CD14 and toll-like receptors 2 and 4 are required for fibrillar Aβ-stimulated microglial activation

Journal of Neuroscience

Volumn 29, Issue 38, 2009, Pages 11982-11992

  Reed Geaghan, Erin G ^a   Savage, Julie C ^a   Hise, Amy G ^a   Landreth, Gary E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CD14 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN; ANIMALS; ANTIGENS, CD14; CELLS, CULTURED; MACROPHAGE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHAGOCYTOSIS; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 70349323417     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3158-09.2009     Document Type: Article

References (106)

1. Aderem A (2002) How to eat something bigger than your head. Cell 110:5-8.
2. Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593-623.
3. Ago T, Nunoi H, Ito T, Sumimoto H (1999) Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47(phox). Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47(phox), thereby activating the oxidase. J Biol Chem 274:33644-33653. (Pubitemid 129511677)
4. Ago T, Kuribayashi F, Hiroaki H, Takeya R, Ito T, Kohda D, Sumimoto H (2003) Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc Natl Acad Sci U S A 100:4474-4479. (Pubitemid 36457755)
5. Akira S (2001) Toll-like receptors and innate immunity. Adv Immunol 78:1-56.
6. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
7. Arbibe L, Mira JP, Teusch N, Kline L, Guha M, Mackman N, Godowski PJ, Ulevitch RJ, Knaus UG (2000) Toll-like receptor 2-mediated NFkappa B activation requires a Rac1-dependent pathway. Nat Immunol 1:533-540.
8. Babior BM (1999) NADPH oxidase: an update. Blood 93:1464-1476.
9. Baeuerle PA, Baltimore D (1988) I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 242:540-546. (Pubitemid 18263193)
10. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23:2665-2674. (Pubitemid 36418601)
11. Beaty CD, Franklin TL, Uehara Y, Wilson CB (1994) Lipopolysaccharide- induced cytokine production in human monocytes: role of tyrosine phosphorylation in transmembrane signal transduction. Eur J Immunol 24:1278-1284. (Pubitemid 24169507)
12. Beg AA, Baldwin AS Jr (1993) The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev 7:2064-2070. (Pubitemid 2010879)
13. Bergendi L, Benes L, Duracková Z, Ferencik M (1999) Chemistry, physiology and pathology of free radicals. Life Sci 65:1865-1874. (Pubitemid 29506920)
14. Bhat NR, Zhang P, Lee JC, Hogan EL (1998) Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J Neurosci 18:1633-1641. (Pubitemid 28103071)
15. Bianca VD, Dusi S, Bianchini E, Dal Prà I, Rossi F (1999) beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem 274:15493-15499. (Pubitemid 129518900)
16. Blander JM, Medzhitov R (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304:1014-1018.
17. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F (1990) Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 27:229-237. (Pubitemid 20146292)
18. Bornemann KD, Wiederhold KH, Pauli C, Ermini F, Stalder M, Schnell L, Sommer B, Jucker M, Staufenbiel M (2001) Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am J Pathol 158:63-73. (Pubitemid 32096472)
19. Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503-506.
20. Brockman JA, Scherer DC, McKinsey TA, Hall SM, Qi X, Lee WY, Ballard DW (1995) Coupling of a signal response domain in I kappa B alpha to multiple pathways for NF-kappa B activation. Mol Cell Biol 15:2809-2818.
21. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U (1995) Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
22. Burdick D, Soreghan B, Kwon M, Kosmoski J, Knauer M, Henschen A, Yates J, Cotman C, Glabe C (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J Biol Chem 267:546-554.
23. Chen ZJ, Parent L, Maniatis T (1996) Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84:853-862. (Pubitemid 26106855)
24. Combs CK, Johnson DE, Cannady SB, Lehman TM, Landreth GE (1999) Identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of beta-amyloid and prion proteins. J Neurosci 19:928-939.
25. Combs CK, Karlo JC, Kao SC, Landreth GE (2001) beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21:1179-1188.
26. Cox D, Chang P, Zhang Q, Reddy PG, Bokoch GM, Greenberg S (1997) Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J Exp Med 186:1487-1494. (Pubitemid 27479808)
27. Dang PM, Stensballe A, Boussetta T, Raad H, Dewas C, Kroviarski Y, Hayem G, Jensen ON, Gougerot-Pocidalo MA, El-Benna J (2006) A specific p47phox -serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 116:2033-2043. (Pubitemid 44033327)
28. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758. (Pubitemid 43085841)
29. DeLeo FR, Quinn MT (1996) Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J Leukoc Biol 60:677-691. (Pubitemid 27041655)
30. El Bekay R, Alba G, Reyes ME, Chacón P, Vega A, Martín-Nieto J, Jiménez J, Ramos E, Oliván J, Pintado E, Sobrino F (2007) Rac2 GTPase activation by angiotensin II is modulated by Ca2+/calcineurin and mitogen-activated protein kinases in human neutrophils. J Mol Endocrinol 39:351-363.
31. El Benna J, Faust RP, Johnson JL, Babior BM (1996) Phosphorylation of the respiratory burst oxidase subunit p47phox as determined by two-dimensional phosphopeptide mapping. Phosphorylation by protein kinase C, protein kinase A, and a mitogen-activated protein kinase. J Biol Chem 271:6374-6378. (Pubitemid 26095447)
32. English BK, Ihle JN, Myracle A, Yi T (1993) Hck tyrosine kinase activity modulates tumor necrosis factor production by murine macrophages. J Exp Med 178:1017-1022. (Pubitemid 23260439)
33. Fassbender K, Walter S, Kühl S, Landmann R, Ishii K, Bertsch T, Stalder AK, Muehlhauser F, Liu Y, Ulmer AJ, Rivest S, Lentschat A, Gulbins E, Jucker M, Staufenbiel M, Brechtel K, Walter J, Multhaup G, Penke B, Adachi Y, et al. (2004) The LPS receptor (CD14) links innate immunity with Alzheimer's disease. FASEB J 18:203-205.
34. Ferrer I (2004) Stress kinases involved in tau phosphorylation in Alzheimer's disease, tauopathies and APP transgenic mice. Neurotox Res 6:469-475.
35. Finco TS, Beg AA, Baldwin AS Jr (1994) Inducible phosphorylation of I kappa B alpha is not sufficient for its dissociation from NF-kappa B and is inhibited by protease inhibitors. Proc Natl Acad Sci U S A 91:11884-11888.
36. Flanary BE, Sammons NW, Nguyen C, Walker D, Streit WJ (2007) Evidence that aging and amyloid promote microglial cell senescence. Rejuvenation Res 10:61-74. (Pubitemid 46449433)
37. Floden AM, Combs CK (2006) Beta-amyloid stimulates murine postnatal and adult microglia cultures in a unique manner. J Neurosci 26:4644-4648.
38. Gangloff SC, Hijiya N, Haziot A, Goyert SM (1999) Lipopolysaccharide structure influences the macrophage response via CD14-independent and CD14-dependent pathways. Clin Infect Dis 28:491-496. (Pubitemid 29242522)
39. Geng Y, Gulbins E, Altman A, Lotz M (1994) Monocyte deactivation by interleukin 10 via inhibition of tyrosine kinase activity and the Ras signaling pathway. Proc Natl Acad Sci U S A 91:8602-8606. (Pubitemid 24273712)
40. Giovannini MG, Scali C, Prosperi C, Bellucci A, Vannucchi MG, Rosi S, Pepeu G, Casamenti F (2002) Beta-amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: involvement of the p38MAPK pathway. Neurobiol Dis 11:257-274. (Pubitemid 36135690)
41. Gregory CD, Devitt A (1999) CD14 and apoptosis. Apoptosis 4:11-20.
42. Heine H, Kirschning CJ, Lien E, Monks BG, Rothe M, Golenbock DT (1999) Cutting edge: cells that carry A null allele for toll-like receptor 2 are capable of responding to endotoxin. J Immunol 162:6971-6975. (Pubitemid 29277661)
43. Heinzelmann M, Polk HC Jr, Miller FN (1998) Modulation of lipopolysaccharide-induced monocyte activation by heparin-binding protein and fucoidan. Infect Immun 66:5842-5847. (Pubitemid 28531843)
44. Hensley K, Floyd RA, Zheng NY, Nael R, Robinson KA, Nguyen X, Pye QN, Stewart CA, Geddes J, Markesbery WR, Patel E, Johnson GV, Bing G (1999) p38 kinase is activated in the Alzheimer's disease brain. J Neurochem 72:2053-2058. (Pubitemid 29186010)
45. Ishibashi Y, Claus S, Relman DA (1994) Bordetella pertussis filamentous hemagglutinin interacts with a leukocyte signal transduction complex and stimulates bacterial adherence to monocyte CR3 (CD11b/CD18). J Exp Med 180:1225-1233. (Pubitemid 24289596)
46. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24:173-182. (Pubitemid 19271472)
47. Jana M, Palencia CA, Pahan K (2008) Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer's disease. J Immunol 181:7254-7262.
48. Jin Y, Yan EZ, Fan Y, Zong ZH, Qi ZM, Li Z (2005) Sodium ferulate prevents amyloid-beta-induced neurotoxicity through suppression of p38 MAPK and upregulation of ERK-1/2 and Akt/protein kinase B in rat hippocampus. Acta Pharmacol Sin 26:943-951. (Pubitemid 41153214)
49. Kielian T (2006) Toll-like receptors in central nervous system glial inflammation and homeostasis. J Neurosci Res 83:711-730.
50. Kim SH, Smith CJ, Van Eldik LJ (2004) Importance of MAPK pathways for microglial pro-inflammatory cytokine IL-1 beta production. Neurobiol Aging 25:431-439.
51. Kim WS, Ordija CM, Freeman MW (2003) Activation of signaling pathways by putative scavenger receptor class A (SR-A) ligands requires CD14 but not SR-A. Biochem Biophys Res Commun 310:542-549.
52. 1 integrin-dependent mechanism. J Neurosci 24:9838-9846.
53. Kong L, Ge BX (2008) MyD88-independent activation of a novel actin-Cdc42/Rac pathway is required for Toll-like receptor-stimulated phagocytosis. Cell Res 18:745-755. (Pubitemid 351948225)
54. Kopec KK, Carroll RT (1998) Alzheimer's beta-amyloid peptide 1-42 induces a phagocytic response in murine microglia. J Neurochem 71:2123-2131.
55. Laroux FS, Romero X, Wetzler L, Engel P, Terhorst C (2005) Cutting edge: MyD88 controls phagocyte NADPH oxidase function and killing of gram-negative bacteria. J Immunol 175:5596-5600. (Pubitemid 41508037)
56. Lee DJ, Cox D, Li J, Greenberg S (2000) Rac1 and Cdc42 are required for phagocytosis, but not NF-kappaB-dependent gene expression, in macrophages challenged with Pseudomonas aeruginosa. J Biol Chem 275:141-146. (Pubitemid 30038964)
57. Letiembre M, Liu Y, Walter S, Hao W, Pfander T, Wrede A, Schulz-Schaeffer W, Fassbender K (2009) Screening of innate immune receptors in neurodegenerative diseases: a similar pattern. Neurobiol Aging 30:759-768.
58. Liu Y, Walter S, Stagi M, Cherny D, Letiembre M, Schulz-Schaeffer W, Heine H, Penke B, Neumann H, Fassbender K (2005) LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide. Brain 128:1778-1789. (Pubitemid 41373649)
59. Lorenzo A, Yankner BA (1994) Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc Natl Acad Sci U S A 91:12243-12247. (Pubitemid 24368641)
60. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE (2009) Microglia mediate the clearance of soluble Aβ through fluid phase macropinocytosis. J Neurosci 29:4252-4262.
61. McDonald DR, Brunden KR, Landreth GE (1997) Amyloid fibrils activate tyrosine kinase-dependent signaling and superoxide production in microglia. J Neurosci 17:2284-2294.
62. McDonald DR, Bamberger ME, Combs CK, Landreth GE (1998) β-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J Neurosci 18:4451-4460.
63. Meda L, Bonaiuto C, Baron P, Otvos L Jr, Rossi F, Cassatella MA (1996) Priming of monocyte respiratory burst by beta-amyloid fragment (25-35). Neurosci Lett 219:91-94. (Pubitemid 26396322)
64. Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135-145.
65. Minoretti P, Gazzaruso C, Vito CD, Emanuele E, Bianchi M, Coen E, Reino M, Geroldi D (2006) Effect of the functional toll-like receptor 4 Asp299Gly polymorphism on susceptibility to late-onset Alzheimer's disease. Neurosci Lett 391:147-149. (Pubitemid 41736189)
66. Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ (2006) Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 176:3070-3079. (Pubitemid 43306969)
67. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318. (Pubitemid 40746128)
68. Osada Y, Sunatani T, Kim IS, Nakanishi Y, Shiratsuchi A (2009) Signalling pathway involving GULP, MAPK, and Rac1 for SR-BI-induced phagocytosis of apoptotic cells. J Biochem 145:387-394.
69. Park JY, Kim HY, Jou I, Park SM (2008) GM1 induces p38 and microtubule dependent ramification of rat primary microglia in vitro. Brain Res 1244:13-23.
70. Perlmutter LS, Barron E, Chui HC (1990) Morphologic association between microglia and senile plaque amyloid in Alzheimer's disease. Neurosci Lett 119:32-36. (Pubitemid 20349720)
71. Pfeiffer A, Böttcher A, Orsó E, Kapinsky M, Nagy P, Bodnár A, Spreitzer I, Liebisch G, Drobnik W, Gempel K, Horn M, Holmer S, Hartung T, Multhoff G, Schütz G, Schindler H, Ulmer AJ, Heine H, Stelter F, Schütt C, et al. (2001) Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur J Immunol 31:3153-3164. (Pubitemid 33100507)
72. Pick E (1986) Microassays for superoxide and hydrogen peroxide production and nitroblue tetrazolium reduction using an enzyme immunoassay microplate reader. Methods Enzymol 132:407-421.
73. Pyo H, Jou I, Jung S, Hong S, Joe EH (1998) Mitogen-activated protein kinases activated by lipopolysaccharide and beta-amyloid in cultured rat microglia. Neuroreport 9:871-874. (Pubitemid 28179292)
74. Qin L, Li G, Qian X, Liu Y, Wu X, Liu B, Hong JS, Block ML (2005) Interactive role of the toll-like receptor 4 and reactive oxygen species in LPS-induced microglia activation. Glia 52:78-84. (Pubitemid 41532140)
75. 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J Neurosci 28:5784-5793.
76. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
77. Sánchez-Mejorada G, Rosales C (1998) Signal transduction by immunoglobulin Fc receptors. J Leukoc Biol 63:521-533.
78. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF (2001) Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 276:30188-30198. (Pubitemid 37385100)
79. Saura J, Tusell JM, Serratosa J (2003) High-yield isolation of murine microglia by mild trypsinization. Glia 44:183-189. (Pubitemid 37484470)
80. Savage MJ, Lin YG, Ciallella JR, Flood DG, Scott RW (2002) Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J Neurosci 22:3376-3385.
81. Scholtzova H, Kascsak RJ, Bates KA, Boutajangout A, Kerr DJ, Meeker HC, Mehta PD, Spinner DS, Wisniewski T (2009) Induction of toll-like receptor 9 signaling as a method for ameliorating Alzheimer's disease-related pathology. J Neurosci 29:1846-1854.
82. Selkoe DJ (2000) Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 924:17-25.
83. Sendide K, Reiner NE, Lee JS, Bourgoin S, Talal A, Hmama Z (2005) Crosstalk between CD14 and complement receptor 3 promotes phagocytosis of mycobacteria: regulation by phosphatidylinositol 3-kinase and cytohesin-1. J Immunol 174:4210-4219. (Pubitemid 40396001)
84. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K (2007) Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55:412-424. (Pubitemid 46247127)
85. Smits HA, de Vos NM, Wat JW, van der Bruggen T, Verhoef J, Nottet HS (2001) Intracellular pathways involved in TNF-alpha and superoxide anion release by Abeta(1-42)-stimulated primary human macrophages. J Neuroimmunol 115:144-151. (Pubitemid 32245662)
86. Stefanová I, Corcoran ML, Horak EM, Wahl LM, Bolen JB, Horak ID (1993) Lipopolysaccharide induces activation of CD14-associated protein tyrosine kinase p53/56lyn. J Biol Chem 268:20725-20728. (Pubitemid 23292237)
87. Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14.
88. Sumimoto H, Hata K, Mizuki K, Ito T, Kage Y, Sakaki Y, Fukumaki Y, Nakamura M, Takeshige K (1996) Assembly and activation of the phagocyte NADPH oxidase. Specific interaction of the N-terminal Src homology 3 domain of p47phox with p22phox is required for activation of the NADPH oxidase. J Biol Chem 271:22152-22158. (Pubitemid 26303847)
89. Sun A, Liu M, Nguyen XV, Bing G (2003) P38 MAP kinase is activated at early stages in Alzheimer's disease brain. Exp Neurol 183:394-405. (Pubitemid 37205081)
90. Taborda CP, Casadevall A (2002) CR3 (CD11b/CD18) and CR4 (CD11c/CD18) are involved in complement-independent antibody-mediated phagocytosis of Cryptococcus neoformans. Immunity 16:791-802.
91. Tahara K, Kim HD, Jin JJ, Maxwell JA, Li L, Fukuchi K (2006) Role of toll-like receptor signalling in Abeta uptake and clearance. Brain 129:3006-3019. (Pubitemid 44684521)
92. Tang G, Yue Z, Talloczy Z, Hagemann T, Cho W, Messing A, Sulzer DL, Goldman JE (2008) Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways. Hum Mol Genet 17:1540-1555. (Pubitemid 351737159)
93. Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, Baeuerle PA (1995) Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J 14:2876-2883.
94. Triantafilou M, Brandenburg K, Kusumoto S, Fukase K, Mackie A, Seydel U, Triantafilou K (2004) Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem J 381:527-536. (Pubitemid 38969699)
95. Triantafilou M, Gamper FG, Haston RM, Mouratis MA, Morath S, Hartung T, Triantafilou K (2006) Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J Biol Chem 281:31002-31011. (Pubitemid 44582155)
96. Udan ML, Ajit D, Crouse NR, Nichols MR (2008) Toll-like receptors 2 and 4 mediate Abeta(1-42) activation of the innate immune response in a human monocytic cell line. J Neurochem 104:524-533. (Pubitemid 350293880)
97. Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, Bassetti M, Aderem A (1999) The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401:811-815. (Pubitemid 129515844)
98. Van Muiswinkel FL, Raupp SF, de Vos NM, Smits HA, Verhoef J, Eikelenboom P, Nottet HS (1999) The amino-terminus of the amyloid-beta protein is critical for the cellular binding and consequent activation of the respiratory burst of human macrophages. J Neuroimmunol 96:121-130. (Pubitemid 29179752)
99. van Oosten M, van Amersfoort ES, van Berkel TJ, Kuiper J (2001) Scavenger receptor-like receptors for the binding of lipopolysaccharide and lipoteichoic acid to liver endothelial and Kupffer cells. J Endotoxin Res 7:381-384.
100. Walter S, Letiembre M, Liu Y, Heine H, Penke B, Hao W, Bode B, Manietta N, Walter J, Schulz-Schuffer W, Fassbender K (2007) Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell Physiol Biochem 20:947-956. (Pubitemid 350059737)
101. Wilkinson B, Koenigsknecht-Talboo J, Grommes C, Lee CY, Landreth G (2006) Fibrillar beta-amyloid-stimulated intracellular signaling cascades require Vav for induction of respiratory burst and phagocytosis in monocytes and microglia. J Biol Chem 281:20842-20850. (Pubitemid 44115425)
102. Wong WS, Simon DI, Rosoff PM, Rao NK, Chapman HA (1996) Mechanisms of pertussis toxin-induced myelomonocytic cell adhesion: role of Mac-1(CD11b/CD18) and urokinase receptor (CD87). Immunology 88:90-97.
103. Yamamori T, Inanami O, Nagahata H, Cui Y, Kuwabara M (2000) Roles of p38 MAPK, PKC and PI3-K in the signaling pathways of NADPH oxidase activation and phagocytosis in bovine polymorphonuclear leukocytes. FEBS Lett 467:253-258.
104. Yan SR, Al-Hertani W, Byers D, Bortolussi R (2002) Lipopolysaccharide- binding protein- and CD14-dependent activation of mitogen-activated protein kinase p38 by lipopolysaccharide in human neutrophils is associated with priming of respiratory burst. Infect Immun 70:4068-4074. (Pubitemid 34790914)
105. Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA (2000) Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol 59:880-888. (Pubitemid 30781851)
106. Zuluaga S, Gutiérrez-Uzquiza A, Bragado P, Alvarez-Barrientos A, Benito M, Nebreda AR, Porras A (2007) p38alpha MAPK can positively or negatively regulate Rac-1 activity depending on the presence of serum. FEBS Lett 581:3819-3825.