Toll-like receptor signaling in endogenous neuroprotection and stroke

Neuroscience

Volumn 158, Issue 3, 2009, Pages 1007-1020

  Marsh, B J ^a   Williams Karnesky, R L ^a   Stenzel Poore, M P ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

inflammation; lipopolysaccharide; preconditioning; reprogramming; tolerance; type I interferon

Indexed keywords

BETA INTERFERON; CHEMOKINE; CPG OLIGODEOXYNUCLEOTIDE; CYCLOHEXIMIDE; CYTOKINE; DEXAMETHASONE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEAT SHOCK PROTEIN 60; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; CELL INFILTRATION; CEREBROVASCULAR ACCIDENT; DISSOCIATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; INFLAMMATION; INSULIN RESISTANCE; ISCHEMIC PRECONDITIONING; MOLECULAR INTERACTION; NERVE CELL DIFFERENTIATION; NEUROPROTECTION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STROKE;

ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; CYTOPROTECTION; ENCEPHALITIS; GENE EXPRESSION REGULATION; HUMANS; IMMUNE TOLERANCE; NERVE DEGENERATION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 59349116736     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.07.067     Document Type: Review

References (109)

1. AHA. Heart Disease and Stroke Statistical Update (2005)
2. Ahmed S., He Y., Nassief A., Xu J., Xu X., and Hsu C. Effects of lipopolysaccharide priming on acute ischemic brain injury. Stroke 31 (2000) 193-199
3. Aneja R., Odoms K., Dunsmore K., Shanley T.P., and Wong H.R. Extracellular heat shock protein-70 induces endotoxin tolerance in THP-1 cells. J Immunol 177 (2006) 7184-7192
4. Bagchi A., Herrup E.A., Warren H.S., Trigilio J., Shin H.S., Valentine C., and Hellman J. MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J Immunol 178 (2007) 1164-1171
5. Bastide M., Gele P., Petrault O., Pu Q., Caliz A., Robin E., Deplanque D., Duriez P., and Bordet R. Delayed cerebrovascular protective effect of lipopolysaccharide in parallel to brain ischemic tolerance. J Cereb Blood Flow Metab 23 (2003) 399-405
6. Bond R., Rerkasem K., Shearman C.P., and Rothwell P.M. Time trends in the published risks of stroke and death due to endarterectomy for symptomatic carotid stenosis. Cerebrovasc Dis 18 (2004) 37-46
7. Bordet R., Deplanque D., Maboudou P., Puisieux F., Pu Q., Robin E., Martin A., Bastide M., Leys D., Lhermitte M., and Dupuis B. Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J Cereb Blood Flow Metab 20 (2000) 1190-1196
8. Bosca L., Bodelon O.G., Hortelano S., Casellas A., and Bosch F. Anti-inflammatory action of type I interferons deduced from mice expressing interferon beta. Gene Ther 7 (2000) 817-825
9. Boutros T., Croze E., and Yong V.W. Interferon-beta is a potent promoter of nerve growth factor production by astrocytes. J Neurochem 69 (1997) 939-946
10. Broad A., Kirby J.A., and Jones D.E. Toll-like receptor interactions: tolerance of MyD88-dependent cytokines but enhancement of MyD88-independent interferon-beta production. Immunology 120 (2007) 103-111
11. Bsibsi M., Persoon-Deen C., Verwer R.W., Meeuwsen S., Ravid R., and Van Noort J.M. Toll-like receptor 3 on adult human astrocytes triggers production of neuroprotective mediators. Glia 53 (2006) 688-695
12. Bsibsi M., Ravid R., Gveric D., and van Noort J.M. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61 (2002) 1013-1021
13. Bucerius J., Gummert J.F., Borger M.A., Walther T., Doll N., Onnasch J.F., Metz S., Falk V., and Mohr F.W. Stroke after cardiac surgery: a risk factor analysis of 16,184 consecutive adult patients. Ann Thorac Surg 75 (2003) 472-478
14. +-ATPase and constant membrane potential in hepatocytes: support for channel arrest. Am J Physiol 265 (1993) R1020-R1025
15. Candelario-Jalil E., Yang Y., and Rosenberg G.A. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158 (2009) 983-994
16. Cao C.X., Yang Q.W., Lv F.L., Cui J., Fu H.B., and Wang J.Z. Reduced cerebral ischemia-reperfusion injury in Toll-like receptor 4 deficient mice. Biochem Biophys Res Comm 353 (2007) 509-514
17. Carpentier P.A., Begolka W.S., Olson J.K., Elhofy A., Karpus W.J., and Miller S.D. Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49 (2005) 360-374
18. Caso J.R., Pradillo J.M., Hurtado O., Lorenzo P., Moro M.A., and Lizasoain I. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115 (2007) 1599-1608
19. Chakravarty S., and Herkenham M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 25 (2005) 1788-1796
20. Constantin D., Cordenier A., Robinson K., Ala'Aldeen D.A., and Murphy S. Neisseria meningitidis-induced death of cerebrovascular endothelium: mechanisms triggering transcriptional activation of inducible nitric oxide synthase. J Neurochem 89 (2004) 1166-1174
21. Dalpke A.H., Lehner M.D., Hartung T., and Heeg K. Differential effects of CpG-DNA in Toll-like receptor-2/-4/-9 tolerance and cross-tolerance. Immunology 116 (2005) 203-212
22. Dave K.R., Saul I., Busto R., Ginsberg M.D., Sick T.J., and Perez-Pinzon M.A. Ischemic preconditioning preserves mitochondrial function after global cerebral ischemia in rat hippocampus. J Cereb Blood Flow Metab 21 (2001) 1401-1410
23. Davis J.E., Gabler N.K., Walker-Daniels J., and Spurlock M.E. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity 16 (2008) 1248-1255
24. Dawson D.A., Furuya K., Gotoh J., Nakao Y., and Hallenbeck J.M. Cerebrovascular hemodynamics and ischemic tolerance: lipopolysaccharide-induced resistance to focal cerebral ischemia is not due to changes in severity of the initial ischemic insult, but is associated with preservation of microvascular perfusion. J Cereb Blood Flow Metab 19 (1999) 616-623
25. Dirnagl U., and Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning?. Neuropharmacology 55 (2008) 334-344
26. Ekdahl C.T., Kokaia Z., and Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158 (2009) 1021-1029
27. Endres M., Fan G., Hirt L., Fujii M., Matsushita K., Liu X., Jaenisch R., and Moskowitz M.A. Ischemic brain damage in mice after selectively modifying BDNF or NT4 gene expression. J Cereb Blood Flow Metab 20 (2000) 139-144
28. Faraco G., Fossati S., Bianchi M.E., Patrone M., Pedrazzi M., Sparatore B., Moroni F., and Chiarugi A. High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J Neurochem 103 (2007) 590-603
29. Ferlito M., Romanenko O.G., Ashton S., Squadrito F., Halushka P.V., and Cook J.A. Effect of cross-tolerance between endotoxin and TNF-alpha or IL-1beta on cellular signaling and mediator production. J Leukoc Biol 70 (2001) 821-829
30. Furuya K., Zhu L., Kawahara N., Abe O., and Kirino T. Differences in infarct evolution between lipopolysaccharide-induced tolerant and nontolerant conditions to focal cerebral ischemia. J Neurosurg 103 (2005) 715-723
31. Ginis I., Jaiswal R., Klimanis D., Liu J., Greenspon J., and Hallenbeck J. TNFa induced tolerance to ischemic injury involves differential control of NF-kB transactivation: the role of NF-kB association with p300 adaptor. J Cereb Blood Flow Metab 22 (2002) 142-152
32. Ginis I., Schweizer U., Brenner M., Liu J., Azzam N., Spatz M., and Hallenbeck J. TNF-alpha pretreatment prevents subsequent activation of cultured brain cells with TNF-alpha and hypoxia via ceramide. Am J Physiol 276 (1999) C1171
33. Ha T., Li Y., Hua F., Ma J., Gao X., Kelley J., Zhao A., Haddad G.E., Williams D.L., William Browder I., Kao R.L., and Li C. Reduced cardiac hypertrophy in toll-like receptor 4-deficient mice following pressure overload. Cardiovasc Res 68 (2005) 224-234
34. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., and Moskowitz M.A. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Natl Acad Sci U S A 94 (1997) 2007-2012
35. Hickey E.J., You X., Kaimaktchiev V., Stenzel-Poore M., and Ungerleider R.M. Lipopolysaccharide preconditioning induces robust protection against brain injury resulting from deep hypothermic circulatory arrest. J Thorac Cardiovasc Surg 133 (2007) 1588-1596
36. Hua F., Ma J., Ha T., Xia Y., Kelley J., Williams D.L., Kao R.L., Browder I.W., Schweitzer J.B., Kalbfleisch J.H., and Li C. Activation of Toll-like receptor 4 signaling contributes to hippocampal neuronal death following global cerebral ischemia/reperfusion. J Neuroimmunol 190 (2007) 101-111
37. Hua L., Kim M., Brosnan C., and Lee S. Modulation of astrocyte inducible nitric oxide synthase and cytokine expression by interferon β is associated with induction and inhibition of interferon γ-activated sequence binding activity. J Neurochem 83 (2002) 1120-1128
38. Jack C.S., Arbour N., Manusow J., Montgrain V., Blain M., McCrea E., Shapiro A., and Antel J.P. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175 (2005) 4320-4330
39. Jiang D., Liang J., Li Y., and Noble P.W. The role of Toll-like receptors in non-infectious lung injury. Cell Res 16 (2006) 693-701
40. Jin S., Kawanokuchi J., Mizuno T., Wang J., Sonobe Y., Takeuchi H., and Suzumura A. Interferon-beta is neuroprotective against the toxicity induced by activated microglia. Brain Res 1179 (2007) 140-146
41. Kagan J.C., Su T., Horng T., Chow A., Akira S., and Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 9 (2008) 361-368
42. Kerschensteiner M., Meinal E., and Hohlfeld R. Neuro-immune crosstalk in CNS diseases. Neuroscience 158 (2009) 1122-1132
43. Kinouchi H., Sharp F.R., Hill M.P., Koistinaho J., Sagar S.M., and Chan P.H. Induction of 70-kDa heat shock protein and hsp70 mRNA following transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 13 (1993) 105-115
44. Kobayashi K., Hernandex L., Galan J., Janeway J., Medzhitov R., and Flavell R. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110 (2002) 191-202
45. Kraus J., Ling A.K., Hamm S., Voigt K., Oschmann P., and Engelhardt B. Interferon-beta stabilizes barrier characteristics of brain endothelial cells in vitro. Ann Neurol 56 (2004) 192-205
46. Kunz A., Park L., Abe T., Gallo E.F., Anrather J., Zhou P., and Iadecola C. Neurovascular protection by ischemic tolerance: role of nitric oxide and reactive oxygen species. J Neurosci 27 (2007) 7083-7093
47. Laflamme N., and Rivest S. 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 (2001) 155-163
48. Laflamme N., Soucy G., and Rivest S. Circulating cell wall components derived from gram-negative, not gram-positive, bacteria cause a profound induction of the gene-encoding Toll-like receptor 2 in the CNS. J Neurochem 79 (2001) 648-657
49. Lafon M., Megret F., Lafage M., and Prehaud C. The innate immune facet of brain: human neurons express TLR-3 and sense viral dsRNA. J Mol Neurosci 29 (2006) 185-194
50. Lehnardt S., Lehmann S., Kaul D., Tschimmel K., Hoffmann O., Cho S., Krueger C., Nitsch R., Meisel A., and Weber J.R. Toll-like receptor 2 mediates CNS injury in focal cerebral ischemia. J Neuroimmunol 190 (2007) 28-33
51. Lehnardt S., Schott E., Trimbuch T., Laubisch D., Krueger C., Wulczyn G., Nitsch R., and Weber J.R. A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J Neurosci 28 (2008) 2320-2331
52. Liu H., Xin L., Chan B.P.L., Teoh R., Tang B.L., and Tan Y.H. Interferon beta administration confers a beneficial outcome in a rabbit model of thromboembolic cerebral ischemia. Neurosci Lett 327 (2002) 146-148
53. Liuzzi G.M., Latronico T., Fasano A., Carlone G., and Riccio P. Interferon-beta inhibits the expression of metalloproteinases in rat glial cell cultures: implications for multiple sclerosis pathogenesis and treatment. Mult Scler 10 (2004) 290-297
54. Lloyd-Jones K.L., Kelly M.M., and Kubes P. Varying importance of soluble and membrane CD14 in endothelial detection of lipopolysaccharide. J Immunol 181 (2008) 1446-1453
55. Lopez-Collazo E., Hortelano S., Rojas A., and Bosca L. Triggering of peritoneal macrophages with IFN-alpha/beta attenuates the expression of inducible nitric oxide synthase through a decrease in NF-kappaB activation. J Immunol 160 (1998) 2889-2895
56. Ma Y., Li J., Chiu I., Wang Y., Sloane J.A., Lu J., Kosaras B., Sidman R.L., Volpe J.J., and Vartanian T. Toll-like receptor 8 functions as a negative regulator of neurite outgrowth and inducer of neuronal apoptosis. J Cell Biol 175 (2006) 209-215
57. McFalls E.O., Sluiter W., Schoonderwoerd K., Manintveld O.C., Lamers J.M., Bezstarosti K., van Beusekom H.M., Sikora J., Ward H.B., Merkus D., and Duncker D.J. Mitochondrial adaptations within chronically ischemic swine myocardium. J Mol Cell Cardiol 41 (2006) 980-988
58. McKhann G.M., Grega M.A., Borowicz Jr. L.M., Baumgartner W.A., and Selnes O.A. Stroke and encephalopathy after cardiac surgery: an update. Stroke 37 (2006) 562-571
59. McKimmie C.S., and Fazakerley J.K. In response to pathogens, glial cells dynamically and differentially regulate Toll-like receptor gene expression. J Neuroimmunol 169 (2005) 116-125
60. Medvedev A.E., Lentschat A., Wahl L.M., Golenbock D.T., and Vogel S.N. Dysregulation of LPS-induced Toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase1 activation in endotoxin-tolerant cells. J Immunol 169 (2002) 5209-5216
61. Murphey E.D., and Traber D.L. Protective effect of tumor necrosis factor-alpha against subsequent endotoxemia in mice is mediated, in part, by interleukin-10. Crit Care Med 29 (2001) 1761-1766
62. Murray C.J., and Lopez A.D. Alternative projections of mortality and disability by cause 1990-2020: Global Burden of Disease Study. Lancet 349 (1997) 1498-1504
63. Nawashiro H., Tasaki K., Ruetzler C.A., and Hallenbeck J.M. TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 17 (1997) 483-490
64. Nhu Q.M., Cuesta N., and Vogel S.N. Transcriptional regulation of lipopolysaccharide (LPS)-induced Toll-like receptor (TLR) expression in murine macrophages: role of interferon regulatory factors 1 (IRF-1) and 2 (IRF-2). J Endotoxin Res 12 (2006) 285-295
65. Noble R. The development of resistance by rats and guinea pigs to amounts of trauma usually fatal. Am J Physiol 38 (1943) 346-351
66. Olson J.K., and Miller S.D. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173 (2004) 3916-3924
67. Oyama J., Blais Jr. C., Liu X., Pu M., Kobzik L., Kelly R.A., and Bourcier T. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 109 (2004) 784-789
68. Palmer G., Mezin F., Juge-Aubry C.E., Plater-Zyberk C., Gabay C., and Guerne P.A. Interferon beta stimulates interleukin 1 receptor antagonist production in human articular chondrocytes and synovial fibroblasts. Ann Rheum Dis 63 (2004) 43-49
69. Porter M.H., Arnold M., and Langhans W. TNF-alpha tolerance blocks LPS-induced hypophagia but LPS tolerance fails to prevent TNF-alpha-induced hypophagia. Am J Physiol 274 (1998) R741-R745
70. Prehaud C., Megret F., Lafage M., and Lafon M. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 79 (2005) 12893-12904
71. Relton J.K., Martin D., Thompson R.C., and Russell D.A. Peripheral administration of interleukin-1 receptor antagonist inhibits brain damage after focal cerebral ischemia in the rat. Exp Neurol 138 (1996) 206-213
72. Rolls A., Shechter R., London A., Ziv Y., Ronen A., Levy R., and Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 9 (2007) 1081-1088
73. Rosenzweig H.L., Lessov N.S., Henshall D.C., Minami M., Simon R.P., and Stenzel-Poore M.P. Endotoxin preconditioning prevents the cellular inflammatory response during ischemic neuroprotection in mice. Stroke 35 (2004) 2576-2581
74. Rosenzweig H.L., Minami M., Lessov N.S., Coste S.C., Stevens S.L., Henshall D.C., Meller R., Simon R.P., and Stenzel-Poore M.P. Endotoxin preconditioning protects against the cytotoxic effects of TNFa after stroke: a novel role for TNFa in LPS-ischemic tolerance. J Cereb Blood Flow Metab 27 (2007) 1663-1674
75. Sakata Y., Dong J.W., Vallejo J.G., Huang C.H., Baker J.S., Tracey K.J., Tacheuchi O., Akira S., and Mann D.L. Toll-like receptor 2 modulates left ventricular function following ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 292 (2007) H503-H509
76. Schneider A., Martin-Villalba A., Weih F., Vogel J., Wirth T., and Schwaninger M. NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 5 (1999) 554-559
77. Seguin R., Moditi Z., Rotondo R., Biernacki K., Wosik K., Prat A., and Antel J.P. Human brain endothelial cells supply support for monocyte immunoregulatory functions. J Neuroimmunol 135 (2003) 96-106
78. Shen X.D., Ke B., Zhai Y., Gao F., Busuttil R.W., Cheng G., and Kupiec-Weglinski J.W. Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury. Am J Transplant 5 (2005) 1793-1800
79. Shi M., Deng W., Bi E., Mao K., Ji Y., Lin G., Wu X., Tao Z., Li Z., Cai X., Sun S., Xiang C., and Sun B. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 9 (2008) 369-377
80. Shigeoka A.A., Holscher T.D., King A.J., Hall F.W., Kiosses W.B., Tobias P.S., Mackman N., and McKay D.B. TLR2 is constitutively expressed within the kidney and participates in ischemic renal injury through both MyD88-dependent and -independent pathways. J Immunol 178 (2007) 6252-6258
81. Shishido T., Nozaki N., Yamaguchi S., Shibata Y., Nitobe J., Miyamoto T., Takahashi H., Arimoto T., Maeda K., Yamakawa M., Takeuchi O., Akira S., Takeishi Y., and Kubota I. Toll-like receptor-2 modulates ventricular remodeling after myocardial infarction. Circulation 108 (2003) 2905-2910
82. Singh A.K., and Jiang Y. How does peripheral lipopolysaccharide induce gene expression in the brain of rats?. Toxicology 201 (2004) 197-207
83. Sly L.M., Rauh M.J., Kalesnikoff J., Song C.H., and Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21 (2004) 227-239
84. Spera P.A., Ellison J.A., Feuerstein G.Z., and Barone F.C. IL-10 reduces rat brain injury following focal stroke. Neurosci Lett 251 (1998) 189-192
85. Stenzel-Poore M.P., Stevens S.L., King J.S., and Simon R.P. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38 (2007) 680-685
86. Stenzel-Poore M.P., Stevens S.L., Xiong Z., Lessov N.S., Harrington C.A., Mori M., Meller R., Rosenzweig H.L., Tobar E., Shaw T.E., Chu X., and Simon R.P. Effect of ischemic preconditioning on genomic response to cerebral ischemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362 (2003) 1028-1037
87. Stevens S.L., Ciesielski T.M., Marsh B.J., Yang T., Homen D.S., Boule J.L., Lessov N.S., Simon R.P., and Stenzel-Poore M.P. Toll-like receptor 9: a new target of ischemic preconditioning in the brain. J Cereb Blood Flow Metab 28 (2008) 1040-1047
88. Stewart V.C., Giovannoni G., Land J.M., McDonald W.I., Clark J.B., and Heales S.J. Pretreatment of astrocytes with interferon-alpha/beta impairs interferon-gamma induction of nitric oxide synthase. J Neurochem 68 (1997) 2547-2551
89. Stewart V.C., Land J.M., Clark J.B., and Heales S.J. Pretreatment of astrocytes with interferon-alpha/beta prevents neuronal mitochondrial respiratory chain damage. J Neurochem 70 (1998) 432-434
90. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int Immunol 17 (2005) 1-14
91. Tasaki K., Ruetzler C.A., Ohtsuki T., Martin D., Nawashiro H., and Hallenbeck J.M. Lipopolysaccharide pre-treatment induces resistance against subsequent focal cerebral ischemic damage in spontaneously hypertensive rats. Brain Res 748 (1997) 267-270
92. Tobias P.S., and Curtiss L.K. Toll-like receptors in atherosclerosis. Biochem Soc Trans 35 (2007) 1453-1455
93. Truettner J., Busto R., Zhao W., Ginsberg M.D., and Perez-Pinzon M.A. Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain Res Mol Brain Res 103 (2002) 106-115
94. Tsukumo D.M., Carvalho-Filho M.A., Carvalheira J.B., Prada P.O., Hirabara S.M., Schenka A.A., Araujo E.P., Vassallo J., Curi R., Velloso L.A., and Saad M.J. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56 (2007) 1986-1998
95. Veldhuis W., Derksen J., Floris S., van der Meide P., de Vries H., Schepers J., Vos I., Dijkstra C., Kappelle L., Nicolay K., and Bar P. Interferon-beta blocks infiltration of inflammatory cells and reduces infarct volume after ischemic stroke in the rat. J Cereb Blood Flow Metab 23 (2003) 1029-1039
96. Veldhuis W.B., Floris S., van der Meide P.H., Vos I.M., de Vries H.E., Dijkstra C.D., Bar P.R., and Nicolay K. Interferon-beta prevents cytokine-induced neutrophil infiltration and attenuates blood-brain barrier disruption. J Cereb Blood Flow Metab 23 (2003) 1060-1069
97. Vogel S.N., Fitzgerald K.A., and Fenton M.J. TLRs: differential adapter utilization by toll-like receptors mediates TLR-specific patterns of gene expression. Mol Intervent 3 (2003) 466-477
98. Wu L.Y., Ding A.S., Zhao T., Ma Z.M., Wang F.Z., and Fan M. Involvement of increased stability of mitochondrial membrane potential and overexpression of Bcl-2 in enhanced anoxic tolerance induced by hypoxic preconditioning in cultured hypothalamic neurons. Brain Res 999 (2004) 149-154
99. Yadav J.S., Wholey M.H., Kuntz R.E., Fayad P., Katzen B.T., Mishkel G.J., Bajwa T.K., Whitlow P., Strickman N.E., Jaff M.R., Popma J.J., Snead D.B., Cutlip D.E., Firth B.G., and Ouriel K. Protected carotid-artery stenting versus endarterectomy in high-risk patients. N Engl J Med 351 (2004) 1493-1501
100. Yeh H.J., He Y.Y., Xu J., Hsu C.Y., and Deuel T.F. Upregulation of pleiotrophin gene expression in developing microvasculature, macrophages, and astrocytes after acute ischemic brain injury. J Neurosci 18 (1998) 3699-3707
101. Yusuf S., Reddy S., Ounpuu S., and Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 104 (2001) 2746-2753
102. Yusuf S., Reddy S., Ounpuu S., and Anand S. Global burden of cardiovascular diseases: part II: variations in cardiovascular disease by specific ethnic groups and geographic regions and prevention strategies. Circulation 104 (2001) 2855-2864
103. Zarember K.A., and Godowski P.J. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 168 (2002) 554-561
104. Zhai Y., Shen X.D., O'Connell R., Gao F., Lassman C., Busuttil R.W., Cheng G., and Kupiec-Weglinski J.W. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 173 (2004) 7115-7119
105. Zhan R.Z., Fujihara H., Baba H., Yamakura T., and Shimoji K. Ischemic preconditioning is capable of inducing mitochondrial tolerance in the rat brain. Anesthesiology 97 (2002) 896-901
106. Zhang W., Potrovita I., Tarabin V., Herrmann O., Beer V., Weih F., Schneider A., and Schwaninger M. Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J Cereb Blood Flow Metab 25 (2005) 30-40
107. Zhang X., Shan P., Jiang G., Cohn L., and Lee P.J. Toll-like receptor 4 deficiency causes pulmonary emphysema. J Clin Invest 116 (2006) 3050-3059
108. Zhou M.L., Shi J.X., Hang C.H., Zhang F.F., Gao J., and Yin H.X. Expression of Toll-like receptor 4 in the brain in a rabbit experimental subarachnoid haemorrhage model. Inflamm Res 56 (2007) 93-97
109. Ziegler G., Harhausen D., Schepers C., Hoffmann O., Rohr C., Prinz V., Konig J., Lehrach H., Nietfeld W., and Trendelenburg G. TLR2 has a detrimental role in mouse transient focal cerebral ischemia. Biochem Biophys Res Comm 359 (2007) 574-579