Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway
Neutrophils have the ability to capture and kill microbes extracellularly through the formation of neutrophil extracellular traps (NETs). These are DNA and protein structures that neutrophils release extracellularly and are believed to function as a defense mechanism against microbes. The classic NE...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2017-03-01
|
Series: | Frontiers in Immunology |
Subjects: | |
Online Access: | http://journal.frontiersin.org/article/10.3389/fimmu.2017.00257/full |
id |
doaj-2b60433c76284ca6b9bb0ba91c5a4241 |
---|---|
record_format |
Article |
spelling |
doaj-2b60433c76284ca6b9bb0ba91c5a42412020-11-25T02:18:32ZengFrontiers Media S.A.Frontiers in Immunology1664-32242017-03-01810.3389/fimmu.2017.00257235488Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent PathwayHalla Björnsdottir0Agnes Dahlstrand Rudin1Felix P. Klose2Jonas Elmwall3Amanda Welin4Marios Stylianou5Karin Christenson6Constantin F. Urban7Huamei Forsman8Claes Dahlgren9Anna Karlsson10Johan Bylund11Department of Oral Microbiology and Immunology, Institute of Odontology, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenDepartment of Oral Microbiology and Immunology, Institute of Odontology, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenDepartment of Oral Microbiology and Immunology, Institute of Odontology, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenThe Phagocyte Research Laboratory, Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenThe Phagocyte Research Laboratory, Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenAntifungal Immunity Group, Department of Clinical Microbiology, Umeå University, Umeå, SwedenDepartment of Oral Microbiology and Immunology, Institute of Odontology, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenAntifungal Immunity Group, Department of Clinical Microbiology, Umeå University, Umeå, SwedenThe Phagocyte Research Laboratory, Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenThe Phagocyte Research Laboratory, Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenThe Phagocyte Research Laboratory, Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenDepartment of Oral Microbiology and Immunology, Institute of Odontology, Sahlgrenska Academy at University of Gothenburg, Gothenburg, SwedenNeutrophils have the ability to capture and kill microbes extracellularly through the formation of neutrophil extracellular traps (NETs). These are DNA and protein structures that neutrophils release extracellularly and are believed to function as a defense mechanism against microbes. The classic NET formation process, triggered by, e.g., bacteria, fungi, or by direct stimulation of protein kinase C through phorbol myristate acetate, is an active process that takes several hours and relies on the production of reactive oxygen species (ROS) that are further modified by myeloperoxidase (MPO). We show here that NET-like structures can also be formed by neutrophils after interaction with phenol-soluble modulin α (PSMα) that are cytotoxic membrane-disturbing peptides, secreted from community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA). The PSMα-induced NETs contained the typical protein markers and were able to capture microbes. The PSMα-induced NET structures were disintegrated upon prolonged exposure to DNase-positive S. aureus but not on exposure to DNase-negative Candida albicans. Opposed to classic NETosis, PSMα-triggered NET formation occurred very rapidly, independently of ROS or MPO, and was also manifest at 4°C. These data indicate that rapid NETs release may result from cytotoxic membrane disturbance by PSMα peptides, a process that may be of importance for CA-MRSA virulence.http://journal.frontiersin.org/article/10.3389/fimmu.2017.00257/fullcommunity-acquired methicillin-resistant Staphylococcus aureusPSMNETsROSFPR2MPO |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Halla Björnsdottir Agnes Dahlstrand Rudin Felix P. Klose Jonas Elmwall Amanda Welin Marios Stylianou Karin Christenson Constantin F. Urban Huamei Forsman Claes Dahlgren Anna Karlsson Johan Bylund |
spellingShingle |
Halla Björnsdottir Agnes Dahlstrand Rudin Felix P. Klose Jonas Elmwall Amanda Welin Marios Stylianou Karin Christenson Constantin F. Urban Huamei Forsman Claes Dahlgren Anna Karlsson Johan Bylund Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway Frontiers in Immunology community-acquired methicillin-resistant Staphylococcus aureus PSM NETs ROS FPR2 MPO |
author_facet |
Halla Björnsdottir Agnes Dahlstrand Rudin Felix P. Klose Jonas Elmwall Amanda Welin Marios Stylianou Karin Christenson Constantin F. Urban Huamei Forsman Claes Dahlgren Anna Karlsson Johan Bylund |
author_sort |
Halla Björnsdottir |
title |
Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway |
title_short |
Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway |
title_full |
Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway |
title_fullStr |
Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway |
title_full_unstemmed |
Phenol-Soluble Modulin α Peptide Toxins from Aggressive Staphylococcus aureus Induce Rapid Formation of Neutrophil Extracellular Traps through a Reactive Oxygen Species-Independent Pathway |
title_sort |
phenol-soluble modulin α peptide toxins from aggressive staphylococcus aureus induce rapid formation of neutrophil extracellular traps through a reactive oxygen species-independent pathway |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Immunology |
issn |
1664-3224 |
publishDate |
2017-03-01 |
description |
Neutrophils have the ability to capture and kill microbes extracellularly through the formation of neutrophil extracellular traps (NETs). These are DNA and protein structures that neutrophils release extracellularly and are believed to function as a defense mechanism against microbes. The classic NET formation process, triggered by, e.g., bacteria, fungi, or by direct stimulation of protein kinase C through phorbol myristate acetate, is an active process that takes several hours and relies on the production of reactive oxygen species (ROS) that are further modified by myeloperoxidase (MPO). We show here that NET-like structures can also be formed by neutrophils after interaction with phenol-soluble modulin α (PSMα) that are cytotoxic membrane-disturbing peptides, secreted from community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA). The PSMα-induced NETs contained the typical protein markers and were able to capture microbes. The PSMα-induced NET structures were disintegrated upon prolonged exposure to DNase-positive S. aureus but not on exposure to DNase-negative Candida albicans. Opposed to classic NETosis, PSMα-triggered NET formation occurred very rapidly, independently of ROS or MPO, and was also manifest at 4°C. These data indicate that rapid NETs release may result from cytotoxic membrane disturbance by PSMα peptides, a process that may be of importance for CA-MRSA virulence. |
topic |
community-acquired methicillin-resistant Staphylococcus aureus PSM NETs ROS FPR2 MPO |
url |
http://journal.frontiersin.org/article/10.3389/fimmu.2017.00257/full |
work_keys_str_mv |
AT hallabjornsdottir phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT agnesdahlstrandrudin phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT felixpklose phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT jonaselmwall phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT amandawelin phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT mariosstylianou phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT karinchristenson phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT constantinfurban phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT huameiforsman phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT claesdahlgren phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT annakarlsson phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway AT johanbylund phenolsolublemodulinapeptidetoxinsfromaggressivestaphylococcusaureusinducerapidformationofneutrophilextracellulartrapsthroughareactiveoxygenspeciesindependentpathway |
_version_ |
1724881481218654208 |