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Review Articles

Dribbling through the host defence: targeting the TLRs by pathogens

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Pages 354-368 | Received 16 May 2018, Accepted 04 Apr 2019, Published online: 26 Jun 2019

References

  • Abend JR, Ramalingam D, Kieffer-Kwon P, Uldrick TS, Yarchoan R, Ziegelbauer JM. 2012. Kaposi’s sarcoma-associated herpesvirus micrornas target IRAK1 and MYD88, two components of the Toll-like receptor/Interleukin-1R signaling cascade, to reduce inflammatory-cytokine expression. J Virol. 86:11663–11674.
  • Ahmed A, Dolasia K, Mukhopadhyay S. 2018. Mycobacterium tuberculosis PPE18 protein reduces inflammation and increases survival in animal model of sepsis. J Immunol. 200:3587–3598.
  • Andersen-Nissen E, Smith KD, Strobe KL, Barrett SLR, Cookson BT, Logan SM, Aderem A. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA. 102:9247–9252.
  • Arbues A, Malaga W, Constant P, Guilhot C, Prandi J, Astarie-Dequeker C. 2016. Trisaccharides of phenolic glycolipids confer advantages to pathogenic mycobacteria through manipulation of host-cell pattern-recognition receptors. ACS Chem Biol. 11:2865–2875.
  • Barton GM. 2007. Viral recognition by Toll-like receptors. Semin Immunol. 19:33–40.
  • Bhat KH, Ahmed A, Kumar S, Sharma P, Mukhopadhyay S. 2012. Role of PPE18 protein in intracellular survival and pathogenicity of Mycobacterium tuberculosis in mice. PLoS One. 7:e52601.
  • Bhat KH, Chaitanya CK, Parveen N, Varman R, Ghosh S, Mukhopadhyay S. 2012. Proline-proline-glutamic acid (PPE) protein Rv1168c of Mycobacterium tuberculosis augments transcription from HIV-1 long terminal repeat promoter. J Biol Chem. 287:16930–16946.
  • Blanc L, Gilleron M, Prandi J, Song OR, Jang MS, Gicquel B, Drocourt D, Neyrolles O, Brodin P, Tiraby G, et al. 2017. Mycobacterium tuberculosis inhibits human innate immune responses via the production of TLR2 antagonist glycolipids. Proc Natl Acad Sci USA. 114:11205–11210.
  • Blander JM. 2008. Phagocytosis and antigen presentation: a partnership initiated by Toll-like receptors. Ann Rheum Dis. 67:iii44–iii49.
  • Blohmke CJ, Victor RE, Hirschfeld AF, Elias IM, Hancock DG, Lane CR, Davidson AGF, Wilcox PG, Smith KD, Overhage J. 2008. Innate immunity mediated by TLR5 as a novel antiinflammatory target for cystic fibrosis lung disease. J Immunol. 180:7764–7773.
  • Boneca IG, Dussurget O, Cabanes D, Nahori MA, Sousa S, Lecuit M, Psylinakis E, Bouriotis V, Hugot JP, Giovannini M, et al. 2007. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci USA. 104:997–1002.
  • Bowie, A, Kiss-Toth, E, Symons, J A, Smith, G L, Dower, S K, O'Neill, L A. 2000. A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc Natl Acad Sci U S A.97:10162–10167. 10920188 10.1073/pnas.160027697.
  • Bowie AG, Unterholzner L. 2008. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol. 8:911–922.
  • Buchta CM, Bishop GA. 2014. Toll-like receptors and B cells: functions and mechanisms. Immunol Res. 59:12–22.
  • Capolunghi F, Rosado MM, Cascioli S, Girolami E, Bordasco S, Vivarelli M, Ruggiero B, Cortis E, Insalaco A, Fanto N, et al. 2010. Pharmacological inhibition of TLR9 activation blocks autoantibody production in human B cells from SLE patients. Rheumatology. 49:2281–2289.
  • Chai LYA, Vonk AG, Kullberg BJ, Verweij PE, Verschueren I, van der Meer JWM, Joosten LAB, Latgé JP, Netea MG. 2011. Aspergillus fumigatus cell wall components differentially modulate host TLR2 and TLR4 responses. Microbes Infect. 13:151–159.
  • Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, Togarsimalemath SK, Chandra N, Mishra S, Ajitkumar P, Joshi B, et al. 2010. The multifunctional PE_PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J Biol Chem. 285:30389–30403.
  • Chen Y, Chen J, Wang H, Shi J, Wu K, Liu S, Liu Y, Wu J. 2013. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 9:e1003248.
  • Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, et al. 2008. Subversion of Toll-like receptor signaling by a unique family of bacterial toll/interleukin-1 receptor domain–containing proteins. Nat Med. 14:399–406.
  • Clark IA. 1978. Does endotoxin cause both the disease and parasite death in acute malaria and babesiosis? Lancet. 2:75–77.
  • Conze DB, Wu CJ, Thomas JA, Landstrom A, Ashwell JD. 2008. Lys63-linked polyubiquitination of IRAK-1 is required for interleukin-1 receptor- and Toll-like receptor-mediated NF-kappaB activation. Mol Cell Biol. 28:3538–3547.
  • Das K, Garnica O, Dhandayuthapani S. 2016. Modulation of host miRNAs by intracellular bacterial pathogens. Front Cell Infect Microbiol. 6:79.
  • Delneste Y, Beauvillain C, Jeannin P. 2007. Innate immunity: structure and function of TLRs. Med Sci (Paris). 23:67–73.
  • De Nardo D. 2015. Toll-like receptors: activation, signalling and transcriptional modulation. Cytokine. 74:181–189.
  • Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, Bebien M, Lawrence T, van Rijt LS, Lambrecht BN, Sirard JC, et al. 2008. Sustained desensitization to bacterial Toll-like receptor ligands after resolutionof respiratory influenza infection. J Exp Med. 205:323–329.
  • Dolasia K, Bisht MK, Pradhan G, Udgata A, Mukhopadhyay S. 2018. TLRs/NLRs: shaping the landscape of host immunity. Int Rev Immunol. 37:3–19.
  • Dominguez-Villar M, Gautron A-S, de Marcken M, Keller MJ, Hafler DA. 2015. TLR7 induces anergy in human CD4(+) T cells. Nat Immunol. 16:118–128.
  • Fathallah I, Parroche P, Gruffat H, Zannetti C, Johansson H, Yue J, Manet E, Tommasino M, Sylla BS, Hasan UA. 2010. EBV latent membrane protein 1 is a negative regulator of TLR9. J Immunol. 185:6439–6447.
  • Fidock MD, Souberbielle BE, Laxton C, Rawal J, Delpuech-Adams O, Corey TP, Colman P, Kumar V, Cheng JB, Wright K, et al. 2011. The innate immune response, clinical outcomes, and ex vivo HCV antiviral efficacy of a TLR7 agonist (PF-4878691). Clin Pharmacol Ther. 89:821–829.
  • Flannery S, Bowie AG. 2010. The interleukin-1 receptor-associated kinases: critical regulators of innate immune signalling. Biochem Pharmacol. 80:1981–1991.
  • Franklin BS, Ishizaka ST, Lamphier M, Gusovsky F, Hansen H, Rose J, Zheng W, Ataíde MA, de Oliveira RB, Golenbock DT, et al. 2011. Therapeutical targeting of nucleic acid-sensing Toll-like receptors prevents experimental cerebral malaria. Proc Natl Acad Sci USA. 108:3689–3694.
  • Gibson DL, Ma C, Bergstrom KSB, Huang JT, Man C, Vallance BA. 2008. MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell Microbiol. 10:618–631.
  • Gunzer M, Riemann H, Basoglu Y, Hillmer A, Weishaupt C, Balkow S, Benninghoff B, Ernst B, Steinert M, Scholzen T, et al. 2005. Systemic administration of a TLR7 ligand leads to transient immune incompetence due to peripheral-blood leukocyte depletion. Blood. 106:2424–2432.
  • Gupta P, Giri J, Srivastav S, Chande AG, Mukhopadhyaya R, Das PK, Ukil A. 2014. Leishmania donovani targets tumor necrosis factor receptor-associated factor (TRAF) 3 for impairing TLR4-mediated host response. Faseb J. 28:1756–1768.
  • Harding CV, Boom WH. 2010. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol. 8:296–307.
  • Hernandez JC, Arteaga J, Paul S, Kumar A, Latz E, Urcuqui-Inchima S. 2011. Up-regulation of TLR2 and TLR4 in dendritic cells in response to HIV type 1 and coinfection with opportunistic pathogens. AIDS Res Hum Retroviruses. 27:1099–1109.
  • Hisaeda H, Tetsutani K, Imai T, Moriya C, Tu L, Hamano S, Duan X, Chou B, Ishida H, Aramaki A, et al. 2008. Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J Immunol. 180:2496–2503.
  • Hornef MW, Wick MJ, Rhen M, Normark S. 2002. Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol. 3:1033–1040.
  • Hussain Bhat K, Mukhopadhyay S. 2015. Macrophage takeover and the host-bacilli interplay during tuberculosis. Future Microbiol. 10:853–872.
  • Into T, Inomata M, Takayama E, Takigawa T. 2012. Autophagy in regulation of Toll-like receptor signaling. Cell Signal. 24:1150–1162.
  • Jin B, Sun T, Yu XH, Yang YX, Yeo A. 2012. The effects of TLR activation on T-cell development and differentiation. Clin Dev Immunol. 2012:836485.
  • Kasperkovitz PV, Khan NS, Tam JM, Mansour MK, Davids PJ, Vyas JM. 2011. Toll-like receptor 9 modulates macrophage antifungal effector function during innate recognition of Candida albicans and Saccharomyces cerevisiae. Infect Immun. 79:4858–4867.
  • Kawai T, Akira S. 2007. Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med. 13:460–469.
  • Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, Yamamoto M, Terai K, Matsuda M, Inoue J, Uematsu S, et al. 2004. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol. 5:1061–1068.
  • Keating SE, Maloney GM, Moran EM, Bowie AG. 2007. IRAK-2 participates in multiple Toll-like receptor signaling pathways to NFkappaB via activation of TRAF6 ubiquitination. J Biol Chem. 282:33435–33443.
  • Koeppen K, Hampton TH, Jarek M, Scharfe M, Gerber SA, Mielcarz DW, Demers EG, Dolben EL, Hammond JH, Hogan DA, et al. 2016. A novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog. 12:e1005672.
  • Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. 1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 86:973–983.
  • Le Negrate G. 2012. Viral interference with innate immunity by preventing NF-κB activity. Cell Microbiol. 14:168–181.
  • Lin SC, Lo YC, Wu H. 2010. Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature. 465:885–890.
  • Matsunaga N, Tsuchimori N, Matsumoto T, Ii M. 2011. TAK-242 (Resatorvid), a small-molecule inhibitor of toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol. 79:34–41.
  • McMahon-Pratt D, Alexander J. 2004. Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol Rev. 201:206–224.
  • Medzhitov R. 2009. Approaching the asymptote: 20 years later. Immunity. 30:766–775.
  • Motshwene PG, Moncrieffe MC, Grossmann JG, Kao C, Ayaluru M, Sandercock AM, Robinson CV, Latz E, Gay NJ. 2009. An oligomeric signaling platform formed by the Toll-like receptor signal transducers MyD88 and IRAK-4. J Biol Chem. 284:25404–25411.
  • Murphy TF, Parameswaran GI. 2009. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis. 49:124–131.
  • Nair S, Pandey AD, Mukhopadhyay S. 2011. The PPE18 protein of Mycobacterium tuberculosis inhibits NF-κB/rel-mediated proinflammatory cytokine production by upregulating and phosphorylating suppressor of cytokine signaling 3 protein. J Immunol. 186:5413–5424.
  • Nair S, Ramaswamy PA, Ghosh S, Joshi DC, Pathak N, Siddiqui I, Sharma P, Hasnain SE, Mande SC, Mukhopadhyay S. 2009. The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage. J Immunol. 183:6269–6281.
  • Netea MG, Van der Meer JWM, Kullberg BJ. 2006. Role of the dual interaction of fungal pathogens with pattern recognition receptors in the activation and modulation of host defence. Clin Microbiol Infect. 12:404–409.
  • Neves P, Lampropoulou V, Calderon-Gomez E, Roch T, Stervbo U, Shen P, Kühl AA, Loddenkemper C, Haury M, Nedospasov SA, et al. 2010. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium Infection. Immunity. 33:777–790.
  • Ngo VN, Young RM, Schmitz R, Jhavar S, Xiao W, Lim KH, Kohlhammer H, Xu W, Yang Y, Zhao H, et al. 2011. Oncogenically active MYD88 mutations in human lymphoma. Nature. 470:115–119.
  • Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol. 167:910–918.
  • Nothelfer K, Arena ET, Pinaud L, Neunlist M, Mozeleski B, Belotserkovsky I, Parsot C, Dinadayala P, Burger-Kentischer A, Raqib R, et al. 2014. B lymphocytes undergo TLR2-dependent apoptosis upon Shigella infection. J Exp Med. 211:1215–1229.
  • Nothelfer K, Sansonetti PJ, Phalipon A. 2015. Pathogen manipulation of B cells: the best defence is a good offence. Nat Rev Microbiol. 13:173–184.
  • 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.
  • Ordureau A, Smith H, Windheim M, Peggie M, Carrick E, Morrice N, Cohen P. 2008. The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys 63 -linked polyubiquitination of IRAK1. Biochem J. 409:43–52.
  • Panda SK, Kumar S, Tupperwar NC, Vaidya T, George A, Rath S, Bal V, Ravindran B. 2012. Chitohexaose activates macrophages by alternate pathway through TLR4 and blocks endotoxemia. PLoS Pathog. 8:e1002717.
  • Parveen N, Varman R, Nair S, Das G, Ghosh S, Mukhopadhyay S. 2013. Endocytosis of Mycobacterium tuberculosis heat shock protein 60 is required to induce interleukin-10 production in macrophages. J Biol Chem. 288:24956–24971.
  • Pathak SK, Basu S, Basu KK, Banerjee A, Pathak S, Bhattacharyya A, Kaisho T, Kundu M, Basu J. 2007. Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol. 8:610–618.
  • Perez-Lopez A, Behnsen J, Nuccio SP, Raffatellu M. 2016. Mucosal immunity to pathogenic intestinal bacteria. Nat Rev Immunol. 16:135–148.
  • Pietras EM, Saha SK, Cheng G. 2006. The interferon response to bacterial and viral infections. J Endotoxin Res. 12:246–250.
  • Radhakrishnan GK, Yu Q, Harms JS, Splitter GA. 2009. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem. 284:9892–9898.
  • Reuven EM, Ali M, Rotem E, Schwarzer R, Schwarzter R, Gramatica A, Futerman AH, Shai Y. 2014. The HIV-1 envelope transmembrane domain binds TLR2 through a distinct dimerization motif and inhibits TLR2-mediated responses. PLoS Pathog. 10:e1004248.
  • Romero CD, Varma TK, Hobbs JB, Reyes A, Driver B, Sherwood ER. 2011. The Toll-like receptor 4 agonist monophosphoryl lipid a augments innate host resistance to systemic bacterial infection. Infect Immun. 79:3576–3587.
  • Savva A, Roger T. 2013. Targeting Toll-like receptors: promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front Immunol. 4:387.
  • Sengupta D, Koblansky A, Gaines J, Brown T, West AP, Zhang D, Nishikawa T, Park SG, Roop RM, 2nd, Ghosh S. 2010. Subversion of innate immune responses by Brucella through the targeted degradation of the TLR signaling adapter, MAL. J Immunol. 184:956–964.
  • Shweash M, Adrienne McGachy H, Schroeder J, Neamatallah T, Bryant CE, Millington O, Mottram JC, Alexander J, Plevin R. 2011. Leishmania mexicana promastigotes inhibit macrophage IL-12 production via TLR-4 dependent COX-2, iNOS and arginase-1 expression. Mol Immunol. 48:1800–1808.
  • Sing A, Rost D, Tvardovskaia N, Roggenkamp A, Wiedemann A, Kirschning CJ, Aepfelbacher M, Heesemann J. 2002. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J Exp Med. 196:1017–1024.
  • Spear AM, Loman NJ, Atkins HS, Pallen MJ. 2009. Microbial TIR domains: not necessarily agents of subversion? Trends Microbiol. 17:393–398.
  • Srivastav S, Kar S, Chande AG, Mukhopadhyaya R, Das PK. 2012. Leishmania donovani exploits host deubiquitinating enzyme A20, a negative regulator of TLR Signaling, to subvert host immune response. J Immunol. 189:924–934.
  • Stahl M, Ries J, Vermeulen J, Yang H, Sham HP, Crowley SM, Badayeva Y, Turvey SE, Gaynor EC, Li X, et al. 2014. A novel mouse model of Campylobacter jejuni gastroenteritis reveals key pro-inflammatory and tissue protective roles for Toll-like Receptor signaling during infection. PLoS Pathog. 10:e1004264.
  • Sweet CR, Conlon J, Golenbock DT, Goguen J, Silverman N. 2007. YopJ targets TRAF proteins to inhibit TLR-mediated NF-kappaB, MAPK and IRF3 signal transduction. Cell Microbiol. 9:2700–2715.
  • Tanaka A, Nakamura S, Seki M, Fukudome K, Iwanaga N, Imamura Y, Miyazaki T, Izumikawa K, Kakeya H, Yanagihara K, et al. 2013. Toll-like receptor 4 agonistic antibody promotes innate immunity against severe pneumonia induced by coinfection with influenza virus and Streptococcus pneumoniae. Clin Vaccine Immunol. 20:977–985.
  • Uchiyama S, Andreoni F, Schuepbach RA, Nizet V, Zinkernagel AS. 2012. DNase Sda1 allows invasive M1T1 Group A Streptococcus to prevent TLR9-dependent recognition. PLoS Pathog. 8:e1002736.
  • Udgata A, Qureshi R, Mukhopadhyay S. 2016. Transduction of functionally contrasting signals by two Mycobacterial PPE proteins downstream of TLR2 Receptors. J Immunol. 197:1776–1787.
  • Valverde-Villegas JM, Dos Santos BP, de Medeiros RM, Mattevi VS, Lazzaretti RK, Sprinz E, Kuhmmer R, Chies JA. 2017. Endosomal toll-like receptor gene polymorphisms and susceptibility to HIV and HCV co-infection – Differential influence in individuals with distinct ethnic background. Hum Immunol. 78:221–226.
  • van der Kleij D, Latz E, Brouwers JFHM, Kruize YCM, Schmitz M, Kurt-Jones EA, Espevik T, de Jong EC, Kapsenberg ML, Golenbock DT, et al. 2002. A novel host-parasite lipid cross-talk: Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J Biol Chem. 277:48122–48129.
  • van Gent M, Braem SGE, de Jong A, Delagic N, Peeters JGC, Boer IGJ, Moynagh PN, Kremmer E, Wiertz EJ, Ovaa H, et al. 2014. Epstein–Barr virus large tegument protein BPLF1 contributes to innate immune evasion through interference with Toll-like receptor signaling. PLoS Pathog. 10:e1003960.
  • Vincent IE, Zannetti C, Lucifora J, Norder H, Protzer U, Hainaut P, Zoulim F, Tommasino M, Trépo C, Hasan U, et al. 2011. Hepatitis B virus impairs TLR9 expression and function in plasmacytoid dendritic cells. PLoS One. 6:e26315.
  • Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. 2004. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med. 10:1366–1373.
  • Weck MM, Grünebach F, Werth D, Sinzger C, Bringmann A, Brossart P. 2007. TLR ligands differentially affect uptake and presentation of cellular antigens. Blood. 109:3890–3894.
  • Wong YN, Rossignol D, Rose JR, Kao R, Carter A, Lynn M. 2003. Safety, pharmacokinetics, and pharmacodynamics of E5564, a lipid A antagonist, during an ascending single-dose clinical study . J Clin Pharmacol. 43:735–742.
  • Xu H, Sobue T, Thompson A, Xie Z, Poon K, Ricker A, Cervantes J, Diaz PI, Dongari-Bagtzoglou A. 2014. Streptococcal co-infection augments Candida pathogenicity by amplifying the mucosal inflammatory response. Cell Microbiol. 16:214–231.
  • Yamaguchi M, Kitagawa Y, Zhou M, Itoh M, Gotoh B. 2014. An anti-interferon activity shared by paramyxovirus C proteins: inhibition of Toll-like receptor 7/9-dependent alpha interferon induction. FEBS Lett. 588:28–34.
  • Yamamoto H, Abe Y, Miyazato A, Tanno D, Tanaka M, Miyasaka T, Ishii K, Kawakami K. 2011. Cryptococcus neoformans suppresses the activation of bone marrow–derived dendritic cells stimulated with its own DNA, but not with DNA from other fungi. FEMS Immunol Med Microbiol. 63:363–372.
  • Yan D, Wang X, Luo L, Cao X, Ge B. 2012. Inhibition of TLR signaling by a bacterial protein containing immunoreceptor tyrosine-based inhibitory motifs. Nat Immunol. 13:1063–1071.
  • Yokoyama R, Itoh S, Kamoshida G, Takii T, Fujii S, Tsuji T, Onozaki K. 2012. Staphylococcal superantigen-like protein 3 binds to the Toll-like receptor 2 extracellular domain and inhibits cytokine production induced by Staphylococcus aureus, cell wall component, or lipopeptides in murine macrophages. Infect Immun. 80:2816–2825.

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