Neuroprotective effects of ultra-low-molecular-weight heparin on cerebral ischemia/reperfusion injury in rats: Involvement of apoptosis, inflammatory reaction and energy metabolism

International Journal of Molecular Sciences

Volumn 14, Issue 1, 2013, Pages 1932-1939

  Zhang, Zhi Guo ^a   Sun, Xin ^a   Zhang, Qing Zhu ^b   Yang, Hua ^c  

^a Department of Pharmacy The 88th Hospital of PLA ^*  (China)

^b SHANDONG UNIVERSITY   (China)

^c SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Energy metabolism; Inflammatory reaction; Middle cerebral artery occlusion (MCAO); Ultra low molecular weight heparin (ULMWH)

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CASPASE 3; HEPARIN DERIVATIVE; INTERCELLULAR ADHESION MOLECULE 1; LACTIC ACID; LOW MOLECULAR WEIGHT HEPARIN; MESSENGER RNA; ULTRA LOW MOLECULAR WEIGHT HEPARIN; UNCLASSIFIED DRUG; FIBRINOLYTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG DOSE COMPARISON; ENERGY METABOLISM; GENE EXPRESSION; HIPPOCAMPUS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; RAT; SPECTROPHOTOMETRY; ANIMAL; BRAIN DISEASES; DRUG EFFECTS; INFLAMMATION; METABOLISM; PATHOLOGY; REPERFUSION INJURY; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; APOPTOSIS; BRAIN DISEASES; ENERGY METABOLISM; FIBRINOLYTIC AGENTS; HEPARIN, LOW-MOLECULAR-WEIGHT; INFLAMMATION; MALE; RATS; RATS, WISTAR; REPERFUSION INJURY;

EID: 84878637310     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14011932     Document Type: Article

References (23)

1. Kao, T.K.; Qu, Y.C.; Kuo, J.S.; Chen, W.Y.; Liao, S.L.; Wu, C.W.; Chen, C.J.; Ling, N.N.; Zhang, Y.H.; Peng, W.H. Neuroprotection by tetramethylpyrazine against ischemic brain injury in rats. Neurochem. Int. 2006, 48, 166-176.
2. Hao, L.N.; Zhang, Q.Z.; Yu, T.G.; Cheng, Y.N.; Ji, S.L. Antagonistic effects of ultra-low-molecular-weight heparin on Aβ25-35-induced apoptosis in cultured rat cortical neurons. Brain Res. 2011, 1368, 1-10.
3. Yu, T.G.; Zhang, Q.Z.; Zhang, Z.G.; Wang, W.W.; Ji, S.L.; Du, G.H. Protective Effect of Ultra Low Molecular Weight Heparin on Glutamate-Induced Apoptosis in Cortical Cells. Yonsei Med. J. 2008, 49, 486-495.
4. Zhang, Z.G.; Zhang, Q.Z.; Cheng, Y.N.; Ji, S.L.; Du, G.H. Antagonistic effects of Ultra-Low-Molecular-Weight Heparin against cerebral ischemia/reperfusion injury in rats. Pharmacol. Res. 2007, 56, 350-355.
5. Tian, J.W.; Fu, F.H.; Geng, M.Y.; Jiang, Y.T.; Yang, J.X.; Jiang, W.; Wang, C.; Liu, K. Neuroprotective effect of 20(S)-ginsenoside Rg3 on cerebral ischemia in rats. Neurosci. Lett. 2005, 374, 92-97.
6. Yue, F.; Zhang, W.; Guo, J. The alterations of brain lactate, lactate dehydrogenase, creatine phosphokinase and its influence on these of peripheral blood or liver tissue and entero-barrier during brain hypoperfusion. Chin. J. Pathophysiol. 1999, 15, 1106-1119.
7. Hoxworth, J.M.; Xu, K.; Zhou, Y.; Lust, W.D.; LaManna, J.C. Cerebral metabolic profile, selective neuron loss, and survival of acute and chronic hyperglycemic rats following cardiac arrest and resuscitation. Brain Res. 1999, 821, 467-479.
8. Kirino, T. Delayed neuronal death. Neuropathology 2000, 20, S95-S97.
9. Zhang, W.R.; Hayashi, T.; Sasaki, C.; Sato, K.; Nagano, I. Attenuation of oxidative DNA damage with a novel antioxidant EPC-K1 in rat brain neuronal cells after transient middle cerebral artery occlusion. Neurol. Res. 2001, 23, 676-680.
10. Khan, M.; Sekhon, B.; Jatana, M.; Giri, S.; Gilg, A.G. Administration of N-acetylcysteine after focal cerebral ischemia protects brain and reduces inflammation in a rat model of experimental stroke. J. Neurosci. Res. 2004, 76, 519-527.
11. Yamada, A.; Isono, M.; Hori, S.; Shimomura, T.; Nakano, T. Temporal and spatial profile of apoptotic cells after focal cerebral ischemia in rats. Neurol. Med. Chir. 1999, 39, 575-583.
12. Hu, X.; Johansson, I.M.; Brannstrom, T.; Olsson, T.; Wester, P. Long-lasting neuronal apoptotic cell death in regions with severe ischemia after photothrombotic ring stroke in rats. Acta Neuropathol. 2002, 104, 462-470.
13. Jean, W.C.; Spellman, S.R.; Nussbaum, E.S.; Low, W.C. Reperfusion injury after focal cerebral ischemia: role of inflammation and the therapeutic horizon. Neurosurgery 1998, 43, 1382-1397.
14. Liu, S.J.; Zhou, S.W.; Xue, C.S. Effect of tetrandrine on neutrophilic recruitment response to brain ischemia/reperfusion. Acta Pharmacol. Sin. 2001, 22, 971-975.
15. Bowes, M.P.; Zivin, J.A.; Rothlein, R. Monoclonal antibody to the ICAM-1 adhesion site reduces neurological damage in a rabbit cerebral embolism stroke model. Exp. Neurol. 1993, 119, 215-219.
16. Chopp, M.; Li, Y.; Jiang, N.; Zhang, R.L.; Prostak, J. Antibodies against adhesion molecules reduce apoptosis after transient middle cerebral artery occlusion in rat brain. J. Cereb. Blood Flow Metab. 1996, 16, 578-584.
17. Kanemoto, Y.; Nakase, H.; Akita, N.; Sakaki, T. Effects of antiintercellular adhesion molecule-1 antibody on reperfusion injury induced by late reperfusion in the rat middle cerebral artery occlusion model. Neurosurgery 2002, 51, 1034-1041.
18. Vemuganti, R.; Dempsey, R.J.; Bowen, K.K. Inhibition of intercellular adhesion molecule-1 protein expression by antisense oligonucleotides is neuroprotective after transient middle cerebral artery occlusion in rat. Stroke 2004, 35, 179-184.
19. Connolly, E.S., Jr.; Winfree, C.J.; Springer, T.A.; Naka, Y.; Liao, H. Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J. Clin. Invest. 1996, 97, 209-216.
20. Kitagawa, K.; Matsumoto, M.; Mabuchi, T.; Yagita, Y.; Ohtsuki, T. Deficiency of intercellular adhesion molecule 1 attenuates microcirculatory disturbance and infarction size in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1998, 18, 1336-1345.
21. Wu, G.D.; Zhou, H.J.; Wu, X.H. Apoptosis of human umbilical vein endothelial cells induced by artesunate. Vascul. Pharmacol. 2004, 41, 205-212.
22. Chen, P.; Scicli, G.M.; Guo, M.; Fenstermacher, J.D.; Dahl, D.; Edwards, P.A.; Scicli, A.G. Role of angiotensin II in retinal leukostasis in the diabetic rat. Exp. Eye Res. 2006, 83, 1041-1051.
23. Shimamura, M.; Garcia, J.M.; Prough, D.S.; Dewitt, D.S.; Uchida, T.; Shah, S.A.; Avila, M.A.; Hellmich, H.L. Analysis of long-term gene expression in neurons of the hippocampal subfields following traumatic brain injury in rats. Neuroscience 2005, 131, 87-97.