Targeting NLRP3 and Staphylococcal pore‐forming toxin receptors in human‐induced pluripotent stem cell‐derived macrophages

Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front‐line immune cells. The mechanism by which leukocidins kill innate immune cells and trigger inflammation during S. aureus lung infection, however, remains unresolved. Here, we explored human‐i...

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Published inJournal of leukocyte biology Vol. 108; no. 3; pp. 967 - 981
Main Authors Chow, Seong H., Deo, Pankaj, Yeung, Amy T. Y., Kostoulias, Xenia P., Jeon, Yusun, Gao, Mei‐Ling, Seidi, Azadeh, Olivier, Françios Alwyn Benson, Sridhar, Sushmita, Nethercott, Cara, Cameron, David, Robertson, Avril A. B., Robert, Remy, Mackay, Charles R., Traven, Ana, Jin, Zi‐Bing, Hale, Christine, Dougan, Gordon, Peleg, Anton Y., Naderer, Thomas
Format Journal Article
LanguageEnglish
Published United States 01.09.2020
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Abstract Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front‐line immune cells. The mechanism by which leukocidins kill innate immune cells and trigger inflammation during S. aureus lung infection, however, remains unresolved. Here, we explored human‐induced pluripotent stem cell‐derived macrophages (hiPSC‐dMs) to study the interaction of the leukocidins Panton–Valentine leukocidin (PVL) and LukAB with lung macrophages, which are the initial leukocidin targets during S. aureus lung invasion. hiPSC‐dMs were susceptible to the leukocidins PVL and LukAB and both leukocidins triggered NLPR3 inflammasome activation resulting in IL‐1β secretion. hiPSC‐dM cell death after LukAB exposure, however, was only temporarily dependent of NLRP3, although NLRP3 triggered marked cell death after PVL treatment. CRISPR/Cas9‐mediated deletion of the PVL receptor, C5aR1, protected hiPSC‐dMs from PVL cytotoxicity, despite the expression of other leukocidin receptors, such as CD45. PVL‐deficient S. aureus had reduced ability to induce lung IL‐1β levels in human C5aR1 knock‐in mice. Unexpectedly, inhibiting NLRP3 activity resulted in increased wild‐type S. aureus lung burdens. Our findings suggest that NLRP3 induces macrophage death and IL‐1β secretion after PVL exposure and controls S. aureus lung burdens. S. aureus leukocidin PVL triggers NLRP3 mediated cell death in human stem‐cell derived macrophages and humanized C5aR1 macrophages, leading to increased bacterial lung burdens.
AbstractList Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front-line immune cells. The mechanism by which leukocidins kill innate immune cells and trigger inflammation during S. aureus lung infection, however, remains unresolved. Here, we explored human-induced pluripotent stem cell-derived macrophages (hiPSC-dMs) to study the interaction of the leukocidins Panton-Valentine leukocidin (PVL) and LukAB with lung macrophages, which are the initial leukocidin targets during S. aureus lung invasion. hiPSC-dMs were susceptible to the leukocidins PVL and LukAB and both leukocidins triggered NLPR3 inflammasome activation resulting in IL-1β secretion. hiPSC-dM cell death after LukAB exposure, however, was only temporarily dependent of NLRP3, although NLRP3 triggered marked cell death after PVL treatment. CRISPR/Cas9-mediated deletion of the PVL receptor, C5aR1, protected hiPSC-dMs from PVL cytotoxicity, despite the expression of other leukocidin receptors, such as CD45. PVL-deficient S. aureus had reduced ability to induce lung IL-1β levels in human C5aR1 knock-in mice. Unexpectedly, inhibiting NLRP3 activity resulted in increased wild-type S. aureus lung burdens. Our findings suggest that NLRP3 induces macrophage death and IL-1β secretion after PVL exposure and controls S. aureus lung burdens.
Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front‐line immune cells. The mechanism by which leukocidins kill innate immune cells and trigger inflammation during S. aureus lung infection, however, remains unresolved. Here, we explored human‐induced pluripotent stem cell‐derived macrophages (hiPSC‐dMs) to study the interaction of the leukocidins Panton–Valentine leukocidin (PVL) and LukAB with lung macrophages, which are the initial leukocidin targets during S. aureus lung invasion. hiPSC‐dMs were susceptible to the leukocidins PVL and LukAB and both leukocidins triggered NLPR3 inflammasome activation resulting in IL‐1β secretion. hiPSC‐dM cell death after LukAB exposure, however, was only temporarily dependent of NLRP3, although NLRP3 triggered marked cell death after PVL treatment. CRISPR/Cas9‐mediated deletion of the PVL receptor, C5aR1, protected hiPSC‐dMs from PVL cytotoxicity, despite the expression of other leukocidin receptors, such as CD45. PVL‐deficient S. aureus had reduced ability to induce lung IL‐1β levels in human C5aR1 knock‐in mice. Unexpectedly, inhibiting NLRP3 activity resulted in increased wild‐type S. aureus lung burdens. Our findings suggest that NLRP3 induces macrophage death and IL‐1β secretion after PVL exposure and controls S. aureus lung burdens. S. aureus leukocidin PVL triggers NLRP3 mediated cell death in human stem‐cell derived macrophages and humanized C5aR1 macrophages, leading to increased bacterial lung burdens.
Author Mackay, Charles R.
Robertson, Avril A. B.
Seidi, Azadeh
Peleg, Anton Y.
Hale, Christine
Dougan, Gordon
Jeon, Yusun
Sridhar, Sushmita
Cameron, David
Robert, Remy
Naderer, Thomas
Gao, Mei‐Ling
Kostoulias, Xenia P.
Jin, Zi‐Bing
Nethercott, Cara
Chow, Seong H.
Deo, Pankaj
Traven, Ana
Yeung, Amy T. Y.
Olivier, Françios Alwyn Benson
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Keywords NLRP3
macrophage
pneumonia
toxin
inflammation
staphylococcus
Language English
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Snippet Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front‐line immune cells. The mechanism by which...
Staphylococcus aureus causes necrotizing pneumonia by secreting toxins such as leukocidins that target front-line immune cells. The mechanism by which...
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wiley
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StartPage 967
SubjectTerms Animals
Bacterial Proteins - antagonists & inhibitors
Bacterial Toxins - antagonists & inhibitors
CD11b Antigen - immunology
Cell Differentiation
Cells, Cultured
CRISPR-Cas Systems
Exotoxins - antagonists & inhibitors
Exotoxins - deficiency
Gene Knock-In Techniques
Humans
Induced Pluripotent Stem Cells - cytology
inflammation
Interleukin-1beta - metabolism
Leukocidins - antagonists & inhibitors
Leukocyte Common Antigens - physiology
Lung - immunology
Lung - microbiology
macrophage
Macrophages - cytology
Macrophages - drug effects
Macrophages - immunology
Mice
Mice, Inbred C57BL
Monocytes - cytology
NLR Family, Pyrin Domain-Containing 3 Protein - antagonists & inhibitors
NLRP3
Peptide Fragments - immunology
pneumonia
Pneumonia, Staphylococcal - immunology
Protein Subunits
Receptor, Anaphylatoxin C5a - deficiency
Receptor, Anaphylatoxin C5a - drug effects
Receptor, Anaphylatoxin C5a - genetics
Receptor, Anaphylatoxin C5a - physiology
Recombinant Proteins - metabolism
staphylococcus
Staphylococcus aureus - physiology
toxin
Title Targeting NLRP3 and Staphylococcal pore‐forming toxin receptors in human‐induced pluripotent stem cell‐derived macrophages
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2FJLB.4MA0420-497R
https://www.ncbi.nlm.nih.gov/pubmed/32531864
Volume 108
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