The SYK side of TLR4: Signalling mechanisms in response to LPS and minimally oxidized LDL

British Journal of Pharmacology

Volumn 167, Issue 5, 2012, Pages 990-999

  Miller, Yury I ^a   Choi, Soo Ho ^a   Wiesner, Philipp ^a   Bae, Yun Soo ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Ewha Womans University   (South Korea)

Author keywords

atherosclerosis; inflammation; innate immunity; lipid uptake; macrophage; oxidized low density lipoprotein; reactive oxygen species; signalling; spleen tyrosine kinase; toll like receptor 4

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; FOSTAMATINIB; LIPOPOLYSACCHARIDE; METHOTREXATE; MINIMALLY OXIDIZED LOW DENSITY LIPOPROTEIN; MYELOID DIFFERENTIATION FACTOR 88; OXIDIZED LOW DENSITY LIPOPROTEIN; PLACEBO; PROTEIN KINASE SYK; PROTEIN KINASE SYK INHIBITOR; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ATHEROGENESIS; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; BIOLOGICAL ACTIVITY; CHRONIC INFLAMMATION; CYTOKINE RELEASE; CYTOSKELETON; DRUG MECHANISM; DRUG TARGETING; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FOAM CELL; HOST RANGE; HUMAN; LIGAND BINDING; MACROPHAGE FUNCTION; MONOCYTE; NEUTROPHIL; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR BINDING; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; LIPOPROTEINS, LDL; MACROPHAGES; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84867304046     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02097.x     Document Type: Review

References (98)

1. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC, et al,. (2008). Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 87: 1219-1223. (Pubitemid 351679761)
2. Ameziane N, Beillat T, Verpillat P, Chollet-Martin S, Aumont MC, Seknadji P, et al,. (2003). Association of the Toll-like receptor 4 gene Asp299Gly polymorphism with acute coronary events. Arterioscler Thromb Vasc Biol 23: e61-e64.
3. Arndt PG, Suzuki N, Avdi NJ, Malcolm KC, Worthen GS, (2004). Lipopolysaccharide-induced c-Jun NH2-terminal kinase activation in human neutrophils: role of phosphatidylinositol 3-kinase and Syk-mediated pathways. J Biol Chem 279: 10883-10891. (Pubitemid 38401578)
4. Bae YS, Lee JH, Choi SH, Kim S, Almazan F, Witztum JL, et al,. (2009). Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein: toll-like receptor 4- and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circ Res 104: 210-218.
5. Bjorkbacka H, Kunjathoor VV, Moore KJ, Koehn S, Ordija CM, Lee MA, et al,. (2004). Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat Med 10: 416-421. (Pubitemid 38508522)
6. Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, Leitinger N, (2002). Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 419: 77-81. (Pubitemid 34987873)
7. Boekholdt SM, Agema WR, Peters RJ, Zwinderman AH, Van Der Wall EE, Reitsma PH, et al,. (2003). Variants of toll-like receptor 4 modify the efficacy of statin therapy and the risk of cardiovascular events. Circulation 107: 2416-2421. (Pubitemid 36605222)
8. Bowen WS, Minns LA, Johnson DA, Mitchell TC, Hutton MM, Evans JT, (2012). Selective TRIF-dependent signaling by a synthetic toll-like receptor 4 agonist. Sci Signal 5: ra13.
9. Cani PD, Delzenne NM, (2009). Interplay between obesity and associated metabolic disorders: new insights into the gut microbiota. Curr Opin Pharmacol 9: 737-743.
10. Chaudhary A, Fresquez TM, Naranjo MJ, (2007). Tyrosine kinase Syk associates with toll-like receptor 4 and regulates signaling in human monocytic cells. Immunol Cell Biol 85: 249-256. (Pubitemid 46701428)
11. Choi S-H, Harkewicz R, Lee JH, Boullier A, Almazan F, Li AC, et al,. (2009). Lipoprotein accumulation in macrophages via toll-like receptor-4-dependent fluid phase uptake. Circ Res 104: 1355-1363.
12. Choi SH, Wiesner P, Almazan F, Kim J, Miller YI, (2012). Spleen tyrosine kinase regulates AP-1 dependent transcriptional response to minimally oxidized LDL. PLoS ONE 7: e32378.
13. Coenen K, Gruen M, Lee-Young R, Puglisi M, Wasserman D, Hasty A, (2009). Impact of macrophage toll-like receptor 4 deficiency on macrophage infiltration into adipose tissue and the artery wall in mice. Diabetologia 52: 318-328.
14. Cyrus T, Witztum JL, Rader DJ, Tangirala R, Fazio S, Linton MF, et al,. (1999). Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J Clin Invest 103: 1597-1604.
15. Cyrus T, Pratico D, Zhao L, Witztum JL, Rader DJ, Rokach J, et al,. (2001). Absence of 12/15-lipoxygenase expression decreases lipid peroxidation and atherogenesis in apolipoprotein e-deficient mice. Circulation 103: 2277-2282. (Pubitemid 32433718)
16. Edfeldt K, Swedenborg J, Hansson GK, Yan ZQ, (2002). Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation 105: 1158-1161. (Pubitemid 34225814)
17. Elsori DH, Yakubenko VP, Roome T, Thiagarajan PS, Bhattacharjee A, Yadav SP, et al,. (2011). Protein kinase C delta is a critical component of Dectin-1 signaling in primary human monocytes. J Leukoc Biol 90: 599-611.
18. Erridge C, (2008). The roles of pathogen-associated molecular patterns in atherosclerosis. Trends Cardiovasc Med 18: 52-56. (Pubitemid 351282493)
19. Ezaki M, Witztum JL, Steinberg D, (1995). Lipoperoxides in LDL incubated with fibroblasts that overexpress 15-lipoxygenase. J Lipid Res 36: 1996-2004.
20. Fang L, Harkewicz R, Hartvigsen K, Wiesner P, Choi SH, Almazan F, et al,. (2010). Oxidized cholesteryl esters and phospholipids in zebrafish larvae fed a high-cholesterol diet: macrophage binding and activation. J Biol Chem 285: 32343-32351.
21. Gangloff M, (2012). Different dimerisation mode for TLR4 upon endosomal acidification? Trends Biochem Sci 37: 92-98.
22. Geng HL, Lu HQ, Zhang LZ, Zhang H, Zhou L, Wang H, et al,. (2006). Increased expression of Toll like receptor 4 on peripheral-blood mononuclear cells in patients with coronary arteriosclerosis disease. Clin Exp Immunol 143: 269-273.
23. George J, Afek A, Shaish A, Levkovitz H, Bloom N, Cyrus T, et al,. (2001). 12/15-Lipoxygenase gene disruption attenuates atherogenesis in LDL receptor-deficient mice. Circulation 104: 1646-1650. (Pubitemid 32947528)
24. Glass CK, Witztum JL, (2001). Atherosclerosis. The road ahead. Cell 104: 503-516.
25. Hamerman JA, Tchao NK, Lowell CA, Lanier LL, (2005). Enhanced Toll-like receptor responses in the absence of signaling adaptor DAP12. Nat Immunol 6: 579-586. (Pubitemid 41710728)
26. Han C, Jin J, Xu S, Liu H, Li N, Cao X, (2010). Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat Immunol 11: 734-742.
27. Harkewicz R, Hartvigsen K, Almazan F, Dennis EA, Witztum JL, Miller YI, (2008). Cholesteryl ester hydroperoxides are biologically active components of minimally oxidized LDL. J Biol Chem 283: 10241-10251.
28. Heine GH, Ortiz A, Massy ZA, Lindholm B, Wiecek A, Martinez-Castelao A, et al,. (2012). Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat Rev Nephrol 8: 362-369.
29. Higashimori M, Tatro JB, Moore KJ, Mendelsohn ME, Galper JB, Beasley D, (2011). Role of Toll-like receptor 4 in intimal foam cell accumulation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 31: 50-57.
30. Hilgendorf I, Eisele S, Remer I, Schmitz J, Zeschky K, Colberg C, et al,. (2011). The oral spleen tyrosine kinase inhibitor fostamatinib attenuates inflammation and atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 31: 1991-1999.
31. Hiratsuka S, Watanabe A, Sakurai Y, Kashi-Takamura S, Ishibashi S, Miyake K, et al,. (2008). The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10: 1349-1355.
32. Huo Y, Zhao L, Hyman MC, Shashkin P, Harry BL, Burcin T, et al,. (2004). Critical role of macrophage 12/15-lipoxygenase for atherosclerosis in apolipoprotein E-deficient mice. Circulation 110: 2024-2031. (Pubitemid 39331917)
33. Hutchins PM, Moore EE, Murphy RC, (2011). Electrospray tandem mass spectrometry reveals extensive and non-specific oxidation of cholesterol esters in human peripheral vascular lesions. J Lipid Res 52: 2070-2083.
34. Ii M, Matsunaga N, Hazeki K, Nakamura K, Takashima K, Seya T, et al,. (2006). A novel cyclohexene derivative, ethyl (6R)-6-[N-(2-Chloro-4- fluorophenyl)sulfamoyl]cyclohex-1-ene-1-carboxylate (TAK-242), selectively inhibits toll-like receptor 4-mediated cytokine production through suppression of intracellular signaling. Mol Pharmacol 69: 1288-1295.
35. Jakus Z, Fodor S, Abram CL, Lowell CA, Mocsai A, (2007). Immunoreceptor-like signaling by [beta]2 and [beta]3 integrins. Trends Cell Biol 17: 493-501. (Pubitemid 47562769)
36. Kalayoglu MV, Libby P, Byrne GI, (2002). Chlamydia pneumoniae as an emerging risk factor in cardiovascular disease. JAMA 288: 2724-2731. (Pubitemid 35403786)
37. Katsargyris A, Tsiodras S, Theocharis S, Giaginis K, Vasileiou I, Bakoyiannis C, et al,. (2011). Toll-like receptor 4 immunohistochemical expression is enhanced in macrophages of symptomatic carotid atherosclerotic plaques. Cerebrovasc Dis 31: 29-36.
38. Kawai T, Akira S, (2007). TLR signaling. Semin Immunol 19: 24-32. (Pubitemid 46498752)
39. Kenny EF, O'Neill LAJ, (2008). Signalling adaptors used by Toll-like receptors: an update. Cytokine 43: 342-349.
40. Kerrigan AM, Brown GD, (2011). Syk-coupled C-type lectins in immunity. Trends Immunol 32: 151-156.
41. Kiechl S, Lorenz E, Reindl M, Wiedermann CJ, Oberhollenzer F, Bonora E, et al,. (2002). Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med 347: 185-192. (Pubitemid 34764822)
42. Laugerette F, Vors C, Peretti N, Michalski MC, (2011). Complex links between dietary lipids, endogenous endotoxins and metabolic inflammation. Biochimie 93: 39-45.
43. Lee MS, Kim YJ, (2007). Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 76: 447-480.
44. Leitinger N, (2003). Cholesteryl ester oxidation products in atherosclerosis. Mol Aspects Med 24: 239-250. (Pubitemid 36945024)
45. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA, (1996). The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in drosophila adults. Cell 86: 973-983. (Pubitemid 26336801)
46. Levin MC, Jirholt P, Wramstedt A, Johansson ME, Lundberg AM, Trajkovska MG, et al,. (2011). Rip2 deficiency leads to increased atherosclerosis despite decreased inflammation. Circ Res 109: 1210-1218.
47. Ley K, Miller YI, Hedrick CC, (2011). Monocyte and macrophage dynamics during atherogenesis. Arterioscler Thromb Vasc Biol 31: 1506-1516.
48. Lowell CA, (2011). Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: signaling cross talk. Cold Spring Harb Persp Biol 3: a002352.
49. Lu R, Pan H, Shively JE, (2012). CEACAM1 negatively regulates IL-1beta production in LPS activated neutrophils by recruiting SHP-1 to a SYK-TLR4-CEACAM1 complex. PLoS Pathog 8: e1002597.
50. McGettrick AF, O'Neill LA, (2010). Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22: 20-27.
51. Medvedev AE, Piao W, Shoenfelt J, Rhee SH, Chen H, Basu S, et al,. (2007). Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J Biol Chem 282: 16042-16053. (Pubitemid 47100380)
52. Methe H, Kim JO, Kofler S, Weis M, Nabauer M, Koglin J, (2005). Expansion of circulating toll-like receptor 4-positive monocytes in patients with acute coronary syndrome. Circulation 111: 2654-2661. (Pubitemid 40740866)
53. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, et al,. (2004). Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. PNAS 101: 10679-10684. (Pubitemid 38955802)
54. Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, et al,. (2009). Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 15: 774-780.
55. Miller YI, Worrall DS, Funk CD, Feramisco JR, Witztum JL, (2003a). Actin polymerization in macrophages in response to oxidized LDL and apoptotic cells: role of 12/15-lipoxygenase and phosphoinositide 3-kinase. Mol Biol Cell 14: 4196-4206. (Pubitemid 37186320)
56. Miller YI, Viriyakosol S, Binder CJ, Feramisco JR, Kirkland TN, Witztum JL, (2003b). Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J Biol Chem 278: 1561-1568. (Pubitemid 36801384)
57. Miller YI, Viriyakosol S, Worrall DS, Boullier A, Butler S, Witztum JL, (2005). Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Biol 25: 1213-1219. (Pubitemid 40776611)
58. Miller YI, Choi SH, Fang L, Harkewicz R, (2009). Toll-like receptor-4 and lipoprotein accumulation in macrophages. Trends Cardiovasc Med 7: 227-232.
59. Miller YI, Choi S-H, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, et al,. (2011). Oxidation-specific epitopes are danger associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res 108: 235-248.
60. Mocsai A, Ruland J, Tybulewicz VLJ, (2010). The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 10: 387-402.
61. Nagai Y, Akashi S, Nagafuku M, Ogata M, Iwakura Y, Akira S, et al,. (2002). Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 3: 667-672. (Pubitemid 34752476)
62. Natarajan R, Nadler JL, (2003). Lipoxygenases and lipid signaling in vascular cells in diabetes. Front Biosci 8: s783-s795. (Pubitemid 39140196)
63. Netea MG, Hijmans A, van Wissen S, Smilde TJ, Trip MD, Kullberg BJ, et al,. (2004). Toll-like receptor-4 Asp299Gly polymorphism does not influence progression of atherosclerosis in patients with familial hypercholesterolaemia. Eur J Clin Invest 34: 94-99. (Pubitemid 38253608)
64. Newton K, Dixit VM, (2012). Signaling in innate immunity and inflammation. Cold Spring Harbor Persp Biol 4: a006049.
65. Owens AP, III, Rateri DL, Howatt DA, Moore KJ, Tobias PS, Curtiss LK, et al,. (2011). MyD88 deficiency attenuates angiotensin II-induced abdominal aortic aneurysm formation independent of signaling through Toll-like receptors 2 and 4. Arterioscler Thromb Vasc Biol 31: 2813-2819.
66. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO, (2009). The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
67. Patricia MK, Natarajan R, Dooley AN, Hernandez F, Gu JL, Berliner JA, et al,. (2001). Adenoviral delivery of a leukocyte-type 12 lipoxygenase ribozyme inhibits effects of glucose and platelet-derived growth factor in vascular endothelial and smooth muscle cells. Circ Res 88: 659-665. (Pubitemid 32378134)
68. Poeckel D, Zemski Berry KA, Murphy RC, Funk CD, (2009). Dual 12/15- and 5-lipoxygenase deficiency in macrophages alters arachidonic acid metabolism and attenuates peritonitis and atherosclerosis in APOE knockout mice. J Biol Chem 284: 21077-21089.
69. Poltorak A, He X, Smirnova I, Liu MY, Huffel CV, Du X, et al,. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088. (Pubitemid 29001265)
70. Pussinen PJ, Tuomisto K, Jousilahti P, Havulinna AS, Sundvall J, Salomaa V, (2007). Endotoxemia, immune response to periodontal pathogens, and systemic inflammation associate with incident cardiovascular disease events. Arterioscler Thromb Vasc Biol 27: 1433-1439. (Pubitemid 46809435)
71. Reismann P, Lichy C, Rudofsky G, Humpert PM, Genius J, Si TD, et al,. (2004). Lack of association between polymorphisms of the toll-like receptor 4 gene and cerebral ischemia. J Neurol 251: 853-858. (Pubitemid 39005971)
72. Rong S, Cao Q, Liu M, Seo J, Jia L, Boudyguina E, et al,. (2012). Macrophage 12/15 lipoxygenase expression increases plasma and hepatic lipid levels and exacerbates atherosclerosis. J Lipid Res 53: 686-695.
73. Rossignol DP, Lynn M, (2005). TLR4 antagonists for endotoxemia and beyond. Curr Opin Investig Drugs 6: 496-502. (Pubitemid 40613971)
74. Rowe SJ, Allen L, Ridger VC, Hellewell PG, Whyte MKB, (2002). Caspase-1-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J Immunol 169: 6401-6407. (Pubitemid 36903489)
75. Scannapieco FA, Bush RB, Paju S, (2003). Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol 8: 38-53.
76. Schmitz G, Orso E, (2002). CD14 signalling in lipid rafts: new ligands and co-receptors. Curr Opin Lipidol 13: 513-521. (Pubitemid 35231931)
77. Shalova IN, Kajiji T, Lim JY, Gomez-Pina V, Fernandez-Ruiz I, Arnalich F, et al,. (2012). CD16 regulates TRIF-dependent TLR4 response in human monocytes and their subsets. J Immunol 188: 3584-3593.
78. Shibata T, Motoi Y, Tanimura N, Yamakawa N, Kashi-Takamura S, Miyake K, (2011). Intracellular TLR4/MD-2 in macrophages senses Gram-negative bacteria and induces a unique set of LPS-dependent genes. Int Immunol 23: 503-510.
79. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, et al,. (2010). CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11: 155-161.
80. Stoletov K, Fang L, Choi SH, Hartvigsen K, Hansen LF, Hall C, et al,. (2009). Vascular lipid accumulation, lipoprotein oxidation, and macrophage lipid uptake in hypercholesterolemic zebrafish. Circ Res 104: 952-960.
81. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, Grant EP, et al,. (2006). Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
82. Takashima K, Matsunaga N, Yoshimatsu M, Hazeki K, Kaisho T, Uekata M, et al,. (2009). Analysis of binding site for the novel small-molecule TLR4 signal transduction inhibitor TAK-242 and its therapeutic effect on mouse sepsis model. Br J Pharmacol 157: 1250-1262.
83. Tiemi Shio M, Eisenbarth SC, Savaria M, Vinet AF, Bellemare MJE, Harder KW, et al,. (2009). Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 5: e1000559.
84. Triantafilou M, Triantafilou K, (2010). Membrane partitioning: is location everything when it comes to endotoxin recognition? Subcell Biochem 53: 173-184.
85. Upston JM, Niu X, Brown AJ, Mashima R, Wang H, Senthilmohan R, et al,. (2002). Disease stage-dependent accumulation of lipid and protein oxidation products in human atherosclerosis. Am J Pathol 160: 701-710. (Pubitemid 34160348)
86. von Schlieffen E, Oskolkova OV, Schabbauer G, Gruber F, Bluml S, Genest M, et al,. (2009). Multi-hit inhibition of circulating and cell-associated components of the toll-like receptor 4 pathway by oxidized phospholipids. Arterioscler Thromb Vasc Biol 29: 356-362.
87. Walton KA, Cole AL, Yeh M, Subbanagounder G, Krutzik SR, Modlin RL, et al,. (2003). Specific phospholipid oxidation products inhibit ligand activation of toll-like receptors 4 and 2. Arterioscler Thromb Vasc Biol 23: 1197-1203. (Pubitemid 36871273)
88. Wiesner P, Choi SH, Almazan F, Benner C, Huang W, Diehl CJ, et al,. (2010). Low doses of lipopolysaccharide and minimally oxidized low-density lipoprotein cooperatively activate macrophages via nuclear factor {kappa}B and activator protein-1. Possible mechanism for acceleration of atherosclerosis by subclinical endotoxemia. Circ Res 107: 56-65.
89. Wittebole X, Castanares-Zapatero D, Laterre PF, (2010). Toll-like receptor 4 modulation as a strategy to treat sepsis. Mediators Inflamm 2010: 568396.
90. Woodside DG, Obergfell A, Talapatra A, Calderwood DA, Shattil SJ, Ginsberg MH, (2002). The N-terminal SH2 domains of Syk and ZAP-70 mediate phosphotyrosine-independent binding to integrin cytoplasmic domains. J Biol Chem 277: 39401-39408. (Pubitemid 35190914)
91. Xie P, Cao YS, Su P, Li YH, Gao ZL, Borst MM, (2010). Expression of toll-like receptor 4, tumor necrosis factor-alpha, matrix metalloproteinase-9 and effects of benazepril in patients with acute coronary syndromes. Clin Med Insights Cardiol 4: 89-93.
92. Xu XH, Shah PK, Faure E, Equils O, Thomas L, Fishbein MC, et al,. (2001). Toll-Like receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circulation 104: 3103-3108. (Pubitemid 34014065)
93. Yang IA, Holloway JW, Ye S, (2003). TLR4 Asp299Gly polymorphism is not associated with coronary artery stenosis. Atherosclerosis 170: 187-190. (Pubitemid 37086707)
94. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, et al,. (1990). Colocalization of 15-lipoxygenase mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci USA 87: 6959-6963.
95. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Sigal E, Sarkioja T, Witztum JL, et al,. (1991). Gene expression in macrophage-rich human atherosclerotic lesions. 15-lipoxygenase and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation specific lipid-protein adducts. J Clin Invest 87: 1146-1152.
96. Zanoni I, Ostuni R, Marek L, Barresi S, Barbalat R, Barton G, et al,. (2011). CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880.
97. Zarbock A, Ley K, (2011). Protein tyrosine kinases in neutrophil activation and recruitment. Arch Biochem Biophys 510: 112-119.
98. Zhao L, Pratico D, Rader DJ, Funk CD, (2005). 12/15-Lipoxygenase gene disruption and vitamin E administration diminish atherosclerosis and oxidative stress in apolipoprotein E deficient mice through a final common pathway. Prostaglandins Other Lipid Mediat 78: 185-193. (Pubitemid 41636842)