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Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling.

Ve T, Vajjhala PR, Hedger A, Croll T, DiMaio F, Horsefield S, Yu X, Lavrencic P, Hassan Z, Morgan GP, Mansell A, Mobli M, O'Carroll A, Chauvin B, Gambin Y, Sierecki E, Landsberg MJ, Stacey KJ, Egelman EH, Kobe B
Nat Struct Mol Biol 24 743-751 (2017)
Cited: 77 times
EuropePMC logo PMID: 28759049

Abstract

Toll-like receptor (TLR) signaling is a key innate immunity response to pathogens. Recruitment of signaling adapters such as MAL (TIRAP) and MyD88 to the TLRs requires Toll/interleukin-1 receptor (TIR)-domain interactions, which remain structurally elusive. Here we show that MAL TIR domains spontaneously and reversibly form filaments in vitro. They also form cofilaments with TLR4 TIR domains and induce formation of MyD88 assemblies. A 7-Å-resolution cryo-EM structure reveals a stable MAL protofilament consisting of two parallel strands of TIR-domain subunits in a BB-loop-mediated head-to-tail arrangement. Interface residues that are important for the interaction are conserved among different TIR domains. Although large filaments of TLR4, MAL or MyD88 are unlikely to form during cellular signaling, structure-guided mutagenesis, combined with in vivo interaction assays, demonstrated that the MAL interactions defined within the filament represent a template for a conserved mode of TIR-domain interaction involved in both TLR and interleukin-1 receptor signaling.

Articles - 5uzb mentioned but not cited (7)

  1. Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling. Ve T, Vajjhala PR, Hedger A, Croll T, DiMaio F, Horsefield S, Yu X, Lavrencic P, Hassan Z, Morgan GP, Mansell A, Mobli M, O'Carroll A, Chauvin B, Gambin Y, Sierecki E, Landsberg MJ, Stacey KJ, Egelman EH, Kobe B. Nat Struct Mol Biol 24 743-751 (2017)
  2. MyD88 TIR domain higher-order assembly interactions revealed by microcrystal electron diffraction and serial femtosecond crystallography. Clabbers MTB, Holmes S, Muusse TW, Vajjhala PR, Thygesen SJ, Malde AK, Hunter DJB, Croll TI, Flueckiger L, Nanson JD, Rahaman MH, Aquila A, Hunter MS, Liang M, Yoon CH, Zhao J, Zatsepin NA, Abbey B, Sierecki E, Gambin Y, Stacey KJ, Darmanin C, Kobe B, Xu H, Ve T. Nat Commun 12 2578 (2021)
  3. A survey of TIR domain sequence and structure divergence. Toshchakov VY, Neuwald AF. Immunogenetics 72 181-203 (2020)
  4. Blocking TIR Domain Interactions in TLR9 Signaling. Javmen A, Szmacinski H, Lakowicz JR, Toshchakov VY. J. Immunol. 201 995-1006 (2018)
  5. Three-Dimensional Graph Matching to Identify Secondary Structure Correspondence of Medium-Resolution Cryo-EM Density Maps. Behkamal B, Naghibzadeh M, Saberi MR, Tehranizadeh ZA, Pagnani A, Al Nasr K. Biomolecules 11 1773 (2021)
  6. Full-Atom Model of the Agonist LPS-Bound Toll-like Receptor 4 Dimer in a Membrane Environment. Matamoros-Recio A, Franco-Gonzalez JF, Perez-Regidor L, Billod JM, Guzman-Caldentey J, Martin-Santamaria S. Chemistry 27 15406-15425 (2021)
  7. LPTD: a novel linear programming-based topology determination method for cryo-EM maps. Behkamal B, Naghibzadeh M, Pagnani A, Saberi MR, Al Nasr K. Bioinformatics 38 2734-2741 (2022)


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  1. Structural and functional understanding of the toll-like receptors. Asami J, Shimizu T. Protein Sci 30 761-772 (2021)
  2. Molecular innovations in plant TIR-based immunity signaling. Lapin D, Johanndrees O, Wu Z, Li X, Parker JE. Plant Cell 34 1479-1496 (2022)
  3. The Evolutionary Origins of Programmed Cell Death Signaling. Hofmann K. Cold Spring Harb Perspect Biol 12 a036442 (2020)
  4. Higher-order assemblies in immune signaling: supramolecular complexes and phase separation. Xia S, Chen Z, Shen C, Fu TM. Protein Cell 12 680-694 (2021)
  5. Mechanics of a molecular mousetrap-nucleation-limited innate immune signaling. Rodríguez Gama A, Miller T, Halfmann R. Biophys J 120 1150-1160 (2021)
  6. Molecular insights into the biochemical functions and signalling mechanisms of plant NLRs. Liu X, Wan L. Mol Plant Pathol 23 772-780 (2022)
  7. Targeting the TLR signalosome with TIR domain-derived cell-permeable decoy peptides: the current state and perspectives. Toshchakov VY, Javmen A. Innate Immun 26 35-47 (2020)
  8. Understanding early TLR signaling through the Myddosome. Balka KR, De Nardo D. J. Leukoc. Biol. 105 339-351 (2019)
  9. Below the surface: The inner lives of TLR4 and TLR9. Marongiu L, Gornati L, Artuso I, Zanoni I, Granucci F. J. Leukoc. Biol. 106 147-160 (2019)
  10. Progress in Research on TLR4-Mediated Inflammatory Response Mechanisms in Brain Injury after Subarachnoid Hemorrhage. Wang L, Geng G, Zhu T, Chen W, Li X, Gu J, Jiang E. Cells 11 3781 (2022)
  11. Toll-Like Receptors as a Therapeutic Target in the Era of Immunotherapies. Farooq M, Batool M, Kim MS, Choi S. Front Cell Dev Biol 9 756315 (2021)
  12. Immune signalling by supramolecular assemblies. Kumar S, Jain S. Immunology 155 435-445 (2018)
  13. Molecular Mechanisms of Action of Emodin: As an Anti-Cardiovascular Disease Drug. Li Q, Gao J, Pang X, Chen A, Wang Y. Front Pharmacol 11 559607 (2020)
  14. Recent Advances in the Development of Toll-like Receptor Agonist-Based Vaccine Adjuvants for Infectious Diseases. Yang JX, Tseng JC, Yu GY, Luo Y, Huang CF, Hong YR, Chuang TH. Pharmaceutics 14 423 (2022)
  15. Structural Evolution of TIR-Domain Signalosomes. Nimma S, Gu W, Maruta N, Li Y, Pan M, Saikot FK, Lim BYJ, McGuinness HY, Zaoti ZF, Li S, Desa S, Manik MK, Nanson JD, Kobe B. Front Immunol 12 784484 (2021)
  16. The Railmap of Type I Interferon Induction: Subcellular Network Plan and How Viruses Can Change Tracks. Weber L, Vieyres G. Cells 11 3149 (2022)
  17. When Innate Immunity Meets Angiogenesis-The Role of Toll-Like Receptors in Endothelial Cells and Pulmonary Hypertension. Bhagwani A, Thompson AAR, Farkas L. Front Med (Lausanne) 7 352 (2020)

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  1. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Martin R, Qi T, Zhang H, Liu F, King M, Toth C, Nogales E, Staskawicz BJ. Science 370 eabd9993 (2020)
  2. Innate Immune Signaling Organelles Display Natural and Programmable Signaling Flexibility. Tan Y, Kagan JC. Cell 177 384-398.e11 (2019)
  3. Structural basis of SARM1 activation, substrate recognition, and inhibition by small molecules. Shi Y, Kerry PS, Nanson JD, Bosanac T, Sasaki Y, Krauss R, Saikot FK, Adams SE, Mosaiab T, Masic V, Mao X, Rose F, Vasquez E, Furrer M, Cunnea K, Brearley A, Gu W, Luo Z, Brillault L, Landsberg MJ, DiAntonio A, Kobe B, Milbrandt J, Hughes RO, Ve T. Mol Cell 82 1643-1659.e10 (2022)
  4. Activation of Toll-like receptors nucleates assembly of the MyDDosome signaling hub. Latty SL, Sakai J, Hopkins L, Verstak B, Paramo T, Berglund NA, Cammarota E, Cicuta P, Gay NJ, Bond PJ, Klenerman D, Bryant CE. Elife 7 (2018)
  5. SIGIRR Mutation in Human Necrotizing Enterocolitis (NEC) Disrupts STAT3-Dependent microRNA Expression in Neonatal Gut. Yu W, Haque I, Venkatraman A, Menden HL, Mabry SM, Roy BC, Xia S, Prokop JW, Umar S, Geurts AM, Sampath V. Cell Mol Gastroenterol Hepatol 13 425-440 (2022)
  6. A phase transition enhances the catalytic activity of SARM1, an NAD+ glycohydrolase involved in neurodegeneration. Loring HS, Czech VL, Icso JD, O'Connor L, Parelkar SS, Byrne AB, Thompson PR. Elife 10 e66694 (2021)
  7. Computational Insight Into the Structural Organization of Full-Length Toll-Like Receptor 4 Dimer in a Model Phospholipid Bilayer. Patra MC, Kwon HK, Batool M, Choi S. Front Immunol 9 489 (2018)
  8. Cyclic nucleotide-induced helical structure activates a TIR immune effector. Hogrel G, Guild A, Graham S, Rickman H, Grüschow S, Bertrand Q, Spagnolo L, White MF. Nature 608 808-812 (2022)
  9. Discovery of a Novel MyD88 Inhibitor M20 and Its Protection Against Sepsis-Mediated Acute Lung Injury. Song J, Chen D, Pan Y, Shi X, Liu Q, Lu X, Xu X, Chen G, Cai Y. Front Pharmacol 12 775117 (2021)
  10. Auto-inhibition and activation of a short Argonaute-associated TIR-APAZ defense system. Guo L, Huang P, Li Z, Shin YC, Yan P, Lu M, Chen M, Xiao Y. Nat Chem Biol (2023)
  11. Discovery of Novel Pterostilbene Derivatives That Might Treat Sepsis by Attenuating Oxidative Stress and Inflammation through Modulation of MAPKs/NF-κB Signaling Pathways. Fang M, Zou T, Yang X, Zhang Z, Cao P, Han J, Duan Y, Ruan BF, Li QS. Antioxidants (Basel) 10 1333 (2021)
  12. Molecular Mechanisms of the Toll-Like Receptor, STING, MAVS, Inflammasome, and Interferon Pathways. Manes NP, Nita-Lazar A. mSystems e0033621 (2021)
  13. Talin1 controls dendritic cell activation by regulating TLR complex assembly and signaling. Lim TJF, Bunjamin M, Ruedl C, Su IH. J Exp Med 217 (2020)
  14. A Bacterial Quorum Sensing Regulated Protease Inhibits Host Immune Responses by Cleaving Death Domains of Innate Immune Adaptors. Duan X, Boo ZZ, Chua SL, Chong KHC, Long Z, Yang R, Zhou Y, Janela B, Chotirmall SH, Ginhoux F, Hu Q, Wu B, Yang L. Adv Sci (Weinh) 10 e2304891 (2023)
  15. A Split-Luciferase Reporter Recognizing GFP and mCherry Tags to Facilitate Studies of Protein-Protein Interactions. Moustaqil M, Bhumkar A, Gonzalez L, Raoul L, Hunter DJB, Carrive P, Sierecki E, Gambin Y. Int J Mol Sci 18 (2017)
  16. Agmatine Alleviates Epileptic Seizures and Hippocampal Neuronal Damage by Inhibiting Gasdermin D-Mediated Pyroptosis. Li X, Lin J, Hua Y, Gong J, Ding S, Du Y, Wang X, Zheng R, Xu H. Front Pharmacol 12 627557 (2021)
  17. Development of a Novel Backbone Cyclic Peptide Inhibitor of the Innate Immune TLR/IL1R Signaling Protein MyD88. Dishon S, Schumacher A, Fanous J, Talhami A, Kassis I, Karussis D, Gilon C, Hoffman A, Nussbaum G. Sci Rep 8 9476 (2018)
  18. Emodin alleviates lung ischemia-reperfusion injury by suppressing gasdermin D-mediated pyroptosis in rats. Jin T, Ai F, Zhou J, Kong L, Xiong Z, Wang D, Lu R, Chen Z, Zhang M. Clin Respir J 17 241-250 (2023)
  19. Insight into Phosphatidylinositol-Dependent Membrane Localization of the Innate Immune Adaptor Protein Toll/Interleukin 1 Receptor Domain-Containing Adaptor Protein. Patra MC, Choi S. Front Immunol 9 75 (2018)
  20. MyD88 Death-Domain Oligomerization Determines Myddosome Architecture: Implications for Toll-like Receptor Signaling. Moncrieffe MC, Bollschweiler D, Li B, Penczek PA, Hopkins L, Bryant CE, Klenerman D, Gay NJ. Structure 28 281-289.e3 (2020)
  21. Pathological mutations differentially affect the self-assembly and polymerisation of the innate immune system signalling adaptor molecule MyD88. O'Carroll A, Chauvin B, Brown JWP, Meagher A, Coyle J, Schill J, Bhumkhar A, Hunter DJB, Ve T, Kobe B, Sierecki E, Gambin Y. BMC Biol. 16 149 (2018)
  22. SARS-CoV-2 proteases PLpro and 3CLpro cleave IRF3 and critical modulators of inflammatory pathways (NLRP12 and TAB1): implications for disease presentation across species. Moustaqil M, Ollivier E, Chiu HP, Van Tol S, Rudolffi-Soto P, Stevens C, Bhumkar A, Hunter DJB, Freiberg AN, Jacques D, Lee B, Sierecki E, Gambin Y. Emerg Microbes Infect 10 178-195 (2021)
  23. Schisandrin B Attenuates Diabetic Cardiomyopathy by Targeting MyD88 and Inhibiting MyD88-Dependent Inflammation. Luo W, Lin K, Hua J, Han J, Zhang Q, Chen L, Khan ZA, Wu G, Wang Y, Liang G. Adv Sci (Weinh) 9 e2202590 (2022)
  24. TMEA, a Polyphenol in Sanguisorba officinalis, Promotes Thrombocytopoiesis by Upregulating PI3K/Akt Signaling. Li H, Jiang X, Shen X, Sun Y, Jiang N, Zeng J, Lin J, Yue L, Lai J, Li Y, Wu A, Wang L, Qin D, Huang F, Mei Q, Yang J, Wu J. Front Cell Dev Biol 9 708331 (2021)
  25. Tailored Modulation of Cellular Pro-inflammatory Responses With Disaccharide Lipid A Mimetics. Heine H, Adanitsch F, Peternelj TT, Haegman M, Kasper C, Ittig S, Beyaert R, Jerala R, Zamyatina A. Front Immunol 12 631797 (2021)
  26. The Single Nucleotide Polymorphism Mal-D96N Mice Provide New Insights into Functionality of Mal in TLR Immune Responses. Dowling JK, Tate MD, Rosli S, Bourke NM, Bitto N, Lauterbach MA, Cheung S, Ve T, Kobe B, Golenbock D, Mansell A. J Immunol 202 2384-2396 (2019)
  27. A novel strategy to block mitotic progression for targeted therapy. Chi JJ, Li H, Zhou Z, Izquierdo-Ferrer J, Xue Y, Wavelet CM, Schiltz GE, Zhang B, Cristofanilli M, Lu X, Bahar I, Wan Y. EBioMedicine 49 40-54 (2019)
  28. Activation mechanism of a short argonaute-TIR prokaryotic immune system. Ni D, Lu X, Stahlberg H, Ekundayo B. Sci Adv 9 eadh9002 (2023)
  29. Comparative characterization of microRNA-71 of Echinococcus granulosus exosomes. Yan L, Li Y, Li R, Liu M, He X, Yang X, Cho WC, Ayaz M, Kandil OM, Yang Y, Song H, Zheng Y. Parasite 30 55 (2023)
  30. Data-Driven Modeling Identifies TIRAP-Independent MyD88 Activation Complex and Myddosome Assembly Strategy in LPS/TLR4 Signaling. Li X, Zhong CQ, Yin Z, Qi H, Xu F, He Q, Shuai J. Int J Mol Sci 21 (2020)
  31. Emodin alleviates myocardial ischemia/reperfusion injury by inhibiting gasdermin D-mediated pyroptosis in cardiomyocytes. Ye B, Chen X, Dai S, Han J, Liang X, Lin S, Cai X, Huang Z, Huang W. Drug Des Devel Ther 13 975-990 (2019)
  32. Exosomes From Adipose-Derived Stem Cells Suppress the Progression of Chronic Endometritis. Wang B, Li L, Yu R. Cell Transplant 32 9636897231173736 (2023)
  33. Extracellular Vesicles-mediated recombinant IL-10 protects against ascending infection-associated preterm birth by reducing fetal inflammatory response. Kammala AK, Mosebarger A, Radnaa E, Rowlinson E, Vora N, Fortunato SJ, Sharma S, Safarzadeh M, Menon R. Front Immunol 14 1196453 (2023)
  34. Flow cytometric reporter assays provide robust functional analysis of signaling complexes. Muusse TW, Lee MYL, Kim H, Parat MO, Nanson JD, Kobe B, Vajjhala PR, Stacey KJ. J Biol Chem 298 102666 (2022)
  35. Frontline Science: Targeting the TLR7 signalosome assembly. Javmen A, Szmacinski H, Lakowicz JR, Toshchakov VY. J Leukoc Biol 108 1697-1706 (2020)
  36. Heterologous Expression and Assembly of Human TLR Signaling Components in Saccharomyces cerevisiae. Coronas-Serna JM, Del Val E, Kagan JC, Molina M, Cid VJ. Biomolecules 11 1737 (2021)
  37. Human and Bacterial Toll-Interleukin Receptor Domains Exhibit Distinct Dynamic Features and Functions. Lee E, Redzic JS, Nemkov T, Saviola AJ, Dzieciatkowska M, Hansen KC, D'Alessandro A, Dinarello C, Eisenmesser EZ. Molecules 27 4494 (2022)
  38. Inflammation conditional genome editing mediated by the CRISPR-Cas9 system. Yuan T, Tang H, Xu X, Shao J, Wu G, Cho YC, Ping Y, Liang G. iScience 26 106872 (2023)
  39. NMR characterization of an assembling RHIM (RIP homotypic interaction motif) amyloid reveals a cryptic region for self-recognition. Pham CLL, Titaux-Delgado GA, Varghese NR, Polonio P, Wilde KL, Sunde M, Mompeán M. J Biol Chem 299 104568 (2023)
  40. Negative Regulation of TLR Signaling by BCAP Requires Dimerization of Its DBB Domain. Lauenstein JU, Scherm MJ, Udgata A, Moncrieffe MC, Fisher DI, Gay NJ. J Immunol 204 2269-2276 (2020)
  41. Nucleic-acid-triggered NADase activation of a short prokaryotic Argonaute. Gao X, Shang K, Zhu K, Wang L, Mu Z, Fu X, Yu X, Qin B, Zhu H, Ding W, Cui S. Nature (2023)
  42. Patchouli Alcohol Modulates the Pregnancy X Receptor/Toll-like Receptor 4/Nuclear Factor Kappa B Axis to Suppress Osteoclastogenesis. Lu Q, Jiang C, Hou J, Qian H, Chu F, Zhang W, Ye M, Chen Z, Liu J, Yao H, Zhang J, Xu J, Wang T, Fan S, Wang Q. Front Pharmacol 12 684976 (2021)
  43. Role of self-organising myddosome oligomers in inflammatory signalling by Toll-like receptors. Gay NJ. BMC Biol. 17 15 (2019)
  44. Small Molecules as Toll-like Receptor 4 Modulators Drug and In-House Computational Repurposing. Pérez-Regidor L, Guzmán-Caldentey J, Oberhauser N, Punzón C, Balogh B, Pedro JR, Falomir E, Nurisso A, Mátyus P, Menéndez JC, de Andrés B, Fresno M, Martín-Santamaría S. Biomedicines 10 2326 (2022)
  45. Structural analysis of the Toll-like receptor 15 TIR domain. Ko KY, Song WS, Park J, Lee GS, Yoon SI. IUCrJ 10 352-362 (2023)
  46. Structural basis of the IL-1 receptor TIR domain-mediated IL-1 signaling. Zhou J, Xiao Y, Ren Y, Ge J, Wang X. iScience 25 104508 (2022)
  47. Structure of a prokaryotic SEFIR domain reveals two novel SEFIR-SEFIR interaction modes. Yang H, Zhu Y, Chen X, Li X, Ye S, Zhang R. J. Struct. Biol. 203 81-89 (2018)
  48. TLR3 forms a laterally aligned multimeric complex along double-stranded RNA for efficient signal transduction. Sakaniwa K, Fujimura A, Shibata T, Shigematsu H, Ekimoto T, Yamamoto M, Ikeguchi M, Miyake K, Ohto U, Shimizu T. Nat Commun 14 164 (2023)
  49. TLR4 signaling and macrophage inflammatory responses are dampened by GIV/Girdin. Swanson L, Katkar GD, Tam J, Pranadinata RF, Chareddy Y, Coates J, Anandachar MS, Castillo V, Olson J, Nizet V, Kufareva I, Das S, Ghosh P. Proc Natl Acad Sci U S A 117 26895-26906 (2020)
  50. TLR5-Derived, TIR-Interacting Decoy Peptides to Inhibit TLR Signaling. Javmen A, Zou J, Nallar SC, Szmacinski H, Lakowicz JR, Gewirtz AT, Toshchakov VY. J Immunol 210 1419-1427 (2023)
  51. Target ssDNA activates the NADase activity of prokaryotic SPARTA immune system. Zhang JT, Wei XY, Cui N, Tian R, Jia N. Nat Chem Biol (2023)
  52. The TLR4/ERK/PD‑L1 axis may contribute to NSCLC initiation. Kang X, Li P, Zhang C, Zhao Y, Hu H, Wen G. Int J Oncol 57 456-465 (2020)
  53. The transmembrane adapter SCIMP recruits tyrosine kinase Syk to phosphorylate Toll-like receptors to mediate selective inflammatory outputs. Liu L, Lucas RM, Nanson JD, Li Y, Whitfield J, Curson JEB, Tuladhar N, Alexandrov K, Mobli M, Sweet MJ, Kobe B, Stow JL, Luo L. J Biol Chem 298 101857 (2022)


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