Isoflurane preconditioning provides neuroprotection against stroke by regulating the expression of the TLR4 signalling pathway to alleviate microglial activation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sun, Meiyan ^a   Deng, Bin ^a,c   Zhao, Xiaoyong ^a,d   Gao, Changjun ^a   Yang, Lu ^a   Zhao, Hui ^a   Yu, Daihua ^a   Zhang, Feng ^e   Xu, Lixian ^c   Chen, Lei ^b   Sun, Xude ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b Department of Gynaecology and Obstetrics Nave General Hospital   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d WEIFANG MEDICAL UNIVERSITY   (China)

^e NONE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CHAPERONIN 60; I KAPPA B; I KAPPA B KINASE ALPHA; ISOFLURANE; MYELOID DIFFERENTIATION FACTOR 88; NEUROPROTECTIVE AGENT; NFKBIA PROTEIN, RAT; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ANIMAL; APOPTOSIS; BRAIN INFARCTION; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; ISCHEMIC PRECONDITIONING; MALE; METABOLISM; MICROGLIA; MOLECULAR MODEL; PATHOLOGY; PATHOPHYSIOLOGY; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STROKE;

ANIMALS; APOPTOSIS; BIOMARKERS; BRAIN INFARCTION; CELLS, CULTURED; CHAPERONIN 60; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE EXPRESSION REGULATION; I-KAPPA B PROTEINS; ISCHEMIC PRECONDITIONING; ISOFLURANE; MALE; MICROGLIA; MODELS, MOLECULAR; MYELOID DIFFERENTIATION FACTOR 88; NEUROPROTECTIVE AGENTS; NF-KAPPAB INHIBITOR ALPHA; RATS; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STROKE; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84934943914     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11445     Document Type: Article

References (60)

1. Nagasawa, H. & Kogure, K. Correlation between cerebral blood flow and histologic changes in a new rat model of middle cerebral artery occlusion. Stroke 20, 1037-43 (1989).
2. Song, D. Y. et al. Role of activating transcription factor 3 in ischemic penumbra region following transient middle cerebral artery occlusion and reperfusion injury. Neurosci Res 70, 428-34 (2011).
3. Jin, R., Yang, G. & Li, G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 87, 779-89 (2010).
4. Wang, S. et al. Neuroprotection of Scutellarin is mediated by inhibition of microglial inflammatory activation. Neuroscience 185, 150-60 (2011).
5. Wood, P. L. Microglia as a unique cellular target in the treatment of stroke: potential neurotoxic mediators produced by activated microglia. Neurol Res 17, 242-8 (1995).
6. Neumann, H., Kotter, M. R. & Franklin, R. J. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132, 288-95 (2009).
7. Tambuyzer, B. R., Ponsaerts, P. & Nouwen, E. J. Microglia: gatekeepers of central nervous system immunology. J Leukoc Biol 85, 352-70 (2009).
8. Li, L. & Zuo, Z. Isoflurane preconditioning improves short-term and long-term neurological outcome after focal brain ischemia in adult rats. Neuroscience 164, 497-506 (2009).
9. Xiong, L. et al. Hyperbaric oxygen preconditioning induces neuroprotection against ischemia in transient not permanent middle cerebral artery occlusion rat model. Chin Med J (Engl) 113, 836-9 (2000).
10. Zhao, P. & Zuo, Z. Isoflurane preconditioning induces neuroprotection that is inducible nitric oxide synthase-dependent in neonatal rats. Anesthesiology 101, 695-703 (2004).
11. Kitano, H. et al. Gender-specific response to isoflurane preconditioning in focal cerebral ischemia. J Cereb Blood Flow Metab 27, 1377-86 (2007).
12. Li, L., Peng, L. & Zuo, Z. Isoflurane preconditioning increases B-cell lymphoma-2 expression and reduces cytochrome c release from the mitochondria in the ischemic penumbra of rat brain. Eur J Pharmacol 586, 106-13 (2008).
13. Xu, X., Kim, J. A. & Zuo, Z. Isoflurane preconditioning reduces mouse microglial activation and injury induced by lipopolysaccharide and interferon-gamma. Neuroscience 154, 1002-8 (2008).
14. Takeda, K. & Akira, S. Toll-like receptors in innate immunity. Int Immunol 17, 1-14 (2005).
15. Lehnardt, S. et al. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100, 8514-9 (2003).
16. Capiralla, H. et al. Resveratrol mitigates lipopolysaccharide- and Abeta-mediated microglial inflammation by inhibiting the TLR4/NF-kappaB/STAT signaling cascade. J Neurochem 120, 461-72 (2012).
17. Facci, L. et al. Toll-like receptors 2, -3 and -4 prime microglia but not astrocytes across central nervous system regions for ATPdependent interleukin-1beta release. Sci Rep 4, 6824 (2014).
18. Tanga, F. Y., Nutile-McMenemy, N. & DeLeo, J. A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci U S A 102, 5856-61 (2005).
19. Xiao, Z. et al. Protective role of isoflurane pretreatment in rats with focal cerebral ischemia and the underlying molecular mechanism. Mol Med Rep 12, 675-83 (2015).
20. Hyakkoku, K. et al. Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia. Neuroscience 171, 258-67 (2010).
21. Yao, L. et al. Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia. J Neuroinflammation 10, 23 (2013).
22. Wang, F. et al. Neuroprotective effect of acute ethanol administration in a rat with transient cerebral ischemia. Stroke 43, 205-10 (2012).
23. Zhao, Y. et al. Electroacupuncture pretreatment induces tolerance against focal cerebral ischemia through activation of canonical Notch pathway. BMC Neurosci 13, 111 (2012).
24. Rogers, D. C., Campbell, C. A., Stretton, J. L. & Mackay, K. B. Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 28, 2060-5; discussion 2066 (1997).
25. Swanson, R. A. et al. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10, 290-3 (1990).
26. Deng, B. et al. Neuroprotective effects of sevoflurane against electromagnetic pulse-induced brain injury through inhibition of neuronal oxidative stress and apoptosis. PLoS One 9, e91019 (2014).
27. Deng, B. et al. Targeted delivery of neurogenin-2 protein in the treatment for cerebral ischemia-reperfusion injury. Biomaterials 34, 8786-97 (2013).
28. Kaushal, V. & Schlichter, L. C. Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J Neurosci 28, 2221-30 (2008).
29. Tao, X. et al. Dioscin ameliorates cerebral ischemia/reperfusion injury through the downregulation of TLR4 signaling via HMGB-1 inhibition. Free Radic Biol Med doi: 10.1016/j.freeradbiomed.2015.03.003. [Epub ahead of print] (2015).
30. Zeng, Y. et al. Hyperbaric oxygen preconditioning protects cortical neurons against oxygen-glucose deprivation injury: role of peroxisome proliferator-activated receptor-gamma. Brain Res 1452, 140-50 (2012).
31. Kawamoto, T., Ii, M., Kitazaki, T., Iizawa, Y. & Kimura, H. TAK-242 selectively suppresses Toll-like receptor 4-signaling mediated by the intracellular domain. Eur J Pharmacol 584, 40-8 (2008).
32. Wang, X. Investigational anti-inflammatory agents for the treatment of ischaemic brain injury. Expert Opin Investig Drugs 14, 393-409 (2005).
33. Yilmaz, G. & Granger, D. N. Cell adhesion molecules and ischemic stroke. Neurol Res 30, 783-93 (2008).
34. Emsley, H. C. & Hopkins, S. J. Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol 7, 341-53 (2008).
35. McColl, B. W., Allan, S. M. & Rothwell, N. J. Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158, 1049-61 (2009).
36. Aloisi, F. Immune function of microglia. Glia 36, 165-79 (2001).
37. Nakajima, K. & Kohsaka, S. Microglia: activation and their significance in the central nervous system. J Biochem 130, 169-75 (2001).
38. Polazzi, E. & Monti, B. Microglia and neuroprotection: from in vitro studies to therapeutic applications. Prog Neurobiol 92, 293-315 (2010).
39. Tam, W. Y. & Ma, C. H. Bipolar/rod-shaped microglia are proliferating microglia with distinct M1/M2 phenotypes. Sci Rep 4, 7279 (2014).
40. Dean, J. M. et al. Microglial MyD88 signaling regulates acute neuronal toxicity of LPS-stimulated microglia in vitro. Brain Behav Immun 24, 776-83 (2010).
41. Tsan, M. F. & Gao, B. Endogenous ligands of Toll-like receptors. J Leukoc Biol 76, 514-9 (2004).
42. Li, Y. et al. Myocardial ischemia activates an injurious innate immune signaling via cardiac heat shock protein 60 and Toll-like receptor 4. J Biol Chem 286, 31308-19 (2011).
43. Lehnardt, S. et al. 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, 2320-31 (2008).
44. Zhang, Z., Chopp, M. & Powers, C. Temporal profile of microglial response following transient (2 h) middle cerebral artery occlusion. Brain Res 744, 189-98 (1997).
45. Wang, J. et al. Geniposide reduces inflammatory responses of oxygen-glucose deprived rat microglial cells via inhibition of the TLR4 signaling pathway. Neurochem Res 37, 2235-48 (2012).
46. An, G. Z. et al. [Effect of long-term power frequency electromagnetic field exposure on proliferation and apoptosis of SRA01/04 cells]. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 31, 246-50 (2013).
47. Marsh, B. J., Williams-Karnesky, R. L. & Stenzel-Poore, M. P. Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 158, 1007-20 (2009).
48. Brasil, L. J. et al. Halothane induces oxidative stress and NF-kappaB activation in rat liver: protective effect of propofol. Toxicology 227, 53-61 (2006).
49. Garcia-Mediavilla, V. et al. The anti-inflammatory flavones quercetin and kaempferol cause inhibition of inducible nitric oxide synthase, cyclooxygenase-2 and reactive C-protein, and down-regulation of the nuclear factor kappaB pathway in Chang Liver cells. Eur J Pharmacol 557, 221-9 (2007).
50. Nurmi, A. et al. Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke 35, 987-91 (2004).
51. Kaushal, V. & Schlichter, L. C. Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J Neurosci 28, 2221-30 (2008).
52. Astrup, J., Siesjo, B. K. & Symon, L. Thresholds in cerebral ischemia - the ischemic penumbra. Stroke 12, 723-5 (1981).
53. Zheng, S. & Zuo, Z. Isoflurane preconditioning induces neuroprotection against ischemia via activation of P38 mitogen-activated protein kinases. Mol Pharmacol 65, 1172-80 (2004).
54. Mazze, R. I., Rice, S. A. & Baden, J. M. Halothane, isoflurane, and enflurane MAC in pregnant and nonpregnant female and male mice and rats. Anesthesiology 62, 339-41 (1985).
55. Orliaguet, G. et al. Minimum alveolar concentration of volatile anesthetics in rats during postnatal maturation. Anesthesiology 95, 734-9 (2001).
56. Zheng, S. & Zuo, Z. Isoflurane preconditioning reduces purkinje cell death in an in vitro model of rat cerebellar ischemia. Neuroscience 118, 99-106 (2003).
57. Carpenter, R. L., Eger, E. N., Johnson, B. H., Unadkat, J. D. & Sheiner, L. B. The extent of metabolism of inhaled anesthetics in humans. Anesthesiology 65, 201-5 (1986).
58. Gwak, M. S., Cao, L., Li, L. & Zuo, Z. Isoflurane preconditioning reduces oxygen-glucose deprivation-induced neuronal injury via B-cell lymphoma 2 protein. Environ Toxicol Pharmacol 31, 262-5 (2011).
59. Cahill, J., Calvert, J. W. & Zhang, J. H. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 26, 1341-53 (2006).
60. Ferrer, I. & Planas, A. M. Signaling of cell death and cell survival following focal cerebral ischemia: life and death struggle in the penumbra. J Neuropathol Exp Neurol 62, 329-39 (2003).