Inhibition of lethal inflammatory responses through the targeting of membrane-associated Toll-like receptor 4 signaling complexes with a Smad6-derived peptide

EMBO Molecular Medicine

Volumn 7, Issue 5, 2015, Pages 577-592

  Lee, Youn Sook ^a   Park, Jin Seok ^a   Jung, Su Myung ^a   Kim, Sang Doo ^a   Kim, Jun Hwan ^a   Lee, Jae Young ^a   Jung, Kyeong Cheon ^b   Mamura, Mizuko ^c,d   Lee, Sangho ^a   Kim, Seong Jin ^e   Bae, Yoe Sik ^a   Park, Seok Hee ^a  

^a Sungkyunkwan University   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c TOKYO MEDICAL UNIVERSITY   (Japan)

^d Kyungpook National University School of Medicine   (South Korea)

^e CHA University   (South Korea)

Author keywords

Inflammation; Pellino 1; Sepsis; Smad6; TLR4

Indexed keywords

CEPHALOSPORIN; CHEMOKINE RECEPTOR CXCR2; CXCL2 CHEMOKINE; G PROTEIN COUPLED RECEPTOR KINASE 2; GAMMA INTERFERON; GENTAMICIN; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; PALMITIC ACID; PELLINO 1 PROTEIN; PROTEIN; RIP1 PROTEIN; SMAD6 PROTEIN; SMADUCIN 6 PROTEIN; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; IMMUNOSUPPRESSIVE AGENT; NUCLEAR PROTEIN; OLIGOPEPTIDE; PELI1 PROTEIN, MOUSE; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BACTERIUM COLONY; CELL MIGRATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG MEGADOSE; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INFLAMMATION; INFLAMMATORY DISEASE; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; LOW DRUG DOSE; MORTALITY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEPSIS; SEPTIC SHOCK; SURVIVAL RATE; THERAPY EFFECT; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; ENDOTOXEMIA; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

ANIMALS; ANTI-INFLAMMATORY AGENTS; DISEASE MODELS, ANIMAL; ENDOTOXEMIA; IMMUNOSUPPRESSIVE AGENTS; MICE; NUCLEAR PROTEINS; OLIGOPEPTIDES; PROTEIN BINDING; SEPSIS; SIGNAL TRANSDUCTION; SMAD6 PROTEIN; TOLL-LIKE RECEPTOR 4; TREATMENT OUTCOME; UBIQUITIN-PROTEIN LIGASES;

EID: 84929049688     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201404653     Document Type: Article

References (63)

1. Alves-Filho JC, Freitas A, Souto FO, Spiller F, Paula-Neto H, Silva JS, Gazzinelli RT, Teixeira MM, Ferreira SH, Cunha FQ (2009) Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc Natl Acad Sci USA 106: 4018-4023
2. Alves-Filho JC, Sonego F, Souto FO, Freitas A, Verri WA Jr, Auxiliadora-Martins M, Basile-Filho A, McKenzie AN, Xu D, Cunha FQ et al (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 16: 708-712
3. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201
4. Blobe GC, Schiemann WP, Lodish HF (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342: 1350-1358
5. Butler MP, Hanly JA, Moynagh PN (2007) Kinase active IRAKs promote polyubiquitination and degradation of the Pellino family: direct evidence for Pellino proteins being E3 ubiquitin ligases. J Biol Chem 282: 29729-29737
6. Cavaillon JM, Adib-Conquy M, Fitting C, Adrie C, Payen D (2003) Cytokine cascade in sepsis. Scand J Infect Dis 35: 535-544
7. Chang M, Jin W, Sun SC (2009) Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat Immunol 10: 1089-1095
8. Chang M, Jin W, Chang JH, Xiao Y, Brittain GC, Yu J, Zhou X, Wang YH, Cheng X, Li P et al (2011) The ubiquitin ligase Peli1 negatively regulates T cell activation and prevents autoimmunity. Nat Immunol 12: 1002-1009
9. Choi KC, Lee YS, Lim S, Choi HK, Lee CH, Lee EK, Hong S, Kim IH, Kim SJ, Park SH (2006) Smad6 negatively regulates interleukin 1-receptor-Toll-like receptor signaling through direct interaction with the adaptor Pellino-1. Nat Immunol 7: 1057-1065
10. Cisowski J, O'Callaghan K, Kuliopulos A, Yang J, Nguyen N, Deng Q, Yang E, Fogel M, Tressel S, Foley C et al (2011) Targeting protease-activated receptor-1 with cell-penetrating pepducins in lung cancer. Am J Pathol 179: 513-523
11. Cochran AG (2000) Antagonists of protein-protein interactions. Chem Biol 7: R85-R94
12. Cohen J (2002) The immunopathogenesis of sepsis. Nature 420: 885-891
13. Corazza N, Kassahn D, Jakob S, Badmann A, Brunner T (2009) TRAIL-induced apoptosis: between tumor therapy and immunopathology. Ann N Y Acad Sci 1171: 50-58
14. Covic L, Misra M, Badar J, Singh C, Kuliopulos A (2002) Pepducin-based intervention of thrombin-receptor signaling and systemic platelet activation. Nat Med 8: 1161-1165
15. Covic L, Tchernychev B, Jacques S, Kuliopulos A (2007) Pharmacology and in vivo efficacy of pepducins in hemostasis and arterial thrombosis. In Handbook of Cell-Penetrating Peptides, Langel U (ed.), pp 245-257. Boca Raton, FL: CRC Press
16. Cummings CJ, Martin TR, Frevert CW, Quan JM, Wong VA, Mongovin SM, Hagen TR, Steinberg KP, Goodman RB (1999) Expression and function of the chemokine receptors CXCR1 and CXCR2 in sepsis. J Immunol 162: 2341-2346
17. Dejager L, Vandevyver S, Ballegeer M, Van Wonterghem E, An LL, Riggs J, Kolbeck R, Libert C (2014) Pharmacological inhibition of type I interferon signaling protects mice against lethal sepsis. J Infect Dis 209: 960-970
18. Diehl GE, Yue HH, Hsieh K, Kuang AA, Ho M, Morici LA, Lenz LL, Cado D, Riley LW, Winoto A (2004) TRAIL-R as a negative regulator of innate immune cell responses. Immunity 21: 877-889
19. Grosshans J, Schnorrer F, Nusslein-Volhard C (1999) Oligomerisation of Tube and Pelle leads to nuclear localisation of dorsal. Mech Dev 81: 127-138
20. Gurung P, Rai D, Condotta SA, Babcock JC, Badovinac VP, Griffith TS (2011) Immune unresponsiveness to secondary heterologous bacterial infection after sepsis induction is TRAIL dependent. J Immunol 187: 2148-2154
21. Hata A, Lagna G, Massague J, Hemmati-Brivanlou A (1998) Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12: 186-197
22. Higueruelo AP, Jubb H, Blundell TL (2013) Protein-protein interactions as druggable targets: recent technological advances. Curr Opin Pharmacol 13: 791-796
23. Hotchkiss RS, Tinsley KW, Swanson PE, Chang KC, Cobb JP, Buchman TG, Korsmeyer SJ, Karl IE (1999) Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc Natl Acad Sci USA 96: 14541-14546
24. Hotchkiss RS, Nicholson DW (2006) Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 6: 813-822
25. Hubbard WJ, Choudhry M, Schwacha MG, Kerby JD, Rue LW 3rd, Bland KI, Chaudry IH (2005) Cecal ligation and puncture. Shock 24(Suppl 1): 52-57
26. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K (1997) Smad6 inhibits signalling by the TGF-beta superfamily. Nature 389: 622-626
27. Inoue Y, Imamura T (2008) Regulation of TGF-beta family signaling by E3 ubiquitin ligases. Cancer Sci 99: 2107-2112
28. Ishida W, Hamamoto T, Kusanagi K, Yagi K, Kawabata M, Takehara K, Sampath TK, Kato M, Miyazono K (2000) J Biol Chem 275: 6075-6079
29. Jiang Z, Johnson HJ, Nie H, Qin J, Bird TA, Li X (2003) Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J Biol Chem 278: 10952-10956
30. Jung SM, Lee JH, Park J, Oh YS, Lee SK, Park JS, Lee YS, Kim JH, Lee JY, Bae YS et al (2013) Smad6 inhibits non-canonical signalling by recruiting the deubiquitinase A20 to TRAF6. Nat Commun 4: 2562
31. Kaiser WJ, Offermann MK (2005) Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J Immunol 174: 4942-4952
32. Kayagaki N, Yamaguchi N, Nakayama M, Eto H, Okumura K, Yagita H (1999) Type I interferons (IFNs) regulate tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression on human T cells: a novel mechanism for the antitumor effects of type I IFNs. J Exp Med 189: 1451-1460
33. Kim BC, Lee HJ, Park SH, Lee SR, Karpova TS, McNally JG, Felici A, Lee DK, Kim SJ (2004) Jab1/CSN5, a component of the COP9 signalosome, regulates transforming growth factor beta signaling by binding to Smad7 and promoting its degradation. Mol Cell Biol 24: 2251-2262
34. Kim SD, Kim YK, Lee HY, Kim YS, Jeon SG, Baek SH, Song DK, Ryu SH, Bae YS (2010) The agonists of formyl peptide receptors prevent development of severe sepsis after microbial infection. J Immunol 185: 4302-4310
35. Kirikae T, Nakano M, Morrison DC (1997) Antibiotic-induced endotoxin release from bacteria and its clinical significance. Microbiol Immunol 41: 285-294
36. Lee YS, Park JS, Kim JH, Jung SM, Lee JY, Kim SJ, Park SH (2011) Smad6-specific recruitment of Smurf E3 ligases mediates TGF-beta1-induced degradation of MyD88 in TLR4 signalling. Nat Commun 2: 460
37. Lin CC, Huoh YS, Schmitz KR, Jensen LE, Ferguson KM (2008) Pellino proteins contain a cryptic FHA domain that mediates interaction with phosphorylated IRAK1. Structure 16: 1806-1816
38. Loniewski K, Shi Y, Pestka J, Parameswaran N (2008) Toll-like receptors differentially regulate GPCR kinases and arrestins in primary macrophages. Mol Immunol 45: 2312-2322
39. Morén A, Imamura T, Miyazono K, Heldin CH, Moustakas A (2005) Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J Biol Chem 280: 22115-22123
40. Moynagh PN (2009) The Pellino family: IRAK E3 ligases with emerging roles in innate immune signalling. Trends Immunol 30: 33-42
41. Moynagh PN (2014) The roles of Pellino E3 ubiquitin ligases in immunity. Nat Rev Immunol 14: 122-131
42. Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182
43. Ofengein D, Yuan J (2013) Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat Rev Mol Cell Biol 14: 727-736
44. Opal SM, Laterre PF, Francois B, LaRosa SP, Angus DC, Mira JP, Wittebole X, Dugernier T, Perrotin D, Tidswell M et al (2013) Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA 309: 1154-1162
45. 63-linked polyubiquitination of IRAK1. Biochem J 409: 43-52
46. Rice TW, Wheeler AP, Bernard GR, Vincent JL, Angus DC, Aikawa N, Demeyer I, Sainati S, Amlot N, Cao C et al (2010) A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med 38: 1685-1694
47. Schauvliege R, Janssens S, Beyaert R (2006) Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett 580: 4697-4702
48. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285: 1569-1572
49. Siednienko J, Jackson R, Mellett M, Delagic N, Yang S, Wang B, Tang LS, Callanan JJ, Mahon BP, Moynagh PN (2012) Pellino3 targets the IRF7 pathway and facilitates autoregulation of TLR3- and viral-induced expression of type I interferons. Nat Immunol 13: 1055-1062
50. Smith H, Liu XY, Dai L, Goh ET, Chan AT, Xi J, Seh CC, Qureshi IA, Lescar J, Ruedl C et al (2011) The role of TBK1 and IKKepsilon in the expression and activation of Pellino 1. Biochem J 434: 537-548
51. Stearns-Kurosawa DJ, Osuchowski MF, Valentine C, Kurosawa S, Remick DG (2011) The pathogenesis of sepsis. Annu Rev Pathol 6: 19-48
52. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820
53. Tressel SL, Koukos G, Tchernychev B, Jacques SL, Covic L, Kuliopulos A (2011) Pharmacology, biodistribution, and efficacy of GPCR-based pepducins in disease moldels. Methods Mol Biol 683: 259-275
54. Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL, Mochizuki H (2008) Role of Toll-like receptors in the development of sepsis. Shock 29: 315-321
55. Unsinger J, Kazama H, McDonough JS, Griffith TS, Hotchkiss RS, Ferguson TA (2010) Sepsis-induced apoptosis leads to active suppression of delayed-type hypersensitivity by CD8+ regulatory T cells through a TRAIL-dependent mechanism. J Immunol 184: 6766-6772
56. Valente P, Fernandez-Carvajal A, Camprubi-Robles M, Gomis A, Quirce S, Viana F, Fernandez-Ballester G, Gonzalez-Ros JM, Belmonte C, Planells-Cases R et al (2011) Membrane-tethered peptides patterned after the TRP domain (TRPducins) selectively inhibit TRPV1 channel activity. FASEB J 25: 1628-1640
57. Vroon A, Heijnen CJ, Kavelaars A (2006) GRKs and arrestins: regulators of migration and inflammation. J Leukoc Biol 80: 1214-1221
58. Weighardt H, Holzmann B (2007) Role of Toll-like receptor responses for sepsis pathogenesis. Immunobiology 212: 715-722
59. Wilson AJ (2009) Inhibition of protein-protein interactions using designed molecules. Chem Soc Rev 38: 3289-3300
60. Wittebole X, Castanares-Zapatero D, Laterre PF (2010) Toll-like receptor 4 modulation as a strategy to treat sepsis. Mediators Inflamm 2010: 568396
61. Xiao Y, Jin J, Chang M, Chang JH, Hu H, Zhou X, Brittain GC, Stansberg C, Torkildsen O, Wang X et al (2013) Peli1 promotes microglia-mediated CNS inflammation by regulating Traf3 degradation. Nat Med 19: 595-602
62. Yang S, Wang B, Humphries F, Jackson R, Healy ME, Bergin R, Aviello G, Hall B, McNamara D, Darby T et al (2013a) Pellino3 ubiquitinates RIP2 and mediates Nod2-induced signaling and protective effects in colitis. Nat Immunol 14: 927-936
63. Yang S, Wang B, Tang LS, Siednienko J, Callanan JJ, Moynagh PN (2013b) Pellino3 targets RIP1 and regulates the pro-apoptotic effects of TNF-alpha. Nat Commun 4: 2583