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 in | Journal of leukocyte biology Vol. 108; no. 3; pp. 967 - 981 |
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Main Authors | , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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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. |
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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 |
Author_xml | – sequence: 1 givenname: Seong H. surname: Chow fullname: Chow, Seong H. organization: Monash University – sequence: 2 givenname: Pankaj surname: Deo fullname: Deo, Pankaj organization: Monash University – sequence: 3 givenname: Amy T. Y. surname: Yeung fullname: Yeung, Amy T. Y. organization: Wellcome Genome Campus – sequence: 4 givenname: Xenia P. surname: Kostoulias fullname: Kostoulias, Xenia P. organization: Monash University – sequence: 5 givenname: Yusun surname: Jeon fullname: Jeon, Yusun organization: Monash University – sequence: 6 givenname: Mei‐Ling surname: Gao fullname: Gao, Mei‐Ling organization: Optometry and Visual Science – sequence: 7 givenname: Azadeh surname: Seidi fullname: Seidi, Azadeh organization: Monash University – sequence: 8 givenname: Françios Alwyn Benson surname: Olivier fullname: Olivier, Françios Alwyn Benson organization: Monash University – sequence: 9 givenname: Sushmita surname: Sridhar fullname: Sridhar, Sushmita organization: Wellcome Genome Campus – sequence: 10 givenname: Cara surname: Nethercott fullname: Nethercott, Cara organization: Monash University – sequence: 11 givenname: David surname: Cameron fullname: Cameron, David organization: Monash University – sequence: 12 givenname: Avril A. B. surname: Robertson fullname: Robertson, Avril A. B. organization: The University of Queensland – sequence: 13 givenname: Remy surname: Robert fullname: Robert, Remy organization: Monash University – sequence: 14 givenname: Charles R. surname: Mackay fullname: Mackay, Charles R. organization: Monash University – sequence: 15 givenname: Ana surname: Traven fullname: Traven, Ana organization: Monash University – sequence: 16 givenname: Zi‐Bing surname: Jin fullname: Jin, Zi‐Bing organization: Optometry and Visual Science – sequence: 17 givenname: Christine surname: Hale fullname: Hale, Christine organization: Wellcome Genome Campus – sequence: 18 givenname: Gordon surname: Dougan fullname: Dougan, Gordon organization: Addenbrookes Hospital – sequence: 19 givenname: Anton Y. surname: Peleg fullname: Peleg, Anton Y. email: anton.peleg@monash.edu organization: Monash University – sequence: 20 givenname: Thomas orcidid: 0000-0002-4392-3863 surname: Naderer fullname: Naderer, Thomas email: thomas.naderer@monash.edu organization: Monash University |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32531864$$D View this record in MEDLINE/PubMed |
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Keywords | NLRP3 macrophage pneumonia toxin inflammation staphylococcus |
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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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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 |
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