Erythropoietin attenuates hyperoxia-induced oxidative stress in the developing rat brain

Brain, Behavior, and Immunity

Volumn 24, Issue 5, 2010, Pages 792-799

  Sifringer, Marco ^a   Brait, Daniela ^a   Weichelt, Ulrike ^a   Zimmerman, Gabriel ^b   Endesfelder, Stefanie ^a   Brehmer, Felix ^a   von Haefen, Clarissa ^a   Friedman, Alon ^a,c   Soreq, Hermona ^b   Bendix, Ivo ^d   Gerstner, Bettina ^e   Felderhoff Mueser, Ursula ^d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

^e JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Acetylcholinesterase; Developing brain; Erythropoietin; Glutathione; Heme oxygenase; Hyperoxia; Lipid peroxidation; Oxidative stress

Indexed keywords

ACETYLCHOLINESTERASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEME OXYGENASE 1; MALONALDEHYDE; MESSENGER RNA; OXYGEN; RECOMBINANT ERYTHROPOIETIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HYPEROXIA; IMMATURITY; INFLAMMATION; LIPID PEROXIDATION; NEUROPROTECTION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; OXYGEN TOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; ERYTHROPOIETIN, RECOMBINANT; FEMALE; GLUTATHIONE; HEME OXYGENASE-1; HYPEROXIA; LIPID PEROXIDATION; MALE; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

EID: 77953611300     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.08.010     Document Type: Article

References (67)

1. Abraham N.G., Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol. Rev. 2008, 60:79-127.
2. Ahn E.S., Robertson C.L., Vereczki V., Hoffman G.E., Fiskum G. Normoxic ventilatory resuscitation following controlled cortical impact reduces peroxynitrite-mediated protein nitration in the hippocampus. J. Neurosurg. 2008, 108:124-131.
3. Bains J.S., Shaw C.A. Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res. Brain Res. Rev. 1997, 25:335-358.
4. Berson A., Knobloch M., Hanan M., Diamant S., Sharoni M., Schuppli D., Geyer B.C., Ravid R., Mor T.S., Nitsch R.M., Soreq H. Changes in readthrough acetylcholinesterase expression modulate amyloid-beta pathology. Brain 2008, 131:109-119.
5. Beutler E., Duron O., Kelly B.M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 1963, 61:882-888.
6. Burger D., Xiang F., Hammoud L., Lu X., Feng Q. Role of heme oxygenase-1 in the cardioprotective effects of erythropoietin during myocardial ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H84-H93.
7. Calò L.A., Stanic L., Davis P.A., Pagnin E., Munaretto G., Fusaro M., Landini S., Semplicini A., Piccoli A. Effect of epoetin on HO-1 mRNA level and plasma antioxidants in hemodialysis patients. Int. J. Clin. Pharmacol. Ther. 2003, 41:187-192.
8. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
9. Collins M.P., Lorenz J.M., Jetton J.R., Paneth N. Hypocapnia and other ventilation-related risk factors for cerebral palsy in low birth weight infants. Pediatr. Res. 2001, 50:712-719.
10. Cooper A.J., Kristal B.S. Multiple roles of glutathione in the central nervous system. Biol. Chem. 1997, 378:793-802.
11. -) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen. J. Neurophysiol. 2007, 98:1030-1041.
12. Demers E.J., McPherson R.J., Juul S.E. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr. Res. 2005, 58:297-301.
13. Deshane J., Wright M., Agarwal A. Heme oxygenase-1 expression in disease states. Acta Biochim. Pol. 2005, 52:273-284.
14. Deulofeut R., Critz A., Adams-Chapman I., Sola A. Avoiding hyperoxia in infants < or = 1250g is associated with improved short- and long-term outcomes. J. Perinatol. 2006, 26:700-705.
15. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves crosstalk between Jak2 and NF-kappaB signalling cascades. Nature 2001, 412:641-647.
16. Dringen R. Metabolism and functions of glutathione in brain. Prog. Neurobiol. 2000, 62:649-671.
17. Dzietko M., Boos V., Sifringer M., Polley O., Gerstner B., Genz K., Endesfelder S., Boerner C., Jacotot E., Chauvier D., Obladen M., Buehrer C. A critical role for Fas/CD-95 dependent signaling pathways in the pathogenesis of hyperoxia-induced brain injury. Ann. Neurol. 2008, 64:664-673.
18. Felderhoff-Mueser U., Bittigau P., Sifringer M., Jarosz B., Korobowicz E., Mahler L., Piening T., Moysich A., Grune T., Thor F., Heumann R., Buehrer C., Ikonomidou C. Oxygen causes cell death in the developing brain. Neurobiol. Dis. 2004, 17:273-282.
19. Felderhoff-Mueser U., Sifringer M., Polley O., Dzietko M., Leineweber B., Mahler L., Baier M., Bittigau P., Obladen M., Ikonomidou C., Buehrer C. Caspase-1-processed interleukins in hyperoxia-induced cell death in the developing brain. Ann. Neurol. 2005, 57:50-59.
20. Genc S., Akhisaroglu M., Kuralay F., Genc K. Erythropoietin restores glutathione peroxidase activity in 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine-induced neurotoxicity in C57BL mice and stimulates murine astroglial glutathione peroxidase production in vitro. Neurosci. Lett. 2002, 321:73-76.
21. Gerstner B., Bührer C., Rheinländer C., Polley O., Schüller A., Berns M., Obladen M., Felderhoff-Mueser U. Maturation-dependent oligodendrocyte apoptosis caused by hyperoxia. J. Neurosci. Res. 2006, 84:306-315.
22. Gerstner B., DeSilva T.M., Genz K., Armstrong A., Brehmer F., Neve R.L., Felderhoff-Mueser U., Volpe J.J., Rosenberg P.A. Hyperoxia causes maturation-dependent cell death in the developing white matter. J. Neurosci. 2008, 28:1236-1245.
23. Gerstner B., Sifringer M., Dzietko M., Schüller A., Lee J., Simons S., Obladen M., Volpe J.J., Rosenberg P.A., Felderhoff-Mueser U. Estradiol attenuates hyperoxia-induced cell death in the developing white matter. Ann. Neurol. 2007, 61:562-573.
24. Ghezzi P., Brines M. Erythropoietin as an antiapoptotic, tissue-protective cytokine. Cell Death Differ. 2004, 11:S37-S44.
25. Gilboa-Geffen A., Lacoste P.P., Soreq L., Cizeron-Clairac G., Le Panse R., Truffault F., Shaked I., Soreq H., Berrih-Aknin S. The thymic theme of acetylcholinesterase splice variants in myasthenia gravis. Blood 2007, 109:4383-4391.
26. Giustarini D., Rossi R., Milzani A., Colombo R., Dalle-Donne I. S-Glutathionylation: from redox regulation of protein functions to human diseases. J. Cell. Mol. Med. 2004, 8:201-212.
27. Grisaru D., Pick M., Perry C., Sklan E.H., Almog R., Goldberg I., Naparstek E., Lessing J.B., Soreq H., Deutsch V. Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. J. Immunol. 2006, 176:27-35.
28. Guan L., Wen T., Zhang Y., Wang X., Zhao J. Induction of heme oxygenase-1 with hemin attenuates hippocampal injury in rats after acute carbon monoxide poisoning. Toxicology 2009, 262:146-152.
29. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 2006, 97:1634-1658.
30. Hamrick S.E., Miller S.P., Leonard C., Glidden D.V., Goldstein R., Ramaswamy V., Piecuch R., Ferriero D.M. Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J. Pediatr. 2004, 145:593-599.
31. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione. Anal. Biochem. 1976, 74:77-82.
32. Hoehn T., Felderhoff-Mueser U., Maschewski K., Stadelmann C., Sifringer M., Bittigau P., Koehne P., Hoppenz M., Obladen M., Buehrer C. Hyperoxia causes inducible nitric oxide synthase-mediated cellular damage to the immature rat brain. Pediatr. Res. 2003, 54:179-184.
33. Janaky R., Ogita K., Pasqualotto B.A., Bains J.S., Oja S.S., Yoneda Y., Shaw C.A. Glutathione and signal transduction in the mammalian CNS. J. Neurochem. 1999, 73:889-902.
34. Juul S., Felderhoff-Mueser U. Epo and other hematopoietic factors. Semin. Fetal Neonatal Med. 2007, 12:250-258.
35. Kaindl A.M., Sifringer M., Koppelstaetter A., Genz K., Loeber R., Boerner C., Stuwe J., Klose J., Felderhoff-Mueser U. Erythropoietin protects the developing brain from hyperoxia-induced cell death and proteome changes. Ann. Neurol. 2008, 64:523-534.
36. Katavetin P., Inagi R., Miyata T., Shao J., Sassa R., Adler S., Eto N., Kato H., Fujita T., Nangaku M. Erythropoietin induces heme oxygenase-1 expression and attenuates oxidative stress. Biochem. Biophys. Res. Commun. 2007, 359:928-934.
37. Kaufer D., Friedman A., Seidman S., Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 1998, 393:373-377.
38. Keller M., Yang J., Griesmaier E., Gorna A., Sarkozy G., Urbanek M., Gressens P., Simbruner G. Erythropoietin is neuroprotective against NMDA-receptor-mediated excitotoxic brain injury in newborn mice. Neurobiol. Dis. 2006, 24:357-366.
39. Kumral A., Gonenc S., Acikgoz O., Sonmez A., Genc K., Yilmaz O., Gokmen N., Duman N., Ozkan H. Erythropoietin increases glutathione peroxidase enzyme activity and decreases lipid peroxidation levels in hypoxic-ischemic brain injury in neonatal rats. Biol. Neonate 2005, 87:15-18.
40. Kwak D.J., Kwak S.D., Gauda E.B. The effect of hyperoxia on reactive oxygen species (ROS) in rat petrosal ganglion neurons during development using organotypic slices. Pediatr. Res. 2006, 60:371-376.
41. Li R.C., Saleem S., Zhen G., Cao W., Zhuang H., Lee J., Smith A., Altruda F., Tolosano E., Doré S. Heme-hemopexin complex attenuates neuronal cell death and stroke damage. J. Cereb. Blood Flow Metab. 2009, 29:953-964.
42. Li F., Chong Z.Z., Maiese K. Microglial integrity is maintained by erythropoietin through integration of Akt and its substrates of glycogen synthase kinase-3beta, beta-catenin, and nuclear factor-kappaB. Curr. Neurovasc. Res. 2006, 3:187-201.
43. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25:402-408.
44. Maltepe E., Saugstad O.D. Oxygen in health and disease: regulation of oxygen homeostasis-clinical implications. Pediatr. Res. 2009, 65:261-268.
45. Mariani E., Polidori M.C., Cherubini A., Mecocci P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2005, 827:65-75.
46. Meshorer E., Erb C., Gazit R., Pavlovsky L., Kaufer D., Friedman A., Glick D., Ben-Arie N., Soreq H. Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science 2002, 295:508-512.
47. Metz C.N., Tracey K.J. It takes nerve to dampen inflammation. Nat. Immunol. 2005, 6:756-757.
48. Mori H., Oikawa M., Tamagami T., Kumaki H., Nakaune R., Amano J., Akinaga Y., Fukui K., Abe K., Urano S. Oxidized proteins in astrocytes generated in a hyperbaric atmosphere induce neuronal apoptosis. J. Alzheimers Dis. 2007, 11:165-174.
49. Morse D., Choi A.M. Heme oxygenase-1: the " emerging molecule" has arrived. Am. J. Respir. Cell Mol. Biol. 2002, 27:8-16.
50. Ofek K., Krabbe K.S., Evron T., Debecco M., Nielsen A.R., Brunnsgaad H., Yirmiya R., Soreq H., Pedersen B.K. Cholinergic status modulations in human volunteers under acute inflammation. J. Mol. Med. 2007, 85:1239-1251.
51. Pick M., Perry C., Lapidot T., Guimaraes-Sternberg C., Naparstek E., Deutsch V., Soreq H. Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood 2006, 107:3397-3406.
52. Poot M., Teubert H., Rabinovitch P.S., Kavanagh T.J. De novo synthesis of glutathione is required for both entry into and progression through the cell cycle. J. Cell. Physiol. 1995, 163:555-560.
53. Sagara J., Makino N. Glutathione induces neuronal differentiation in rat bone marrow stromal cells. Neurochem. Res. 2008, 33:16-21.
54. Sakanaka M., Wen T.C., Matsuda S., Masuda S., Morishita E., Nagao M., Sasaki R. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc. Natl. Acad. Sci. USA 1998, 95:4635-4640.
55. Saleem S., Zhuang H., Biswal S., Christen Y., Doré S. Ginkgo biloba extract neuroprotective action is dependent on heme oxygenase 1 in ischemic reperfusion brain injury. Stroke 2008, 39:3389-3396.
56. Saugstad O.D. Is oxygen more toxic than currently believed?. Pediatrics 2001, 108:1203-1205.
57. Short E.J., Klein N.K., Lewis B.A., Fulton S., Eisengart S., Kercsmar C., Baley J., Singer L.T. Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes. Pediatrics 2003, 112:359.
58. Sifringer M., Genz K., Brait D., Brehmer F., Löber R., Weichelt U., Kaindl A.M., Gerstner B., Felderhoff-Mueser U. Erythropoietin attenuates hyperoxia-induced cell death by modulation of inflammatory mediators and matrix metalloproteinases. Dev. Neurosci. 2009, 31:394-402.
59. Sola A., Wen T.C., Hamrick S.E., Ferriero D.M. Potential for protection and repair following injury to the developing brain: a role for erythropoietin?. Pediatr. Res. 2005, 57:R110-R117.
60. Solaroglu I., Solaroglu A., Kaptanoglu E., Dede S., Haberal A., Beskonakli E., Kilinc K. Erythropoietin prevents ischemia-reperfusion from inducing oxidative damage in fetal rat brain. Childs Nerv. Syst. 2003, 19:19-22.
61. Sommerburg O., Grune T., Klee S., Ungemach F.R., Siems W.G. Formation of 4-hydroxynonenal and further aldehydic mediators of inflammation during bromotrochloromethane treatment of liver cells. Mediat. Inflamm. 1993, 2:27-31.
62. Tateishi N., Higashi T., Naruse A., Nakashima K., Shiozaki H. Rat liver glutathione: possible role as a reservoir of cysteine. J. Nutr. 1977, 107:51-60.
63. van der Kooij M.A., Groenendaal F., Kavelaars A., Heijnen C.J., van Bel F. Neuroprotective properties and mechanisms of erythropoietin in in vitro and in vivo experimental models for hypoxia/ischemia. Brain Res. Rev. 2008, 59:22-33.
64. Vreman H.J., Stevenson D.K. Heme oxygenase activity as measured by carbon monoxide production. Anal. Biochem. 1988, 168:31-38.
65. Wong S.H.J., Knight J.A., Hopfer S.M., Zaharia O., Leach C.N., Sunderman F.W. Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin. Chem. 1987, 33:214-220.
66. Xiong Y., Chopp M., Lee C.P. Erythropoietin improves brain mitochondrial function in rats after traumatic brain injury. Neurol. Res. 2009, 31:496-502.
67. Zimmerman G., Soreq H. Termination and beyond: acetylcholinesterase as a modulator of synaptic transmission. Cell Tissue Res. 2006, 326:655-669.