Exercise Preconditioning Regulates the Toll-Like Receptor 4/Nuclear Factor-κB Signaling Pathway and Reduces Cerebral Ischemia/Reperfusion Inflammatory Injury: A Study in Rats

Journal of Stroke and Cerebrovascular Diseases

Volumn 25, Issue 11, 2016, Pages 2770-2779

  Zhu, Luwen ^a   Ye, Tao ^a   Tang, Qiang ^a   Wang, Yan ^a   Wu, Xiaojun ^a   Li, Hongyu ^a   Jiang, Yunfei ^a  

^a HEILONGJIANG UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

cerebral ischemia reperfusion; Exercise preconditioning; inflammatory response; TLR4 NF B signaling pathway

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; AUTACOID; IL1B PROTEIN, RAT; TLR4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BRAIN ISCHEMIA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXERCISE; EXERCISE PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; SHAM PROCEDURE; SIGNAL TRANSDUCTION; TRANSIENT MIDDLE CEREBRAL ARTERY OCCLUSION; TREADMILL EXERCISE; ANIMAL; ANIMAL BEHAVIOR; BLOOD; BRAIN CORTEX; DISEASE MODEL; INFARCTION, MIDDLE CEREBRAL ARTERY; KINESIOTHERAPY; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; RUNNING; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EXERCISE THERAPY; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; MALE; MOTOR ACTIVITY; NF-KAPPA B; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RUNNING; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84994076471     PISSN: 10523057     EISSN: 15328511     Source Type: Journal    
DOI: 10.1016/j.jstrokecerebrovasdis.2016.07.033     Document Type: Article

References (42)

1. 1 Meschia, J.F., Bushnell, C., Boden-Albala, B., et al. Guidelines for the primary prevention of stroke: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 45 (2014), 3754–3832.
2. 2 Murray, C.J., Lopez, A.D., Measuring the global burden of disease. N Engl J Med 369 (2013), 448–457.
3. 3 Lansberg, M.G., Bluhmki, E., Thijs, V.N., Efficacy and safety of tissue plasminogen activator 3 to 4.5 hours after acute ischemic stroke: a meta-analysis. Stroke 40 (2009), 2438–2441.
4. 4 Ansar, S., Chatzikonstantinou, E., Thiagarajah, R., et al. Pro-inflammatory mediators and apoptosis correlate to rt-PA response in a novel mouse model of thromboembolic stroke. PLoS ONE, 9, 2014 e85849.
5. 5 Stetler, R.A., Leak, R.K., Gan, Y., et al. Preconditioning provides neuroprotection in models of CNS disease: paradigms and clinical significance. Prog Neurobiol 114 (2014), 58–83.
6. 6 Ang, E., Wong, P., Moochhala, S., et al. Neuroprotection associated with running: is it a result of increased endogenous neurotrophic factors?. Neuroscience 118 (2003), 335–345.
7. 7 Endres, M., Gertz, K., Lindauer, U., et al. Mechanisms of stroke protection by physical activity. Ann Neurol 54 (2003), 582–590.
8. 8 Li, J., Luan, X., Clark, J.C., et al. Neuroprotection against transient cerebral ischemia by exercise pre-conditioning in rats. Neurol Res 26 (2004), 404–408.
9. 9 Ding, Y.H., Ding, Y.C., Li, J., et al. Exercise pre-conditioning strengthens brain microvascular integrity in a rat stroke model. Neurol Res 28 (2006), 184–189.
10. 10 Tahamtan, M., Allahtavakoli, M., Abbasnejad, M., et al. Exercise preconditioning improves behavioral functions following transient cerebral ischemia induced by 4-vessel occlusion (4-VO) in rats. Arch Iran Med 16 (2013), 697–704.
11. 11 Zhang, L., Hu, X., Luo, J., et al. Physical exercise improves functional recovery through mitigation of autophagy, attenuation of apoptosis and enhancement of neurogenesis after MCAO in rats. BMC Neurosci, 14, 2013, 46.
12. 12 Yang, X., He, Z., Zhang, Q., et al. Pre-ischemic treadmill training for prevention of ischemic brain injury via regulation of glutamate and its transporter GLT-1. Int J Mol Sci 13 (2012), 9447–9459.
13. 13 Wang, X., Zhang, M., Yang, S.D., et al. Pre-ischemic treadmill training alleviates brain damage via GLT-1-mediated signal pathway after ischemic stroke in rats. Neuroscience 274 (2014), 393–402.
14. 14 Ding, Y.H., Mrizek, M., Wu, Y.M., Exercise preconditioning ameliorates brain inflammatory injury via TNF signaling pathway. Stroke, 37, 2006, 730.
15. 15 Guo, M., Lin, V., Davis, W., et al. Preischemic induction of TNF-alpha by physical exercise reduces blood-brain barrier dysfunction in stroke. J Cereb Blood Flow Metab 28 (2008), 1422–1430.
16. 16 Patel, F.J., Volkmann, D.T., Taylor, G.W., et al. IL-37 reduces inflammatory response after cerebral ischemia and reperfusion injury through down-regulation of pro-inflammatory cytokines. Cytokine 69 (2014), 234–239.
17. 17 Chen, S., Yin, Z.-J., Jiang, C., et al. Asiaticoside attenuates memory impairment induced by transient cerebral ischemia–reperfusion in mice through anti-inflammatory mechanism. Pharmacol Biochem Behav 122 (2014), 7–15.
18. 18 Chen, B., Liao, W.-Q., Xu, N., et al. Adiponectin protects against cerebral ischemia–reperfusion injury through anti-inflammatory action. Brain Res 1273 (2009), 129–137.
19. 19 Akira, S., Takeda, K., Toll-like receptor signaling. Nat Rev Immunol 4 (2004), 499–511.
20. 20 Yang, Q.W., Lu, F.L., Zhou, Y., et al. HMBG1 mediates ischemia-reperfusion injury by TRIF-adaptor independent Toll-like receptor 4 signaling. J Cereb Blood Flow Metab 31 (2011), 593–605.
21. 21 Brea, D., Blanco, M., Ramos-Cabrer, P., et al. Toll-like receptors 2 and 4 in ischemic stroke: outcome and therapeutic values. J Cereb Blood Flow Metab 31 (2011), 1424–1431.
22. 22 Wang, Y.C., Lin, S., Yang, Q.W., Toll-like receptors in cerebral ischemic inflammatory injury. J Neuroinflammation, 8, 2011, 134.
23. 23 Georgel, P., Jiang, Z., Kunz, S., et al. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362 (2007), 304–313.
24. 24 Gao, Y., Fang, X., Sun, H., et al. Toll-like receptor 4-mediated myeloid differentiation factor 88-dependent signaling pathway is activated by cerebral ischemia-reperfusion in hippocampal CA1 region in mice. Biol Pharm Bull 32 (2009), 1665–1671.
25. 25 Ding, Y., Li, J., Luan, X., et al. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 124 (2004), 583–591.
26. 26 Ding, Y.H., Li, J., Yao, W.X., et al. Exercise preconditioning upregulates cerebral integrins and enhances cerebrovascular integrity in ischemic rats. Acta Neuropathol 112 (2006), 74–84.
27. 27 Longa, E.Z., Weinstein, P.R., Carlson, S., et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20 (1989), 84–91.
28. 28 Bederson, J.B., Pitts, L.H., Germano, S.M., et al. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17 (1986), 1304–1308.
29. 29 Zhou, F., Guo, J., Cheng, J., et al. Electroacupuncture increased cerebral blood flow and reduced ischemic brain injury: dependence on stimulation intensity and frequency. J Appl Physiol 111 (2011), 1877–1887.
30. 30 Guo, M., Cox, B., Mahale, S., et al. Pre-ischemic exercise reduces matrix metalloproteinase-9 expression and ameliorates blood-brain barrier dysfunction in stroke. Neuroscience 151 (2008), 340–351.
31. 31 Dornbos, D. 3rd, Zwagerman, N., Guo, M., et al. Preischemic exercise reduces brain damage by ameliorating metabolic disorder in ischemia/reperfusion injury. J Neurosci Res 91 (2013), 818–827.
32. 32 Zhang, Q., Zhang, L., Yang, X., et al. The effects of exercise preconditioning on cerebral blood flow change and endothelin-1 expression after cerebral ischemia in rats. J Stroke Cerebrovasc Dis 23 (2014), 1696–1702.
33. 33 Feng, R., Zhang, M., Wang, X., et al. Pre-ischemic exercise alleviates oxidative damage following ischemic stroke in rats. Exp Ther Med 8 (2014), 1325–1329.
34. 34 Wang, X., Zhang, M., Feng, R., et al. Exercise pre-conditioning alleviates brain damage via excitatory amino acid transporter 2 and extracellular signal-regulated kinase 1/2 following ischemic stroke in rats. Mol Med Rep 11 (2015), 1523–1527.
35. 35 Zhang, L., Niu, W., He, Z., et al. Autophagy suppression by exercise pretreatment and p38 inhibition is neuroprotective in cerebral ischemia. Brain Res 1587 (2014), 127–132.
36. 36 Wang, Q., Tang, X.N., Yenari, M.A., The inflammatory response in stroke. J Neuroimmunol 184 (2007), 53–68.
37. 37 Amantea, D., Certo, M., Russo, R., et al. Early reperfusion injury is associated to MMP2 and IL-1β elevation in cortical neurons of rats subjected to middle cerebral artery occlusion. Neuroscience 277 (2014), 755–763.
38. 38 Tuttolomondo, A., Di Raimondo, D., di Sciacca, R., et al. Inflammatory cytokines in acute ischemic stroke. Curr Pharm Des 14 (2008), 3574–3589.
39. 39 Arslan, F., Keogh, B., McGuirk, P., et al. TLR2 and TLR4 in ischemia reperfusion injury. Mediators Inflamm, 2010, 2010, 704202.
40. 40 Liu, H.S., Zhang, Y.L., Liu, X.M., Formation and actions of endogenetic toxins from dynamic changes of inflammatory factors of local cerebral ischemia reperfusion. J Beijing Univ Tradit Chin Med 4 (2007), 246–248.
41. 41 Zhao, M., Zhou, A., Xu, L., et al. The role of TLR4-mediated PTEN/PI3K/AKT/NF-κB signaling pathway in neuroinflammation in hippocampal neurons. Neuroscience 269 (2014), 93–101.
42. 42 Lan, L., Tao, J., Chen, A., et al. Electroacupuncture exerts anti-inflammatory effects in cerebral ischemia-reperfusion injured rats via suppression of the TLR4/NF-kappaB pathway. Int J Mol Med 31 (2013), 75–80.