TAK1 restricts spontaneous NLRP3 activation and cell death to control myeloid proliferation

The NOD-like receptor (NLR)-P3 inflammasome is a global sensor of infection and stress. Elevated NLRP3 activation levels are associated with human diseases, but the mechanisms controlling NLRP3 inflammasome activation are largely unknown. Here, we show that TGF-β activated kinase-1 (TAK1) is a centr...

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Veröffentlicht in:The Journal of experimental medicine Jg. 215; H. 4; S. 1023
Hauptverfasser: Malireddi, R K Subbarao, Gurung, Prajwal, Mavuluri, Jayadev, Dasari, Tejasvi Krishna, Klco, Jeffery M, Chi, Hongbo, Kanneganti, Thirumala-Devi
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States 02.04.2018
ISSN:1540-9538, 1540-9538
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Abstract The NOD-like receptor (NLR)-P3 inflammasome is a global sensor of infection and stress. Elevated NLRP3 activation levels are associated with human diseases, but the mechanisms controlling NLRP3 inflammasome activation are largely unknown. Here, we show that TGF-β activated kinase-1 (TAK1) is a central regulator of NLRP3 inflammasome activation and spontaneous cell death. Absence of TAK1 in macrophages induced spontaneous activation of the NLRP3 inflammasome without requiring toll-like receptor (TLR) priming and subsequent activating signals, suggesting a distinctive role for TAK1 in maintaining NLRP3 inflammasome homeostasis. Autocrine tumor necrosis factor (TNF) signaling in the absence of TAK1 induced spontaneous RIPK1-dependent NLRP3 inflammasome activation and cell death. We further showed that TAK1 suppressed homeostatic NF-κB and extracellular signal-related kinase (ERK) activation to limit spontaneous TNF production. Moreover, the spontaneous inflammation resulting from TAK1-deficient macrophages drives myeloid proliferation in mice, and was rescued by RIPK1 deficiency. Overall, these studies identify a critical role for TAK1 in maintaining NLRP3 inflammasome quiescence and preserving cellular homeostasis and survival.
AbstractList The NOD-like receptor (NLR)-P3 inflammasome is a global sensor of infection and stress. Elevated NLRP3 activation levels are associated with human diseases, but the mechanisms controlling NLRP3 inflammasome activation are largely unknown. Here, we show that TGF-β activated kinase-1 (TAK1) is a central regulator of NLRP3 inflammasome activation and spontaneous cell death. Absence of TAK1 in macrophages induced spontaneous activation of the NLRP3 inflammasome without requiring toll-like receptor (TLR) priming and subsequent activating signals, suggesting a distinctive role for TAK1 in maintaining NLRP3 inflammasome homeostasis. Autocrine tumor necrosis factor (TNF) signaling in the absence of TAK1 induced spontaneous RIPK1-dependent NLRP3 inflammasome activation and cell death. We further showed that TAK1 suppressed homeostatic NF-κB and extracellular signal-related kinase (ERK) activation to limit spontaneous TNF production. Moreover, the spontaneous inflammation resulting from TAK1-deficient macrophages drives myeloid proliferation in mice, and was rescued by RIPK1 deficiency. Overall, these studies identify a critical role for TAK1 in maintaining NLRP3 inflammasome quiescence and preserving cellular homeostasis and survival.
The NOD-like receptor (NLR)-P3 inflammasome is a global sensor of infection and stress. Elevated NLRP3 activation levels are associated with human diseases, but the mechanisms controlling NLRP3 inflammasome activation are largely unknown. Here, we show that TGF-β activated kinase-1 (TAK1) is a central regulator of NLRP3 inflammasome activation and spontaneous cell death. Absence of TAK1 in macrophages induced spontaneous activation of the NLRP3 inflammasome without requiring toll-like receptor (TLR) priming and subsequent activating signals, suggesting a distinctive role for TAK1 in maintaining NLRP3 inflammasome homeostasis. Autocrine tumor necrosis factor (TNF) signaling in the absence of TAK1 induced spontaneous RIPK1-dependent NLRP3 inflammasome activation and cell death. We further showed that TAK1 suppressed homeostatic NF-κB and extracellular signal-related kinase (ERK) activation to limit spontaneous TNF production. Moreover, the spontaneous inflammation resulting from TAK1-deficient macrophages drives myeloid proliferation in mice, and was rescued by RIPK1 deficiency. Overall, these studies identify a critical role for TAK1 in maintaining NLRP3 inflammasome quiescence and preserving cellular homeostasis and survival.The NOD-like receptor (NLR)-P3 inflammasome is a global sensor of infection and stress. Elevated NLRP3 activation levels are associated with human diseases, but the mechanisms controlling NLRP3 inflammasome activation are largely unknown. Here, we show that TGF-β activated kinase-1 (TAK1) is a central regulator of NLRP3 inflammasome activation and spontaneous cell death. Absence of TAK1 in macrophages induced spontaneous activation of the NLRP3 inflammasome without requiring toll-like receptor (TLR) priming and subsequent activating signals, suggesting a distinctive role for TAK1 in maintaining NLRP3 inflammasome homeostasis. Autocrine tumor necrosis factor (TNF) signaling in the absence of TAK1 induced spontaneous RIPK1-dependent NLRP3 inflammasome activation and cell death. We further showed that TAK1 suppressed homeostatic NF-κB and extracellular signal-related kinase (ERK) activation to limit spontaneous TNF production. Moreover, the spontaneous inflammation resulting from TAK1-deficient macrophages drives myeloid proliferation in mice, and was rescued by RIPK1 deficiency. Overall, these studies identify a critical role for TAK1 in maintaining NLRP3 inflammasome quiescence and preserving cellular homeostasis and survival.
Author Mavuluri, Jayadev
Kanneganti, Thirumala-Devi
Malireddi, R K Subbarao
Gurung, Prajwal
Dasari, Tejasvi Krishna
Klco, Jeffery M
Chi, Hongbo
Author_xml – sequence: 1
  givenname: R K Subbarao
  surname: Malireddi
  fullname: Malireddi, R K Subbarao
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN
– sequence: 2
  givenname: Prajwal
  surname: Gurung
  fullname: Gurung, Prajwal
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN
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  givenname: Jayadev
  surname: Mavuluri
  fullname: Mavuluri, Jayadev
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN
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  givenname: Tejasvi Krishna
  surname: Dasari
  fullname: Dasari, Tejasvi Krishna
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN
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  givenname: Jeffery M
  orcidid: 0000-0003-2961-6960
  surname: Klco
  fullname: Klco, Jeffery M
  organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN
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  orcidid: 0000-0002-9997-2496
  surname: Chi
  fullname: Chi, Hongbo
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN
– sequence: 7
  givenname: Thirumala-Devi
  orcidid: 0000-0002-6395-6443
  surname: Kanneganti
  fullname: Kanneganti, Thirumala-Devi
  email: Thirumala-Devi.Kanneganti@StJude.org
  organization: Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN Thirumala-Devi.Kanneganti@StJude.org
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29500178$$D View this record in MEDLINE/PubMed
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Title TAK1 restricts spontaneous NLRP3 activation and cell death to control myeloid proliferation
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