TAK1 signaling activity links the mast cell cytokine response and degranulation in allergic inflammation.
Animals
Bone Marrow Cells
/ drug effects
Calcium
/ metabolism
Cell Degranulation
/ drug effects
Cytokines
/ metabolism
Female
Gene Expression Regulation
/ drug effects
Hypersensitivity
/ enzymology
Immunoglobulin E
/ metabolism
Inflammation
/ genetics
Inflammation Mediators
/ metabolism
MAP Kinase Kinase Kinases
/ antagonists & inhibitors
Mast Cells
/ drug effects
Mice, Inbred C57BL
Models, Biological
NF-KappaB Inhibitor alpha
/ genetics
NF-kappa B
/ metabolism
Phosphorylation
/ drug effects
Phosphoserine
/ metabolism
Proto-Oncogene Proteins c-kit
/ metabolism
RNA, Messenger
/ genetics
Receptors, IgE
/ metabolism
Signal Transduction
Zearalenone
/ analogs & derivatives
FcεRI
MAPK signaling
NF-κB signaling
allergen-specific IgE
c-kit
Journal
Journal of leukocyte biology
ISSN: 1938-3673
Titre abrégé: J Leukoc Biol
Pays: England
ID NLM: 8405628
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
19
10
2018
revised:
13
02
2020
accepted:
15
02
2020
pubmed:
29
2
2020
medline:
13
8
2020
entrez:
29
2
2020
Statut:
ppublish
Résumé
Mast cells drive the inappropriate immune response characteristic of allergic inflammatory disorders via release of pro-inflammatory mediators in response to environmental cues detected by the IgE-FcεRI complex. The role of TGF-β-activated kinase 1 (TAK1), a participant in related signaling in other contexts, remains unknown in allergy. We detect novel activation of TAK1 at Ser412 in response to IgE-mediated activation under SCF-c-kit potentiation in a mast cell-driven response characteristic of allergic inflammation, which is potently blocked by TAK1 inhibitor 5Z-7-oxozeaenol (OZ). We, therefore, interrogated the role of TAK1 in a series of mast cell-mediated responses using IgE-sensitized murine bone marrow-derived mast cells, stimulated with allergen under several TAK1 inhibition strategies. TAK1 inhibition by OZ resulted in significant impairment in the phosphorylation of MAPKs p38, ERK, and JNK; and mediation of the NF-κB pathway via IκBα. Impaired gene expression and near abrogation in release of pro-inflammatory cytokines TNF, IL-6, IL-13, and chemokines CCL1, and CCL2 was detected. Finally, a significant inhibition of mast cell degranulation, accompanied by an impairment in calcium mobilization, was observed in TAK1-inhibited cells. These results suggest that TAK1 acts as a signaling node, not only linking the MAPK and NF-κB pathways in driving the late-phase response, but also initiation of the degranulation mechanism of the mast cell early-phase response following allergen recognition and may warrant consideration in future therapeutic development.
Identifiants
pubmed: 32108376
doi: 10.1002/JLB.2A0220-401RRR
doi:
Substances chimiques
7-oxozeanol
0
Cytokines
0
FcepsilonRIalpha protein, mouse
0
Inflammation Mediators
0
NF-kappa B
0
Nfkbia protein, mouse
0
RNA, Messenger
0
Receptors, IgE
0
NF-KappaB Inhibitor alpha
139874-52-5
Phosphoserine
17885-08-4
Immunoglobulin E
37341-29-0
Zearalenone
5W827M159J
Proto-Oncogene Proteins c-kit
EC 2.7.10.1
MAP Kinase Kinase Kinases
EC 2.7.11.25
MAP kinase kinase kinase 7
EC 2.7.11.25
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
649-661Informations de copyright
©2020 Society for Leukocyte Biology.
Références
Galli SJ, Tsai M. IgE and mast cells in allergic disease. Nat Med. 2012;18:693-704.
Blank U, Rivera J. The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol. 2004;25:266-273.
Hansen I, Klimek L, Mosges R, Hormann K. Mediators of inflammation in the early and the late phase of allergic rhinitis. Curr Opin Allergy Clin Immunol. 2004;4:159-163.
Meininger CJ, Yano H, Rottapel R, Bernstein A, Zsebo KM, Zetter BR. The c-kit receptor ligand functions as a mast cell chemoattractant. Blood. 1992;79:958-963.
Iemura A, Tsai M, Ando A, Wershil BK, Galli SJ. The c-kit ligand, stem cell factor, promotes mast cell survival by suppressing apoptosis. Am J Pathol. 1994;144:321-328.
Edling CE, Hallberg B. c-Kit-a hematopoietic cell essential receptor tyrosine kinase. Int J Biochem Cell Biol. 2007;39:1995-1998.
Huang B, Lei Z, Zhang GM, et al. SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood. 2008;112:1269-1279.
Metcalfe DD, Baram D, Mekori YA. Mast cells. Physiol Rev. 1997;77:1033-1079.
Metcalfe DD. Mast cells and mastocytosis. Blood. 2008;112:946-956.
Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nat Rev Immunol. 2006;6:218-230.
Landstrom M. The TAK1-TRAF6 signalling pathway. Int J Biochem Cell Biol. 2010;42:585-589.
Ear T, Cloutier A, McDonald PP. Constitutive nuclear expression of the i B kinase complex and its activation in human neutrophils. J Immunol. 2005;175:1834-1842.
Ear T, Fortin CF, Simard FA, McDonald PP. Constitutive association of TGF-beta-activated kinase 1 with the IkappaB kinase complex in the nucleus and cytoplasm of human neutrophils and its impact on downstream processes. J Immunol. 2010;184:3897-3906.
Chen IT, Hsu PH, Hsu WC, Chen NJ, Tseng PH. Polyubiquitination of transforming growth factor beta-activated kinase 1 (TAK1) at lysine 562 residue regulates TLR4-mediated JNK and p38 MAPK activation. Sci Rep. 2015;5:12300.
Zhang C, Baumgartner RA, Yamada K, Beaven MA. Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-alpha and release of arachidonic acid in mast cells. Indications of communication between p38 and p42 MAP kinases. J Biol Chem. 1997;272:13397-13402.
MacNeil AJ, Yang YJ, Lin TJ. MAPK kinase 3 specifically regulates Fc epsilonRI-mediated IL-4 production by mast cells. J Immunol. 2011;187:3374-3382.
Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. Philos Trans R Soc Lond B Biol Sci. 1996;351:127-134.
Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol. 1997;9:240-246.
Lorentz A, Klopp I, Gebhardt T, Manns MP, Bischoff SC. Role of activator protein 1, nuclear factor-kappaB, and nuclear factor of activated T cells in IgE receptor-mediated cytokine expression in mature human mast cells. J Allergy Clin Immunol. 2003;111:1062-1068.
Andrade MV, Iwaki S, Ropert C, Gazzinelli RT, Cunha-Melo JR, Beaven MA. Amplification of cytokine production through synergistic activation of NFAT and AP-1 following stimulation of mast cells with antigen and IL-33. Eur J Immunol. 2011;41:760-772.
MacNeil AJ, Junkins RD, Wu Z, Lin TJ. Stem cell factor induces AP-1-dependent mast cell IL-6 production via MAPK kinase 3 activity. J Leukoc Biol. 2014;95:903-915.
Jeong HJ, Koo HN, Na HJ, et al. Inhibition of TNF-alpha and IL-6 production by Aucubin through blockade of NF-kappaB activation RBL-2H3 mast cells. Cytokine. 2002;18:252-259.
Marquardt DL, Walker LL. Dependence of mast cell IgE-mediated cytokine production on nuclear factor-kappaB activity. J Allergy Clin Immunol. 2000;105:500-505.
Wang C, Deng L, Hong M, Akkaraju GG, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature. 2001;412:346-351.
Shim JH, Xiao C, Paschal AE, et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 2005;19:2668-2681.
Drube S, Weber F, Gopfert C, et al. TAK1 and IKK2, novel mediators of SCF-induced signaling and potential targets for c-Kit-driven diseases. Oncotarget. 2015;6:28833-28850.
Vink PM, Smout WM, Driessen-Engels LJ, et al. In vivo knockdown of TAK1 accelerates bone marrow proliferation/differentiation and induces systemic inflammation. PLoS One. 2013;8:e57348.
Ouyang C, Nie L, Gu M, et al. Transforming growth factor (TGF)-beta-activated kinase 1 (TAK1) activation requires phosphorylation of serine 412 by protein kinase A catalytic subunit alpha (PKACalpha) and X-linked protein kinase (PRKX). J Biol Chem. 2014;289:24226-24237.
Mollerherm H, Meier K, Schmies K, et al. Differentiation and functionality of bone marrow-derived mast cells depend on varying physiologic oxygen conditions. Front Immunol. 2017;8:1665.
Fan YH, Cheng J, Vasudevan SA, et al. TAK1 inhibitor 5Z-7-oxozeaenol sensitizes neuroblastoma to chemotherapy. Apoptosis. 2013;18:1224-1234.
Guan S, Lu J, Zhao Y, et al. TAK1 inhibitor 5Z-7-oxozeaenol sensitizes cervical cancer to doxorubicin-induced apoptosis. Oncotarget. 2017;8:33666-33675.
Gong YN, Wang X, Wang J, et al. Chemical probing reveals insights into the signaling mechanism of inflammasome activation. Cell Res. 2010;20:1289-1305.
Tan L, Gurbani D, Weisberg EL, et al. Studies of TAK1-centered polypharmacology with novel covalent TAK1 inhibitors. Bioorg Med Chem. 2017;25:1320-1328.
Kilty I, Jones LH. TAK1 selective inhibition: state of the art and future opportunities. Future Med Chem. 2015;7:23-33.
Nelson DE, Ihekwaba AE, Elliott M, et al. Oscillations in NF-kappaB signaling control the dynamics of gene expression. Science. 2004;306:704-708.
Brown K, Park S, Kanno T, Franzoso G, Siebenlist U. Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc Natl Acad Sci USA. 1993;90:2532-2536.
Shi L, Kishore R, McMullen MR, Nagy LE. Lipopolysaccharide stimulation of ERK1/2 increases TNF-alpha production via Egr-1. Am J Physiol Cell Physiol. 2002;282:C1205-1211.
Kong F, Laryea G, Liu Z, Bhattacharyya S. Transforming growth factor-beta-activated kinase 1 resistance limits glucocorticoid responsiveness to Toll-like receptor 4-mediated inflammation. Immunology. 2015;145:136-149.
Buglio D, Palakurthi S, Byth KF, Younes A. The Tak-1 inhibitor AZ-Tak1 inhibits XIAP, activates Caspase-9, and induces apoptosis in mantle cell lymphoma. Blood. 2009;114:1692.
Buglio D, Palakurti S, Vega F, et al. Inhibition of Tak-1 by AZ-Tak1 impairs NF-κB activation, downregulates XIAP and activates Caspase-9 inducing apoptosis in mantle cell lymphoma. Blood. 2010;116:2852.
Nguyen M, Solle M, Audoly LP, et al. Receptors and signaling mechanisms required for prostaglandin E2-mediated regulation of mast cell degranulation and IL-6 production. J Immunol. 2002;169:4586-4593.
Lorenz D, Wiesner B, Zipper J, et al. Mechanism of peptide-induced mast cell degranulation. Translocation and patch-clamp studies. J Gen Physiol. 1998;112:577-591.
Holowka D, Wilkes M, Stefan C, Baird B. Roles for Ca2+ mobilization and its regulation in mast cell functions: recent progress. Biochem Soc Trans. 2016;44:505-509.
Neubert M, Ridder DA, Bargiotas P, Akira S, Schwaninger M. Acute inhibition of TAK1 protects against neuronal death in cerebral ischemia. Cell Death Differ. 2011;18:1521-1530.
Sato S, Sanjo H, Takeda K, et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol. 2005;6:1087-1095.
Ma FY, Tesch GH, Ozols E, Xie M, Schneider MD, Nikolic-Paterson DJ. TGF-beta1-activated kinase-1 regulates inflammation and fibrosis in the obstructed kidney. Am J Physiol Renal Physiol. 2011;300:F1410-1421.
Wu J, Powell F, Larsen NA, et al. Mechanism and in vitro pharmacology of TAK1 inhibition by (5Z)-7-Oxozeaenol. ACS Chem Biol. 2013;8:643-650.
Zhang D, Yan H, Li H, et al. TGFbeta-activated kinase 1 (TAK1) inhibition by 5Z-7-oxozeaenol attenuates early brain injury after experimental subarachnoid hemorrhage. J Biol Chem. 2015;290:19900-19909.
Kamiyama H, Usui T, Sakurai H, et al. Epoxyquinol B, a naturally occurring pentaketide dimer, inhibits NF-kappaB signaling by crosslinking TAK1. Biosci Biotechnol Biochem. 2008;72:1894-1900.
Goldmann T, Wieghofer P, Muller PF, et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci. 2013;16:1618-1626.
Wan YY, Chi H, Xie M, Schneider MD, Flavell RA. The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol. 2006;7:851-858.
Shinohara H, Yasuda T, Kurosaki T. TAK1 adaptor proteins, TAB2 and TAB3, link the signalosome to B-cell receptor-induced IKK activation. FEBS Lett. 2016;590:3264-3269.
Schuman J, Chen Y, Podd A, et al. A critical role of TAK1 in B-cell receptor-mediated nuclear factor kappaB activation. Blood. 2009;113:4566-4574.
Ulleras E, Karlberg M, Moller Westerberg C, et al. NFAT but not NF-kappaB is critical for transcriptional induction of the prosurvival gene A1 after IgE receptor activation in mast cells. Blood. 2008;111:3081-3089.
Zhao Z, Zhong X, Wu T, et al. Identification of a NFKBIA polymorphism associated with lower NFKBIA protein levels and poor survival outcomes in patients with glioblastoma multiforme. Int J Mol Med. 2014;34:1233-1240.
Ying S, Robinson DS, Varney V, et al. TNF alpha mRNA expression in allergic inflammation. Clin Exp Allergy. 1991;21:745-750.
Eskilsson A, Mirrasekhian E, Dufour S, Schwaninger M, Engblom D, Blomqvist A. Immune-induced fever is mediated by IL-6 receptors on brain endothelial cells coupled to STAT3-dependent induction of brain endothelial prostaglandin synthesis. J Neurosci. 2014;34:15957-15961.
Wu Z, Macneil AJ, Junkins R, Li B, Berman JN, Lin TJ. Mast cell FcepsilonRI-induced early growth response 2 regulates CC chemokine ligand 1-dependent CD4+ T cell migration. J Immunol. 2013;190:4500-4507.
Montero-Melendez T, Llor X, Garcia-Planella E, Perretti M, Suarez A. Identification of novel predictor classifiers for inflammatory bowel disease by gene expression profiling. PLoS One. 2013;8:e76235.
Botta C, Di Martino MT, Ciliberto D, et al. A gene expression inflammatory signature specifically predicts multiple myeloma evolution and patients survival. Blood Cancer J. 2016;6:e511.
Zhao Y, Schetter AJ, Yang GB, et al. microRNA and inflammatory gene expression as prognostic marker for overall survival in esophageal squamous cell carcinoma. Int J Cancer. 2013;132:2901-2909.
Kaneda MM, Messer KS, Ralainirina N, et al. PI3Kgamma is a molecular switch that controls immune suppression. Nature. 2016;539:437-442.
Rajasekaran K, Chu H, Kumar P, et al. Transforming growth factor-beta-activated kinase 1 regulates natural killer cell-mediated cytotoxicity and cytokine production. J Biol Chem. 2011;286:31213-31224.
Sanjo H, Tokumaru S, Akira S, Taki S. Conditional deletion of TAK1 in T cells reveals a pivotal role of TCRalphabeta+ intraepithelial lymphocytes in preventing lymphopenia-associated colitis. PLoS One. 2015;10:e0128761.
Nakatsumi H, Matsumoto M, Nakayama KI. Noncanonical pathway for regulation of CCL2 expression by an mTORC1-FOXK1 axis promotes recruitment of tumor-associated macrophages. Cell Rep. 2017;21:2471-2486.
Urb M, Sheppard DC. The role of mast cells in the defence against pathogens. PLoS Pathog. 2012;8:e1002619.
Wedemeyer J, Tsai M, Galli SJ. Roles of mast cells and basophils in innate and acquired immunity. Curr Opin Immunol. 2000;12:624-631.
Bansode RR, Plundrich NJ, Randolph PD, Lila MA, Williams LL. Peanut flour aggregation with polyphenolic extracts derived from peanut skin inhibits IgE binding capacity and attenuates RBL-2H3 cells degranulation via MAPK signaling pathway. Food Chem. 2018;263:307-314.
Lianto P, Ogutu FO, Zhang Y, He F, Che H. Inhibitory effects of quail egg on mast cells degranulation by suppressing PAR2-mediated MAPK and NF-kB activation. Food Nutr Res. 2018;62.
Choi HS, Kim KM. Tanshinones inhibit mast cell degranulation by interfering with IgE receptor-mediated tyrosine phosphorylation of PLCgamma2 and MAPK. Planta Med. 2004;70:178-180.