Microglial-specific depletion of TAK1 is neuroprotective in the acute phase after ischemic stroke.
Animals
Biomarkers
Blood Glucose
Brain Infarction
/ etiology
Brain Ischemia
/ diagnosis
Cell Survival
Cells, Cultured
Cytokines
/ metabolism
Disease Models, Animal
Disease Susceptibility
Genotype
Inflammation Mediators
/ metabolism
MAP Kinase Kinase 4
/ metabolism
MAP Kinase Kinase Kinases
/ genetics
Mice
Mice, Knockout
Mice, Transgenic
Microglia
/ metabolism
Neuroprotection
/ genetics
Oxygen Consumption
Phosphorylation
Reperfusion Injury
/ etiology
Stroke
/ diagnosis
p38 Mitogen-Activated Protein Kinases
/ metabolism
Ischemia-reperfusion injury
Microglia
Neuroinflammation
Stroke
TAK1
Journal
Journal of molecular medicine (Berlin, Germany)
ISSN: 1432-1440
Titre abrégé: J Mol Med (Berl)
Pays: Germany
ID NLM: 9504370
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
23
01
2020
accepted:
22
04
2020
revised:
01
04
2020
pubmed:
10
5
2020
medline:
8
6
2021
entrez:
9
5
2020
Statut:
ppublish
Résumé
Transforming growth factor-β-activated kinase 1 (TAK1) is upregulated after cerebral ischemia and contributes to an aggravation of brain injury. TAK1 acts as a key regulator of NF-ΚB and the MAP kinases JNK and p38 and modulates post-ischemic neuroinflammation and apoptosis. Microglia are the main TAK1-expressing immunocompetent cells of the brain. However, little is known about the function and regulation of microglial TAK1 after cerebral ischemia. Tamoxifen-dependent conditional depletion of TAK1 in microglial cells was induced in Cx3cr1
Identifiants
pubmed: 32382778
doi: 10.1007/s00109-020-01916-9
pii: 10.1007/s00109-020-01916-9
pmc: PMC7297861
doi:
Substances chimiques
Biomarkers
0
Blood Glucose
0
Cytokines
0
Inflammation Mediators
0
p38 Mitogen-Activated Protein Kinases
EC 2.7.11.24
MAP Kinase Kinase Kinases
EC 2.7.11.25
MAP kinase kinase kinase 7
EC 2.7.11.25
MAP Kinase Kinase 4
EC 2.7.12.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
833-847Références
Chen R-L, Balami JS, Esiri MM, Chen L-K, Buchan AM (2010) Ischemic stroke in the elderly: an overview of evidence. Nat Rev Neurol 6(5):256–265
pubmed: 20368741
doi: 10.1038/nrneurol.2010.36
Heitsch LE, Panagos PD (2013) Treating the elderly stroke patient: complications, controversies, and best care metrics. Clin Geriatr Med 29(1):231–255
pubmed: 23177609
doi: 10.1016/j.cger.2012.10.001
Leigh R, Knutsson L, Zhou J, van Zijl PC (2018) Imaging the physiological evolution of the ischemic penumbra in acute ischemic stroke. J Cereb Blood Flow Metab 38(9):1500–1516
pubmed: 28345479
doi: 10.1177/0271678X17700913
Liu R, Yuan H, Yuan F, Yang SH (2012) Neuroprotection targeting ischemic penumbra and beyond for the treatment of ischemic stroke. Neurol Res 34(4):331–337
pubmed: 22643076
doi: 10.1179/1743132812Y.0000000020
Thirugnanachandran T, Ma H, Singhal S, Slater LA, Davis SM, Donnan GA, Phan T (2018) Refining the ischemic penumbra with topography. Int J Stroke 13(3):277–284
pubmed: 29140184
doi: 10.1177/1747493017743056
Anrather J, Iadecola C (2016) Inflammation and stroke: an overview. Neurotherapeutics 13(4):661–670
pubmed: 27730544
pmcid: 5081118
doi: 10.1007/s13311-016-0483-x
Radak D, Katsiki N, Resanovic I, Jovanovic A, Sudar-Milovanovic E, Zafirovic S, A. Mousad S, R. Isenovic E (2017) Apoptosis and acute brain ischemia in ischemic stroke. Curr Vasc Pharmacol 15(2):115–122
pubmed: 27823556
doi: 10.2174/1570161115666161104095522
Doll DN, Barr TL, Simpkins JW (2014) Cytokines: their role in stroke and potential use as biomarkers and therapeutic targets. Aging Dis 5(5):294–306
pubmed: 25276489
pmcid: 4173796
Siniscalchi A, Iannacchero R, Anticoli S, Romana Pezzella F, De Sarro G, Gallelli L (2015) Anti-inflammatory strategies in stroke: a potential therapeutic target. Curr Vasc Pharmacol 14(1):98–105
doi: 10.2174/1570161113666150923111329
Nijboer CH, Heijnen CJ, Groenendaal F, van Bel F, Kavelaars A (2009) Alternate pathways preserve tumor necrosis factor-alpha production after nuclear factor-kappaB inhibition in neonatal cerebral hypoxia-ischemia. Stroke 40(10):3362–3368
pubmed: 19628795
doi: 10.1161/STROKEAHA.109.560250
Ridder DA, Schwaninger M (2009) NF-kappaB signaling in cerebral ischemia. Neuroscience 158(3):995–1006
pubmed: 18675321
doi: 10.1016/j.neuroscience.2008.07.007
Kim SI, Choi ME (2012) TGF-beta-activated kinase-1: new insights into the mechanism of TGF-beta signaling and kidney disease. Kidney Res Clin Pract 31(2):94–105
pubmed: 26889415
pmcid: 4715161
doi: 10.1016/j.krcp.2012.04.322
Mihaly SR, Ninomiya-Tsuji J, Morioka S (2014) TAK1 control of cell death. Cell Death Differ 21(11):1667–1676
pubmed: 25146924
pmcid: 4211365
doi: 10.1038/cdd.2014.123
Sakurai H (2012) Targeting of TAK1 in inflammatory disorders and cancer. Trends Pharmacol Sci 33(10):522–530
pubmed: 22795313
doi: 10.1016/j.tips.2012.06.007
Dai L, Aye Thu C, Liu XY, Xi J, Cheung PC (2012) TAK1, more than just innate immunity. IUBMB Life 64(10):825–834
pubmed: 22941947
doi: 10.1002/iub.1078
Weng T, Koh CG (2017) POPX2 phosphatase regulates apoptosis through the TAK1-IKK-NF-kappaB pathway. Cell Death Dis 8(9):e3051
pubmed: 28906490
pmcid: 5636987
doi: 10.1038/cddis.2017.443
Ajibade AA, Wang HY, Wang RF (2013) Cell type-specific function of TAK1 in innate immune signaling. Trends Immunol 34(7):307–316
pubmed: 23664135
doi: 10.1016/j.it.2013.03.007
Poplutz M, Levikova M, Luscher-Firzlaff J, Lesina M, Algul H, Luscher B et al (2017) Endotoxin tolerance in mast cells, its consequences for IgE-mediated signalling, and the effects of BCL3 deficiency. Sci Rep 7(1):4534
pubmed: 28674400
pmcid: 5495797
doi: 10.1038/s41598-017-04890-4
Smith JA, Das A, Ray SK, Banik NL (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 87(1):10–20
pubmed: 22024597
doi: 10.1016/j.brainresbull.2011.10.004
Mukandala G, Tynan R, Lanigan S, O'Connor JJ (2016) The effects of hypoxia and inflammation on synaptic signaling in the CNS. Brain Sci. 6(1)
Zhou J, Fan Y, Zhong J, Huang Z, Huang T, Lin S, Chen H (2018) TAK1 mediates excessive autophagy via p38 and ERK in cisplatin-induced acute kidney injury. J Cell Mol Med 22(5):2908–2921
pubmed: 29504713
pmcid: 5908118
doi: 10.1111/jcmm.13585
Omori E, Matsumoto K, Sanjo H, Sato S, Akira S, Smart RC, Ninomiya-Tsuji J (2006) TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J Biol Chem 281(28):19610–19617
pubmed: 16675448
pmcid: 1797070
doi: 10.1074/jbc.M603384200
Zhang D, Yan H, Li H, Hao S, Zhuang Z, Liu M, Sun Q, Yang Y, Zhou M, Li K, Hang C (2015) TGFbeta-activated kinase 1 (TAK1) inhibition by 5Z-7-Oxozeaenol attenuates early brain injury after experimental subarachnoid hemorrhage. J Biol Chem 290(32):19900–19909
pubmed: 26100626
pmcid: 4528149
doi: 10.1074/jbc.M115.636795
Neubert M, Ridder DA, Bargiotas P, Akira S, Schwaninger M (2011) Acute inhibition of TAK1 protects against neuronal death in cerebral ischemia. Cell Death Differ 18(9):1521–1530
pubmed: 21475303
pmcid: 3178433
doi: 10.1038/cdd.2011.29
White BJ, Tarabishy S, Venna VR, Manwani B, Benashski S, McCullough LD et al (2012) Protection from cerebral ischemia by inhibition of TGFbeta-activated kinase. Exp Neurol 237(1):238–245
pubmed: 22683931
pmcid: 3418439
doi: 10.1016/j.expneurol.2012.05.019
Fu R, Shen Q, Xu P, Luo JJ, Tang Y (2014) Phagocytosis of microglia in the central nervous system diseases. Mol Neurobiol 49(3):1422–1434
pubmed: 24395130
pmcid: 4012154
doi: 10.1007/s12035-013-8620-6
Jin X, Yamashita T (2016) Microglia in central nervous system repair after injury. J Biochem 159(5):491–496
pubmed: 26861995
doi: 10.1093/jb/mvw009
Streit WJ (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40(2):133–139
pubmed: 12379901
doi: 10.1002/glia.10154
Jin WN, Shi SX, Li Z, Li M, Wood K, Gonzales RJ et al (2017) Depletion of microglia exacerbates postischemic inflammation and brain injury. J Cereb Blood Flow Metab 37(6):2224–2236
pubmed: 28273719
pmcid: 5444553
doi: 10.1177/0271678X17694185
Goldmann T, Wieghofer P, Muller PF, Wolf Y, Varol D, Yona S et al (2013) A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16(11):1618–1626
pubmed: 24077561
doi: 10.1038/nn.3531
Ulbrich C, Zendedel A, Habib P, Kipp M, Beyer C, Dang J (2012) Long-term cerebral cortex protection and behavioral stabilization by gonadal steroid hormones after transient focal hypoxia. J Steroid Biochem Mol Biol 131(1–2):10–16
pubmed: 22326729
doi: 10.1016/j.jsbmb.2012.01.007
Habib P, Dreymueller D, Ludwig A, Beyer C, Dang J (2013) Sex steroid hormone-mediated functional regulation of microglia-like BV-2 cells during hypoxia. J Steroid Biochem Mol Biol 138:195–205
pubmed: 23792783
doi: 10.1016/j.jsbmb.2013.06.003
Habib P, Stamm AS, Zeyen T, Noristani R, Slowik A, Beyer C, et al. (2019) EPO regulates neuroprotective transmembrane BAX inhibitor-1 motif-containing (TMBIM) family members GRINA and FAIM2 after cerebral ischemia-reperfusion injury. Exp Neurol 112978
Ebrahimi T, Rust M, Kaiser SN, Slowik A, Beyer C, Koczulla AR et al (2018) Alpha1-antitrypsin mitigates NLRP3-inflammasome activation in amyloid beta1–42-stimulated murine astrocytes. J Neuroinflammation 15(1):282
pubmed: 30261895
pmcid: 6158809
doi: 10.1186/s12974-018-1319-x
McDonald JH (2014) Handbook of Biological Statistics (3rd ed.). Sparky House Publishing, Baltimore, Maryland
Wu J, Powell F, Larsen NA, Lai Z, Byth KF, Read J, Gu RF, Roth M, Toader D, Saeh JC, Chen H (2013) Mechanism and in vitro pharmacology of TAK1 inhibition by (5Z)-7-Oxozeaenol. ACS Chem Biol 8(3):643–650
pubmed: 23272696
doi: 10.1021/cb3005897
Ninomiya-Tsuji J, Kajino T, Ono K, Ohtomo T, Matsumoto M, Shiina M, Mihara M, Tsuchiya M, Matsumoto K (2003) A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1 MAPK kinase kinase. J Biol Chem 278(20):18485–18490
pubmed: 12624112
doi: 10.1074/jbc.M207453200
Zhao SC, Ma LS, Chu ZH, Xu H, Wu WQ, Liu F (2017) Regulation of microglial activation in stroke. Acta Pharmacol Sin 38(4):445–458
pubmed: 28260801
pmcid: 5386316
doi: 10.1038/aps.2016.162
Serdar M, Kempe K, Rizazad M, Herz J, Bendix I, Felderhoff-Muser U et al (2019) Early pro-inflammatory microglia activation after inflammation-sensitized hypoxic-ischemic brain injury in neonatal rats. Front Cell Neurosci 13:237
pubmed: 31178702
pmcid: 6543767
doi: 10.3389/fncel.2019.00237
Wolf Y, Yona S, Kim KW, Jung S (2013) Microglia, seen from the CX3CR1 angle. Front Cell Neurosci 7:26
pubmed: 23507975
pmcid: 3600435
doi: 10.3389/fncel.2013.00026
Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20(11):4106–4114
pubmed: 10805752
pmcid: 85780
doi: 10.1128/MCB.20.11.4106-4114.2000
Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang DR, Kidd G, Dombrowski S, Dutta RJ, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9(7):917–924
pubmed: 16732273
doi: 10.1038/nn1715
Zhao XF, Alam MM, Liao Y, Huang T, Mathur R, Zhu X, et al. (2019) Targeting microglia using Cx3cr1-cre lines: revisiting the specificity. eNeuro. 6(4)
Liput DJ (2018) Cre-recombinase dependent germline deletion of a conditional allele in the Rgs9 cre mouse line. Front Neural Circuits 12:68
pubmed: 30254571
pmcid: 6141680
doi: 10.3389/fncir.2018.00068
Haimon Z, Volaski A, Orthgiess J, Boura-Halfon S, Varol D, Shemer A, Yona S, Zuckerman B, David E, Chappell-Maor L, Bechmann I, Gericke M, Ulitsky I, Jung S (2018) Re-evaluating microglia expression profiles using RiboTag and cell isolation strategies. Nat Immunol 19(6):636–644
pubmed: 29777220
pmcid: 5986066
doi: 10.1038/s41590-018-0110-6
Mehta SH, Dhandapani KM, De Sevilla LM, Webb RC, Mahesh VB, Brann DW (2003) Tamoxifen, a selective estrogen receptor modulator, reduces ischemic damage caused by middle cerebral artery occlusion in the ovariectomized female rat. Neuroendocrinology 77(1):44–50
pubmed: 12624540
doi: 10.1159/000068332
Galatro TF, Holtman IR, Lerario AM, Vainchtein ID, Brouwer N, Sola PR, Veras MM, Pereira TF, Leite REP, Möller T, Wes PD, Sogayar MC, Laman JD, den Dunnen W, Pasqualucci CA, Oba-Shinjo SM, Boddeke EWGM, Marie SKN, Eggen BJL (2017) Transcriptomic analysis of purified human cortical microglia reveals age-associated changes. Nat Neurosci 20(8):1162–1171
pubmed: 28671693
doi: 10.1038/nn.4597
Cornejo F, von Bernhardi R (2016) Age-dependent changes in the activation and regulation of microglia. Adv Exp Med Biol 949:205–226
pubmed: 27714691
doi: 10.1007/978-3-319-40764-7_10
Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27(10):2596–2605
pubmed: 17344397
pmcid: 6672496
doi: 10.1523/JNEUROSCI.5360-06.2007
Xiong XY, Liu L, Yang QW (2016) Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog Neurobiol 142:23–44
pubmed: 27166859
doi: 10.1016/j.pneurobio.2016.05.001
Malireddi RKS, Gurung P, Mavuluri J, Dasari TK, Klco JM, Chi H, Kanneganti TD (2018) TAK1 restricts spontaneous NLRP3 activation and cell death to control myeloid proliferation. J Exp Med 215(4):1023–1034
pubmed: 29500178
pmcid: 5881469
doi: 10.1084/jem.20171922
Chauhan A, Hudobenko J, Al Mamun A, Koellhoffer EC, Patrizz A, Ritzel RM et al (2018) Myeloid-specific TAK1 deletion results in reduced brain monocyte infiltration and improved outcomes after stroke. J Neuroinflammation 15(1):148
pubmed: 29776451
pmcid: 5960093
doi: 10.1186/s12974-018-1188-3