Neuroprotection by local intra-arterial infusion of erythropoietin after focal cerebral ischemia in rats

Neurological Research

Volumn 33, Issue 5, 2011, Pages 520-528

  Dang, Sha ^a,c   Liu, Xiangrong ^a,c   Fu, Paul ^d   Gong, Wei ^a,c   Yan, Feng ^a,c   Han, Pingxin ^a,c   Ding, Yuchuan ^d   Ji, Xunming ^a,b   Luo, Yumin ^c  

^a Cerebrovascular Diseases Research Institute   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Erythropoietin; Ischemia; Neuroprotection; Reperfusion

Indexed keywords

ERYTHROPOIETIN; MITOGEN ACTIVATED PROTEIN KINASE; VASCULOTROPIN;

APOPTOSIS; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG MECHANISM; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NICK END LABELING; NONHUMAN; RAT; REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; INFARCTION, MIDDLE CEREBRAL ARTERY; INFUSIONS, INTRA-ARTERIAL; MALE; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY;

EID: 79958726940     PISSN: 01616412     EISSN: None     Source Type: Journal    
DOI: 10.1179/016164111X13007856084287     Document Type: Article

References (43)

1. Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 1999;19: 643-51.
2. Malhotra S, Savitz SI, Ocava L, Rosenbaum DM. Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack. J Neurosci Res 2006;83:19-27.
3. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 2000;97:10526-31.
4. Sirèn AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 2001;98:4044-9.
5. Konishi Y, Chui DH, Hirose H, Kunishita T, Tabira T. Trophic effect of erythropoietin and other hematopoietic factors on central cholinergic neurons in vitro and in vivo. Brain Res 1993;609:29-35.
6. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek, L, Lewczuk, P, Stiefel et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 2002;8:495-505.
7. Casadevall N, Nataf J, Viron B, Kolta A, Kiladjian JJ, Martin- Dupont P, et al. Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin. N Engl J Med 2002;346:469-75.
8. Erbayraktar S, Grasso G, Sfacteria A, Xie QW, Coleman T, Kreilgaard M, et al. Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo. Proc Natl Acad Sci USA 2003;100:6741-6.
9. Haiden N, Klebermass K, Cardona F, Schwindt J, Berger A, Kohlhauser-Vollmuth C, et al. A randomized controlled trial of the effects of adding vitamin B12 and folate to erythropoietin for the treatment of anemia of prematurity. Pediactrics 2006;118:180-8.
10. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989;20:84-91.
11. Ding Y, Li J, Rafols JA, Phillis JW, Diaz FG. Prereperfusion saline infusion into ischemic territory reduces inflammatory injury after transient middle cerebral artery occlusion in rats. Stroke 2002;33:2492-8.
12. Belayev L, Alonso OF, Busto R, Zhao W, Ginsberg MD. Middle cerebral artery occlusion in the rat by intraluminal suture. Stroke 1996;27:1616-23.
13. Ding Y, Zhou Y, Lai Q, Li J, Park H, Diaz FG. Impaired motor activity and motor learning function in rat with middle cerebral artery occlusion. Behav Brain Res 2002;132:29-36.
14. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 1990;10:290-3.
15. Vosler PS, Chen J. Potential molecular targets for translationalstroke research. Stroke 2009;40:S119-20.
16. Kooij MA, Groenendaal F, Kavelaars A, Heijnen CJ, van Bel F. Neuroprotective properties and mechanisms of erythropoietin in vitro and in vivo experimental models for hypoxia/ ischemia. Brain Res Rev 2008;59:22-33.
17. Matsushita H, Johnston MV, Lange MS, Wilson MA. Protective effect of erythropoietin in neonatal hypoxic ischemia in mice. Neuroreport 2003;14:1757-61.
18. Sun Y, Zhou C, Polk P, Nanda A, Zhang JH. Mechanisms of erythropoietin-induced brain protection in neonatal hypoxia-ischemia rat model. J Cereb Blood Flow Metab 2004;24:259-70.
19. Spandou E, Papadopoulou Z, Soubasi V, Karkavelas G, Simeonidou C, Pazaiti A, et al. Erythropoietin prevents long-term sensorimotor deficits and brain injury following neonatal hypoxia-ischemia in rats. Brain Res 2005;1045:22-30.
20. McClure MM, Threlkeld SW, Fitch RH. Auditory processing and learning/memory following erythropoietin administration in neonatally hypoxic-ischemic injured rats. Brain Res 2007;1132:203-9.
21. Kumral A, Uysal N, Tugyan K, Sonmez A, Yilmaz O, Gokmen N, et al. Erythropoietin improves long-term spatial memory deficits and brain. Behav Brain Res 2004;153:77-86.
22. Spandou E, Papadopoulou Z, Soubasi V, Karkavelas G, Simeonidou C, Pazaiti A, et al. Erythropoietin prevents long-termsensorimotor deficits and brain injury following neonatal hypoxia-ischemia in rats. Brain Res 2005;1045:22-30.
23. Kellert BA, Ronald J. A comparison of high-dose recombinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr Res 2007;61:451-5.
24. Sola A, Rogido M, Lee BH, Genetta T, Wen TC. Erythropoietin after focal cerebral ischemia activates the Janus kinase-signal transducer and activator of transcription signaling pathway and improves brain injury in postnatal day 7 rats. Pediatr Res 2005;57:481-7.
25. Wei L, Han BH, Li Y, Keogh CL, Holtzman DM, Yu SP. Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats. J Pharmacol Exp Ther 2006;317:109-16.
26. Wen TC, Rogido M, Peng H, Genetta T, Moore J, Sola A. Gender differences in long-term beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience 2006;139:803-11.
27. Gonzalez FF, McQuillen P, Mu D, Chang Y, Wendland M, Vexler Z, et al. Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev Neurosci 2007;29:321-30.
28. Bahcekapili N, Üzüm G, Gökkusu C, Kuru A, Ziylan YZ. The relationship between erythropoietin pretreatment with blood-brain barrier and lipid peroxidation after ischemia/reperfusion in rats. Life Sci 2007;80:1245-1.
29. Zhang F, Wang S, Cao G, Gao Y, Chen J. Signal transducers and activators of transcription 5 contributes to erythropoietinmediated neuroprotection against hippocampal neuronal death after transient global cerebral ischemia. Neurobiol Dis 2007;25:45-53.
30. Ding Y, Li J, Luan X, Lai Q, McAllister JP 2nd, Phillis JW, et al. Local saline infusion into ischemic territory induces regional brain cooling and neuroprotection in rats with transient middle cerebral artery occlusion. Neurosurgery 2004;54:956-65.
31. Woitzik J, Schilling L. A new method for superselective middle cerebral artery infusion in the rat. J Neurosurg 2007;106:872-8.
32. Green AR, Shuaib A. Therapeutic strategies for the treatment of stroke. Drug Discov Today 2006;11:681-93.
33. Lees KR, Zivin JA, Ashwood T, Davalos A, Davis SM, Diener HC, et al. NXY-057 for acute ischemic stroke. N Engl J Med 2006;354:588-600.
34. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, et al. Nxy-059 for the treatment of acute ischemic stroke. N Engl J Med 2007;357:562-71.
35. Enlimomab Acute Stroke Trial Investigators. Use of anti- ICAM-1 therapy in ischemic stroke: results of the Enlimomab Acute Stroke Trial. Neurology 2001;57:1428-34.
36. Ginsberg MD. Current status of neuroprotection for cerebral ischemia: synoptic overview. Stroke 2009;40:S111-4.
37. Ferrer I, Friguls B, Dalfo E, Planas AM. Early modifications in the expression of mitogen-activated protein kinase (MAPK/ ERK), stress-activated kinases SAPK/JNK and p38, and their phosphorylated substrates following focal cerebral ischemia. Acta Neuropathol (Berl) 2003;105:425-37.
38. Irving EA, Barone FC, Reith AD, Hadingham SJ, Parsons AA. Differential activation of MAPK/ERK and p38/SAPK in neurons and glia following focal cerebral ischaemia in the rat. Brain Res Mol Brain Res 2000;77:65-75.
39. Gu Z, Jiang Q, Zhang G. Extracellular signal-regulated kinase 1/2 activation in hippocampus after cerebral ischemia may not interfere with postischemic cell death. Brain Res 2001;901:79-84.
40. Zablocka B, Dluzniewska J, Zajac H, Domanska-Janik K. Opposite reaction of ERK and JNK in ischemia vulnerable and resistant regions of hippocampus: involvement of mitochondria. Brain Res Mol Brain Res 2003;110:245-52.
41. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 2005;19:2026-8.
42. Li Y, Lu Z, Keogh CL, Yu SP, Wei L. Erythropoietin-induced neurovascular protection, angiogenesis, and cerebral blood flow restoration after focal ischemia in mice. J Cereb Blood Flow Metab 2007;27:1043-54.
43. Hayashi T, Noshita N, Sugawara T, Chan PH. Temporal profile of angiogenesis and expression of related genes in the brain after ischemia. J Cereb Blood Flow Metab 2003;23:166-80.