Astrocytic toll-like receptor 3 is associated with ischemic preconditioning- induced protection against brain ischemia in rodents

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Pan, Lin Na ^a,b   Zhu, Wei ^c,d   Li, Yang ^a   Xu, Lin ^a,e   Guo, Lian Jun ^a,e   Lu, Qing ^a,e   Wang, Jian ^d  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Second Hospital of Nanchang   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Key Laboratory of Drug Target Research and Pharmacodynamic Evaluation   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL INTERLEUKIN RECEPTOR DOMAIN CONTAINING ADAPTOR INDUCING INTERFERON BETA; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; OXYGEN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN DAMAGE; BRAIN INFARCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; CYTOKINE RELEASE; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; MALE; MOUSE; NEUROPROTECTION; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; BRAIN CORTEX; CELL CULTURE; CEREBRAL ARTERY DISEASE; COMPLICATION; DEFICIENCY; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ASTROCYTES; BRAIN; BRAIN ISCHEMIA; CELLS, CULTURED; CEREBRAL CORTEX; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; INTERLEUKIN-6; ISCHEMIC PRECONDITIONING; MALE; MICE; OXYGEN; PHOSPHORYLATION; POLY I-C; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TRANSCRIPTION FACTOR RELA;

EID: 84902593609     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099526     Document Type: Article

References (50)

1. Shpargel KB, Jalabi W, Jin Y, Dadabayev A, Penn MS, et al. (2008) Preconditioning paradigms and pathways in the brain. Cleve Clin J Med 75 Suppl 2: S77-S82.
2. Liu XQ, Sheng R, Qin ZH (2009) The neuroprotective mechanism of brain ischemic preconditioning. Acta Pharmacol Sin 30: 1071-1080.
3. Wang J, Dore S (2007) Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab 27: 894-908. (Pubitemid 46659028)
4. Wang J (2010) Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog Neurobiol 92: 463-477.
5. Li L, Lundkvist A, Andersson D, Wilhelmsson U, Nagai N, et al. (2008) Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab 28: 468-481. (Pubitemid 351304260)
6. Barreto G, White RE, Ouyang Y, Xu L, Giffard RG (2011) Astrocytes: targets for neuroprotection in stroke. Cent Nerv Syst Agents Med Chem 11: 164-173.
7. Gabryel B, Trzeciak HI (2001) Role of astrocytes in pathogenesis of ischemic brain injury. Neurotox Res 3: 205-221. (Pubitemid 32936867)
8. Harari OA, Liao JK (2010) NF-kappaB and innate immunity in ischemic stroke. Ann N Y Acad Sci 1207: 32-40.
9. Lakhan SE, Kirchgessner A, Hofer M (2009) Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J Transl Med 7: 97.
10. Kilic U, Kilic E, Matter CM, Bassetti CL, Hermann DM (2008) TLR-4 deficiency protects against focal cerebral ischemia and axotomy-induced neurodegeneration. Neurobiol Dis 31: 33-40.
11. Zhou Y, Wang Y, Wang J, Anne SR, Yang QW (2014) Inflammation in intracerebral hemorrhage: From mechanisms to clinical translation. Prog Neurobiol 115C: 25-44.
12. Marsh BJ, Stenzel-Poore MP (2008) Toll-like receptors: novel pharmacological targets for the treatment of neurological diseases. Curr Opin Pharmacol 8: 8-13. (Pubitemid 351181026)
13. Veldhuis WB, Derksen JW, Floris S, Van Der Meide PH, De Vries HE, et al. (2003) Interferon-beta blocks infiltration of inflammatory cells and reduces infarct volume after ischemic stroke in the rat. J Cereb Blood Flow Metab 23: 1029-1039. (Pubitemid 37082428)
14. Veldhuis WB, Floris S, van der Meide PH, Vos IM, de Vries HE, et al. (2003) Interferon-beta prevents cytokine-induced neutrophil infiltration and attenuates blood-brain barrier disruption. J Cereb Blood Flow Metab 23: 1060-1069. (Pubitemid 37082431)
15. Grilli M, Barbieri I, Basudev H, Brusa R, Casati C, et al. (2000) Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur J Neurosci 12: 2265-2272. (Pubitemid 30497024)
16. Cao CX, Yang QW, Lv FL, Cui J, Fu HB, et al. (2007) Reduced cerebral ischemia-reperfusion injury in Toll-like receptor 4 deficient mice. Biochem Biophys Res Commun 353: 509-514. (Pubitemid 46023466)
17. Caso JR, Pradillo JM, Hurtado O, Lorenzo P, Moro MA, et al. (2007) Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115: 1599-1608. (Pubitemid 46648645)
18. Hyakkoku K, Hamanaka J, Tsuruma K, Shimazawa M, Tanaka H, et al. (2010) Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia. Neuroscience 171: 258-267.
19. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, et al. (2007) Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A 104: 13798-13803. (Pubitemid 350003400)
20. Pradillo JM, Fernandez-Lopez D, Garcia-Yebenes I, Sobrado M, Hurtado O, et al. (2009) Toll-like receptor 4 is involved in neuroprotection afforded by ischemic preconditioning. J Neurochem 109: 287-294.
21. Marsh BJ, Williams-Karnesky RL, Stenzel-Poore MP (2009) Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 158: 1007-1020.
22. Vartanian KB, Stevens SL, Marsh BJ, Williams-Karnesky R, Lessov NS, et al. (2011) LPS preconditioning redirects TLR signaling following stroke: TRIFIRF3 plays a seminal role in mediating tolerance to ischemic injury. J Neuroinflammation 8: 140.
23. Bsibsi M, Persoon-Deen C, Verwer RW, Meeuwsen S, Ravid R, et al. (2006) Toll-like receptor 3 on adult human astrocytes triggers production of neuroprotective mediators. Glia 53: 688-695.
24. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, et al. (2009) Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: a critical role for IRF3. J Neurosci 29: 9839-9849.
25. Borysiewicz E, Doppalapudi S, Kirschman LT, Konat GW (2013) TLR3 ligation protects human astrocytes against oxidative stress. J Neuroimmunol 255: 54-59.
26. Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, et al. (2008) TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 205: 2609-2621.
27. McCusker RH, Kelley KW (2013) Immune-neural connections: how the immune system's response to infectious agents influences behavior. J Exp Biol 216: 84-98.
28. Cho S, Park EM, Zhou P, Frys K, Ross ME, et al. (2005) Obligatory role of inducible nitric oxide synthase in ischemic preconditioning. J Cereb Blood Flow Metab 25: 493-501.
29. Lu Q, Xia N, Xu H, Guo L, Wenzel P, et al. (2011) Betulinic acid protects against cerebral ischemia-reperfusion injury in mice by reducing oxidative and nitrosative stress. Nitric Oxide 24: 132-138.
30. Zan L, Zhang X, Xi Y, Wu H, Song Y, et al. (2014) Src regulates angiogenic factors and vascular permeability after focal cerebral ischemia-reperfusion. Neuroscience 262: 118-128.
31. Wu H, Wu T, Li M, Wang J (2012) Efficacy of the lipid-soluble iron chelator 2,29-dipyridyl against hemorrhagic brain injury. Neurobiol Dis 45: 388-394.
32. Wu T, Wu H, Wang J, Wang J (2011) Expression and cellular localization of cyclooxygenases and prostaglandin E synthases in the hemorrhagic brain. J Neuroinflammation 8: 22.
33. Wang J, Dore S (2008) Heme oxygenase 2 deficiency increases brain swelling and inflammation after intracerebral hemorrhage. Neuroscience 155: 1133-1141.
34. Koyama Y, Kotani M, Sawamura T, Kuribayashi M, Konishi R, et al. (2013) Different actions of endothelin-1 on chemokine production in rat cultured astrocytes: reduction of CX3CL1/fractalkine and an increase in CCL2/MCP-1 and CXCL1/CINC-1. J Neuroinflammation 10: 51.
35. Sparapani M, Buonamici L, Ciani E, Battelli MG, Ceccarelli G, et al. (1997) Toxicity of ricin and volkensin, two ribosome-inactivating proteins, to microglia, astrocyte, and neuron cultures. Glia 20: 203-209. (Pubitemid 27324306)
36. Liu C, Wu J, Xu K, Cai F, Gu J, et al. (2010) Neuroprotection by baicalein in ischemic brain injury involves PTEN/AKT pathway. J Neurochem 112: 1500-1512.
37. Wang J, Zhuang H, Dore S (2006) Heme oxygenase 2 is neuroprotective against intracerebral hemorrhage. Neurobiol Dis 22: 473-476. (Pubitemid 43842118)
38. Chang CF, Cho S, Wang J (2014) (-)-Epicatechin protects hemorrhagic brain via synergistic Nrf2 pathways. Ann Clin Transl Neurol 1: 258-271.
39. Vande VB, Hanssens JL (2007) Cytotoxicity of two bonding adhesives assessed by three-dimensional cell culture. Angle Orthod 77: 716-722.
40. Barreto GE, Gonzalez J, Torres Y, Morales L (2011) Astrocytic-neuronal crosstalk: implications for neuroprotection from brain injury. Neurosci Res 71: 107-113.
41. Hanke ML, Kielian T (2011) Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin Sci (Lond) 121: 367-387.
42. Liu H, Xin L, Chan BP, Teoh R, Tang BL, et al. (2002) Interferon-beta administration confers a beneficial outcome in a rabbit model of thromboembolic cerebral ischemia. Neurosci Lett 327: 146-148. (Pubitemid 34722428)
43. Hecker M, Hartmann C, Kandulski O, Paap BK, Koczan D, et al. (2013) Interferon-beta therapy in multiple sclerosis: the short-term and long-term effects on the patients' individual gene expression in peripheral blood. Mol Neurobiol.
44. Bowen KK, Naylor M, Vemuganti R (2006) Prevention of inflammation is a mechanism of preconditioning-induced neuroprotection against focal cerebral ischemia. Neurochem Int 49: 127-135. (Pubitemid 43867070)
45. Shi M, Deng W, Bi E, Mao K, Ji Y, et al. (2008) TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 9: 369-377. (Pubitemid 351405106)
46. Gesuete R, Packard AE, Vartanian KB, Conrad VK, Stevens SL, et al. (2012) Poly-ICLC preconditioning protects the blood-brain barrier against ischemic injury in vitro through type I interferon signaling. J Neurochem 123 Suppl 2: 75-85.
47. Pan LN, Zhu W, Li C, Xu XL, Guo LJ, et al. (2012) Toll-like receptor 3 agonist Poly I:C protects against simulated cerebral ischemia in vitro and in vivo. Acta Pharmacol Sin 33: 1246-1253.
48. Packard AE, Hedges JC, Bahjat FR, Stevens SL, Conlin MJ, et al. (2012) Poly-IC preconditioning protects against cerebral and renal ischemia-reperfusion injury. J Cereb Blood Flow Metab 32: 242-247.
49. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, et al. (2009) Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 206: 1589-1602.
50. McCartney S, Vermi W, Gilfillan S, Cella M, Murphy TL, et al. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J Exp Med 206: 2967-2976.