ROS-dependent S-palmitoylation activates cleaved and intact gasdermin D
Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT) 1 – 10 . Here we report that GS...
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| Published in | Nature (London) Vol. 630; no. 8016; pp. 437 - 446 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
13.06.2024
Nature Publishing Group |
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| Online Access | Get full text |
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| Abstract | Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT)
1
–
10
. Here we report that GSDMD Cys191 is
S
-palmitoylated and that palmitoylation is required for pore formation.
S
-palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family.
Gasdermin D Cys191 is
S
-palmitoylated, and palmitoylation is required for pore formation. |
|---|---|
| AbstractList | Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT)
. Here we report that GSDMD Cys191 is S-palmitoylated and that palmitoylation is required for pore formation. S-palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family. Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT) 1 – 10 . Here we report that GSDMD Cys191 is S -palmitoylated and that palmitoylation is required for pore formation. S -palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family. Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT)110. Here we report that GSDMD Cysl91 is 5-palmitoylated and that palmitoylation is required for pore formation. 5-palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family. Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT) 1 – 10 . Here we report that GSDMD Cys191 is S -palmitoylated and that palmitoylation is required for pore formation. S -palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family. Gasdermin D Cys191 is S -palmitoylated, and palmitoylation is required for pore formation. Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT)1-10. Here we report that GSDMD Cys191 is S-palmitoylated and that palmitoylation is required for pore formation. S-palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family.Gasdermin D (GSDMD) is the common effector for cytokine secretion and pyroptosis downstream of inflammasome activation and was previously shown to form large transmembrane pores after cleavage by inflammatory caspases to generate the GSDMD N-terminal domain (GSDMD-NT)1-10. Here we report that GSDMD Cys191 is S-palmitoylated and that palmitoylation is required for pore formation. S-palmitoylation, which does not affect GSDMD cleavage, is augmented by mitochondria-generated reactive oxygen species (ROS). Cleavage-deficient GSDMD (D275A) is also palmitoylated after inflammasome stimulation or treatment with ROS activators and causes pyroptosis, although less efficiently than palmitoylated GSDMD-NT. Palmitoylated, but not unpalmitoylated, full-length GSDMD induces liposome leakage and forms a pore similar in structure to GSDMD-NT pores shown by cryogenic electron microscopy. ZDHHC5 and ZDHHC9 are the major palmitoyltransferases that mediate GSDMD palmitoylation, and their expression is upregulated by inflammasome activation and ROS. The other human gasdermins are also palmitoylated at their N termini. These data challenge the concept that cleavage is the only trigger for GSDMD activation. They suggest that reversible palmitoylation is a checkpoint for pore formation by both GSDMD-NT and intact GSDMD that functions as a general switch for the activation of this pore-forming family. |
| Author | Walker, Caitlin Wu, Hao Oh, Sungwhan F. David, Liron Balasubramanian, Arumugam El-Baba, Tarick J. Ma, Xiyu Fontana, Pietro Dong, Ying Luo, Hongbo R. Devant, Pascal Banerjee, Anirban Healy, Liam B. Lutomski, Corinne A. Goh, Byoungsook Puthenveetil, Robbins Kagan, Jonathan C. Gu, Bowen Robinson, Carol V. Du, Gang Miao, Rui Lieberman, Judy Pi, Xiong |
| AuthorAffiliation | 6 Department of Pediatrics, Harvard Medical School, Boston, MA, USA 10 Section on Structural and Chemical Biology, Neurosciences and Cellular and Structural Biology Division, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA 5 Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Boston, MA, USA 9 Department of Laboratory Medicine, Boston Children’s Hospital, Boston, MA, USA 11 Present address: Department of Life Sciences, Ben-Gurion University of the Negev, Be’er Sheva, Israel 7 Harvard Medical School and Division of Gastroenterology, Boston Children’s Hospital, Boston, MA, USA 8 Department of Pathology, Dana-Farber/Harvard Cancer Center, Harvard Medical School, Boston, MA, USA 2 Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Boston, MA, USA 12 Present address: Seqirus, Cambridge, MA, USA 1 D |
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| Author_xml | – sequence: 1 givenname: Gang orcidid: 0000-0003-0805-4778 surname: Du fullname: Du, Gang email: gdu@crystal.harvard.edu organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital – sequence: 2 givenname: Liam B. orcidid: 0000-0002-2640-1596 surname: Healy fullname: Healy, Liam B. organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital – sequence: 3 givenname: Liron orcidid: 0000-0002-9750-543X surname: David fullname: David, Liron email: david@crystal.harvard.edu organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Seqirus – sequence: 4 givenname: Caitlin orcidid: 0000-0003-0977-8276 surname: Walker fullname: Walker, Caitlin organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Department of Life Sciences, Ben-Gurion University of the Negev – sequence: 5 givenname: Tarick J. orcidid: 0000-0003-4497-9938 surname: El-Baba fullname: El-Baba, Tarick J. organization: Department of Chemistry, University of Oxford, Kavli Institute for NanoScience Discovery, University of Oxford – sequence: 6 givenname: Corinne A. orcidid: 0000-0001-7509-103X surname: Lutomski fullname: Lutomski, Corinne A. organization: Department of Chemistry, University of Oxford, Kavli Institute for NanoScience Discovery, University of Oxford – sequence: 7 givenname: Byoungsook orcidid: 0000-0002-7894-7259 surname: Goh fullname: Goh, Byoungsook organization: Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital – sequence: 8 givenname: Bowen orcidid: 0000-0003-2629-9963 surname: Gu fullname: Gu, Bowen organization: Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Department of Pediatrics, Harvard Medical School – sequence: 9 givenname: Xiong orcidid: 0000-0001-8835-6914 surname: Pi fullname: Pi, Xiong organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital – sequence: 10 givenname: Pascal orcidid: 0000-0001-9743-6764 surname: Devant fullname: Devant, Pascal organization: Harvard Medical School and Division of Gastroenterology, Boston Children’s Hospital – sequence: 11 givenname: Pietro orcidid: 0000-0003-3215-3784 surname: Fontana fullname: Fontana, Pietro organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital – sequence: 12 givenname: Ying surname: Dong 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38599239$$D View this record in MEDLINE/PubMed |
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| Language | English |
| License | 2024. The Author(s), under exclusive licence to Springer Nature Limited. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally: Gang Du, Liam B. Healy. Author contributions H.W., G.D., L.B.H., L.D., C.W. and J.L. conceived the study. G.D. designed and performed most of the experiments. L.B.H. designed and performed most of the remaining experiments. T.J.E.-B. and C.A.L. designed and performed intact MS under C.V.R.’s supervision. B. Goh and G.D. designed and performed UPLC–MS/MS analysis with S.F.O. and H.W.’s supervision. B. Gu performed CRISPR–Cas9 knockout of ZDHHC5 and ZDHHC9 under J.L.’s supervision. P.D. prepared primary BMDMs under J.C.K.’s supervision. A. Balasubramanian and H.R.L. provided siRNAs for knocking down ZDHHC genes. X.P. helped with cryo-EM data processing for full-length GSDMD pore structure. P.F. and Y.D. helped with GSDMD and CASP1 expression, respectively. R.M. provided Crls1- or Plscr3-KO iBMDMs. X.M. attempted knock-in of the Halo tag to GSDMD in THP-1 cells. R.P. and A. Banerjee provided Heatil screen constructs. H.W., L.B.H., G.D. and J.L. wrote the manuscript with input from all of the authors. |
| ORCID | 0000-0003-0977-8276 0000-0002-7281-8579 0000-0001-7509-103X 0000-0002-8545-0451 0000-0001-8835-6914 0000-0001-9743-6764 0000-0002-6200-4715 0000-0003-3215-3784 0000-0002-7894-7259 0000-0002-2640-1596 0000-0003-2364-2746 0000-0003-4497-9938 0000-0003-2629-9963 0000-0003-1494-6801 0000-0002-7333-8542 0000-0002-0280-7903 0000-0001-7829-5505 0000-0003-0805-4778 0000-0002-9750-543X |
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| PublicationDate | 2024-06-13 |
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| Title | ROS-dependent S-palmitoylation activates cleaved and intact gasdermin D |
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