Activation of p38 MAPK participates in brain ischemic tolerance induced by limb ischemic preconditioning by up-regulating HSP 70

Experimental Neurology

Volumn 224, Issue 2, 2010, Pages 347-355

  Sun, Xiao Cai ^a   Xian, Xiao Hui ^b   Li, Wen Bin ^a,b   Li, Li ^a   Yan, Cai Zhen ^a   Li, Qing Jun ^a   Zhang, Min ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

^b Brain Aging and Cognitive Neuroscience Laboratory of Hebei Province   (China)

Author keywords

Brain ischemic tolerance; Hippocampus; HSP 70; Limb ischemic preconditioning; P38 MAPK

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE P38; QUERCETIN; THIONINE;

ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; LIMB ISCHEMIA; MALE; NERVE CELL NECROSIS; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; DISEASE SUSCEPTIBILITY; ENZYME ACTIVATION; HINDLIMB; HSP70 HEAT-SHOCK PROTEINS; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; MALE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; QUERCETIN; RATS; RATS, WISTAR; UP-REGULATION;

EID: 77954658607     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.04.009     Document Type: Article

References (48)

1. Aoki M., Abe K., Kawagoe J., Nakamura S., Kogure K. Acceleration of HSP70 and HSC70 heat shock gene expression following transient ischemia in the preconditioned gerbil hippocampus. J. Cereb. Blood Flow Metab. 1993, 13:781-788.
2. Aoki M., Abe K., Kawagoe J., Nakamura S., Kogure K. The preconditioned hippocampus accelerates HSP70 heat shock gene expression following transient ischemia in the gerbil. Neurosci. Lett. 1993, 155:7-10.
3. Banerjee Mustafi S., Chakraborty P.K., Dey R.S., Raha S. Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperones 2009, 14:579-589.
4. Bedirli A., Kerem M., Pasaoglu H., Erdem O., Ofluoglu E., Sakrak O. Effects of ischemic preconditioning on regenerative capacity of hepatocyte in the ischemically damaged rat livers. J. Surg. Res. 2005, 125:42-48.
5. Blanquet P.R., Mariani J., Fournier B. Temporal assessment of histone H3 phospho-acetylation and casein kinase 2 activation in dentate gyrus from ischemic rats. Brain Res. 2009, 1302:10-20.
6. Cho J.Y., Kim I.S., Jang Y.H., Kim A.R., Lee S.R. Protective effect of quercetin, a natural flavonoid against neuronal damage after transient global cerebral ischemia. Neurosci. Lett. 2006, 404:330-335.
7. Escobedo I., Peraile I., Orio L., Colado M.I., O'Shea E. Evidence for a role of Hsp70 in the neuroprotection induced by heat shock pre-treatment against 3, 4-methylenedioxymethamphetamine toxicity in rat brain. J. Neurochem. 2007, 101:1272-1283.
8. Feinstein D.L., Galea E., Aquino D.A., Li G.C., Xu H., Reis D.J. Heat shock protein 70 suppresses astroglial-inducible nitric-oxide synthase expression by decreasing NFkappaB activation. J. Biol. Chem. 1996, 271:17724-17732.
9. Ge P.F., Luo T.F., Zhang J.Z., Chen D.W., Luan Y.X., Fu S.L. Ischemic preconditioning induces chaperone hsp70 expression and inhibits protein aggregation in the CA1 neurons of rats. Neurosci. Bull. 2008, 24:288-296.
10. Gho B.C., Schoemaker R.G., van den Doel M.A., Duncker D.J., Verdouw P.D. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 1996, 94:2193-2200.
11. Glantz L., Avramovich A., Trembovler V., Gurvitz V., Kohen R., Eidelman L.A., Shohami E. Ischemic preconditioning increases antioxidants in the brain and peripheral organs after cerebral ischemia. Exp. Neurol. 2005, 192:117-124.
12. Harkin D.W., Barros D'Sa A.A., McCallion K., Hoper M., Campbell F.C. Ischemic preconditioning before lower limb ischemia-reperfusion protects against acute lung injury. J. Vasc. Surg. 2002, 35:1264-1273.
13. Hung J.J., Cheng T.J., Lai Y.K., Chang M.D. Differential activation of p38 mitogen-activated protein kinase and extracellular signal-regulated protein kinases confers cadmium-induced HSP70 expression in 9L rat brain tumor cells. J. Biol. Chem. 1998, 273:31924-31931.
14. Kato H., Liu Y., Araki T., Kogure K. Temporal profile of the effects of pretreatment with brief cerebral ischemia on the neuronal damage following secondary ischemic insult in the gerbil: cumulative damage and protective effects. Brain Res. 1991, 553:238-242.
15. Kharbanda R.K., Mortensen U.M., White P.A., Kristiansen S.B., Schmidt M.R., Hoschtitzky J.A., Vogel M., Sorensen K., Redington A.N., MacAllister R. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 2002, 106:2881-2883.
16. Khomenko I.P., Bakhtina L.Y., Zelenina O.M., Kruglov S.V., Manukhina E.B., Bayda L.A., Malyshev I.Y. Role of heat shock proteins HSP70 and HSP32 in the protective effect of adaptation of cultured HT22 hippocampal cells to oxidative stress. Bull. Exp. Biol. Med. 2007, 144:174-177.
17. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K. 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 1990, 528:21-24.
18. Ko J.A., Yanai R., Quan W.Y., Morishige N., Nishida T. Up-regulation of HSP70 by the fibronectin-derived peptide PHSRN in human corneal epithelial cells. Biochem. Biophys. Res. Commun. 2008, 370:424-428.
19. Lennmyr F., Ericsson A., Gerwins P., Ahlström H., Terént A. Increased brain injury and vascular leakage after pretreatment with p38-inhibitor SB 203580 in transient ischemia. Acta Neurol. Scand. 2003, 108:339-345.
20. Lepore D.A., Morrison W.A. Ischemic preconditioning: lack of delayed protection against skeletal muscle ischemia-reperfusion. Microsurgery 2000, 20:350-355.
21. Magrané J., Rosen K.M., Smith R.C., Walsh K., Gouras G.K., Querfurth H.W. Intraneuronal beta-amyloid expression downregulates the Akt survival pathway and blunts the stress response. J. Neurosci. 2005, 25:10960-10969.
22. Maliutina IaV., Semina O.V., Semenets T.N., Budagova K.R., Shinkarkina A.P., Kabakov A.E., Poverennyi A.M. The protective effect of thermal treatment before irradiation on CFUs from bone marrow of mice: a potential involvement of heat shock proteins. Radiats. Biol. Radioecol. 2001, 41:153-156.
23. Matsumori Y., Northington F.J., Hong S.M., Kayama T., Sheldon R.A., Vexler Z.S., Ferriero D.M., Weinstein P.R., Liu J. Reduction of caspase-8 and -9 cleavage is associated with increased c-FLIP and increased binding of Apaf-1 and Hsp70 after neonatal hypoxic/ischemic injury in mice overexpressing Hsp70. Stroke 2006, 37:507-512.
24. Nakata N., Kato H., Kogure K. Inhibition of ischaemic tolerance in the gerbil hippocampus by quercetin and anti-heat shock protein-70 antibody. Neuroreport 1993, 4:695-698.
25. Nishimura M., Sugino T., Nozaki K., Takagi Y., Hattori I., Hayashi J., Hashimoto N., Moriguchi T., Nishida E. Activation of p38 kinase in the gerbil hippocampus showing ischemic tolerance. J. Cereb. Blood Flow Metab. 2003, 23:1052-1059.
26. Nowak T.S. Localization of 70kDa stress protein mRNA induction in gerbil brain after ischemia. J. Cereb. Blood Flow Metab. 1991, 11:432-439.
27. Ozawa H., Shioda S., Dohi K., Matsumoto H., Mizushima H., Zhou C.J., Funahashi H., Nakai Y., Nakajo S., Matsumoto K. Delayed neuronal cell death in the rat hippocampus is mediated by the mitogen-activated protein kinase signal transduction pathway. Neurosci. Lett. 1999, 262:57-60.
28. Padmini E., Usha Rani M. Impact of seasonal variation on HSP70 expression quantitated in stressed fish hepatocytes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151:278-285.
29. Pan T., Li X., Xie W., Jankovic J., Le W. Valproic acid-mediated Hsp70 induction and anti-apoptotic neuroprotection in SH-SY5Y cells. FEBS Lett. 2005, 579:6716-6720.
30. Park K.M., Chen A., Bonventre J.V. Prevention of kidney ischemia/ reperfusion-induced functional injury and JNK, p38, and MAPK kinase activation by remote ischemic pretreatment. J. Biol. Chem. 2001, 276:11870-11876.
31. Pulsinelli W.A., Brierley J.B. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 1979, 10:267-272.
32. Rafiee P., Theriot M.E., Nelson V.M., Heidemann J., Kanaa Y., Horowitz S.A., Rogaczewski A., Johnson C.P., Ali I., Shaker R., Binion D.G. Human esophageal microvascular endothelial cells respond to acidic pH stress by PI3K/AKT and p38 MAPK-regulated induction of Hsp70 and Hsp27. Am. J. Physiol. Cell Physiol. 2006, 291:C931-C945.
33. Ravagnan L., Gurbuxani S., Susin S.A., Maisse C., Daugas E., Zamzami N., Mak T., Jäättelä M., Penninger J.M., Garrido C., Kroemer G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol. 2001, 3:839-843.
34. Rehman H., Connor H.D., Ramshesh V.K., Theruvath T.P., Mason R.P., Wright G.L., Lemasters J.J., Zhong Z. Ischemic preconditioning prevents free radical production and mitochondrial depolarization in small-for-size rat liver grafts. Transplantation 2008, 85:1322-1331.
35. Roberts G.G., Di Loreto M.J., Marshall M., Wang J., DeGracia D.J. Hippocampal cellular stress responses after global brain ischemia and reperfusion. Antioxid. Redox Signal. 2007, 9:2265-2275.
36. Sato M., Cordis G.A., Maulik N., Das D.K. SAPKs regulation of ischemic preconditioning. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H901-H907.
37. Saxena P., Bala A., Campbell K., Meloni B., d'Udekem Y., Konstantinov I.E. Does remote ischemic preconditioning prevent delayed hippocampal neuronal death following transient global cerebral ischemia in rats?. Perfusion 2009, 24:207-211.
38. Simon R.P., Cho H., Gwinn R., Lowenstein D.H. The temporal profile of 72-kDa heat-shock protein expression following global ischemia. J. Neurosci. 1991, 11:881-889.
39. Sun Y., Jin K., Peel A., Mao X.O., Xie L., Greenberg D.A. Neuroglobin protects the brain from experimental stroke in vivo. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3497-3500.
40. Sun X.C., Li W.B., Li Q.J., Zhang M., Xian X.H., Qi J., Jin R.L. Limb ischemic preconditioning induces brain ischemic tolerance via p38 MAPK. Brain Res. 2006, 1084:165-174.
41. Takaoka A., Nakae I., Mitsunami K., Yabe T., Morikawa S., Inubushi T., Kinoshita M. Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of "remote preconditioning". J. Am. Coll. Cardiol. 1999, 33:556-564.
42. Uehara T., Kaneko M., Tanaka S., Okuma Y., Nomura Y. Possible involvement of p38 MAP kinase in HSP70 expression induced by hypoxia in rat primary astrocytes. Brain Res. 1999, 823:226-230.
43. Vass K., Welch W.J., Nowak T.S. Localization of 70-kDa stress protein induction in gerbil brain after ischemia. Acta Neuropathol. (Berl). 1988, 77:128-135.
44. Wu D.C., Ye W., Che X.M., Yang G.Y. Activation of mitogen-activated protein kinases after permanent cerebral artery occlusion in mouse brain. J. Cereb. Blood Flow Metab. 2000, 20:1320-1330.
45. Yagita Y., Kitagawa K., Ohtsuki T., Tanaka S., Hori M., Matsumoto M. Induction of the HSP110/105 family in the rat hippocampus in cerebral ischemia and ischemic tolerance. J. Cereb. Blood Flow Metab. 2001, 21:811-819.
46. Zhang M., Li W.B., Geng J.X., Li Q.J., Sun X.C., Xian X.H., Qi J., Li S.Q. The upregulation of glial glutamate transporter-1 participates in the induction of brain ischemic tolerance in rats. J. Cereb. Blood Flow Metab. 2007, 27:1352-1368.
47. Zhao H.G., Li W.B., Liu H.Q., Feng R.F., Li Q.J., Chen X.L., Zhou A.M., Ai J. Limb ischemic preconditioning decreases cerebral ischemia-reperfusion injuries in rats. Chin. J. Appl. Physiol. 2004, 29:50-53.
48. Zhao H.G., Sun X.C., Xian X.H., Li W.B., Zhang M., Li Q.J. The role of nitric oxide in the neuroprotection of limb ischemic preconditioning in rats. Neurochem. Res. 2007, 32:1919-1926.