sorting of sucrase–isomaltase |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cell and Developmental Biology |
issn |
2296-634X |
publishDate |
2021-08-01 |
description |
Staphylococcus aureus is an important nosocomial and community-acquired facultative intracellular pathogen. Many studies have reported that S. aureus infections are associated with intestinal symptoms, but little is known about the molecular mechanisms implicated in S. aureus-induced alterations of intestinal functions. In this study, we investigated the implication of lipid rafts in the interaction of S. aureus with Caco-2 cells. To assess potential alterations in the lipid raft structure and effects on the hydrolytic function, we utilized sucrase–isomaltase (SI) as the major intestinal α-glucosidase that is associated with and sorted to the apical membrane via lipid rafts. Seven days post-confluent, Caco-2 cells were infected with S. aureus Newman and further incubated for an additional 2 days. After 48 h, the levels of SI expression as well as the enzymatic function of this protein were assessed in the infected versus non-infected cells. Analysis of the sorting behavior of SI to the apical membrane constituted another crucial aspect in studying the effects of S. aureus on Caco-2 cells. For this purpose, the apical membranes or brush border membranes (BBMs; referred to as P2 fraction) were separated in both infected and non-infected cells from the basolateral and intracellular membranes (referred to as P1 fraction) by employing a cationic-based procedure using CaCl2. The data show that there is no significant change in the overall expression levels of SI in the infected versus non-infected cells as assessed by Western blotting analysis using monoclonal anti-SI antibodies. By contrast, a significant decrease in the localization as well as the specific hydrolytic activities of SI toward sucrose and isomaltose (Palatinose) was observed in the BBM (P2 fraction) in Caco-2 cells 48 h post-infection. Concomitantly, the specific SI activities increased in the basolateral membrane/intracellular fraction (P1). Noteworthy, the specific activity of SI in the BBM of infected cells was markedly reduced as compared with that of the non-infected counterparts. The data accumulated from this study strongly suggest that infections with S. aureus influence the final step in the lipid raft-associated trafficking of human SI and thereby may trigger secondary functional gastrointestinal disorders. |
topic |
S. aureus human sucrase–isomaltase brush border membranes lipid rafts sucrase–isomaltase |
url |
https://www.frontiersin.org/articles/10.3389/fcell.2021.699970/full |
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