Erythropoietin is neuroprotective against NMDA-receptor-mediated excitotoxic brain injury in newborn mice

Neurobiology of Disease

Volumn 24, Issue 2, 2006, Pages 357-366

  Keller, Matthias ^a   Yang, Jingli ^a,c   Griesmaier, Elke ^a   Gorna, Agnieszka ^a   Sarkozy, Gergely ^d   Urbanek, Martina ^a   Gressens, Pierre ^b   Simbruner, Georg ^a  

^a Neuropediatrics and Metabolic Diseases   (Austria)

^b HÔPITAL ROBERT DEBRÉ   (France)

^c ZHENGZHOU UNIVERSITY   (China)

^d SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Brain injury; Erythropoietin; Excitotoxicity; Newborn

Indexed keywords

IBOTENIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECOMBINANT ERYTHROPOIETIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DRUG EFFECT; EXCITOTOXICITY; FEMALE; HEMATOPOIESIS; LEUKOMALACIA; MALE; MOUSE; MOUSE STRAIN; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SEX DIFFERENCE; SINGLE DRUG DOSE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; ERYTHROPOIETIN; FEMALE; GLUTAMIC ACID; HUMANS; IBOTENIC ACID; INFANT, NEWBORN; INJECTIONS, INTRAVENTRICULAR; LEUKOMALACIA, PERIVENTRICULAR; MALE; MICE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; RECEPTORS, ERYTHROPOIETIN; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; TIME FACTORS;

EID: 33750107287     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.07.007     Document Type: Article

References (41)

1. Acarin L., Gonzalez B., Castro A.J., and Castellano B. Primary cortical glial reaction versus secondary thalamic glial response in the excitotoxically injured young brain: microglial/macrophage response and major histocompatibility complex class I and II expression. Neuroscience 89 (1999) 549-565
2. Bernaudin M., Marti H.H., Roussel S., Divoux D., Nouvelot A., MacKenzie E.T., and Petit E. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 19 (1999) 643-651
3. Brown M.S., Baron A.E., France E.K., and Hamman R.F. Association between higher cumulative doses of recombinant erythropoietin and risk for retinopathy of prematurity. J. AAPOS 10 (2006) 143-149
4. Buemi M., Allegra A., Corica F., Floccari F., D'Avella D., Aloisi C., Calapai G., Iacopino G., and Frisina N. Intravenous recombinant erythropoietin does not lead to an increase in cerebrospinal fluid erythropoietin concentration. Nephrol. Dial. Transplant. 15 (2000) 422-423
5. Chang Y.S., Mu D., Wendland M., Sheldon R.A., Vexler Z.S., McQuillen P.S., and Ferriero D.M. Erythropoietin improves functional and histological outcome in neonatal stroke. Pediatr. Res. 58 (2005) 106-111
6. Dammann O., and Leviton A. Inflammatory brain damage in preterm newborns-Dry numbers, wet lab, and causal inferences 7238. Early Hum. Dev. 79 (2004) 1-15
7. Dzietko M., Felderhoff-Mueser U., Sifringer M., Krutz B., Bittigau P., Thor F., Heumann R., Buhrer C., Ikonomidou C., and Hansen H.H. Erythropoietin protects the developing brain against N-methyl-d-aspartate receptor antagonist neurotoxicity. Neurobiol. Dis. 15 (2004) 177-187
8. Ehrenreich H., Hasselblatt M., Dembowski C., Cepek L., Lewczuk P., Stiefel M., Rustenbeck H.H., Breiter N., Jacob S., Knerlich F., Bohn M., Poser W., Ruther E., Kochen M., Gefeller O., Gleiter C., Wessel T.C., De Ryck M., Itri L., Prange H., Cerami A., Brines M., and Siren A.L. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol. Med. 8 (2002) 495-505
9. Erbayraktar Z., Gokmen N., Yilmaz O., Ghezzi P., Villa P., Fratelli M., Casagrande S., Leist M., Helboe L., Gerwein J., Christensen S., Geist M.A., Pedersen L.O., Cerami-Hand C., Wuerth J.P., Cerami A., and Brines M. Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6741-6746
10. Ferriero, D.M., 2006. EPO increases neurogenesis after neonatal stroke. 25-5-0006. Ref Type: Conference Proceeding.
11. Follett P.L., Rosenberg P.A., Volpe J.J., and Jensen F.E. NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci. 20 (2000) 9235-9241
12. Haynes R.L., Baud O., Li J., Kinney H.C., Volpe J.J., and Folkerth D.R. Oxidative and nitrative injury in periventricular leukomalacia: a review 5 178. Brain Pathol. 15 (2005) 225-233
13. Hilton G.D., Nunez J.L., and McCarthy M.M. Sex differences in response to kainic acid and estradiol in the hippocampus of newborn rats. Neuroscience 116 (2003) 383-391
14. Holden C. Sex and the suffering brain. Science 308 (2005) 1574
15. Juul S.E., Stallings S.A., and Christensen R.D. Erythropoietin in the cerebrospinal fluid of neonates who sustained CNS injury. Pediatr. Res. 46 (1999) 543-547
16. Juul S.E., McPherson R.J., Farrell F.X., Jolliffe L., Ness D.J., and Gleason C.A. Erythropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol. Neonate 85 (2004) 138-144
17. Keller M., Simbruner G., and G.A.G.E.U.M.G.S.S.L.G.P. Systemic application of granulocyte-colony stimulating factor and stem cell factor exacerbates excitotoxic brain injury in newborn mice. Pediatr. Res. 59 (2006) 549-553
18. Kumral A., Ozer E., Yilmaz O., Akhisaroglu M., Gokmen N., Duman N., Ulukus C., Genc S., and Ozkan H. Neuroprotective effect of erythropoietin on hypoxic-ischemic brain injury in neonatal rats. Biol. Neonate 83 (2003) 224-228
19. Lambert J.F., Benoit B.O., Colvin G.A., Carlson J., Delville Y., and Quesenberry P.J. Quick sex determination of mouse fetuses. J. Neurosci. Methods 95 (2000) 127-132
20. Leist M., Ghezzi P., Grasso G., Bianchi R., Villa P., Fratelli M., Savino C., Bianchi M., Nielsen J., Gerwien J., Kallunki P., Larsen A.K., Helboe L., Christensen S., Pedersen L.O., Nielsen M., Torup L., Sager T., Sfacteria A., Erbayraktar S., Erbayraktar Z., Gokmen N., Yilmaz O., Cerami-Hand C., Xie Q.W., Coleman T., Cerami A., and Brines M. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305 (2004) 239-242
21. Loeliger M., Watson C.S., Reynolds J.D., Penning D.H., Harding R., Bocking A.D., and Rees S.M. Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep 1. Neuroscience 116 (2003) 705-714
22. Marret S., Mukendi R., Gadisseux J.F., Gressens P., and Evrard P. Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions. J. Neuropathol. Exp. Neurol. 54 (1995) 358-370
23. McDonald T.P., Cottrell M.B., Clift R.E., Cullen W.C., and Lin F.K. High doses of recombinant erythropoietin stimulate platelet production in mice. Exp. Hematol. 15 (1987) 719-721
24. Ment L.R., Vohr B.R., Makuch R.W., Westerveld M., Katz K.H., Schneider K.C., Duncan C.C., Ehrenkranz R., Oh W., Philip A.G., Scott D.T., and Allan W.C. Prevention of intraventricular hemorrhage by indomethacin in male preterm infants. J. Pediatr. 145 (2004) 832-834
25. Morita M., Ohneda O., Yamashita T., Takahashi S., Suzuki N., Nakajima O., Kawauchi S., Ema M., Shibahara S., Udono T., Tomita K., Tamai M., Sogawa K., Yamamoto M., and Fujii-Kuriyama Y. HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J. 22 (2003) 1134-1146
26. Reiss A.L., Kesler S.R., Vohr B., Duncan C.C., Katz K.H., Pajot S., Schneider K.C., Makuch R.W., and Ment L.R. Sex differences in cerebral volumes of 8-year-olds born preterm. J. Pediatr. 145 (2004) 242-249
27. Rice III J.E., Vannucci R.C., and Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9 (1981) 131-141
28. Sakanaka M., Wen T.C., Matsuda S., Masuda S., Morishita E., Nagao M., and Sasaki R. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 4635-4640
29. Serteser M., Ozben T., Gumuslu S., Balkan S., and Balkan E. Biochemical evidence of crossed cerebellar diaschisis in terms of nitric oxide indicators and lipid peroxidation products in rats during focal cerebral ischemia 1. Acta Neurol. Scand. 103 (2001) 43-48
30. Shikama Y., Ishibashi T., Kimura H., Kawaguchi M., Uchida T., and Maruyama Y. Transient effect of erythropoietin on thrombocytopoiesis in vivo in mice. Exp. Hematol. 20 (1992) 216-222
31. Shouman B., Fontaine R.H., Baud O., Schwendimann L., Keller M., Spedding M., Lelievre V., and Gressens P. Endocannabinoids potently protect the newborn brain against AMPA-kainate receptor-mediated excitotoxic damage 1. Br. J. Pharmacol. 148 4 (2006) 442-451
32. Sola A., Rogido M., Lee B.H., Genetta T., and Wen T.C. 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. 57 (2005) 481-487
33. Spandou E., Soubasi V., Papoutsopoulou S., Karkavelas G., Simeonidou C., Kaiki-Astara A., and Guiba-Tziampiri O. Erythropoietin prevents hypoxia/ischemia-induced DNA fragmentation in an experimental model of perinatal asphyxia. Neurosci. Lett. 366 (2004) 24-28
34. Sun Y., Zhou C., Polk P., Nanda A., and Zhang J.H. Mechanisms of erythropoietin-induced brain protection in neonatal hypoxia-ischemia rat model. J. Cereb. Blood Flow Metab. 24 (2004) 259-270
35. Tahraoui S.L. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol. 11 (2001) 56-71
36. Tsai P.T., Ohab J.J., Kertesz N., Groszer M., Matter C., Gao J., Liu X., Wu H., and Carmichael S.T. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery 1. J. Neurosci. 26 (2006) 1269-1274
37. Volpe J.J. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50 (2001) 553-562
38. Wang X., Zhu C., Wang X., Gerwien J.G., Schrattenholz A., Sandberg M., Leist M., and Blomgren K. The nonerythropoietic asialoerythropoietin protects against neonatal hypoxia-ischemia as potently as erythropoietin. J. Neurochem. 91 (2004) 900-910
39. Wen T.C., Rogido M., Peng H., Genetta T., Moore J., and Sola A. Gender differences in long-term beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience 139 (2006) 803-811
40. Yatsiv I., Grigoriadis N., Simeonidou C., Stahel P.F., Schmidt O.I., Alexandrovitch A.G., Tsenter J., and Shohami E. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J. 19 (2005) 1701-1703
41. Zhu C., Wang X., Xu F., Bahr B.A., Shibata M., Uchiyama Y., Hagberg H., and Blomgren K. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ. 12 (2005) 162-176