JNK1 and ERK1/2 modulate lymphocyte homeostasis via BIM and DRP1 upon AICD induction.
Animals
Cell Death
Cell Line, Tumor
Dynamins
/ metabolism
Female
Humans
Lymphocyte Activation
MAP Kinase Signaling System
Male
Mice
Mice, Inbred C57BL
Mitochondria
/ metabolism
Mitochondrial Membranes
/ metabolism
Mitogen-Activated Protein Kinase 3
/ metabolism
Precursor Cell Lymphoblastic Leukemia-Lymphoma
/ immunology
T-Lymphocytes
/ cytology
Journal
Cell death and differentiation
ISSN: 1476-5403
Titre abrégé: Cell Death Differ
Pays: England
ID NLM: 9437445
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
07
11
2019
accepted:
02
04
2020
revised:
31
03
2020
pubmed:
30
4
2020
medline:
9
11
2021
entrez:
30
4
2020
Statut:
ppublish
Résumé
The Activation-Induced Cell Death (AICD) is a stimulation-dependent form of apoptosis used by the organism to shutdown T-cell response once the source of inflammation has been eliminated, while allowing the generation of immune memory. AICD is thought to progress through the activation of the extrinsic Fas/FasL pathway of cell death, leading to cytochrome-C release through caspase-8 and Bid activation. We recently described that, early upon AICD induction, mitochondria undergo structural alterations, which are required to promote cytochrome-C release and execute cell death. Here, we found that such alterations do not depend on the Fas/FasL pathway, which is instead only lately activated to amplify the cell death cascade. Instead, such alterations are primarily dependent on the MAPK proteins JNK1 and ERK1/2, which, in turn, regulate the activity of the pro-fission protein Drp1 and the pro-apoptotic factor Bim. The latter regulates cristae disassembly and cooperate with Drp1 to mediate the Mitochondrial Outer Membrane Permeabilization (MOMP), leading to cytochrome-C release. Interestingly, we found that Bim is also downregulated in T-cell Acute Lymphoblastic Leukemia (T-ALL) cells, this alteration favouring their escape from AICD-mediated control.
Identifiants
pubmed: 32346136
doi: 10.1038/s41418-020-0540-1
pii: 10.1038/s41418-020-0540-1
pmc: PMC7492225
doi:
Substances chimiques
MAPK3 protein, human
EC 2.7.11.24
Mitogen-Activated Protein Kinase 3
EC 2.7.11.24
DNM1L protein, human
EC 3.6.5.5
Dynamins
EC 3.6.5.5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2749-2767Commentaires et corrections
Type : ErratumIn
Références
Volpe E, Sambucci M, Battistini L, Borsellino G. Fas-fas ligand: checkpoint of T cell functions in multiple sclerosis. Front Immunol. 2016;7:382.
pubmed: 27729910
pmcid: 5037862
Arakaki R, Yamada A, Kudo Y, Hayashi Y, Ishimaru N. Mechanism of activation-induced cell death of T cells and regulation of FasL expression. Crit Rev Immunol. 2014;34:301–14.
pubmed: 24941158
Zhang J, Xu X, Liu Y. Activation-induced cell death in T cells and autoimmunity. Cell Mol Immunol. 2004;1:186–92.
pubmed: 16219166
Caruana I, Simula L, Locatelli F, Campello S. T lymphocytes against solid malignancies: winning ways to defeat tumours. Cell Stress. 2018;2:200–12.
pubmed: 31225487
pmcid: 6551626
Ni X, Zhang C, Talpur R, Duvic M. Resistance to activation-induced cell death and bystander cytotoxicity via the fas/fas ligand pathway are implicated in the pathogenesis of cutaneous T cell lymphomas. J Invest Dermatol. 2005;124:741–50.
pubmed: 15816832
Jäättelä M, Tschopp J. Caspase-independent cell death in T lymphocytes. Nat Immunol. 2003;4:416–23.
pubmed: 12719731
Ebert PJ, Cheung J, Yang Y, McNamara E, Hong R, Moskalenko M, et al. MAP kinase inhibition promotes T cell and anti-tumor activity in combination with PD-L1 checkpoint blockade. Immunity. 2016;44:609–21.
pubmed: 26944201
Simula L, Pacella I, Colamatteo A, Procaccini C, Cancila V, Bordi M, et al. Drp1 controls effective T cell immune-surveillance by regulating T cell migration, proliferation, and cMyc-dependent metabolic reprogramming. Cell Rep. 2018;25:3059–73.
pubmed: 30540939
pmcid: 6302735
Wang A, Rud J, Olson CM, Anguita J, Osborne BA. Phosphorylation of Nur77 by the MEK-ERK-RSK cascade induces mitochondrial translocation and apoptosis in T cells. J Immunol. 2009;183:3268–77.
pubmed: 19675165
Fujii Y, Matsuda S, Takayama G, Koyasu S. ERK5 is involved in TCR-induced apoptosis through the modification of Nur77. Genes Cells. 2008;13:411–9.
pubmed: 18429814
Ley R, Ewings KE, Hadfield K, Cook SJ. Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ. 2005;12:1008–14.
pubmed: 15947788
Corrado M, Mariotti FR, Trapani L, Taraborrelli L, Nazio F, Cianfanelli V, et al. Macroautophagy inhibition maintains fragmented mitochondria to foster T cell receptor-dependent apoptosis. EMBO J. 2016;35:1793–809.
pubmed: 27390127
pmcid: 5010050
Estaquier J, Vallette F, Vayssiere J-L, Mignotte B. The mitochondrial pathways of apoptosis. Adv Exp Med Biol. 2012;942:157–83.
Simula L, Nazio F, Campello S. The Mitochondrial dynamics in cancer and immune-surveillance. Semin Cancer Biol. 2017;47:29–42.
pubmed: 28655520
Wan J, Martinvalet D, Ji X, Lois C, Kaech SM, Andrian UHVon, et al. The Bcl-2 family pro-apoptotic molecule, BNIP3 regulates activation-induced cell death of effector cytotoxic T lymphocytes. Immunology. 2003;110:10.
pubmed: 12941136
pmcid: 1783016
Guerrero AD, Welschhans RL, Chen M, Wang J. Cleavage of anti-apoptotic Bcl-2 family members after TCR stimulation contributes to the decision between T cell activation and apoptosis. J Immunol. 2013;190:168–73.
pubmed: 23203923
Zhu L, Yu X, Akatsuka Y, Cooper JA, Anasetti C. Role of mitogen-activated protein kinases in activation-induced apoptosis of T cells. Immunology. 1999;97:26.
pubmed: 10447711
pmcid: 2326808
Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA. 2003;100:2432–7.
pubmed: 12591950
Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P, et al. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA. 2008;105:15803–8.
pubmed: 18838687
Hildeman DA, Zhu Y, Mitchell TC, Bouillet P, Strasser A, Kappler J, et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity. 2002;16:759–67.
pubmed: 12121658
Kim H, Tu H-C, Ren D, Takeuchi O, Jeffers JR, Zambetti GP, et al. Stepwise Activation of BAX and BAK by tBID, BIM, and PUMA Initiates Mitochondrial Apoptosis. Mol Cell. 2009;36:487.
pubmed: 19917256
pmcid: 3163439
Yu R, Liu T, Ning C, Tan F, Jin S-B, Lendahl U, et al. The phosphorylation status of Ser-637 in dynamin-related protein 1 (Drp1) does not determine Drp1 recruitment to mitochondria. J Biol Chem. 2019;294:17262–77.
pubmed: 31533986
pmcid: 6873174
Miyazawa K. Encountering unpredicted off-target effects of pharmacological inhibitors. J Biochem. 2011;150:1–3.
pubmed: 21558088
Shen YH, Godlewski J, Zhu J, Sathyanarayana P, Leaner V, Birrer MJ, et al. Cross-talk between JNK/SAPK and ERK/MAPK Pathways. J Biol Chem. 2003;278:26715–21.
pubmed: 12738796
Kalkavan H, Green DR. MOMP, cell suicide as a BCL-2 family business. Cell Death Differ. 2018;25:46–55.
pubmed: 29053143
Jiang X, Jiang H, Shen Z, Wang X. Activation of mitochondrial protease OMA1 by Bax and Bak promotes cytochrome c release during apoptosis. Proc Natl Acad Sci USA. 2014;111:14782–7.
pubmed: 25275009
Otera H, Miyata N, Kuge O, Mihara K. Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling. J Cell Biol. 2016;212:531–44.
pubmed: 26903540
pmcid: 4772499
Brimmell M, Mendiola R, Mangion J, Packham G. BAX frameshift mutations in cell lines derived from human haemopoietic malignancies are associated with resistance to apoptosis and microsatellite instability. Oncogene. 1998;16:1803–12.
pubmed: 9583678
D’Souza WN, Chang C-F, Fischer AM, Li M, Hedrick SM. The Erk2 MAPK regulates CD8 T cell proliferation and survival. J Immunol. 2008;181:7617–29.
pubmed: 19017950
pmcid: 2847891
Simula L, Campanella M, Campello S. Targeting Drp1 and mitochondrial fission for therapeutic immune modulation. Pharm Res. 2019;146:104317.
Bouillet P, Purton JF, Godfrey DI, Zhang L-C, Coultas L, Puthalakath H, et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature. 2002;415:922–6.
pubmed: 11859372
Yamaguchi R, Lartigue L, Perkins G, Scott RT, Dixit A, Kushnareva Y, et al. Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell. 2008;31:557–69.
pubmed: 18691924
pmcid: 2636708
Zhu Y, Swanson BJ, Wang M, Hildeman DA, Schaefer BC, Liu X, et al. Constitutive association of the proapoptotic protein Bim with Bcl-2-related proteins on mitochondria in T cells. Proc Natl Acad Sci. 2004;101:7681–6.
pubmed: 15136728
Luciano F, Jacquel A, Colosetti P, Herrant M, Cagnol S, Pages G, et al. Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene. 2003;22:6785–93.
pubmed: 14555991
Leung KT, Li KK-H, Sun SS-M, Chan PKS, Ooi VE-C, Chiu LC-M. Activation of the JNK pathway promotes phosphorylation and degradation of BimEL-a novel mechanism of chemoresistance in T-cell acute lymphoblastic leukemia. Carcinogenesis. 2007;29:544–51.
Yin KJ, Lee J-M, Chen SD, Xu J, Hsu CY. Amyloid-beta induces Smac release via AP-1/Bim activation in cerebral endothelial cells. J Neurosci. 2002;22:9764–70.
pubmed: 12427831
pmcid: 6757851
Hu K, Huang Q, Liu C, Li Y, Liu Y, Wang H, et al. c-Jun/Bim upregulation in dopaminergic neurons promotes neurodegeneration in the MPTP mouse model of Parkinson’s disease. Neuroscience. 2019;399:117–24.
pubmed: 30590105
Litwak SA, Pang L, Galic S, Igoillo-Esteve M, Stanley WJ, Turatsinze J-V, et al. JNK activation of BIM promotes hepatic oxidative stress, steatosis, and insulin resistance in obesity. Diabetes. 2017;66:2973–86.
pubmed: 28928277
Kitanaka T, Nakano R, Kitanaka N, Kimura T, Okabayashi K, Narita T, et al. JNK activation is essential for activation of MEK/ERK signaling in IL-1β-induced COX-2 expression in synovial fibroblasts. Sci Rep. 2017;7:39914.
pubmed: 28054591
pmcid: 5215076
Merritt C, Enslen H, Diehl N, Conze D, Davis RJ, Rincón M. Activation of p38 mitogen-activated protein kinase in vivo selectively induces apoptosis of CD8(+) but not CD4(+) T cells. Mol Cell Biol. 2000;20:936–46.
pubmed: 10629051
pmcid: 85211
Singh R, Wang Y, Xiang Y, Tanaka KE, Gaarde WA, Czaja MJ. Differential effects of JNK1 and JNK2 inhibition on murine steatohepatitis and insulin resistance. Hepatology. 2009;49:87–96.
pubmed: 19053047
pmcid: 2614457
Sabapathy K, Hu Y, Kallunki T, Schreiber M, David J-P, Jochum W, et al. JNK2 is required for efficient T-cell activation and apoptosis but not for normal lymphocyte development. Curr Biol. 1999;9:116–25.
pubmed: 10021384
Buck MD, O’Sullivan D, Klein Geltink RI, Curtis JD, Chang CH, Sanin DE, et al. Mitochondrial dynamics controls T cell fate through metabolic programming. Cell. 2016;166:63–76.
pubmed: 27293185
pmcid: 4974356
Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Köntgen F, et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 1999;286:1735–8.
pubmed: 10576740
Serafin V, Lissandron V, Buldini B, Bresolin S, Paganin M, Grillo F, et al. Phosphoproteomic analysis reveals hyperactivation of mTOR/STAT3 and LCK/Calcineurin axes in pediatric early T-cell precursor ALL. Leukemia. 2017;31:1007–11.
pubmed: 28082737
Kassahn D, Nachbur U, Conus S, Micheau O, Schneider P, Simon H-U, et al. Distinct requirements for activation-induced cell surface expression of preformed Fas/CD95 ligand and cytolytic granule markers in T cells. Cell Death Differ. 2009;16:115–24.
pubmed: 19079288
Ke H, Harris R, Coloff JL, Jin JY, Leshin B, De Marval PM et al. The c-Jun NH 2 -terminal kinase 2 plays a dominant role in human epidermal neoplasia. Cancer Res. 2010. https://doi.org/10.1158/0008-5472.CAN-09-2923 .
Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F. The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem. 2001;276:12030–4.
pubmed: 11134038