Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid
The innate immune system plays a critical role in the rapid recognition and elimination of pathogens through pattern recognition receptors (PRRs). Among these PRRs are the C-type lectins (CTLs) langerin, mannan-binding lectin (MBL), and surfactant protein D (SP-D), which recognize carbohydrate patte...
Saved in:
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-01-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1504886/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1823858684333129728 |
|---|---|
| author | Kirstine Mejlstrup Hymøller Kirstine Mejlstrup Hymøller Stig Hill Christiansen Stig Hill Christiansen Anders Grønnegaard Schlosser Uffe B. Skov Sørensen Jean C. Lee Steffen Thiel Steffen Thiel |
| author_facet | Kirstine Mejlstrup Hymøller Kirstine Mejlstrup Hymøller Stig Hill Christiansen Stig Hill Christiansen Anders Grønnegaard Schlosser Uffe B. Skov Sørensen Jean C. Lee Steffen Thiel Steffen Thiel |
| author_sort | Kirstine Mejlstrup Hymøller |
| collection | DOAJ |
| description | The innate immune system plays a critical role in the rapid recognition and elimination of pathogens through pattern recognition receptors (PRRs). Among these PRRs are the C-type lectins (CTLs) langerin, mannan-binding lectin (MBL), and surfactant protein D (SP-D), which recognize carbohydrate patterns on pathogens. Each represents proteins from different compartments of the body and employs separate effector mechanisms. We have investigated their interaction with the Gram-positive opportunistic pathogen Staphylococcus aureus, a bacterium whose cell wall contains two key glycopolymers: capsular polysaccharide (CP) and wall teichoic acid (WTA). Using a langerin-expressing cell line and recombinant langerin, MBL, and SP-D, we demonstrated that langerin, MBL, and SP-D all recognize nonencapsulated S. aureus. However, the bacterium may produce CP that effectively shields S. aureus from recognition by all three CTLs. Experiments utilizing mutant S. aureus strains confirmed that WTA is a ligand for MBL, but that langerin likely interacts with an additional unknown ligand. A competition assay revealed that MBL and SP-D inhibit langerin’s interaction with S. aureus, highlighting the intricate redundancy and cooperation within the innate immune system. This study highlights the dynamic interplay of langerin, MBL, and SP-D in recognizing specific surface structures on S. aureus and provides insight into how this pathogen evades innate immune recognition. |
| format | Article |
| id | doaj-art-313410ed28f440ffbc94fe849127bec8 |
| institution | Kabale University |
| issn | 1664-3224 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj-art-313410ed28f440ffbc94fe849127bec82025-02-11T10:10:06ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-01-011510.3389/fimmu.2024.15048861504886Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acidKirstine Mejlstrup Hymøller0Kirstine Mejlstrup Hymøller1Stig Hill Christiansen2Stig Hill Christiansen3Anders Grønnegaard Schlosser4Uffe B. Skov Sørensen5Jean C. Lee6Steffen Thiel7Steffen Thiel8Department of Biomedicine, Aarhus University, Aarhus, DenmarkThe Centre for Cellular Signal Patterns (CellPAT), Aarhus University, Aarhus, DenmarkDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkThe Centre for Cellular Signal Patterns (CellPAT), Aarhus University, Aarhus, DenmarkDepartment of Inflammation Research, Department of Molecular Medicine, University of Southern Denmark, Odense, DenmarkDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkDivision of Infectious Diseases, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, United StatesDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkThe Centre for Cellular Signal Patterns (CellPAT), Aarhus University, Aarhus, DenmarkThe innate immune system plays a critical role in the rapid recognition and elimination of pathogens through pattern recognition receptors (PRRs). Among these PRRs are the C-type lectins (CTLs) langerin, mannan-binding lectin (MBL), and surfactant protein D (SP-D), which recognize carbohydrate patterns on pathogens. Each represents proteins from different compartments of the body and employs separate effector mechanisms. We have investigated their interaction with the Gram-positive opportunistic pathogen Staphylococcus aureus, a bacterium whose cell wall contains two key glycopolymers: capsular polysaccharide (CP) and wall teichoic acid (WTA). Using a langerin-expressing cell line and recombinant langerin, MBL, and SP-D, we demonstrated that langerin, MBL, and SP-D all recognize nonencapsulated S. aureus. However, the bacterium may produce CP that effectively shields S. aureus from recognition by all three CTLs. Experiments utilizing mutant S. aureus strains confirmed that WTA is a ligand for MBL, but that langerin likely interacts with an additional unknown ligand. A competition assay revealed that MBL and SP-D inhibit langerin’s interaction with S. aureus, highlighting the intricate redundancy and cooperation within the innate immune system. This study highlights the dynamic interplay of langerin, MBL, and SP-D in recognizing specific surface structures on S. aureus and provides insight into how this pathogen evades innate immune recognition.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1504886/fullinnate immunitylangerinmannan-binding lectinsurfactant protein DS. aureusC-type lectins |
| spellingShingle | Kirstine Mejlstrup Hymøller Kirstine Mejlstrup Hymøller Stig Hill Christiansen Stig Hill Christiansen Anders Grønnegaard Schlosser Uffe B. Skov Sørensen Jean C. Lee Steffen Thiel Steffen Thiel Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid Frontiers in Immunology innate immunity langerin mannan-binding lectin surfactant protein D S. aureus C-type lectins |
| title | Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid |
| title_full | Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid |
| title_fullStr | Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid |
| title_full_unstemmed | Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid |
| title_short | Recognition of Staphylococcus aureus by the pattern recognition molecules langerin, mannan-binding lectin, and surfactant protein D: the influence of capsular polysaccharides and wall teichoic acid |
| title_sort | recognition of staphylococcus aureus by the pattern recognition molecules langerin mannan binding lectin and surfactant protein d the influence of capsular polysaccharides and wall teichoic acid |
| topic | innate immunity langerin mannan-binding lectin surfactant protein D S. aureus C-type lectins |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1504886/full |
| work_keys_str_mv | AT kirstinemejlstruphymøller recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT kirstinemejlstruphymøller recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT stighillchristiansen recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT stighillchristiansen recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT andersgrønnegaardschlosser recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT uffebskovsørensen recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT jeanclee recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT steffenthiel recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid AT steffenthiel recognitionofstaphylococcusaureusbythepatternrecognitionmoleculeslangerinmannanbindinglectinandsurfactantproteindtheinfluenceofcapsularpolysaccharidesandwallteichoicacid |