Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack

Journal of Neuroscience Research

Volumn 83, Issue 1, 2006, Pages 19-27

  Malhotra, Samit ^a   Savitz, Sean I ^b   Ocava, Lenore ^a   Rosenbaum, Daniel M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Erythropoietin; Ischemic preconditioning; Neuroprotection; PI 3 kinase

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHATIDYLINOSITOL KINASE; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN REGION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; HEMISPHERE; ISCHEMIC PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; REPERFUSION; SIGNAL TRANSDUCTION; TRANSIENT ISCHEMIC ATTACK;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ENZYME INHIBITORS; ERYTHROPOIETIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; ISCHEMIC ATTACK, TRANSIENT; ISCHEMIC PRECONDITIONING; MALE; RATS; RATS, WISTAR; RECEPTORS, ERYTHROPOIETIN; SIGNAL TRANSDUCTION;

EID: 30344448865     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20705     Document Type: Article

References (37)

1. Alkayed NJ, Goyagi T, Joh HD, Klaus J, Harder DR, Traystman RJ, Hum PD. 2002. Neuroprotection and P450 2C11 upregulation after experimental transient ischemic attack. Stroke 33:1677-1684.
2. Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, Feuerstein GZ. 1998. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29:1937-1950 [discussion 1950-1951].
3. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. 1986. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17:472-476.
4. Bergeron M, Yu AY, Solway KE, Semenza GL, Sharp FR. 1999. Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain. Eur J Neurosci 11:4159-4170.
5. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR. 2000. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 48:285-296.
6. Bernaudin M, Bellail A, Marti HH, Yvon A, Vivien D, Duchatelle I, Mackenzie ET, Petit E. 2000. Neurons and astrocytes express EPO mRNA: oxygen-sensing mechanisms that involve the redox-state of the brain. Glia 30:271-278.
7. Bernaudin M, Nedelec AS, Divoux D, MacKenzie ET, Petit E, Schumann-Bard P. 2002a. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J Cereb Blood Flow Metab 22:393-403.
8. Bernaudin M, Tang Y, Reilly M, Petit E, Sharp FR. 2002b. Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J Biol Chem 277:39728-39738.
9. Blondeau N, Widmann C, Lazdunski M, Heurteaux C. 2001. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J Neurosci 21:4668-4677.
10. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, Itri LM, Cerami A. 2000. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci U S A 97:10526-10531.
11. Cardenas A, Moro MA, Leza JC, O'Shea E, Davalos A, Castillo J, Lorenzo P, Lizasoain I. 2002. Upregulation of TACE/ADAM17 after ischemic preconditioning is involved in brain tolerance. J Cereb Blood Flow Metab 22:1297-1302.
12. Chen J, Graham SH, Zhu RL, Simon RP. 1996. Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16:566-577.
13. Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X, Barone FC. 2000. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res 863:169-181.
14. Digicaylioglu M, Lipton SA. 2001. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412:641-647.
15. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek L, Lewczuk P, Stiefel M, Rustenbeck HH, Breiter N, Jacob S, Knerlich F, Bohn M, Poser W, Ruther E, Kochen M, Gefeller O, Gleiter C, Wessel TC, De Ryck M, Itri L, Prange H, Cerami A, Brines M, Siren AL. 2002. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8:495-505.
16. Gonzalez-Zulueta M, Feldman AB, Klesse LJ, Kalb RG, Dillman JF, Parada LF, Dawson TM, Dawson VL. 2000. Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci U S A 97:436-441.
17. Jones NM, Bergeron M. 2001. Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab 21:1105-1114.
18. Lange-Asschenfeldt C, Raval AP, Dave KR, Mochly-Rosen D, Sick TJ, Perez-Pinzon MA. 2004. Epsilon protein kinase C mediated ischemic tolerance requires activation of the extracellular regulated kinase pathway in the organotypic hippocampal slice. J Cereb Blood Flow Metab 24:636-645.
19. Leist M, Ghezzi P, Grasso G, Bianchi R, Villa P, Fratelli M, Savino C, Bianchi M, Nielsen J, Gerwien J, Kallunki P, Larsen AK, Helboe L, Christensen S, Pedersen LO, Nielsen M, Torup L, Sager T, Sfacteria A, Erbayraktar S, Erbayraktar Z, Gokmen N, Yilmaz O, Cerami-Hand C, Xie QW, Coleman T, Cerami A, Brines M. 2004. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305:239-242.
20. Longa EZ, Weinstein PR, Carlson S, Cummins R. 1989. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91.
21. Meller R, Minami M, Cameron JA, Impey S, Chen D, Lan JQ, Henshall DC, Simon RP. 2005. CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 25:234-246.
22. Miller BA, Perez RS, Shah AR, Gonzales ER, Park TS, Gidday JM. 2001. Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport 12:1663-1669.
23. Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Melle G. 2000. Do transient ischemic attacks have a neuroprotective effect? Neurology 54:2089-2094.
24. Noshita N, Lewen A, Sugawara T, Chan PH. 2001. Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 21:1442-1450.
25. Prass K, Scharff A, Ruscher K, Lowl D, Muselmann C, Victorov I, Kapinya K, Dirnagl U, Meisel A. 2003. Hypoxia-induced stroke tolerance in the mouse is mediated by erythropoietin. Stroke 34:1981-1986.
26. Ratan RR, Siddiq A, Aminova L, Lange PS, Langley B, Ayoub I, Gensert J, Chavez J. 2004. Translation of ischemic preconditioning to the patient: prolyl hydroxylase inhibition and hypoxia inducible factor-1 as novel targets for stroke therapy. Stroke 35(Suppl 1):2687-2689.
27. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, Priller J, Dirnagl U, Meisel A. 2002. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22:10291-10301.
28. Savitz SI, Erhardt JA, Anthony JV, Gupta G, Li X, Barone FC, Rosenbaum DM. 2000. The novel beta-blocker, carvedilol, provides neuroprotection in transient focal stroke. J Cereb Blood Flow Metab 20:1197-1204.
29. Shimizu S, Nagayama T, Jin KL, Zhu L, Loeffert JE, Watkins SC, Graham SH, Simon RP. 2001. bcl-2 Antisense treatment prevents induction of tolerance to focal ischemia in the rat brain. J Cereb Blood Flow Metab 21:233-243.
30. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, Mennini T, Heumann R, Cerami A, Ehrenreich H, Ghezzi P. 2001. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 98:4044-4049.
31. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. 1990. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10:290-293.
32. Truettner J, Busto R, Zhao W, Ginsberg MD, Perez-Pinzon MA. 2002. Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain Res Mol Brain Res 103:106-115.
33. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70:35-602.
34. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. 2004. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35:1732-1737.
35. Wegener S, Gottschalk B, Jovanovic V, Knab R, Fiebach JB, Schellinger PD, Kucinski T, Jungehulsing GJ, Brunecker P, Muller B, Banasik A, Amberger N, Wernecke KD, Siebler M, Rother J, Villringer A, Weih M. 2004. Transient ischemic attacks before ischemic stroke: preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke 35:616-621.
36. Wick A, Wick W, Waltenberger J, Weller M, Dichgans J, Schulz JB. 2002. Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J Neurosci 22:6401-6407.
37. Yano S, Morioka M, Fukunaga K, Kawano T, Hara T, Kai Y, Hamada J, Miyamoto E, Ushio Y. 2001. Activation of Akt/protein kinase B contributes to induction of ischemic tolerance in the CA1 subfield of gerbil hippocampus. J Cereb Blood Flow Metab 21:351-360.