Hepatocytes Are Resistant to Cell Death From Canonical and Non-Canonical Inflammasome-Activated Pyroptosis.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2022
Historique:
received: 11 08 2021
revised: 30 11 2021
accepted: 30 11 2021
pubmed: 11 12 2021
medline: 5 4 2022
entrez: 10 12 2021
Statut: ppublish

Résumé

Pyroptosis, gasdermin-mediated programmed cell death, is readily induced in macrophages by activation of the canonical inflammasome (caspase-1) or by intracellular lipopolysaccharide (LPS)-mediated non-canonical inflammasome (caspase-11) activation. However, whether pyroptosis is induced similarly in hepatocytes is still largely controversial but highly relevant to liver pathologies such as alcoholic/nonalcoholic liver disease, drug-induced liver injury, ischemia-reperfusion and liver transplant injury, or organ damage secondary to sepsis. In this study we found that hepatocytes activate and cleave gasdermin-D (GSDMD) at low levels after treatment with LPS. Overexpression of caspase-1 or caspase-11 p10/p20 activated domains was able to induce typical GSDMD-dependent pyroptosis in hepatocytes both in vitro and in vivo. However, morphologic features of pyroptosis in macrophages (eg, pyroptotic bodies, cell flattening, loss of cell structure) did not occur in pyroptotic hepatocytes, with cell structure remaining relatively intact despite the cell membrane being breached. Our results suggest that hepatocytes activate pyroptosis pathways and cleave GSDMD, but this does not result in cell rupture and confer the same pyroptotic morphologic changes as previously reported in macrophages. This is true even with caspase-1 or caspase-11 artificial overexpression way above levels seen endogenously even after priming or in pathologic conditions. Our novel findings characterize hepatocyte morphology in pyroptosis and suggest alternative use for canonical/non-canonical inflammasome activation/signaling and subsequent GSDMD cleavage because there is no rapid cell death as in macrophages. Improved understanding and recognition of the role of these pathways in hepatocytes may result in novel therapeutics for a range of liver diseases.

Sections du résumé

BACKGROUND
Pyroptosis, gasdermin-mediated programmed cell death, is readily induced in macrophages by activation of the canonical inflammasome (caspase-1) or by intracellular lipopolysaccharide (LPS)-mediated non-canonical inflammasome (caspase-11) activation. However, whether pyroptosis is induced similarly in hepatocytes is still largely controversial but highly relevant to liver pathologies such as alcoholic/nonalcoholic liver disease, drug-induced liver injury, ischemia-reperfusion and liver transplant injury, or organ damage secondary to sepsis.
METHODS AND RESULTS
In this study we found that hepatocytes activate and cleave gasdermin-D (GSDMD) at low levels after treatment with LPS. Overexpression of caspase-1 or caspase-11 p10/p20 activated domains was able to induce typical GSDMD-dependent pyroptosis in hepatocytes both in vitro and in vivo. However, morphologic features of pyroptosis in macrophages (eg, pyroptotic bodies, cell flattening, loss of cell structure) did not occur in pyroptotic hepatocytes, with cell structure remaining relatively intact despite the cell membrane being breached. Our results suggest that hepatocytes activate pyroptosis pathways and cleave GSDMD, but this does not result in cell rupture and confer the same pyroptotic morphologic changes as previously reported in macrophages. This is true even with caspase-1 or caspase-11 artificial overexpression way above levels seen endogenously even after priming or in pathologic conditions.
CONCLUSIONS
Our novel findings characterize hepatocyte morphology in pyroptosis and suggest alternative use for canonical/non-canonical inflammasome activation/signaling and subsequent GSDMD cleavage because there is no rapid cell death as in macrophages. Improved understanding and recognition of the role of these pathways in hepatocytes may result in novel therapeutics for a range of liver diseases.

Identifiants

pubmed: 34890842
pii: S2352-345X(21)00247-2
doi: 10.1016/j.jcmgh.2021.11.009
pmc: PMC8783146
pii:
doi:

Substances chimiques

Inflammasomes 0
Intracellular Signaling Peptides and Proteins 0
Phosphate-Binding Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

739-757

Subventions

Organisme : BLRD VA
ID : IK6 BX004211
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK120531
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL139547
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM102146
Pays : United States
Organisme : BLRD VA
ID : I01 BX004838
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Ping Sun (P)

Department of Hepatobiliary Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania.

Jie Zhong (J)

Department of Burn and Plastic Surgery, The Second Xiangya Hospital of Central South University, Changsha, China.

Hong Liao (H)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania.

Patricia Loughran (P)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania.

Joud Mulla (J)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania.

Guang Fu (G)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Department of General Surgery, The Third Xiangya Hospital, Central South University, Changsha, China.

Da Tang (D)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Department of General Surgery, The Third Xiangya Hospital, Central South University, Changsha, China.

Jie Fan (J)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Research and Development, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, Pennsylvania.

Timothy R Billiar (TR)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania.

Wentao Gao (W)

Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania.

Melanie J Scott (MJ)

Department of Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania; Pittsburgh Liver Research Center, University of Pittsburgh, Pittsburgh, Pennsylvania. Electronic address: scottm@upmc.edu.

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Classifications MeSH