Ubiquitylation of MLKL at lysine 219 positively regulates necroptosis-induced tissue injury and pathogen clearance

Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membran...

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Published inNature communications Vol. 12; no. 1; pp. 3364 - 18
Main Authors Garcia, Laura Ramos, Tenev, Tencho, Newman, Richard, Haich, Rachel O., Liccardi, Gianmaria, John, Sidonie Wicky, Annibaldi, Alessandro, Yu, Lu, Pardo, Mercedes, Young, Samuel N., Fitzgibbon, Cheree, Fernando, Winnie, Guppy, Naomi, Kim, Hyojin, Liang, Lung-Yu, Lucet, Isabelle S., Kueh, Andrew, Roxanis, Ioannis, Gazinska, Patrycja, Sims, Martin, Smyth, Tomoko, Ward, George, Bertin, John, Beal, Allison M., Geddes, Brad, Choudhary, Jyoti S., Murphy, James M., Aurelia Ball, K., Upton, Jason W., Meier, Pascal
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 07.06.2021
Nature Publishing Group
Nature Portfolio
Subjects
13/106
14/34
38/70
631/337/458/582
631/80/458/582
631/80/82/2344
64/60
82/58
96/1
Animals
Apoptosis
Assembly
Cell death
Cell Line
Cells, Cultured
Clearances
Cytotoxicity
HEK293 Cells
Herpesviridae Infections - genetics
Herpesviridae Infections - metabolism
Herpesviridae Infections - virology
HT29 Cells
Humanities and Social Sciences
Humans
Inflammation
Lysine
Lysine - genetics
Lysine - metabolism
Membranes
Mice
Mice, Inbred C57BL
Mice, Knockout
Mortality
multidisciplinary
Muromegalovirus - physiology
Mutation
Necroptosis
Necroptosis - genetics
Necrosis
NIH 3T3 Cells
Oligomerization
Pathogenesis
Pathogens
Phosphorylation
Protein Kinases - genetics
Protein Kinases - metabolism
Rupture
Science
Science (multidisciplinary)
Signalling systems
Skin - metabolism
Skin - pathology
Toxicity
Translocation
Ubiquitin
Ubiquitination
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Abstract Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system. Necroptosis is a form of cell death characterized by membrane rupture via MLKL oligomerization, although mechanistic details remain unclear. Here, the authors show that MLKL ubiquitylation of K219 facilitates high-order membrane assembly and subsequent rupture, promoting cytotoxicity.
AbstractList Necroptosis is a form of cell death characterized by membrane rupture via MLKL oligomerization, although mechanistic details remain unclear. Here, the authors show that MLKL ubiquitylation of K219 facilitates high-order membrane assembly and subsequent rupture, promoting cytotoxicity.
Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system.
Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system.Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system.
Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system. Necroptosis is a form of cell death characterized by membrane rupture via MLKL oligomerization, although mechanistic details remain unclear. Here, the authors show that MLKL ubiquitylation of K219 facilitates high-order membrane assembly and subsequent rupture, promoting cytotoxicity.
Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis is triggered by RIPK3-mediated phosphorylation of MLKL, which is thought to initiate MLKL oligomerisation, membrane translocation and membrane rupture, although the precise mechanism is incompletely understood. Here, we show that K63-linked ubiquitin chains are attached to MLKL during necroptosis and that ubiquitylation of MLKL at K219 significantly contributes to the cytotoxic potential of phosphorylated MLKL. The K219R MLKL mutation protects animals from necroptosis-induced skin damage and renders cells resistant to pathogen-induced necroptosis. Mechanistically, we show that ubiquitylation of MLKL at K219 is required for higher-order assembly of MLKL at membranes, facilitating its rupture and necroptosis. We demonstrate that K219 ubiquitylation licenses MLKL activity to induce lytic cell death, suggesting that necroptotic clearance of pathogens as well as MLKL-dependent pathologies are influenced by the ubiquitin-signalling system.Necroptosis is a form of cell death characterized by membrane rupture via MLKL oligomerization, although mechanistic details remain unclear. Here, the authors show that MLKL ubiquitylation of K219 facilitates high-order membrane assembly and subsequent rupture, promoting cytotoxicity.
ArticleNumber 3364
Author Beal, Allison M.
Liccardi, Gianmaria
Fitzgibbon, Cheree
Liang, Lung-Yu
Murphy, James M.
Haich, Rachel O.
Upton, Jason W.
Ward, George
Kueh, Andrew
Geddes, Brad
Meier, Pascal
Gazinska, Patrycja
Choudhary, Jyoti S.
Newman, Richard
Tenev, Tencho
Young, Samuel N.
Pardo, Mercedes
Roxanis, Ioannis
Smyth, Tomoko
Guppy, Naomi
Lucet, Isabelle S.
Bertin, John
Kim, Hyojin
Annibaldi, Alessandro
Fernando, Winnie
Aurelia Ball, K.
John, Sidonie Wicky
Yu, Lu
Sims, Martin
Garcia, Laura Ramos
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34099649$$D View this record in MEDLINE/PubMed
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  publication-title: Mol. Cell
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    fullname: BK Fiil
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  publication-title: Cell
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    fullname: L Sun
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  publication-title: Cell Death Differ.
  doi: 10.1038/s41418-018-0172-x
  contributor:
    fullname: H Nailwal
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Snippet Necroptosis is a lytic, inflammatory form of cell death that not only contributes to pathogen clearance but can also lead to disease pathogenesis. Necroptosis...
Necroptosis is a form of cell death characterized by membrane rupture via MLKL oligomerization, although mechanistic details remain unclear. Here, the authors...
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SubjectTerms 13/106
14/34
38/70
631/337/458/582
631/80/458/582
631/80/82/2344
64/60
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96/1
Animals
Apoptosis
Assembly
Cell death
Cell Line
Cells, Cultured
Clearances
Cytotoxicity
HEK293 Cells
Herpesviridae Infections - genetics
Herpesviridae Infections - metabolism
Herpesviridae Infections - virology
HT29 Cells
Humanities and Social Sciences
Humans
Inflammation
Lysine
Lysine - genetics
Lysine - metabolism
Membranes
Mice
Mice, Inbred C57BL
Mice, Knockout
Mortality
multidisciplinary
Muromegalovirus - physiology
Mutation
Necroptosis
Necroptosis - genetics
Necrosis
NIH 3T3 Cells
Oligomerization
Pathogenesis
Pathogens
Phosphorylation
Protein Kinases - genetics
Protein Kinases - metabolism
Rupture
Science
Science (multidisciplinary)
Signalling systems
Skin - metabolism
Skin - pathology
Toxicity
Translocation
Ubiquitin
Ubiquitination
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Title Ubiquitylation of MLKL at lysine 219 positively regulates necroptosis-induced tissue injury and pathogen clearance
URI https://link.springer.com/article/10.1038/s41467-021-23474-5
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https://pubmed.ncbi.nlm.nih.gov/PMC8184782
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Volume 12
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