2,286
Views
8
CrossRef citations to date
0
Altmetric
Original Articles

Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion

, , , , , , ORCID Icon, , , , & show all
Pages 734-748 | Received 18 Dec 2018, Accepted 04 May 2019, Published online: 25 May 2019

References

  • Reddick LE, Neal MA. Bacteria fighting back: How pathogens target and subvert the host innate immune system. Mol Cell. 2014;54:321–328. doi: 10.1016/j.molcel.2014.03.010
  • Beutler BA. TLRs and innate immunity. Blood. 2008;113:1399–1407. doi: 10.1182/blood-2008-07-019307
  • Daëron M, Jaeger S, Du Pasquier L, et al. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol Rev. 2008;224:11–43. doi: 10.1111/j.1600-065X.2008.00666.x
  • Blank U, Launay P, Benhamou M, et al. Inhibitory ITAMs as novel regulators of immunity. Immunol Rev Nov. 2009;232:59–71. doi: 10.1111/j.1600-065X.2009.00832.x
  • Zhang J, Somani AK, Siminovitch KA. Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signalling. Semin Immunol. 2000;12:361–378. doi: 10.1006/smim.2000.0223
  • Neel BG, Gu H, Pao L. The ‘shp’ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci. 2003;28:284–293. doi: 10.1016/S0968-0004(03)00091-4
  • Hamerman JA, Tchao NK, Lowell CA, et al. Enhanced toll-like receptor responses in the absence of signaling adaptor DAP12. Nat Immunol. 2005;6:579–586. doi: 10.1038/ni1204
  • An HZ, Hou J, Zhou J, et al. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat Immunol. 2008;9:542–550. doi: 10.1038/ni.1604
  • Khaled AR, Butfiloski EJ, Sobel ES, et al. Functional consequences of the SHP-1 defect in motheaten viable mice: role of NF-κB. Cell Immunol. 1998;185:49–58. doi: 10.1006/cimm.1998.1272
  • Ajibade AA, Wang HY, Wang RF. Cell type-specific function of TAK1 in innate immune signaling. Trends Immunol. 2013;34:307–316. doi: 10.1016/j.it.2013.03.007
  • Shirakabe K, Yamaguchi K, Shibuya H, et al. TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J Biol Chem. 1997;272:8141–8144. doi: 10.1074/jbc.272.13.8141
  • Ninomiya-Tsuji J, Kishimoto K, Hiyama A, et al. The kinase TAK1 can activate the NIK-IκB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature. 1999;398:252–256. doi: 10.1038/18465
  • Lee J, Mira-Arbibe L, Ulevitch RJ. TAK1 regulates multiple protein kinase cascades activated by bacterial lipopolysaccharide. J Leukoc Biol. 2000;68:909–915.
  • Shibuya H, Yamaguchi K, Shirakabe K, et al. TAB1: an activator of the TAK1 MAPKKK in TGF-β signal transduction. Science. 1996;272:1179–1182. doi: 10.1126/science.272.5265.1179
  • Singhirunnusorn P, Suzuki S, Kawasaki N, et al. Critical roles of threonine 187 phosphorylation in cellular stress-induced rapid and transient activation of transforming growth factor-β-activated kinase 1 (TAK1) in a signaling complex containing TAK1-binding protein TAB1 and TAB2. J Biol Chem. 2005;280:7359–7368. doi: 10.1074/jbc.M407537200
  • Ouyang C, Nie L, Gu M, et al. Transforming growth factor (TGF)-β-activated kinase 1 (TAK1) activation requires phosphorylation of serine 412 by protein kinase A catalytic subunit α (PKACα) and X-linked protein kinase (PRKX). J Biol Chem. 2014;289:24226–24237. doi: 10.1074/jbc.M114.559963
  • Lin CC, Kuo C-T, Cheng C-Y, et al. IL-1β promotes A549 cell migration via MAPKs/AP-1 and NF-κB-dependent matrix metalloproteinase-9 expression. Cell Signal. 2009;21:1652–1662. doi: 10.1016/j.cellsig.2009.07.002
  • Kim SI, Kwak JH, Zachariah M, et al. TGF-activated kinase 1 and TAK1-binding protein 1 cooperate to mediate TGF-β1-induced MKK3-p38 MAPK activation and stimulation of type I collagen. AJP: Renal Physiology. 2007;292:F1471–F1478.
  • Chen WP, Tzeng H-J, Ku H-C, et al. Thaliporphine ameliorates cardiac depression in endotoxemic rats through attenuating TLR4 signaling in the downstream of TAK1 phosphorylation and NF-κB signaling. Naunyn Schmiedebergs Arch Pharmacol. 2010;382:441–453. doi: 10.1007/s00210-010-0562-1
  • Phillips AD. Enterohaemorrhagic Escherichia coli O157:H7 target Peyer’s patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut. 2000;47:377–381. doi: 10.1136/gut.47.3.377
  • Donnenberg MS, Whittam TS. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J Clin Invest. 2001;107:539–548. doi: 10.1172/JCI12404
  • Gaytán MO, Martínez-Santos VI, Soto E, et al. Type three secretion system in attaching and effacing pathogens. Front Cell Infect Microbiol ECollection. 2016;6:1–25.
  • Kenny B, DeVinney R, Stein M, et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 1997;91:511–520. doi: 10.1016/S0092-8674(00)80437-7
  • Oh KH, Jung S-M, Shin E, et al. Comparison of enterohemorrhagic Escherichia coli (EHEC) O157 and EHEC non-O157 isolates from patients with diarrhea in Korea. Jpn J Infect Dis. 2017;70:320–322. doi: 10.7883/yoken.JJID.2016.178
  • Vingadassalom DA, Kazlauskas A, Skehan B, et al. Insulin receptor tyrosine kinase substrate links the E. coli O157:H7 actin assembly effectors Tir and EspF(U) during pedestal formation. Proc Natl Acad Sci U.S.A. 2009;106:6754–6759. doi: 10.1073/pnas.0809131106
  • Campellone KG, Rankin S, Pawson T, et al. Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J Cell Biol. 2004;164:407–416. doi: 10.1083/jcb.200306032
  • Elizabeth AC, Meredith MC, Aman K, et al. Microbiota and pathogen proteases modulate type III secretion activity in Enterohemorrhagic Escherichia coli. mBio. 2018;9:e02204–18.
  • Yan D, Quan H, Wang L, et al. Enteropathogenic Escherichia coli Tir recruits cellular SHP-2 through ITIM motifs to suppress host immune response. Cell Signal. 2013;25:1887–1894. doi: 10.1016/j.cellsig.2013.05.020
  • Yan D, Wang X, Luo L, et al. Inhibition of TLR signaling by a bacterial protein containing immunoreceptor tyrosine-based inhibitory motifs. Nat Immunol. 2012;13:1063–1071. doi: 10.1038/ni.2417
  • Zhuang X, Chen Z, He C, et al. Modulation of host signaling in the inflammatory response by enteropathogenic Escherichia coli virulence proteins. Cell Mol Immunol. 2017;14:237–244. doi: 10.1038/cmi.2016.52
  • Laurie P, Philippe JS, Armelle P. Host cell targeting by enteropathogenic bacteria T3SS effectors. Trends Microbiol. 2018;26:266–283. doi: 10.1016/j.tim.2018.01.010
  • Jens CG, Schlüter K, Carius Y, et al. Structural basis for complex formation between human IRSp53 and the translocated intimin receptor Tir of Enterohemorrhagic E. coli. Structure. 2011;19:1294–1306. doi: 10.1016/j.str.2011.06.015
  • Cambier JC. Inhibitory receptors abound? Proc Natl Acad. Sci U.S.A. 1997;94:5993–5995. doi: 10.1073/pnas.94.12.5993
  • Getahun A, Cambier JC. Of ITIMs, ITAMs, and ITAMis: revisiting immunoglobulin Fc receptor signaling. Immunol Rev. 2015;268:66–73. doi: 10.1111/imr.12336
  • Sakurai H, Shigemori N, Hasegawa K, et al. TGF-β-activated kinase 1 stimulates NFκ-B activation by an NFκ-inducing kinase-independent mechanism. Biochem Biophys Res Commun. 1998;243:545–549. doi: 10.1006/bbrc.1998.8124
  • Sakurai H, Miyoshi H, Toriumi W, et al. Functional interactions of transforming growth factor β-activated kinase 1 with IκB kinases to stimulate NF-kappaB activation. J Biol Chem. 1999;274:10641–10648. doi: 10.1074/jbc.274.15.10641
  • Broglie P, Matsumoto K, Akira S, et al. Transforming growth factor beta-activated kinase 1 (TAK1) kinase adaptor, TAK1-binding protein 2, plays dual roles in TAK1 signaling by recruiting both an activator and an inhibitor of TAK1 kinase in tumor necrosis factor signaling pathway. J Biol Chem. 2010;285:2333–2339. doi: 10.1074/jbc.M109.090522
  • Kajino T, Ren H, Iemura S-I, et al. Protein phosphatase 6 down-regulates TAK1 kinase activation in the IL-1 signaling pathway. J Biol Chem. 2006;281:39891–39896. doi: 10.1074/jbc.M608155200
  • Takaesu G, Ninomiya-Tsuji J, Kishida S, et al. Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway. Mol Cell Biol. 2001;21:2475–2484. doi: 10.1128/MCB.21.7.2475-2484.2001
  • Yu Y, Ge N, Xie M, et al. Phosphorylation of Thr-178 and Thr-184 in the TAK1 T-loop is required for interleukin (IL)-1-mediated optimal NFκB and AP-1 activation as well as IL-6 gene expression. J Biol Chem. 2008;283:24497–24505. doi: 10.1074/jbc.M802825200
  • Pathak S, Borodkin VS, Albarbarawi O, et al. O-GlcNAcylation of TAB1 modulates TAK1-mediated cytokine release. EMBO J. 2012;31:1394–1404. doi: 10.1038/emboj.2012.8
  • Barrow AD, Trowsdale J. You say ITAM and I say ITIM, let’s call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol. 2006;36:1646–1653. doi: 10.1002/eji.200636195
  • Sharma Y, Bashir S, Bhardwaj P, et al. Protein tyrosine phosphatase SHP-1: resurgence as new drug target for human autoimmune disorders. Immunol Res. 2016;64:804–819. doi: 10.1007/s12026-016-8805-y
  • Kruger J, Butler JR, Cherapanov V, et al. Deficiency of Src homology 2-containing phosphatase 1 results in abnormalities in murine neutrophil function: studies in motheaten mice. J Immunol. 2000;165:5847–5859. doi: 10.4049/jimmunol.165.10.5847
  • Campellone KG, Leong JM. Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157: H7. Curr Opin Microbiol. 2003;6:82–90. doi: 10.1016/S1369-5274(03)00005-5
  • Celli J, Deng W, Finlay BB. Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell Microbiol. 2000;2:1–9. doi: 10.1046/j.1462-5822.2000.00033.x
  • Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34:637–650. doi: 10.1016/j.immuni.2011.05.006
  • Campellone KG. Cytoskeleton-modulating effectors of enteropathogenic and enterohaemorrhagic Escherichia coli: Tir, EspFU and actin pedestal assembly. FEBS J. 2010;277:2390–2402. doi: 10.1111/j.1742-4658.2010.07653.x