Toll-like receptors' pathway disturbances are associated with increased susceptibility to infections in humans

Archivum Immunologiae et Therapiae Experimentalis

Volumn 61, Issue 6, 2013, Pages 427-443

  Frazão, Josias Brito ^a   Errante, Paolo Ruggero ^a   Condino Neto, Antonio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Immunodeficiencies; IRAK 4; NF kappaB; Recurrent infections; Toll like receptors

Indexed keywords

DOUBLE STRANDED RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 2; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 11; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; B LYMPHOCYTE; BORRELIA INFECTION; CANDIDA ALBICANS; CANDIDIASIS; CELL MEMBRANE; CHICKENPOX; CROHN DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; DROSOPHILA MELANOGASTER; ECTODERMAL DYSPLASIA; ENDOSOME; GENETIC DISORDER; HERPES SIMPLEX ENCEPHALITIS; HOST RESISTANCE; HUMAN; IMMUNE DEFICIENCY; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; LEPROSY; LYME DISEASE; MOLLUSCUM CONTAGIOSUM; MONONUCLEAR CELL; MYCOSIS; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; SYPHILIS; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; VACCINIA; VARICELLA ZOSTER VIRUS; VERRUCA VULGARIS; VIRAL CLEARANCE; VIRUS INFECTION; YERSINIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CYTOKINES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFECTION; INFLAMMATION MEDIATORS; MUTATION; POLYMORPHISM, GENETIC; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84890435435     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-013-0243-0     Document Type: Review

References (182)

1. Abad C, Gonzalez-Escribano MF et al (2011) Association of Toll-like receptor 10 and susceptibility to Crohn's disease independent of NOD2. Genes Immun 12:635-642
2. Adachi O, Kawai T et al (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143-150
3. Akira S, Hemmi H (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 85:85-95
4. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499-511
5. Akira S, Uematsu S et al (2006) Pathogen recognition and innate immunity. Cell 124:783-801
6. Baeuerle PA, Henkel T (1994) Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12:141-179
7. Barchet W, Cella M et al (2005) Plasmacytoid dendritic cells-virus experts of innate immunity. Semin Immunol 17:253-261
8. Beutler B (2004) Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430:257-263
9. Bochud PY, Magaret AS et al (2007) Polymorphisms in TLR2 are associated with increased viral shedding and lesional rate in patients with genital herpes simplex virus Type 2 infection. J Infect Dis 196:505-509
10. Botto M, Kirschfink M et al (2009) Complement in human diseases: lessons from complement deficiencies. Mol Immunol 46:2774-2783
11. Bousfiha A, Picard C et al (2010) Primary immunodeficiencies of protective immunity to primary infections. Clin Immunol 135:204-209
12. Bradley LA, Sweatman AK et al (1994) Mutation detection in the X-linked agammaglobulinemia gene, BTK, using single strand conformation polymorphism analysis. Hum Mol Genet 3:79-83
13. Bsibsi M, Ravid R et al (2002) Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61:1013-1021
14. Bsibsi M, Persoon-Deen C et al (2006) Toll-like receptor 3 on adult human astrocytes triggers production of neuroprotective mediators. Glia 53:688-695
15. Bunk S, Sigel S et al (2010) Internalization and coreceptor expression are critical for TLR2-mediated recognition of lipoteichoic acid in human peripheral blood. J Immunol 185:3708-3717
16. Buwitt-Beckmann U, Heine H et al (2005) Lipopeptide structure determines TLR2 dependent cell activation level. FEBS J 272:6354-6364
17. Cai Z, Pang Y et al (2003) Differential roles of tumor necrosis factor-alpha and interleukin-1 beta in lipopolysaccharide-induced brain injury in the neonatal rat. Brain Res 975:37-47
18. Cardenes M, von Bernuth H et al (2006) Autosomal recessive interleukin-1 receptor-associated kinase 4 deficiency in fourth-degree relatives. J Pediatr 148:549-551
19. Carpentier PA, Begolka WS et al (2005) Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49:360-374
20. Carpentier PA, Duncan DS et al (2008) Glial Toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav Immun 22:140-147
21. Casrouge A, Zhang SY et al (2006) Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314:308-312
22. Chao CC, Hu S et al (1992) Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149:2736-2741
23. Chapel H, Geha R et al (2003) Primary immunodeficiency diseases: an update. Clin Exp Immunol 132:9-15
24. Chapel H, Puel A et al (2005) Shigella sonnei meningitis due to interleukin-1 receptor-associated kinase-4 deficiency: first association with a primary immune deficiency. Clin Infect Dis 40:1227-1231
25. Chapgier A, Kong XF et al (2009) A partial form of recessive STAT1 deficiency in humans. J Clin Invest 119:1502-1514
26. Chin AC, Fournier B et al (2009) CD47 and TLR-2 cross-talk regulates neutrophil transmigration. J Immunol 183:5957-5963
27. Chuang TH, Ulevitch RJ (2000) Cloning and characterization of a sub-family of human Toll-like receptors: hTLR7, hTLR8 and hTLR9. Eur Cytokine Netw 11:372-378
28. Chuang T, Ulevitch RJ (2001) Identification of hTLR10: a novel human Toll-like receptor preferentially expressed in immune cells. Biochim Biophys Acta 1518:157-161
29. Chung J, Gao AG et al (1997) Thrombospondin acts via integrin-associated protein to activate the platelet integrin alphaIIbbeta3. J Biol Chem 272:14740-14746
30. Clemente A, Pons J et al (2011) B cells from common variable immunodeficiency patients fail to differentiate to antibody secreting cells in response to TLR9 ligand (CpG-ODN) or anti-CD40+IL21. Cell Immunol 268:9-15
31. Comeau JL, Lin TJ et al (2008) Staphylococcal pericarditis, and liver and paratracheal abscesses as presentations in two new cases of interleukin-1 receptor associated kinase 4 deficiency. Pediatr Infect Dis J 27:170-174
32. Costa-Carvalho BT, Nudelman V et al (1998) Immune system and infections. J Pediatr 74(Suppl 1):S3-S11
33. Cunningham-Rundles C, Bodian C (1999) Common variable immunodeficiency: clinical and immunological features of 248 patients. Clin Immunol 92:34-48
34. Cunningham-Rundles C, Radigan L et al (2006) TLR9 activation is defective in common variable immune deficiency. J Immunol 176:1978-1987
35. Dasari P, Nicholson IC et al (2005) Expression of Toll-like receptors on B lymphocytes. Cell Immunol 236:140-145
36. Davidson DJ, Currie AJ et al (2006) IRAK-4 mutation (Q293X): rapid detection and characterization of defective post-transcriptional TLR/IL-1R responses in human myeloid and non-myeloid cells. J Immunol 177:8202-8211
37. De Tiege X, Rozenberg F et al (2008) The spectrum of herpes simplex encephalitis in children. Eur J Paediatr Neurol 12:72-81
38. Deering RP, Orange JS (2006) Development of a clinical assay to evaluate Toll-like receptor function. Clin Vaccine Immunol 13:68-76
39. Deininger S, Stadelmaier A et al (2003) Definition of structural prerequisites for lipoteichoic acid-inducible cytokine induction by synthetic derivatives. J Immunol 170:4134-4138
40. Demeure CE, Tanaka H et al (2000) CD47 engagement inhibits cytokine production and maturation of human dendritic cells. J Immunol 164:2193-2199
41. Dorahy DJ, Thorne RF et al (1997) Stimulation of platelet activation and aggregation by a carboxyl-terminal peptide from thrombospondin binding to the integrin-associated protein receptor. J Biol Chem 272:1323-1330
42. Doyle SL, O'Neill LA (2006) Toll-like receptors: from the discovery of NFkappaB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 72:1102-1113
43. Doyle SL, Jefferies CA et al (2005) Bruton's tyrosine kinase is involved in p65-mediated transactivation and phosphorylation of p65 on serine 536 during NFkappaB activation by lipopolysaccharide. J Biol Chem 280:23496-23501
44. Doyle SL, Jefferies CA et al (2007) Signaling by Toll-like receptors 8 and 9 requires Bruton's tyrosine kinase. J Biol Chem 282:36953-36960
45. Dupuis S, Jouanguy E et al (2003) Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat Genet 33:388-391
46. Dziarski R, Gupta D (2005) Staphylococcus aureus peptidoglycan is a Toll-like receptor 2 activator: a reevaluation. Infect Immun 73:5212-5216
47. Dziarski R, Gupta D (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biol 7:232
48. Ear T, McDonald PP (2008) Cytokine generation, promoter activation, and oxidant-independent NF-kappaB activation in a transfectable human neutrophilic cellular model. BMC Immunol 9:14
49. Enoch T, Zinn K et al (1986) Activation of the human beta-interferon gene requires an interferon-inducible factor. Mol Cell Biol 6:801-810
50. Escobar D, Pons J et al (2010) Defective B cell response to TLR9 ligand (CpG-ODN), Streptococcus pneumoniae and Haemophilus influenzae extracts in common variable immunodeficiency patients. Cell Immunol 262:105-111
51. Ezekowitz RA, Sastry K et al (1990) Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J Exp Med 172:1785-1794
52. Farina C, Krumbholz M et al (2005) Preferential expression and function of Toll-like receptor 3 in human astrocytes. J Neuroimmunol 159:12-19
53. Fitzgerald KA, McWhirter SM et al (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491-496
54. Galli SJ, Borregaard N et al (2011) Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol 12:1035-1044
55. Gewirtz AT, Vijay-Kumar M et al (2006) Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease. Am J Physiol Gastrointest Liver Physiol 290:G1157-G1163
56. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23-35
57. Guirado M, Gil H et al (2012) Association between C13ORF31, NOD2, RIPK2 and TLR10 polymorphisms and urothelial bladder cancer. Hum Immunol 73:668-672
58. Guo Y, Audry M et al (2011) Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity. J Exp Med 208:2083-2098
59. Hammarstrom L, Vorechovsky I et al (2000) Selective IgA deficiency (SIgAD) and common variable immunodeficiency (CVID). Clin Exp Immunol 120:225-231
60. Han X, Sterling H et al (2000) CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J Biol Chem 275:37984-37992
61. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394
62. Hansson GK, Edfeldt K (2005) Toll to be paid at the gateway to the vessel wall. Arterioscler Thromb Vasc Biol 25:1085-1087
63. Harte M, Haga IR et al (2003) The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J Exp Med 197:343-351
64. Hasan U, Chaffois C et al (2005) Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88. J Immunol 174:2942-2950
65. Hashimoto S, Tsukada S et al (1996) Identification of Bruton's tyrosine kinase (Btk) gene mutations and characterization of the derived proteins in 35 X-linked agammaglobulinemia families: a nationwide study of Btk deficiency in Japan. Blood 88:561-573
66. Hashimoto M, Tawaratsumida K et al (2006a) Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. Int Immunol 18:355-362
67. Hashimoto M, Tawaratsumida K et al (2006b) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J Immunol 177:3162-3169
68. Hashimoto M, Furuyashiki M et al (2007) Evidence of immunostimulating lipoprotein existing in the natural lipoteichoic acid fraction. Infect Immun 75:1926-1932
69. Hawn TR, Wu H et al (2005) A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus. Proc Natl Acad Sci USA 102:10593-10597
70. Hayashi F, Smith KD et al (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103
71. Herman M, Ciancanelli M et al (2012) Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J Exp Med 209:1567-1582
72. Hermaszewski RA, Webster AD (1993) Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications. Q J Med 86:31-42
73. Hickey MJ, Kubes P (2009) Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol 9:364-375
74. Hochrein H, Schlatter B et al (2004) Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc Natl Acad Sci USA 101:11416-11421
75. Hoebe K, Georgel P et al (2005) CD36 is a sensor of diacylglycerides. Nature 433:523-527
76. Hornung V, Rothenfusser S et al (2002) Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 168:4531-4537
77. Ip WK, Takahashi K et al (2008) Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 205:169-181
78. Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327:291-295
79. Jack CS, Arbour N et al (2005) TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175:4320-4330
80. Janeway CA Jr (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 13:11-16
81. Jefferies CA, Doyle S et al (2003) Bruton's tyrosine kinase is a Toll/interleukin-1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J Biol Chem 278:26258-26264
82. Jimenez-Dalmaroni MJ, Xiao N et al (2009) Soluble CD36 ectodomain binds negatively charged diacylglycerol ligands and acts as a co-receptor for TLR2. PLoS ONE 4:e7411
83. Jin MS, Kim SE et al (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130:1071-1082
84. Jouault T, Ibata-Ombetta S et al (2003) Candida albicans phospholipomannan is sensed through Toll-like receptors. J Infect Dis 188:165-172
85. Kang JY, Nan X et al (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31:873-884
86. Kawai T, Akira S (2007) Antiviral signaling through pattern recognition receptors. J Biochem 141:137-145
87. Khazen W, M'Bika JP et al (2005) Expression of macrophage-selective markers in human and rodent adipocytes. FEBS Lett 579:5631-5634
88. Kopp E, Medzhitov R (2003) Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 15:396-401
89. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318
90. Krombach F, Munzing S et al (1997) Cell size of alveolar macrophages: an interspecies comparison. Environ Health Perspect 105(Suppl 5):1261-1263
91. Krutzik SR, Ochoa MT et al (2003) Activation and regulation of Toll-like receptors 2 and 1 in human leprosy. Nat Med 9:525-532
92. Ku CL, von Bernuth H et al (2007) Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity. J Exp Med 204:2407-2422
93. Ku JK, Kwon HJ et al (2008) Expression of Toll-like receptors in verruca and molluscum contagiosum. J Korean Med Sci 23:307-314
94. Kuhns DB, Long Priel DA et al (1997) Endotoxin and IL-1 hyporesponsiveness in a patient with recurrent bacterial infections. J Immunol 158:3959-3964
95. Lafaille FG, Pessach IM et al (2012) Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 491:769-773
96. Laflamme N, Rivest S (2001) Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating Gram-negative bacterial cell wall components. FASEB J 15:155-163
97. Lai Y, Gallo RL (2008) Toll-like receptors in skin infections and inflammatory diseases. Infect Disord Drug Targets 8:144-155
98. Lehnardt S, Lachance C et al (2002) The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22:2478-2486
99. Lemaitre B, Nicolas E et al (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983
100. Lenardo MJ, Fan CM et al (1989) The involvement of NF-kappa B in beta-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell 57:287-294
101. Li Q, Cherayil BJ (2004) Toll-like receptor 4 mutation impairs the macrophage TNFalpha response to peptidoglycan. Biochem Biophys Res Commun 325:91-96
102. Lindberg FP, Bullard DC et al (1996) Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274:795-798
103. Liu Y, Merlin D et al (2001) The role of CD47 in neutrophil transmigration. Increased rate of migration correlates with increased cell surface expression of CD47. J Biol Chem 276:40156-40166
104. Lokensgard JR, Gekker G et al (1997) Proinflammatory cytokines inhibit HIV-1(SF162) expression in acutely infected human brain cell cultures. J Immunol 158:2449-2455
105. Maguire O, Collins C et al (2011) Quantifying nuclear p65 as a parameter for NF-kappaB activation: correlation between ImageStream cytometry, microscopy, and Western blot. Cytometry A 79:461-469
106. McKimmie CS, Fazakerley JK (2005) In response to pathogens, glial cells dynamically and differentially regulate Toll-like receptor gene expression. J Neuroimmunol 169:116-125
107. Medvedev AE, Lentschat A et al (2003) Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections. J Exp Med 198:521-531
108. Mempel M, Kalali BN et al (2007) Toll-like receptors in dermatology. Dermatol Clin 25:531-540, viii
109. Mizel SB, Honko AN et al (2003) Induction of macrophage nitric oxide production by Gram-negative flagellin involves signaling via heteromeric Toll-like receptor 5/Toll-like receptor 4 complexes. J Immunol 170:6217-6223
110. Moore ML, McKissic EL et al (2004) Fatal disseminated mouse adenovirus type 1 infection in mice lacking B cells or Bruton's tyrosine kinase. J Virol 78:5584-5590
111. Morath S, Geyer A et al (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J Exp Med 193:393-397
112. Morath S, Stadelmaier A et al (2002) Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 195:1635-1640
113. Moreira J, Aragao-Filho WC et al (2012) Human leucocytes response to viable, extended freeze-drying or heat-killed Mycobacterium bovis bacillus Calmette-Guerin. Scand J Immunol 75:96-101
114. Morgan AR, Lam WJ et al (2012) Genetic variation within TLR10 is associated with Crohn's disease in a New Zealand population. Hum Immunol 73:416-420
115. Mulla MJ, Myrtolli K et al (2013) Cutting-edge report: TLR10 plays a role in mediating bacterial peptidoglycan-induced trophoblast apoptosis. Am J Reprod Immunol 69:449-453
116. Murray PJ, Wynn TA (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11:723-737
117. Netea MG, van der Graaf C et al (2004) Toll-like receptors and the host defense against microbial pathogens: bringing specificity to the innate-immune system. J Leukoc Biol 75:749-755
118. Netea MG, Gow NA et al (2006) Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 116:1642-1650
119. Oliveira RB, Ochoa MT et al (2003) Expression of Toll-like receptor 2 on human Schwann cells: a mechanism of nerve damage in leprosy. Infect Immun 71:1427-1433
120. O'Neill LA (2008) When signaling pathways collide: positive and negative regulation of Toll-like receptor signal transduction. Immunity 29:12-20
121. O'Neill LA, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353-364
122. O'Neill LA, Dinarello CA (2000) The IL-1 receptor/Toll-like receptor superfamily: crucial receptors for inflammation and host defense. Immunol Today 21:206-209
123. Oosting M, Ter Hofstede H et al (2011) TLR1/TLR2 heterodimers play an important role in the recognition of Borrelia spirochetes. PLoS ONE 6:e25998
124. Orange JS, Levy O et al (2004) Human nuclear factor kappa B essential modulator mutation can result in immunodeficiency without ectodermal dysplasia. J Allergy Clin Immunol 114:650-656
125. Orange JS, Levy O et al (2005) Human disease resulting from gene mutations that interfere with appropriate nuclear factor-kappaB activation. Immunol Rev 203:21-37
126. Park H, Wahl MI et al (1996) Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity 4:515-525
127. Park HJ, Hahn WH et al (2011) Association between Toll-like receptor 10 (TLR10) gene polymorphisms and childhood IgA nephropathy. Eur J Pediatr 170:503-509
128. Parkos CA, Colgan SP et al (1996) CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J Cell Biol 132:437-450
129. Perez de Diego R, Sancho-Shimizu V et al (2010) Human TRAF3 adaptor molecule deficiency leads to impaired Toll-like receptor 3 response and susceptibility to herpes simplex encephalitis. Immunity 33:400-411
130. Perry VH, Gordon S (1988) Macrophages and microglia in the nervous system. Trends Neurosci 11:273-277
131. Pettersen RD, Hestdal K et al (1999) CD47 signals T cell death. J Immunol 162:7031-7040
132. Picard C, Puel A et al (2003) Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299:2076-2079
133. Picard C, von Bernuth H et al (2010) Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency. Medicine 89:403-425
134. Picard C, Casanova JL et al (2011) Infectious diseases in patients with IRAK-4, MyD88, NEMO, or IkappaBalpha deficiency. Clin Microbiol Rev 24:490-497
135. Poltorak A, He X et al (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088
136. Requena T, Gazquez I et al (2013) Allelic variants in TLR10 gene may influence bilateral affectation and clinical course of Meniere's disease. Immunogenetics 65:345-355
137. Rivieccio MA, John GR et al (2005) The cytokine IL-1beta activates IFN response factor 3 in human fetal astrocytes in culture. J Immunol 174:3719-3726
138. Rivieccio MA, Suh HS et al (2006) TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J Immunol 177:4735-4741
139. Rock FL, Hardiman G et al (1998) A family of human receptors structurally related to Drosophila Toll. Proc Natl Acad Sci USA 95:588-593
140. Ruckdeschel K, Mannel O et al (2001) Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol 166:1823-1831
141. Ryser O, Morell A et al (1988) Primary immunodeficiencies in Switzerland: first report of the national registry in adults and children. J Clin Immunol 8:479-485
142. Salio M, Cerundolo V (2005) Viral immunity: cross-priming with the help of TLR3. Curr Biol 15:R336-R339
143. Sancho-Shimizu V, Perez de Diego R et al (2011) Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 121:4889-4902
144. Sato A, Linehan MM et al (2006) Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci USA 103:17343-17348
145. Schlaepfer E, Audige A et al (2006) TLR7/8 triggering exerts opposing effects in acute versus latent HIV infection. J Immunol 176:2888-2895
146. Schmitz ML, Bacher S et al (2001) I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations. Trends Biochem Sci 26:186-190
147. Schroder NW, Morath S et al (2003) Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 278:15587-15594
148. Schwartz M, Butovsky O et al (2006) Microglial phenotype: is the commitment reversible? Trends Neurosci 29:68-74
149. Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23:197-223
150. Seo HS, Michalek SM et al (2008) Lipoteichoic acid is important in innate immune responses to Gram-positive bacteria. Infect Immun 76:206-213
151. Seya T, Akazawa T et al (2003) Role of Toll-like receptors and their adaptors in adjuvant immunotherapy for cancer. Anticancer Res 23:4369-4376
152. Seya T, Akazawa T et al (2006) Role of Toll-like receptors in adjuvant-augmented immune therapies. Evid Based Complement Alternat Med 3:31-38 discussion 133-137
153. Sharma S, ten Oever BR et al (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151
154. Shearer WT, Paul ME et al (1994) Laboratory assessment of immunodeficiency disorders. Immunol Allergy Clin 14:265-297
155. Si Q, Zhao ML et al (2004) 15-deoxy-Delta12,14-prostaglandin J2 inhibits IFN-inducible protein 10/CXC chemokine ligand 10 expression in human microglia: mechanisms and implications. J Immunol 173:3504-3513
156. Sing A, Rost D et al (2002) Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J Exp Med 196:1017-1024
157. Sivula J, Cordova ZM et al (2012) Toll-like receptor gene polymorphisms confer susceptibility to graft-versus-host disease in allogenic hematopoietic stem cell transplantation. Scand J Immunol 76:336-341
158. Stevens VL, Hsing AW et al (2008) Genetic variation in the Toll-like receptor gene cluster (TLR10-TLR1-TLR6) and prostate cancer risk. Int J Cancer 123:2644-2650
159. Streit WJ, Conde JR et al (2005) Role of microglia in the central nervous system's immune response. Neurol Res 27:685-691
160. Stuart LM, Deng J et al (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170:477-485
161. Suh HS, Zhao ML et al (2007) Astrocyte indoleamine 2,3-dioxygenase is induced by the TLR3 ligand poly(I:C): mechanism of induction and role in antiviral response. J Virol 81:9838-9850
162. Suzuki N, Suzuki S et al (2002) Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 416:750-756
163. Szabo J, Dobay O et al (2007) Recurrent infection with genetically identical pneumococcal isolates in a patient with interleukin-1 receptor-associated kinase-4 deficiency. J Med Microbiol 56(Pt 6):863-865
164. Tada H, Nemoto E et al (2002) Saccharomyces cerevisiae- and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol Immunol 46:503-512
165. Takeuchi O, Hoshino K et al (2000) Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165:5392-5396
166. Town T, Jeng D et al (2006) Microglia recognize double-stranded RNA via TLR3. J Immunol 176:3804-3812
167. Travassos LH, Girardin SE et al (2004) Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep 5:1000-1006
168. Veltkamp M, van Moorsel CH et al (2012) Genetic variation in the Toll-like receptor gene cluster (TLR10-TLR1-TLR6) influences disease course in sarcoidosis. Tissue Antigens 79:25-32
169. Vijayan V, Baumgart-Vogt E et al (2011) Bruton's tyrosine kinase is required for TLR-dependent heme oxygenase-1 gene activation via Nrf2 in macrophages. J Immunol 187:817-827
170. von Aulock S, Hartung T et al (2007) Comment on "Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus". J Immunol 178:2610
171. von Bernuth H, Ku CL et al (2006) A fast procedure for the detection of defects in Toll-like receptor signaling. Pediatrics 118:2498-2503
172. von Bernuth H, Picard C et al (2008) Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321:691-696
173. Wang J, Fei B et al (2010) Quantitative analysis of protein translocations by microfluidic total internal reflection fluorescence flow cytometry. Lab Chip 10:2673-2679
174. Weih F, Warr G et al (1997) Multifocal defects in immune responses in RelB-deficient mice. J Immunol 158:5211-5218
175. WHO (1997) Primary immunodeficiency diseases. Report of a WHO scientific group. Clin Exp Immunol 109(Suppl 1):1-28
176. Winkelstein JA, Marino MC et al (2006) X-linked agammaglobulinemia: report on a United States registry of 201 patients. Medicine 85:193-202
177. Wlasiuk G, Khan S et al (2009) A history of recurrent positive selection at the Toll-like receptor 5 in primates. Mol Biol Evol 26:937-949
178. Xu N, Yao HP et al (2012) Downregulation of TLR7/9 leads to deficient production of IFN-alpha from plasmacytoid dendritic cells in chronic hepatitis B. Inflamm Res 61:997-1004
179. Yang M, Gan H et al (2012) Effect of LPS on the level of TLR4 and on the expression of NF-kappaB and Notch1 in monocytes from patients with type 2 diabetic nephropathy. Zhong Nan Da Xue Xue Bao Yi Xue Ban 37:578-585
180. Zemskov AM, Zemskov VM et al (2005) Problem of specific and nonspecific factors in the induction and regulation of immunological reactions. Zh Mikrobiol Epidemiol Immunobiol 4:105-109
181. Zhang SY, Jouanguy E et al (2007) TLR3 deficiency in patients with herpes simplex encephalitis. Science 317:1522-1527
182. Zheng W, Zheng X et al (2012) TNFalpha and IL-1beta are mediated by both