Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 317, Issue 1, 2006, Pages 109-116

  Wei, Ling ^a,c   Han, Byung H ^c,d   Li, Ying ^a   Keogh, Christine L ^a   Holtzman, David M ^c   Shan, Ping Yu ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOCHROME C; DNA; DNA FRAGMENT; JANUS KINASE 2; PROTEIN BCL 2; RECOMBINANT ERYTHROPOIETIN; STAT5 PROTEIN;

AGAR GEL ELECTROPHORESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL DEATH; CEREBROVASCULAR ACCIDENT; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; DRUG INHIBITION; DRUG MECHANISM; ELECTRON MICROSCOPY; FEMALE; FRAGMENTATION REACTION; MALE; MIDDLE CEREBRAL ARTERY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN ISCHEMIA; CEREBRAL CORTEX; ERYTHROPOIETIN, RECOMBINANT; FEMALE; IN SITU NICK-END LABELING; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR;

EID: 33645111789     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.105.094391     Document Type: Article

References (46)

1. Ashwal S and Pearce WJ (2001) Animal models of neonatal stroke. Curr Opin Pediatr 13:506-516.
2. Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, and Petit E (1999) A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 19:643-651.
3. Chang YS, Mu D, Wendland M, Sheldon RA, Vexler ZS, McQuillen PS, and Ferriero DM (2005) Erythropoietin improves functional and histological outcome in neonatal stroke. Pediatr Res 58:106-111.
4. Cheng Y, Deshmukh M, D'Costa A, Demaro JA, Gidday JM, Shah A, Sun Y, Jacquin MF, Johnson EM, and Holtzman DM (1998) Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Investig 101:1992-1999.
5. Chong ZZ, Kang JQ, and Maiese K (2002) Hematopoietic factor erythropoietin fosters neuroprotection through novel signal transduction cascades. J Cereb Blood Flow Metab 22:503-514.
6. Chong ZZ, Kang JQ, and Maiese K (2003) Apaf-1, Bcl-xL, cytochrome c and caspase-9 form the critical elements for cerebral vascular protection by erythropoietin. J Cereb Blood Flow Metab 23:320-330.
7. Dame C, Bartmann P, Wolber E, Fahnenstich H, Hofmann D, and Fandrey J (2000) Erythropoietin gene expression in different areas of the developing human central nervous system. Brain Res Dev Brain Res 125:69-74.
8. Demers EJ, McPherson RJ, and Juul SE (2005) Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 58:297-301.
9. Digicaylioglu M, Bichet S, Marti HH, Wenger RH, Rivas LA, Bauer C, and Gassmann M (1995) Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci USA 92:3717-3720.
10. Digicaylioglu M and Lipton SA (2001) Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature (Lond) 412:641-647.
11. Dikranian K, Ishimaru MJ, Tenkova T, Labruyere J, Qin YQ, Ikonomidou C, and Olney JW (2001) Apoptosis in the in vivo mammalian forebrain. Neurobiol Dis 8:359-379.
12. Eichenbaum JW, Pevsner PH, Pivawer G, Kleinman GM, Chiriboga L, Stern A, Rosenbach A, Iannuzzi K, and Miller DC (2002) A murine photochemical stroke model with histologic correlates of apoptotic and nonapoptotic mechanisms. J Pharmacol Toxicol Methods 47:67-71.
13. Govaert P, Matthys E, Zecic A, Roelens F, Oostra A, and Vanzieleghem B (2000) Perinatal cortical infarction within middle cerebral artery trunks. Arch Dis Child Fetal Neonatal Ed 82:F59-F63.
14. Han BH and Holtzman DM (2000) BDNF protects the neonatal brain from hypoxicischemic injury in vivo via the ERK pathway. J Neurosci 20:5775-5781.
15. Herlenius E and Lagercrantz H (2004) Development of neurotransmitter systems during critical periods. Exp Neurol 190 (Suppl 1):S8-S21.
16. Johnston MV, Nakajima W, and Hagberg H (2002) Mechanisms of hypoxic neurodegeneration in the developing brain. Neuroscientist 8:212-220.
17. Joyeux-Faure M, Godin-Ribuot D, and Ribuot C (2005) Erythropoietin and myocardial protection: what's new? Fundam Clin Pharmacol 19:439-446.
18. Juul SE (2002) Erythropoietin in the central nervous system and its use to prevent hypoxic-ischemic brain damage. Acta Paediatr Suppl 91:36-42.
19. Kumral A, Ozer E, Yilmaz O, Akhisaroglu M, Gokmen N, Duman N, Ulukus C, Genc S, and Ozkan H (2003) Neuroprotective effect of erythropoietin on hypoxic-ischemic brain injury in neonatal rats. Biol Neonate 83:224-228.
20. Lee J, Croen LA, Backstrand KH, Yoshida CK, Henning LH, Lindan C, Ferriero DM, Fullerton HJ, Barkovich AJ, and Wu YW (2005) Maternal and infant characteristics associated with perinatal arterial stroke in the infant. J Am Med Assoc 293:723-729.
21. Liu CL, Siesjo BK, and Hu BR (2004) Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development. Neuroscience 127:113-123.
22. Luna LG (1968) Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology. McGraw-Hill Companies, New York.
23. Lynch JK, Hirtz DG, DeVeber G, and Nelson KB (2002) Report of the National Institute of Neurological Disorders and Stroke workshop on perinatal and childhood stroke. Pediatrics 109:116-123.
24. Manabat C, Han BH, Wendland M, Derugin N, Fox CK, Choi J, Holtzman DM, Ferriero DM, and Vexler ZS (2003) Reperfusion differentially induces caspase-3 activation in ischemic core and penumbra after stroke in immature brain. Stroke 34:207-213.
25. Marti HH (2004) Erythropoietin and the hypoxic brain. J Exp Biol 207:3233-3242.
26. McIlwain H and Bachelard HS (1971) Chemical and enzymatic makeup of the brain during development and ageing, in Biochemistry and the Central Nervous System (Wilkins W ed) pp 371-412, Lippincott Williams & Wilkins, Baltimore, MD.
27. Muramatsu K, Fukuda A, Togari H, Wada Y, and Nishino H (1997) Vulnerability to cerebral hypoxic-ischemic insult in neonatal but not in adult rats is in parallel with disruption of the blood-brain barrier. Stroke 28:2281-2288, discussion 2288-2289.
28. Nakajima W, Ishida A, Lange MS, Gabrielson KL, Wilson MA, Martin LJ, Blue ME, and Johnston MV (2000) Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 20:7994-8004.
29. Nelson KB and Lynch JK (2004) Stroke in newborn infants. Lancet Neurol 3:150-158.
30. Renolleau S, Aggoun-Zouaoui D, Ben-Ari Y, and Charriaut-Marlangue C (1998) A model of transient unilateral focal ischemia with reperfusion in the P7 neonatal rat: morphological changes indicative of apoptosis. Stroke 29:1454-1460.
31. Renzi MJ, Farrell FX, Bittner A, Galindo JE, Morton M, Trinh H, and Jolliffe LK (2002) Erythropoietin induces changes in gene expression in PC-12 cells. Brain Res Mol Brain Res 104:86-95.
32. Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, and Sasaki R (1998) In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA 95:4635-4640.
33. Sheldon RA, Hall JJ, Noble LJ, and Ferriero DM (2001) Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett 304:165-168.
34. Singer D (1999) Neonatal tolerance to hypoxia: a comparative- physiological approach. Comp Biochem Physiol A Mol Integr Physiol 123:221-234.
35. Sola A, Rogido M, Lee BH, Genetta T, and Wen TC (2005) 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 57:481-487.
36. Spandou E, Papoutsopoulou S, Soubasi V, Karkavelas G, Simeonidou C, Kremenopoulos G, and Guiba-Tziampiri O (2004) Hypoxia-ischemia affects erythropoietin and erythropoietin receptor expression pattern in the neonatal rat brain. Brain Res 1021:167-172.
37. Sun Y, Zhou C, Polk P, Nanda A, and Zhang JH (2004) Mechanisms of erythropoietin-induced brain protection in neonatal hypoxia-ischemia rat model. J Cereb Blood Flow Metab 24:259-270.
38. Vairano M, Dello Russo C, Pozzoli G, Battaglia A, Scambia G, Tringali G, Aloe-Spiriti MA, Preziosi P, and Navarra P (2002) Erythropoietin exerts anti-apoptotic effects on rat microglial cells in vitro. Eur J Neurosci 16:584-592.
39. van Lookeren Campagne M and Gill R (1996) Ultrastructural morphological changes are not characteristic of apoptotic cell death following focal cerebral ischaemia in the rat. Neurosci Lett 213:111-114.
40. Wei L, Erinjeri JP, Rovainen CM, and Woolsey TA (2001) Collateral growth and angiogenesis around cortical stroke. Stroke 32:2179-2184.
41. Wei L, Rovainen CM, and Woolsey TA (1995) Ministrokes in rat barrel cortex. Stroke 26:1459-1462.
42. Wei L, Ying DJ, Cui L, Langsdorf J, and Yu SP (2004) Necrosis, apoptosis and hybrid death in the cortex and thalamus after barrel cortex ischemia in rats. Brain Res 1022:54-61.
43. Wen TC, Rogido M, Genetta T, and Sola A (2004) Permanent focal cerebral ischemia activates erythropoietin receptor in the neonatal rat brain. Neurosci Lett 355:165-168.
44. Wen TC, Sadamoto Y, Tanaka J, Zhu PX, Nakata K, Ma YJ, Hata R, and Sakanaka M (2002) Erythropoietin protects neurons against chemical hypoxia and cerebral ischemic injury by up-regulating Bcl-xL expression. J Neurosci Res 67:795-803.
45. Xiao AY, Wei L, Xia S, Rothman S, and Yu SP (2002) Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci 22:1350-1362.
46. Yager JY and Thornhill JA (1997) The effect of age on susceptibility to hypoxic-ischemic brain damage. Neurosci Biobehav Rev 21:167-174.