Neuroprotective effects of erythropoietin posttreatment against kainate-induced excitotoxicity in mixed spinal cultures

Journal of Neuroscience Research

Volumn 87, Issue 1, 2009, Pages 150-163

  Yoo, Jong Yoon ^a   Won, You Jin ^a   Lee, Jong Hwan ^b   Kim, Jong Uk ^a   Sung, In Young ^a   Hwang, Seung Jun ^a   Kim, Mi Jung ^a   Hong, Hea Nam ^a  

^a University of Ulsan College of Medicine   (South Korea)

^b Konkuk University   (South Korea)

Author keywords

Erythropoietin; KA excitotoxicity; Neuroprotection; Secondary spinal cord injury; Spinal neuronglia culture

Indexed keywords

EPOKINE; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; JANUS KINASE 2; KAINIC ACID; RECOMBINANT ERYTHROPOIETIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; ENZYME ACTIVATION; EXCITOTOXICITY; FEMALE; GLIOSIS; MOTONEURON; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY; SPINAL CORD NERVE CELL;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; ASTROCYTES; CASPASE 3; CELL COUNT; CELLS, CULTURED; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; ERYTHROPOIETIN; EXCITATORY AMINO ACID AGONISTS; HUMANS; IN SITU NICK-END LABELING; JANUS KINASE 2; KAINIC ACID; MOTOR NEURONS; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TISSUE CULTURE TECHNIQUES;

EID: 63049125885     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21832     Document Type: Article

References (45)

1. Arishima Y, Setoguchi T, Yamaura I, Yone K, Komiya S. 2006. Preventive effect of erythropoietin on spinal cord cell apoptosis following acute traumatic injury in rats. Spine 31:2432-2438.
2. Avossa D, Rosato-Siri MD, Mazzarol F, Ballerini L. 2003. Spinal circuits formation: a study of developmentally regulated markers in organotypic cultures of embryonic mouse spinal cord. Neuroscience 122:391-405.
3. Avossa D, Grandolfo M, Mazzarol F, Zatta M, Ballerini L. 2006. Early signs of motoneuron vulnerability in a disease model system: characterization of transverse slice cultures of spinal cord isolated from embryonic ALS mice. Neuroscience 138:1179-1194.
4. Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, Petit E. 1999. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 19:643-651.
5. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/ superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 92:7162-7166.
6. 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.
7. Carriedo SG, Yin HZ, Weiss JH. 1996. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 13:4069-4079.
8. 2+ overload and ROS generation in spinal motor neurons in vitro. J Neurosci 20:240-250.
9. Chin K, Yu X, Beleslin-Cokic B, Liu C, Shen K, Mohrenweiser HW, Noguchi CT. 2000. Production and processing of erythropoietin receptor transcripts in brain. Brain Res Mol Brain Res 81:29-42.
10. Chong ZZ, Lin SH, Kang JQ, Maiese K. 2003. Erythropoietin prevents early and late neuronal demise through modulation of Akt1 and induction of caspase 1, 3, and 8. J Neurosci Res 71:659-669.
11. Digicaylioglu M, Lipton SA. 2001. Erythropoietin mediated neuroprotection involves cross-talk between Jak2 and NF-κB signaling cascades. Nature 412:641-647.
12. Digicaylioglu M, Bichet S, Marti HH, Wenger RH, Rivas LA, Bauer C, Gassmann M. 1995. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci U S A 92:3717-3720.
13. Digicaylioglu M, Garden G, Timberlake S, Fletcher L, Lipton SA. 2004. Acute neuroprotective synergy of erythropoietin and insulin-like growth factor I. Proc Natl Acad Sci U S A 101:9855-9860.
14. Elliott S, Busse L, Bass MB, Lu H, Sarosi I, Sinclair AM, Spahr C, Um M, Van G, Begley CG. 2006. Anti-Epo receptor antibodies do not predict Epo receptor expression. Blood 107:1892-1895.
15. Faden AI, Simon RP. 1988. A potential role for excitotoxins in the pathophysiology of spinal cord injury. Ann Neurol 23:623-626.
16. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. 2004. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143-2155.
17. Grasso G, Sfacteria A, Passalacqua M, Morabito A, Buemi M, Macri B, Brines ML, Tomasello F. 2005. Erythropoietin and erythropoietin receptor expression after experimental spinal cord injury encourages therapy by exogenous erythropoietin. Neurosurgery 56:821-827.
18. Hugon J, Vallat JM, Spencer PS, Leboutet MJ, Barthe D. 1989. Kainic acid induces early and delayed degenerative neuronal changes in rat spinal cord. Neurosci Lett 104:258-262.
19. Juul SE, Anderson DK, Li Y, Christensen RD. 1998. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 43:40-49.
20. Keller M, Yang J, Griesmaier E, Gorna A, Sarkozy G, Urbanek M, Gressens P, Simbruner G. 2006. Erythropoietin is neuroprotective against NMDA-receptor-mediated excitotoxic brain injury in newborn mice. Neurobiol Dis 24:357-366.
21. King VR, Averill SA, Hewazy D, Priestley JV, Torup L, Michael-Titus AT. 2007. Erythropoietin and carbamylated erythropoietin are neuroprotective following spinal cord hemisection in the rat. Eur J Neurosci 26:90-100.
22. Kirkeby A, van Beek J, Nielsen J, Leist M, Helboe L. 2007. Functional and immunochemical characterisation of different antibodies against the erythropoietin receptor. J Neurosci Methods 164:50-58.
23. Knabe W, Siren AL, Ehrenreich H, Kuhn HJ. 2005. Expression patterns of erythropoietin and its receptor in the developing spinal cord and dorsal root ganglia. Anat Embryol 210:209-219.
24. Kretz A, Happold CJ, Marticke JK, Isenmann S. 2005. Erythropoietin promotes regeneration of adult CNS neurons via Jak2/Stat3 and PI3K/AKT pathway activation. Mol Cell Neurosci 29:569-579.
25. Liu D, Xu GY, Pan E, McAdoo DJ. 1999. Neurotoxicity of glutamate at the concentrations released upon spinal cord injury. Neuroscience 93:1383-1389.
26. Maiese K, Li F, Chong ZZ. 2005. New avenues of exploration for erythropoietin. JAMA 293:90-95.
27. Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R. 1997. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76:105-116.
28. Poitry-Yamate CL, Vutskits L, Rauen T. 2002. Neuronal-induced and glutamate-dependent activation of glial glutamate transporter function. J Neurochem 82:987-997.
29. Ridet JL, Malhotra SK, Privat A, Gage FH. 1997. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570-577.
30. 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.
31. Saroff D, Delfs J, Kuznetsov D, Geula C. 2000. Selective vulnerability of spinal cord motor neurons to non-NMDA toxicity. Neuroreport 11:1117-1121.
32. Scheid MP, Woodgett JR. 2001. PKB/AKT: functional insights from genetic models. Nat Rev Mol Cell Biol 2:760-768.
33. Siren AL, Knerlich F, Poser W, Gleiter CH, Bruck W, Ehrenreich H. 2001. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta Neuropathol 101:271-276.
34. Sugawa M, Sakurai Y, Ishikawa-Ieda Y, Suzuki H, Asou H. 2002. Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci Res 44:391-403.
35. Tator CH, Fehlings MG. 1991. Review of the secondary injury theory of acute spinal trauma with emphasis on vascular mechanisms. J Neurosurg 75:15-26.
36. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J, Liu X, Wu H, Carmichael ST. 2006. A critical role of erythropoietin receptor in neurogenesis and poststroke recovery. J Neurosci 26:1269-1274.
37. Urushitani M, Shimohama S, Kihara T, Sawada H, Akaike A, Ibi M, Inoue R, Kitamura Y, Taniguchi T, Kimura J. 1998. Mechanism of selective motor neuronal death after exposure of spinal cord to glutamate: involvement of glutamate-induced nitric oxide in motor neuron toxicity and nonmotor neuron protection. Ann Neurol 44:796-807.
38. 2+-permeable AMPA receptors and selective vulnerability of motor neurons. J Neurol Sci 180:29-34.
39. Van Den Bosch L, Schwaller B, Vleminckx V, Meijers B, Stork S, Ruehlicke T, Van Houtte E, Klaassen H, Celio MR, Missiaen L, Robberecht W, Berchtold MW. 2002. Protective effect of parvalbumin on excitotoxic motor neuron death. Exp Neurol 174:150-161.
40. Vermeiren C, Najimi M, Vanhoutte N, Tilleux S, de Hemptinne I, Maloteaux JM, Hermans E. 2005. Acute up-regulation of glutamate uptake mediated by mGluR5a in reactive astrocytes. J Neurochem 94:405-416.
41. Villa P, Bigini P, Mennini T, Agnello D, Laragione T, Cagnotto A, Viviani B, Marinovich M, Cerami A, Coleman TR, Brines M, Ghezzi P. 2003. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 198:971-975.
42. Witthuhn BA, Quelle FW, Silvennoinen O, Yi T, Tang B, Miura O, Ihle JN. 1993. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell 74:227-236.
43. Yin HZ, Park DD, Lindsay AD, Weiss JH. 1995. Spinal cord neurons are vulnerable to rapidly triggered kainate neurotoxicity in vitro. Brain Res 689:265-270.
44. Yu X, Lin CS, Costantini F, Noguchi CT. 2001. The human erythropoietin receptor gene rescues erythropoiesis and developmental defects in the erythropoietin receptor null mouse. Blood 98:475-477.
45. Yu X, Shacka JJ, Eells JB, Suarez-Quian C, Przygodzki RM, Beleslin-Cokic B, Lin CS, Nikodem VM, Hempstead B, Flanders KC, Costantini F, Noguchi CT. 2002. Erythropoietin receptor signalling is required for normal brain development. Development 129:505-516.