Polyinosinic-polycytidylic acid has therapeutic effects against cerebral ischemia/reperfusion injury through the downregulation of TLR4 signaling via TLR3

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4783-4794

  Wang, Peng Fei ^a   Fang, Huang ^a   Chen, Jing ^a   Lin, Sen ^b   Liu, Yong ^a   Xiong, Xiao Yi ^a   Wang, Yan Chun ^a   Xiong, Ren Ping ^a   Lv, Feng Lin ^c   Wang, Jian ^d   Yang, Qing Wu ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHENGDU MEDICAL COLLEGE   (China)

^c CHONGQING UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; INTERLEUKIN 1BETA; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN BAX; PROTEIN BCL 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL DEGENERATION; CELL SURVIVAL; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; HIPPOCAMPUS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRION; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIVIRAL AGENTS; BRAIN ISCHEMIA; DOWN-REGULATION; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; INTERLEUKIN-1BETA; MALE; MICE; MICE, KNOCKOUT; POLY I-C; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901259205     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303108     Document Type: Article

References (46)

1. Roger, V. L., A. S. Go, D. M. Lloyd-Jones, R. J. Adams, J. D. Berry, T. M. Brown, M. R. Carnethon, S. Dai, G. de Simone, E. S. Ford, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. 2011. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 123: e18-e209.
2. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. 1995. Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. 333: 1581-1587.
3. Iadecola, C., and J. Anrather. 2011. The immunology of stroke: from mechanisms to translation. Nat. Med. 17: 796-808.
4. Moskowitz, M. A., E. H. Lo, and C. Iadecola. 2010. The science of stroke: mechanisms in search of treatments. Neuron 67: 181-198.
5. Doyle, S. L., and L. A. O'Neill. 2006. Toll-like receptors: from the discovery of NFkB to new insights into transcriptional regulations in innate immunity. Biochem. Pharmacol. 72: 1102-1113.
6. Hua, F., J. Ma, T. Ha, Y. Xia, J. Kelley, D. L. Williams, R. L. Kao, I. W. Browder, J. B. Schweitzer, J. H. Kalbfleisch, and C. Li. 2007. Activation of Toll-like receptor 4 signaling contributes to hippocampal neuronal death following global cerebral ischemia/reperfusion. J. Neuroimmunol. 190: 101-111.
7. Harari, O. A., and J. K. Liao. 2010. NF-kB and innate immunity in ischemic stroke. Ann. N. Y. Acad. Sci. 1207: 32-40.
8. Chamorro, A., A. Meisel, A. M. Planas, X. Urra, D. van de Beek, and R. Veltkamp. 2012. The immunology of acute stroke. Nat. Rev. Neurol. 8: 401-410.
9. Cao, C. X., Q. W. Yang, F. L. Lv, J. Cui, H. B. Fu, and J. Z. Wang. 2007. Reduced cerebral ischemia-reperfusion injury in Toll-like receptor 4 deficient mice. Biochem. Biophys. Res. Commun. 353: 509-514.
10. Caso, J. R., J. M. Pradillo, O. Hurtado, P. Lorenzo, M. A. Moro, and I. Lizasoain. 2007. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115: 1599-1608.
11. Hua, F., J. Ma, T. Ha, J. Kelley, D. L. Williams, R. L. Kao, J. H. Kalbfleisch, I. W. Browder, and C. Li. 2008. Preconditioning with a TLR2 specific ligand increases resistance to cerebral ischemia/reperfusion injury. J. Neuroimmunol. 199: 75-82.
12. Vartanian, K. B., S. L. Stevens, B. J. Marsh, R. Williams-Karnesky, N. S. Lessov, and M. P. Stenzel-Poore. 2011. LPS preconditioning redirects TLR signaling following stroke: TRIF-IRF3 plays a seminal role in mediating tolerance to ischemic injury. J. Neuroinflammation 8: 140-151.
13. Leung, P. Y., S. L. Stevens, A. E. Packard, N. S. Lessov, T. Yang, V. K. Conrad, N. N. van den Dungen, R. P. Simon, and M. P. Stenzel-Poore. 2012. Toll-like receptor 7 preconditioning induces robust neuroprotection against stroke by a novel type I interferon-mediated mechanism. Stroke 43: 1383-1389.
14. Stevens, S. L., T. M. Ciesielski, B. J. Marsh, T. Yang, D. S. Homen, J. L. Boule, N. S. Lessov, R. P. Simon, and M. P. Stenzel-Poore. 2008. Toll-like receptor 9: a new target of ischemic preconditioning in the brain. J. Cereb. Blood Flow Metab. 28: 1040-1047.
15. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
16. Hyakkoku, K., J. Hamanaka, K. Tsuruma, M. Shimazawa, H. Tanaka, S. Uematsu, S. Akira, N. Inagaki, H. Nagai, and H. Hara. 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.
17. Packard, A. E., J. C. Hedges, F. R. Bahjat, S. L. Stevens, M. J. Conlin, A. M. Salazar, and M. P. Stenzel-Poore. 2012. Poly-IC preconditioning protects against cerebral and renal ischemia-reperfusion injury. J. Cereb. Blood Flow Metab. 32: 242-247.
18. Pan, L. N., W. Zhu, C. Li, X. L. Xu, L. J. Guo, and Q. Lu. 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.
19. Jiang, W., R. Sun, H. Wei, and Z. Tian. 2005. Toll-like receptor 3 ligand attenuates LPS-induced liver injury by down-regulation of Toll-like receptor 4 expression on macrophages. Proc. Natl. Acad. Sci. USA 102: 17077-17082.
20. Lu, C., L. Liu, Y. Chen, T. Ha, J. Kelley, J. Schweitzer, J. H. Kalbfleisch, R. L. Kao, D. L. Williams, and C. Li. 2011. TLR2 ligand induces protection against cerebral ischemia/reperfusion injury via activation of phosphoinositide 3- kinase/Akt signaling. J. Immunol. 187: 1458-1466.
21. Belayev, L., O. F. Alonso, R. Busto, W. Zhao, and M. D. Ginsberg. 1996. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 27: 1616-1622, discussion 1623.
22. Liu, L., S. K. Herukka, R. Minkeviciene, T. van Groen, and H. Tanila. 2004. Longitudinal observation on CSF Ab42 levels in young to middle-aged amyloid precursor protein/presenilin-1 doubly transgenic mice. Neurobiol. Dis. 17: 516-523.
23. Meller, R., S. L. Stevens, M. Minami, J. A. Cameron, S. King, H. Rosenzweig, K. Doyle, N. S. Lessov, R. P. Simon, and M. P. Stenzel-Poore. 2005. Neuroprotection by osteopontin in stroke. J. Cereb. Blood Flow Metab. 25: 217-225.
24. Wei, Y., M. Yemisci, H. H. Kim, L. M. Yung, H. K. Shin, S. K. Hwang, S. Guo, T. Qin, N. Alsharif, V. Brinkmann, et al. 2011. Fingolimod provides long-term protection in rodent models of cerebral ischemia. Ann. Neurol. 69: 119-129.
25. Solenski, N. J., C. G. diPierro, P. A. Trimmer, A. L. Kwan, and G. A. Helm. 2002. Ultrastructural changes of neuronal mitochondria after transient and permanent cerebral ischemia. Stroke 33: 816-824.
26. Canas, P. T., L. J. Velly, C. N. Labrande, B. A. Guillet, V. Sautou-Miranda, F. M. Masmejean, A. L. Nieoullon, F. M. Gouin, N. J. Bruder, and P. S. Pisano. 2006. Sevoflurane protects rat mixed cerebrocortical neuronal-glial cell cultures against transient oxygen-glucose deprivation: involvement of glutamate uptake and reactive oxygen species. Anesthesiology 105: 990-998.
27. Bond, B. C., D. J. Virley, N. J. Cairns, A. J. Hunter, G. B. Moore, S. J. Moss, A. W. Mudge, F. S. Walsh, E. Jazin, and P. Preece. 2002. The quantification of gene expression in an animal model of brain ischaemia using TaqMan real-time RT-PCR. Brain Res. Mol. Brain Res. 106: 101-116.
28. Yang, Q. W., F. L. Lu, Y. Zhou, L. Wang, Q. Zhong, S. Lin, J. Xiang, J. C. Li, C. Q. Fang, and J. Z. Wang. 2011. HMBG1 mediates ischemia-reperfusion injury by TRIF-adaptor independent Toll-like receptor 4 signaling. J. Cereb. Blood Flow Metab. 31: 593-605.
29. Stetler, R. A., G. Cao, Y. Gao, F. Zhang, S. Wang, Z. Weng, P. Vosler, L. Zhang, A. Signore, S. H. Graham, and J. Chen. 2008. Hsp27 protects against ischemic brain injury via attenuation of a novel stress-response cascade upstream of mitochondrial cell death signaling. J. Neurosci. 28: 13038-13055.
30. Chen, Z. C., W. S. Wu, M. T. Lin, and C. C. Hsu. 2009. Protective effect of transgenic expression of porcine heat shock protein 70 on hypothalamic ischemic and oxidative damage in a mouse model of heatstroke. BMC Neurosci. 10: 111.
31. Li, Y., M. Chopp, N. Jiang, Z. G. Zhang, and C. Zaloga. 1995. Induction of DNA fragmentation after 10 to 120 minutes of focal cerebral ischemia in rats. Stroke 26: 1252-1257, discussion 1257-1258.
32. Lehnardt, S., S. Lehmann, D. Kaul, K. Tschimmel, O. Hoffmann, S. Cho, C. Krueger, R. Nitsch, A. Meisel, and J. R. Weber. 2007. Toll-like receptor 2 mediates CNS injury in focal cerebral ischemia. J. Neuroimmunol. 190: 28-33.
33. Shichita, T., R. Sakaguchi, M. Suzuki, and A. Yoshimura. 2012. Post-ischemic inflammation in the brain. Front. Immunol. 3: 132.
34. Stroke Therapy Academic Industry Roundtable (STAIR). 1999. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30: 2752-2758.
35. Bhuiyan, M. I., and Y. J. Kim. 2010. Mechanisms and prospects of ischemic tolerance induced by cerebral preconditioning. Int. Neurourol. J. 14: 203-212.
36. Stridh, L., A. Mottahedin, M. E. Johansson, R. C. Valdez, F. Northington, X. Wang, and C. Mallard. 2013. Toll-like receptor-3 activation increases the vulnerability of the neonatal brain to hypoxia-ischemia. J. Neurosci. 33: 12041-12051.
37. Puyal, J., A. Vaslin, V. Mottier, and P. G. Clarke. 2009. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann. Neurol. 66: 378-389.
38. Unal-Cevik, I., M. Kilinç, A. Can, Y. Gursoy-Ozdemir, and T. Dalkara. 2004. Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia. Stroke 35: 2189-2194.
39. Rothwell, P. M. 2009. Is intravenous recombinant plasminogen activator effective up to 4.5 h after onset of ischemic stroke?. Nat. Clin. Pract. Cardiovasc. Med. 6: 164-165.
40. Shichita, T., E. Hasegawa, A. Kimura, R. Morita, R. Sakaguchi, I. Takada, T. Sekiya, H. Ooboshi, T. Kitazono, T. Yanagawa, et al. 2012. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 18: 911-917.
41. Broughton, B. R., D. C. Reutens, and C. G. Sobey. 2009. Apoptotic mechanisms after cerebral ischemia. Stroke 40: e331-e339.
42. Yang, H., Y. T. Zhu, R. Cheng, M. Y. Shao, Z. S. Fu, L. Cheng, F. M. Wang, and T. Hu. 2010. Lipopolysaccharide-induced dental pulp cell apoptosis and the expression of Bax and Bcl-2 in vitro. Braz. J. Med. Biol. Res. 43: 1027-1033.
43. Riad, A., S. Bien, M. Gratz, F. Escher, D. Westermann, M. M. Heimesaat, S. Bereswill, T. Krieg, S. B. Felix, H. P. Schultheiss, et al. 2008. Toll-like receptor-4 deficiency attenuates doxorubicin-induced cardiomyopathy in mice. Eur. J. Heart Fail. 10: 233-243.
44. Gupta, A., Z. A. Cooper, M. E. Tulapurkar, R. Potla, T. Maity, J. D. Hasday, and I. S. Singh. 2013. Toll-like receptor agonists and febrile range hyperthermia synergize to induce heat shock protein 70 expression and extracellular release. J. Biol. Chem. 288: 2756-2766.
45. Zietara, N., M. Lyszkiewicz, N. Gekara, J. Puchalka, V. A. Dos Santos, C. R. Hunt, T. K. Pandita, S. Lienenklaus, and S. Weiss. 2009. Absence of IFN-b impairs antigen presentation capacity of splenic dendritic cells via downregulation of heat shock protein 70. J. Immunol. 183: 1099-1109.
46. Shi, M.,W. Deng, E. Bi, K. Mao, Y. Ji, G. Lin, X.Wu, Z. Tao, Z. Li, X. Cai, et al. 2008. TRIM30a negatively regulates TLR-mediated NF-kB activation by targeting TAB2 and TAB3 for degradation. Nat. Immunol. 9: 369-377.