Streptolysin O accelerates the conversion of plasminogen to plasmin

Abstract Group A Streptococcus (GAS) is a human-specific bacterial pathogen that can exploit the plasminogen-plasmin fibrinolysis system to dismantle blood clots and facilitate its spread and survival within the human host. In this study, we use affinity-enrichment mass spectrometry to decipher the...

Full description

Saved in:
Bibliographic Details
Main Authors: Di Tang, Hamed Khakzad, Elisabeth Hjortswang, Lars Malmström, Simon Ekström, Lotta Happonen, Johan Malmström
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54173-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846147597458210816
author Di Tang
Hamed Khakzad
Elisabeth Hjortswang
Lars Malmström
Simon Ekström
Lotta Happonen
Johan Malmström
author_facet Di Tang
Hamed Khakzad
Elisabeth Hjortswang
Lars Malmström
Simon Ekström
Lotta Happonen
Johan Malmström
author_sort Di Tang
collection DOAJ
description Abstract Group A Streptococcus (GAS) is a human-specific bacterial pathogen that can exploit the plasminogen-plasmin fibrinolysis system to dismantle blood clots and facilitate its spread and survival within the human host. In this study, we use affinity-enrichment mass spectrometry to decipher the host-pathogen protein-protein interaction between plasminogen and streptolysin O, a key cytolytic toxin produced by GAS. This interaction accelerates the conversion of plasminogen to plasmin by both the host tissue-type plasminogen activator and streptokinase, a bacterial plasminogen activator secreted by GAS. Integrative structural mass spectrometry analysis shows that the interaction induces local conformational shifts in plasminogen. These changes lead to the formation of a stabilised intermediate plasminogen-streptolysin O complex that becomes significantly more susceptible to proteolytic processing by plasminogen activators. Our findings reveal a conserved and moonlighting pathomechanistic function for streptolysin O that extends beyond its well-characterised cytolytic activity.
format Article
id doaj-art-7a7df040b83f4bdcb65b329cdce788b1
institution Kabale University
issn 2041-1723
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-7a7df040b83f4bdcb65b329cdce788b12024-12-01T12:35:33ZengNature PortfolioNature Communications2041-17232024-11-0115111510.1038/s41467-024-54173-6Streptolysin O accelerates the conversion of plasminogen to plasminDi Tang0Hamed Khakzad1Elisabeth Hjortswang2Lars Malmström3Simon Ekström4Lotta Happonen5Johan Malmström6Division of Infection Medicine, Department of Clinical Sciences Lund, Faculty of Medicine, Lund UniversityUniversité de Lorraine, CNRS, Inria, LORIADivision of Infection Medicine, Department of Clinical Sciences Lund, Faculty of Medicine, Lund UniversityDivision of Infection Medicine, Department of Clinical Sciences Lund, Faculty of Medicine, Lund UniversitySciLifeLab, Integrated Structural Biology Platform, Structural Proteomics Unit Sweden, Lund UniversityDivision of Infection Medicine, Department of Clinical Sciences Lund, Faculty of Medicine, Lund UniversityDivision of Infection Medicine, Department of Clinical Sciences Lund, Faculty of Medicine, Lund UniversityAbstract Group A Streptococcus (GAS) is a human-specific bacterial pathogen that can exploit the plasminogen-plasmin fibrinolysis system to dismantle blood clots and facilitate its spread and survival within the human host. In this study, we use affinity-enrichment mass spectrometry to decipher the host-pathogen protein-protein interaction between plasminogen and streptolysin O, a key cytolytic toxin produced by GAS. This interaction accelerates the conversion of plasminogen to plasmin by both the host tissue-type plasminogen activator and streptokinase, a bacterial plasminogen activator secreted by GAS. Integrative structural mass spectrometry analysis shows that the interaction induces local conformational shifts in plasminogen. These changes lead to the formation of a stabilised intermediate plasminogen-streptolysin O complex that becomes significantly more susceptible to proteolytic processing by plasminogen activators. Our findings reveal a conserved and moonlighting pathomechanistic function for streptolysin O that extends beyond its well-characterised cytolytic activity.https://doi.org/10.1038/s41467-024-54173-6
spellingShingle Di Tang
Hamed Khakzad
Elisabeth Hjortswang
Lars Malmström
Simon Ekström
Lotta Happonen
Johan Malmström
Streptolysin O accelerates the conversion of plasminogen to plasmin
Nature Communications
title Streptolysin O accelerates the conversion of plasminogen to plasmin
title_full Streptolysin O accelerates the conversion of plasminogen to plasmin
title_fullStr Streptolysin O accelerates the conversion of plasminogen to plasmin
title_full_unstemmed Streptolysin O accelerates the conversion of plasminogen to plasmin
title_short Streptolysin O accelerates the conversion of plasminogen to plasmin
title_sort streptolysin o accelerates the conversion of plasminogen to plasmin
url https://doi.org/10.1038/s41467-024-54173-6
work_keys_str_mv AT ditang streptolysinoacceleratestheconversionofplasminogentoplasmin
AT hamedkhakzad streptolysinoacceleratestheconversionofplasminogentoplasmin
AT elisabethhjortswang streptolysinoacceleratestheconversionofplasminogentoplasmin
AT larsmalmstrom streptolysinoacceleratestheconversionofplasminogentoplasmin
AT simonekstrom streptolysinoacceleratestheconversionofplasminogentoplasmin
AT lottahapponen streptolysinoacceleratestheconversionofplasminogentoplasmin
AT johanmalmstrom streptolysinoacceleratestheconversionofplasminogentoplasmin