The role of RIPK3 in liver mitochondria bioenergetics and function.
NAFLD
NASH
RIPK3
mitochondria
necroptosis
Journal
European journal of clinical investigation
ISSN: 1365-2362
Titre abrégé: Eur J Clin Invest
Pays: England
ID NLM: 0245331
Informations de publication
Date de publication:
Mar 2022
Mar 2022
Historique:
revised:
03
07
2021
received:
06
06
2021
accepted:
03
07
2021
pubmed:
6
7
2021
medline:
18
3
2022
entrez:
5
7
2021
Statut:
ppublish
Résumé
Receptor-interacting protein kinase 3 (RIPK3) is a key player of regulated necrosis or necroptosis, an inflammatory form of cell death possibly governing outcomes in chronic liver diseases, such as nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. This narrative review is based on literature search using PubMed. RIPK3 activation depends on post-transcriptional modifications, including phosphorylation, hence coordinating the assembly of macromolecular death complex named 'necrosome', which may also involve diverse mitochondrial components. Curiously, recent studies suggested a potential link between RIPK3 and mitochondrial bioenergetics. RIPK3 can modulate mitochondrial function and quality through the regulation of mitochondrial reactive oxygen species production, sequestration of metabolic enzymes and resident mitochondrial proteins, activity of mitochondrial respiratory chain complexes, mitochondrial biogenesis and fatty acid oxidation. Since mitochondrial dysfunction and RIPK3-mediated necroptosis are intimately involved in chronic liver disease pathogenesis, understanding the role of RIPK3 in mitochondrial bioenergetics and its potential translational application are of great interest.
Sections du résumé
BACKGROUND
BACKGROUND
Receptor-interacting protein kinase 3 (RIPK3) is a key player of regulated necrosis or necroptosis, an inflammatory form of cell death possibly governing outcomes in chronic liver diseases, such as nonalcoholic fatty liver disease and nonalcoholic steatohepatitis.
METHODS
METHODS
This narrative review is based on literature search using PubMed.
RESULTS
RESULTS
RIPK3 activation depends on post-transcriptional modifications, including phosphorylation, hence coordinating the assembly of macromolecular death complex named 'necrosome', which may also involve diverse mitochondrial components. Curiously, recent studies suggested a potential link between RIPK3 and mitochondrial bioenergetics. RIPK3 can modulate mitochondrial function and quality through the regulation of mitochondrial reactive oxygen species production, sequestration of metabolic enzymes and resident mitochondrial proteins, activity of mitochondrial respiratory chain complexes, mitochondrial biogenesis and fatty acid oxidation.
CONCLUSIONS
CONCLUSIONS
Since mitochondrial dysfunction and RIPK3-mediated necroptosis are intimately involved in chronic liver disease pathogenesis, understanding the role of RIPK3 in mitochondrial bioenergetics and its potential translational application are of great interest.
Substances chimiques
RIPK3 protein, human
EC 2.7.11.1
Receptor-Interacting Protein Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13648Subventions
Organisme : EU H2020 Marie Sklodowska-Curie
ID : 722619
Organisme : Fundação para a Ciência e a Tecnologia
ID : PTDC/MED-FAR/29097/2017-LISBOA-01-0145-FEDER-029097
Informations de copyright
© 2021 Stichting European Society for Clinical Investigation Journal Foundation. Published by John Wiley & Sons Ltd.
Références
Bock FJ, Tait SWG. Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol. 2020;21(2):85-100.
Gautheron J, Gores GJ, Rodrigues CMPP. Lytic cell death in metabolic liver disease. J Hepatol. 2020;73(2):394-408.
Mansouri A, Gattolliat CH, Asselah T. Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology. 2018;155(3):629-647.
Galluzzi L, Vitale I, Abrams JM, et al. Molecular definitions of cell death subroutines: recommendations of the nomenclature committee on cell death 2012. Cell Death Differ. 2012;19(1):107-120.
Majdi A, Aoudjehane L, Ratziu V, et al. Inhibition of receptor-interacting protein kinase 1 improves experimental non-alcoholic fatty liver disease. J Hepatol. 2020;72(4):627-635.
Luedde T, Kaplowitz N, Schwabe RF. Cell death and cell death responses in liver disease: Mechanisms and clinical relevance. Gastroenterology. 2014;147(4):765-783.e4.
Martin SJ. Cell death and inflammation: the case for IL-1 family cytokines as the canonical DAMPs of the immune system. FEBS J. 2016;283(14):2599-2615.
Weinlich R, Oberst A, Beere HM, Green DR. Necroptosis in development, inflammation and disease. Nat Rev Mol Cell Biol. 2017;18(2):127-136.
Sun L, Wang H, Wang Z, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012;148(1-2):213-227.
Zhang DW, Shao J, Lin J, et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science (80- ). 2009;325(5938):332-336.
Degterev A, Huang Z, Boyce M, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005;1(2):112-119.
Dara L. The receptor interacting protein kinases in the liver. Semin Liver Dis. 2018;38(1):73-86.
Moriwaki K, Chan FKM. RIP3: a molecular switch for necrosis and inflammation. Genes Dev. 2013;27(15):1640-1649.
Kasof GM, Prosser JC, Liu D, Lorenzi MV, Gomes BC. The RIP-like kinase, RIP3, induces apoptosis and NF-κB nuclear translocation and localizes to mitochondria. FEBS Lett. 2000;473(3):285-291.
Stanger BZ, Leder P, Lee TH, Kim E, Seed B. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell. 1995;81(4):513-523.
Quarato G, Guy CS, Grace CR, et al. Sequential engagement of distinct mlkl phosphatidylinositol-binding sites executes necroptosis. Mol Cell. 2016;61(4):589-601.
Chen W, Zhou Z, Li S, et al. Diverse sequence determinants control human and mouse receptor interacting protein 3 (RIP3) and mixed lineage kinase domain-like (MLKL) interaction in necroptotic signaling. J Biol Chem. 2013;288(23):16247-16261.
Yang Z, Wang Y, Zhang Y, et al. RIP3 targets pyruvate dehydrogenase complex to increase aerobic respiration in TNF-induced necroptosis. Nat Cell Biol. 2018;20(2):186-197.
Mizumura K, Cloonan SM, Nakahira K, et al. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J Clin Invest. 2014;124(9):3987-4003.
Wang Z, Jiang H, Chen S, Du F, Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell. 2012;148(1-2):228-243.
Gan I, Jiang J, Lian D, et al. Mitochondrial permeability regulates cardiac endothelial cell necroptosis and cardiac allograft rejection. Am J Transplant. 2019;19(3):686-698.
Basit F, Van Oppen LMPE, Schöckel L, et al. Mitochondrial complex i inhibition triggers a mitophagy-dependent ROS increase leading to necroptosis and ferroptosis in melanoma cells. Cell Death Dis. 2017;8(3):e2716.
Shi S, Verstegen MMAA, Mezzanotte L, Jonge J, Löwik CWGM, Laan LJW. Necroptotic cell death in liver transplantation and underlying diseases: mechanisms and clinical perspective. Liver Transpl. 2019;25(7):1091-1104.
Afonso MB, Rodrigues PMM, Carvalho T, et al. Necroptosis is a key pathogenic event in human and experimental murine models of non-alcoholic steatohepatitis. Clin Sci. 2015;129(8):721-739.
Afonso MB, Rodrigues PM, Simão AL, et al. Activation of necroptosis in human and experimental cholestasis. Cell Death Dis. 2016;7(9):e2390.
Afonso MB, Rodrigues PM, Mateus-Pinheiro M, et al. RIPK3 acts as a lipid metabolism regulator contributing to inflammation and carcinogenesis in non-alcoholic fatty liver disease. Gut. 2020;1-14, gutjnl-321767.
Schwabe RF, Luedde T. Apoptosis and necroptosis in the liver: a matter of life and death. Nat Rev Gastroenterol Hepatol. 2018;15(12):738-752.
Seehawer M, Heinzmann F, D’Artista L, et al. Necroptosis microenvironment directs lineage commitment in liver cancer. Nature. 2018;562(7725):69-75.
Vanden Berghe T, Kaiser WJ, Bertrand MJM, Vandenabeele P. Molecular crosstalk between apoptosis, necroptosis, and survival signaling. Mol Cell Oncol. 2015;2(4):e975093.
Tang D, Kang R, Vanden BT, Vandenabeele P, Kroemer G. The molecular machinery of regulated cell death. Cell Res. 2019;29(5):347-364.
Wegner KW, Saleh D, Degterev A. Complex pathologic roles of RIPK1 and RIPK3: moving beyond necroptosis. Trends Pharmacol Sci. 2017;38(3):202-225.
Hanna-Addams S, Liu S, Liu H, Chen S, Wang Z. CK1α, CK1δ, and CK1ε are necrosome components which phosphorylate serine 227 of human RIPK3 to activate necroptosis. Proc Natl Acad Sci USA. 2020;117(4):1962-1970.
Zhang Y, Su SS, Zhao S, et al. RIP1 autophosphorylation is promoted by mitochondrial ROS and is essential for RIP3 recruitment into necrosome. Nat Commun. 2017;8(1):14329.
Sun W, Wu X, Gao H, et al. Cytosolic calcium mediates RIP1/RIP3 complex-dependent necroptosis through JNK activation and mitochondrial ROS production in human colon cancer cells. Free Radic Biol Med. 2017;108:433-444.
Hildebrand JM, Tanzer MC, Lucet IS, et al. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc Natl Acad Sci USA. 2014;111(42):15072-15077.
Dondelinger Y, Declercq W, Montessuit S, et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 2014;7(4):971-981.
Murphy JM, Vince JE. Post-translational control of RIPK3 and MLKL mediated necroptotic cell death. F1000Res. 2015;4:1297.
Kearney CJ, Cullen SP, Clancy D, Martin SJ. RIPK1 can function as an inhibitor rather than an initiator of RIPK3-dependent necroptosis. FEBS J. 2014;281(21):4921-4934.
McQuade T, Cho Y, Chan FKM. Positive and negative phosphorylation regulates RIP1- and RIP3-induced programmed necrosis. Biochem J. 2013;456(3):409-415.
Newton K, Dugger DL, Wickliffe KE, et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science. 2014;343(6177):1357-1360.
Newton K. RIPK1 and RIPK3: Critical regulators of inflammation and cell death. Trends Cell Biol. 2015;25(6):347-353.
He S, Liang Y, Shao F, Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci USA. 2011;108(50):20054-20059.
Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe. 2012;11(3):290-297.
Schock SN, Chandra NV, Sun Y, et al. Induction of necroptotic cell death by viral activation of the RIG-I or STING pathway. Cell Death Differ. 2017;24(4):615-625.
Wang X, He Z, Liu H, Yousefi S, Simon H-U. Neutrophil necroptosis is triggered by ligation of adhesion molecules following GM-CSF priming. J Immunol. 2016;197(10):4090-4100.
Wu L, Zhang X, Zheng L, et al. Orchestrates fatty acid metabolism in tumor-associated macrophages and hepatocarcinogenesis. Cancer Immunol Res. 2020;8(5):710-721. Published online.
Pérez-Carreras M, Del Hoyo P, Martín MA, et al. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology. 2003;38(4):999-1007.
Sureshbabu A, Patino E, Ma KC, et al. RIPK3 promotes sepsis-induced acute kidney injury via mitochondrial dysfunction. JCI insight. 2018;3(11):e98411.
Qiu X, Zhang Y, Han J. RIP3 is an upregulator of aerobic metabolism and the enhanced respiration by necrosomal RIP3 feeds back on necrosome to promote necroptosis. Cell Death Differ. 2018;25(5):821-824.
Vanlangenakker N, Vanden Berghe T, Bogaert P, et al. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011;18(4):656-665.
Lv Y, Shao G, Zhang Q, et al. The antimicrobial peptide PFR induces necroptosis mediated by ER stress and elevated cytoplasmic calcium and mitochondrial ros levels: cooperation with ara-c to act against acute myeloid leukemia. Signal Transduct Target Ther. 2019;4(1):1-3.
Tait SWG, Oberst A, Quarato G, et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep. 2013;5(4):878-885.
Williams JA, Ding WX. Targeting Pink1-Parkin-mediated mitophagy for treating liver injury. Pharmacol Res. 2015;102:264-269.
Williams JA, Ni HM, Ding Y, Ding WX. Parkin regulates mitophagy and mitochondrial function to protect against alcohol-induced liver injury and steatosis in mice. Am J Physiol - Gastrointest Liver Physiol. 2015;309(5):G324-G340.
Ni HM, Williams JA, Jaeschke H, Ding WX. Zonated induction of autophagy and mitochondrial spheroids limits acetaminophen-induced necrosis in the liver. Redox Biol. 2013;1(1):427-432.
Deutsch M, Graffeo CS, Rokosh R, et al. Divergent effects of RIP1 or RIP3 blockade in murine models of acute liver injury. Cell Death Dis. 2015;6(5):e1759.
Jaeschke H. Acetaminophen: dose-dependent drug hepatotoxicity and acute liver failure in patients. Dig Dis. 2015;33(4):464-471.
Ding W, Li M, Chen X, et al. Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology. 2010;139(5):1740-1752.
Lu W, Sun J, Yoon JS, et al. Mitochondrial protein PGAM5 regulates mitophagic protection against cell necroptosis. PLoS One. 2016;11(1):e0147792.
Anand R, Langer T, Baker MJ. Proteolytic control of mitochondrial function and morphogenesis. Biochim Biophys Acta - Mol Cell Res. 2013;1833(1):195-204.
Longo M, Meroni M, Paolini E, Macchi C, Dongiovanni P. Mitochondrial dynamics and nonalcoholic fatty liver disease (NAFLD): new perspectives for a fairy-tale ending? Metabolism. 2021;117:154708.
Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098):1062-1065.
Zhang S, Che L, He C, et al. Drp1 and RB interaction to mediate mitochondria-dependent necroptosis induced by cadmium in hepatocytes. Cell Death Dis. 2019;10(7):1-17.
Moriwaki K, Farias Luz N, Balaji S, et al. The mitochondrial phosphatase PGAM5 is dispensable for necroptosis but promotes inflammasome activation in macrophages. J Immunol. 2016;196(1):407-415.
Remijsen Q, Goossens V, Grootjans S, et al. Depletion of RIPK3 or MLKL blocks TNF-driven necroptosis and switches towards a delayed RIPK1 kinase-dependent apoptosis. Cell Death Dis. 2014;5(1):e1004.
Wilkins JM, McConnell C, Tipton PA, Hannink M. A conserved motif mediates both multimer formation and allosteric activation of phosphoglycerate mutase 5. J Biol Chem. 2014;289(36):25137-25148.
He GW, Günther C, Kremer AE, et al. PGAM5-mediated programmed necrosis of hepatocytes drives acute liver injury. Gut. 2017;66(4):716-723.
Wu X, Poulsen KL, Sanz-Garcia C, et al. MLKL-dependent signaling regulates autophagic flux in a murine model of non-alcohol-associated fatty liver and steatohepatitis. J Hepatol. 2020;73(3):616-627.
Ekstedt M, Nasr P, Kechagias S. Natural history of NAFLD/NASH. Curr Hepatol Reports. 2017;16(4):391-397.
Sanyal AJ. Past, present and future perspectives in nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol. 2019;16(6):377-386.
Younossi Z, Anstee QM, Marietti M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15(1):11-20.
Gautheron J, Vucur M, Reisinger F, et al. A positive feedback loop between RIP 3 and JNK controls non-alcoholic steatohepatitis. EMBO Mol Med. 2014;6(8):1062-1074.
Win S, Than TA, Min RWM, Aghajan M, Kaplowitz N. c-Jun N-terminal kinase mediates mouse liver injury through a novel Sab (SH3BP5)-dependent pathway leading to inactivation of intramitochondrial Src. Hepatology. 2016;63(6):1987-2003.
Pessayre D, Fromenty B. NASH: a mitochondrial disease. J Hepatol. 2005;42(6):928-940.
Sunny NE, Bril F, Cusi K. Mitochondrial adaptation in nonalcoholic fatty liver disease: novel mechanisms and treatment strategies. Trends Endocrinol Metab. 2017;28(4):250-260.
Win S, Than TA, Le BHA, García-Ruiz C, Fernandez-Checa JC, Kaplowitz N. Sab (Sh3bp5) dependence of JNK mediated inhibition of mitochondrial respiration in palmitic acid induced hepatocyte lipotoxicity. J Hepatol. 2015;62(6):1367-1374.
Lee YK, Park JE, Lee M, Hardwick JP. Hepatic lipid homeostasis by peroxisome proliferator-activated receptor gamma 2. Liver Res. 2018;2(4):209-215.
Marchesini G, Day CP, Dufour JF, et al. EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. Obes Facts. 2016;9(2):65-90.
Chenxu G, Minxuan X, Yuting Q, et al. Loss of RIP3 initiates annihilation of high-fat diet initialized nonalcoholic hepatosteatosis: A mechanism involving Toll-like receptor 4 and oxidative stress. Free Radic Biol Med. 2019;134:23-41.
Mohammed S, Nicklas EH, Thadathil N, et al. Role of necroptosis in chronic hepatic inflammation and fibrosis in a mouse model of increased oxidative stress. Free Radic Biol Med. 2021;164:315-328.
Heslop KA, Rovini A, Hunt EG, et al. JNK activation and translocation to mitochondria mediates mitochondrial dysfunction and cell death induced by VDAC opening and sorafenib in hepatocarcinoma cells. Biochem Pharmacol. 2020;171:113728.
Lan W, Santofimia-Castaño P, Xia Y, et al. Targeting NUPR1 with the small compound ZZW-115 is an efficient strategy to treat hepatocellular carcinoma. Cancer Lett. 2020;486:8-17.
Saeed WK, Jun DW, Jang K, et al. Mismatched effects of receptor interacting protein kinase-3 on hepatic steatosis and inflammation in nonalcoholic fatty liver disease. World J Gastroenterol. 2018;24(48):5477-5490.