The importance of murine phospho-MLKL-S345 in situ detection for necroptosis assessment in vivo.
Journal
Cell death and differentiation
ISSN: 1476-5403
Titre abrégé: Cell Death Differ
Pays: England
ID NLM: 9437445
Informations de publication
Date de publication:
23 May 2024
23 May 2024
Historique:
received:
20
12
2023
accepted:
07
05
2024
revised:
02
05
2024
medline:
24
5
2024
pubmed:
24
5
2024
entrez:
23
5
2024
Statut:
aheadofprint
Résumé
Necroptosis is a caspase-independent modality of cell death implicated in many inflammatory pathologies. The execution of this pathway requires the formation of a cytosolic platform that comprises RIPK1 and RIPK3 which, in turn, mediates the phosphorylation of the pseudokinase MLKL (S345 in mouse). The activation of this executioner is followed by its oligomerisation and accumulation at the plasma-membrane where it leads to cell death via plasma-membrane destabilisation and consequent permeabilisation. While the biochemical and cellular characterisation of these events have been amply investigated, the study of necroptosis involvement in vivo in animal models is currently limited to the use of Mlkl
Identifiants
pubmed: 38783091
doi: 10.1038/s41418-024-01313-6
pii: 10.1038/s41418-024-01313-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Liccardi G, Annibaldi A. MLKL post-translational modifications: road signs to infection, inflammation and unknown destinations. Cell Death Differ. 2023;30:269–78.
pubmed: 36175538
doi: 10.1038/s41418-022-01061-5
Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol. 2014;15:135–47.
pubmed: 24452471
doi: 10.1038/nrm3737
Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, et al. RIP3, an energy metabolism regulator that switches TNF-Induced cell death from apoptosis to necrosis. Science. 2009;325:332–6.
pubmed: 19498109
doi: 10.1126/science.1172308
He SD, Wang L, Miao L, Wang T, Du FH, Zhao LP, et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 2009;137:1100–11.
pubmed: 19524512
doi: 10.1016/j.cell.2009.05.021
Walczak H. Death receptor-ligand systems in cancer, cell death, and inflammation. Cold Spring Harb Perspect Biol. 2013;5:a008698.
pubmed: 23637280
pmcid: 3632055
doi: 10.1101/cshperspect.a008698
Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1:489–95.
pubmed: 11101870
doi: 10.1038/82732
Matsumura H, Shimizu Y, Ohsawa Y, Kawahara A, Uchiyama Y, Nagata S. Necrotic death pathway in Fas receptor signaling. J Cell Biol. 2000;151:1247–56.
pubmed: 11121439
pmcid: 2190580
doi: 10.1083/jcb.151.6.1247
Vercammen D, Brouckaert G, Denecker G, Van de Craen M, Declercq W, Fiers W, et al. Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J Exp Med. 1998;188:919–30.
pubmed: 9730893
pmcid: 2213397
doi: 10.1084/jem.188.5.919
Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van Herreweghe F, et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ. 2012;19:2003–14.
pubmed: 22814620
pmcid: 3504714
doi: 10.1038/cdd.2012.90
Lafont E, Kantari-Mimoun C, Draber P, De Miguel D, Hartwig T, Reichert M, et al. The linear ubiquitin chain assembly complex regulates TRAIL-induced gene activation and cell death. EMBO J. 2017;36:1147–66.
pubmed: 28258062
pmcid: 5412822
doi: 10.15252/embj.201695699
Montinaro A, Walczak H. Harnessing TRAIL-induced cell death for cancer therapy: a long walk with thrilling discoveries. Cell Death Differ. 2023;30:237–49.
pubmed: 36195672
doi: 10.1038/s41418-022-01059-z
He SD, Liang YQ, Shao F, Wang XD. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci USA. 2011;108:20054–9.
pubmed: 22123964
pmcid: 3250173
doi: 10.1073/pnas.1116302108
Kaiser WJ, Sridharan H, Huang CZ, Mandal P, Upton JW, Gough PJ, et al. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J Biol Chem. 2013;288:31268–79.
pubmed: 24019532
pmcid: 3829437
doi: 10.1074/jbc.M113.462341
Lim J, Park H, Heisler J, Maculins T, Roose-Girma M, Xu M, et al. Autophagy regulates inflammatory programmed cell death via turnover of RHIM-domain proteins. Elife. 2019;8:e44452.
pubmed: 31287416
pmcid: 6615860
doi: 10.7554/eLife.44452
Zhang J, Yang Y, He W, Sun L. Necrosome core machinery: MLKL. Cell Mol Life Sci. 2016;73:2153–63.
pubmed: 27048809
pmcid: 11108342
doi: 10.1007/s00018-016-2190-5
Lin J, Kumari S, Kim C, Van TM, Wachsmuth L, Polykratis A, et al. RIPK1 counteracts ZBP1-mediated necroptosis to inhibit inflammation. Nature. 2016;540:124–8.
pubmed: 27819681
pmcid: 5755685
doi: 10.1038/nature20558
Garcia LR, Tenev T, Newman R, Haich RO, Liccardi G, John SW, et al. Ubiquitylation of MLKL at lysine 219 positively regulates necroptosis-induced tissue injury and pathogen clearance. Nat Commun. 2021;12:3364.
pubmed: 34099649
pmcid: 8184782
doi: 10.1038/s41467-021-23474-5
Liu Z, Dagley LF, Shield-Artin K, Young SN, Bankovacki A, Wang X, et al. Oligomerization-driven MLKL ubiquitylation antagonizes necroptosis. EMBO J. 2021;40:e103718.
pubmed: 34698396
pmcid: 8634140
doi: 10.15252/embj.2019103718
Sun L, Wang H, Wang Z, He S, Chen S, Liao D, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012;148:213–27.
pubmed: 22265413
doi: 10.1016/j.cell.2011.11.031
Su L, Quade B, Wang H, Sun L, Wang X, Rizo J. A plug release mechanism for membrane permeation by MLKL. Structure. 2014;22:1489–500.
pubmed: 25220470
pmcid: 4192069
doi: 10.1016/j.str.2014.07.014
Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell. 2014;54:133–46.
pubmed: 24703947
doi: 10.1016/j.molcel.2014.03.003
Petrie EJ, Sandow JJ, Jacobsen AV, Smith BJ, Griffin MDW, Lucet IS, et al. Conformational switching of the pseudokinase domain promotes human MLKL tetramerization and cell death by necroptosis. Nat Commun. 2018;9:2422.
pubmed: 29930286
pmcid: 6013482
doi: 10.1038/s41467-018-04714-7
Tanzer MC, Tripaydonis A, Webb AI, Young SN, Varghese LN, Hall C, et al. Necroptosis signalling is tuned by phosphorylation of MLKL residues outside the pseudokinase domain activation loop. Biochem J. 2015;471:255–65.
pubmed: 26283547
doi: 10.1042/BJ20150678
Meng Y, Sandow JJ, Czabotar PE, Murphy JM. The regulation of necroptosis by post-translational modifications. Cell Death Differ. 2021;28:861–83.
pubmed: 33462412
pmcid: 7937688
doi: 10.1038/s41418-020-00722-7
Zhu X, Yang N, Yang Y, Yuan F, Yu D, Zhang Y, et al. Spontaneous necroptosis and autoinflammation are blocked by an inhibitory phosphorylation on MLKL during neonatal development. Cell Res. 2022;32:407–10.
pubmed: 34728815
doi: 10.1038/s41422-021-00583-w
Samson AL, Fitzgibbon C, Patel KM, Hildebrand JM, Whitehead LW, Rimes JS, et al. A toolbox for imaging RIPK1, RIPK3, and MLKL in mouse and human cells. Cell Death Differ. 2021;28:2126–44.
pubmed: 33589776
pmcid: 8257593
doi: 10.1038/s41418-021-00742-x
Porter AG, Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999;6:99–104.
pubmed: 10200555
doi: 10.1038/sj.cdd.4400476
Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22:526–39.
pubmed: 25526085
doi: 10.1038/cdd.2014.216
Rojas J, Bermudez V, Palmar J, Martinez MS, Olivar LC, Nava M, et al. Pancreatic beta cell death: novel potential mechanisms in diabetes therapy. J Diabetes Res. 2018;2018:9601801.
pubmed: 29670917
pmcid: 5836465
doi: 10.1155/2018/9601801
Christofferson DE, Yuan JY. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol. 2010;22:263–8.
pubmed: 20045303
pmcid: 2854308
doi: 10.1016/j.ceb.2009.12.003
Fatokun AA, Dawson VL, Dawson TM. Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities. Br J Pharmacol. 2014;171:2000–16.
pubmed: 24684389
pmcid: 3976618
doi: 10.1111/bph.12416
Didenko VV, Ngo H, Baskin DS. Early necrotic DNA degradation – Presence of blunt-ended DNA breaks, 3′ and 5′ overhangs in apoptosis, but only 5′ overhangs in early necrosis. Am J Pathol. 2003;162:1571–8.
pubmed: 12707041
pmcid: 1851179
doi: 10.1016/S0002-9440(10)64291-5
Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol. 2009;7:99–109.
pubmed: 19148178
pmcid: 2910423
doi: 10.1038/nrmicro2070
Kovalenko A, Kim JC, Kang TB, Rajput A, Bogdanov K, Dittrich-Breiholz O, et al. Caspase-8 deficiency in epidermal keratinocytes triggers an inflammatory skin disease. J Exp Med. 2009;206:2161–77.
pubmed: 19720838
pmcid: 2757876
doi: 10.1084/jem.20090616
Schwarzer R, Jiao H, Wachsmuth L, Tresch A, Pasparakis M. FADD and caspase-8 regulate gut homeostasis and inflammation by controlling MLKL- and GSDMD-mediated death of intestinal epithelial cells. Immunity. 2020;52:978–993.e6.
pubmed: 32362323
doi: 10.1016/j.immuni.2020.04.002
Beisner DR, Ch’en IL, Kolla RV, Hoffmann A, Hedrick SM. Cutting edge: innate immunity conferred by B cells is regulated by caspase-8. J Immunol. 2005;175:3469–73.
pubmed: 16148088
doi: 10.4049/jimmunol.175.6.3469
Hafner M, Wenk J, Nenci A, Pasparakis M, Scharffetter-Kochanek K, Smyth N, et al. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis. 2004;38:176–81.
pubmed: 15083518
doi: 10.1002/gene.20016
Mc Guire C, Volckaert T, Wolke U, Sze M, de Rycke R, Waisman A, et al. Oligodendrocyte-specific FADD deletion protects mice from autoimmune-mediated demyelination. J Immunol. 2010;185:7646–53.
doi: 10.4049/jimmunol.1000930
Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277:33275–83.
pubmed: 12065599
doi: 10.1074/jbc.M204935200
Taraborrelli L, Peltzer N, Montinaro A, Kupka S, Rieser E, Hartwig T, et al. LUBAC prevents lethal dermatitis by inhibiting cell death induced by TNF, TRAIL and CD95L. Nat Commun. 2018;9:3910.
Peltzer N, Darding M, Montinaro A, Draber P, Draberova H, Kupka S, et al. LUBAC is essential for embryogenesis by preventing cell death and enabling haematopoiesis. Nature. 2018;557:112–7.
pubmed: 29695863
pmcid: 5947819
doi: 10.1038/s41586-018-0064-8
Salmena L, Lemmers B, Hakem A, Matysiak-Zablocki E, Murakami K, Au PY, et al. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 2003;17:883–95.
pubmed: 12654726
pmcid: 196031
doi: 10.1101/gad.1063703
Newton K, Sun X, Dixit VM. Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol Cell Biol. 2004;24:1464–9.
pubmed: 14749364
pmcid: 344190
doi: 10.1128/MCB.24.4.1464-1469.2004
Martinez Lagunas K, Savcigil DP, Zrilic M, Carvajal Fraile C, Craxton A, Self E, et al. Cleavage of cFLIP restrains cell death during viral infection and tissue injury and favors tissue repair. Sci Adv. 2023;9:eadg2829.
pubmed: 37494451
pmcid: 10371024
doi: 10.1126/sciadv.adg2829
Shrum B, Anantha RV, Xu SX, Donnelly M, Haeryfar SM, McCormick JK, et al. A robust scoring system to evaluate sepsis severity in an animal model. BMC Res Notes. 2014;7:233.
pubmed: 24725742
pmcid: 4022086
doi: 10.1186/1756-0500-7-233
Taylor CR, Shi SR, Barr NJ. Techniques of immunohistochemistry: principles, pitfalls, and standardization. In: Dabbs DJ, editor. Diagnostic immunohistochemistry. 3rd ed. Philadelphia, PA: Saunders/Elsevier; 2011. p. xviii, 941 p.
Shi SR, Key ME, Kalra KL. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem. 1991;39:741–8.
pubmed: 1709656
doi: 10.1177/39.6.1709656
He P, Ai T, Yang ZH, Wu J, Han J. Detection of necroptosis by phospho-MLKL immunohistochemical labeling. STAR Protoc. 2021;2:100251.
pubmed: 33458710
doi: 10.1016/j.xpro.2020.100251
Bankhead P, Loughrey MB, Fernandez JA, Dombrowski Y, McArt DG, Dunne PD, et al. QuPath: open source software for digital pathology image analysis. Sci Rep. 2017;7:16878.
pubmed: 29203879
pmcid: 5715110
doi: 10.1038/s41598-017-17204-5
Pefanis A, Bongoni AK, McRae JL, Salvaris EJ, Fisicaro N, Murphy JM, et al. Dynamics of necroptosis in kidney ischemia-reperfusion injury. Front Immunol. 2023;14:1251452.
pubmed: 38022500
pmcid: 10652410
doi: 10.3389/fimmu.2023.1251452
Ikeda F, Deribe YL, Skanland SS, Stieglitz B, Grabbe C, Franz-Wachtel M, et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature. 2011;471:637–41.
pubmed: 21455181
pmcid: 3085511
doi: 10.1038/nature09814
Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature .2011;471:591–6.
pubmed: 21455173
doi: 10.1038/nature09816
Rickard JA, Anderton H, Etemadi N, Nachbur U, Darding M, Peltzer N, et al. TNFR1-dependent cell death drives inflammation in Sharpin-deficient mice. Elife 2014;3:e03464.
pubmed: 25443632
pmcid: 4270099
doi: 10.7554/eLife.03464
Kumari S, Redouane Y, Lopez-Mosqueda J, Shiraishi R, Romanowska M, Lutzmayer S, et al. Sharpin prevents skin inflammation by inhibiting TNFR1-induced keratinocyte apoptosis. Elife. 2014;3:e03422.
Newton K, Dugger DL, Maltzman A, Greve JM, Hedehus M, Martin-McNulty B, et al. RIPK3 deficiency or catalytically inactive RIPK1 provides greater benefit than MLKL deficiency in mouse models of inflammation and tissue injury. Cell Death Differ. 2016;23:1565–76.
pubmed: 27177019
pmcid: 5072432
doi: 10.1038/cdd.2016.46
Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature. 2011;471:368–72.
pubmed: 21368762
pmcid: 3060292
doi: 10.1038/nature09857
Duprez L, Takahashi N, Van Hauwermeiren F, Vandendriessche B, Goossens V, Vanden Berghe T, et al. RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity. 2011;35:908–18.
pubmed: 22195746
doi: 10.1016/j.immuni.2011.09.020
Rickard JA, O’Donnell JA, Evans JM, Lalaoui N, Poh AR, Rogers T, et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell. 2014;157:1175–88.
pubmed: 24813849
doi: 10.1016/j.cell.2014.04.019
Anderton H, Bandala-Sanchez E, Simpson DS, Rickard JA, Ng AP, Di Rago L, et al. RIPK1 prevents TRADD-driven, but TNFR1 independent, apoptosis during development. Cell Death Differ. 2019;26:877–89.
pubmed: 30185824
doi: 10.1038/s41418-018-0166-8
Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C, Wachsmuth L, et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature. 2014;513:90–4.
pubmed: 25132550
pmcid: 4206266
doi: 10.1038/nature13608
Müller T, Dewitz C, Schmitz J, Schröder AS, Bräsen JH, Stockwell BR, et al. Necroptosis and ferroptosis are alternative cell death pathways that operate in acute kidney failure. Cell Mol Life Sci. 2017;74:3631–45.
pubmed: 28551825
pmcid: 5589788
doi: 10.1007/s00018-017-2547-4
Bertheloot D, Latz E, Franklin BS. Necroptosis, pyroptosis and apoptosis: an intricate game of cell death. Cell Mol Immunol. 2021;18:1106–21.
pubmed: 33785842
pmcid: 8008022
doi: 10.1038/s41423-020-00630-3
Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity. 2013;38:209–23.
pubmed: 23438821
doi: 10.1016/j.immuni.2013.02.003
Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35:495–516.
pubmed: 17562483
pmcid: 2117903
doi: 10.1080/01926230701320337
Jiang MX, Qi L, Li LS, Li YJ. The caspase-3/GSDME signal pathway as a switch between apoptosis and pyroptosis in cancer. Cell Death Discov. 2020;6:112.
Falschlehner C, Schaefer U, Walczak H. Following TRAIL’s path in the immune system. Immunology. 2009;127:145–54.
pubmed: 19476510
pmcid: 2691779
doi: 10.1111/j.1365-2567.2009.03058.x
Welz PS, Wullaert A, Vlantis K, Kondylis V, Fernandez-Majada V, Ermolaeva M, et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature. 2011;477:330–4.
pubmed: 21804564
doi: 10.1038/nature10273
Wittkopf N, Gunther C, Martini E, He G, Amann K, He YW, et al. Cellular FLICE-like inhibitory protein secures intestinal epithelial cell survival and immune homeostasis by regulating caspase-8. Gastroenterology. 2013;145:1369–79.
pubmed: 24036366
doi: 10.1053/j.gastro.2013.08.059
Lu Z, Van Eeckhoutte HP, Liu G, Nair PM, Jones B, Gillis CM, et al. Necroptosis signaling promotes inflammation, airway remodeling, and emphysema in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2021;204:667–81.
pubmed: 34133911
doi: 10.1164/rccm.202009-3442OC
Simpson J, Spann KM, Phipps S. MLKL regulates rapid cell death-independent HMGB1 release in RSV infected airway epithelial cells. Front Cell Dev Biol. 2022;10:890389.
pubmed: 35712662
pmcid: 9194532
doi: 10.3389/fcell.2022.890389
Li S, Zhang Y, Guan Z, Ye M, Li H, You M, et al. SARS-CoV-2 Z-RNA activates the ZBP1-RIPK3 pathway to promote virus-induced inflammatory responses. Cell Res. 2023;33:201–14.
pubmed: 36650286
pmcid: 9844202
doi: 10.1038/s41422-022-00775-y
Bader SM, Cooney JP, Bhandari R, Mackiewicz L, Dayton M, Sheerin D, et al. Necroptosis does not drive disease pathogenesis in a mouse infective model of SARS-CoV-2 in vivo. Cell Death Dis. 2024;15:100.
Mandal P, Berger SB, Pillay S, Moriwaki K, Huang CZ, Guo HY, et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol Cell. 2014;56:481–95.
pubmed: 25459880
pmcid: 4512186
doi: 10.1016/j.molcel.2014.10.021
Vanden Berghe T, Hulpiau P, Martens L, Vandenbroucke RE, Van Wonterghem E, Perry SW, et al. Passenger mutations confound interpretation of all genetically modified congenic mice. Immunity. 2015;43:200–9.
pubmed: 26163370
doi: 10.1016/j.immuni.2015.06.011