Glutathione peroxidase overexpression causes aberrant ERK activation in neonatal mouse cortex after hypoxic preconditioning

Pediatric Research

Volumn 72, Issue 6, 2012, Pages 568-575

  Autheman, Delphine ^a   Sheldon, R Ann ^b   Chaudhuri, Nondini ^a   Von Arx, Sebastian ^a   Siegenthaler, Corinne ^a   Ferriero, Donna M ^b   Christen, Stephan ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; REOXYGENATION;

ANIMALS; ANIMALS, NEWBORN; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTATHIONE PEROXIDASE; MICE; PHOSPHORYLATION;

EID: 84871322482     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1038/pr.2012.124     Document Type: Article

References (43)

1. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009;8:398-412.
2. Sheldon RA, Aminoff A, Lee CL, Christen S, Ferriero DM. Hypoxic preconditioning reverses protection after neonatal hypoxia-ischemia in glutathione peroxidase transgenic murine brain. Pediatr Res 2007;61:666-70.
3. Fullerton HJ, Ditelberg JS, Chen SF, et al. Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann Neurol 1998;44:357-64.
4. Sheldon RA, Jiang X, Francisco C, et al. Manipulation of antioxidant pathways in neonatal murine brain. Pediatr Res 2004;56:656-62.
5. Weisbrot-Lefkowitz M, Reuhl K, Perry B, Chan PH, Inouye M, Mirochnitchenko O. Overexpression of human glutathione peroxidase protects transgenic mice against focal cerebral ischemia/reperfusion damage. Brain Res Mol Brain Res 1998;53:333-8.
6. Sheldon RA, Christen S, Ferriero DM. Genetic and pharmacologic manipulation of oxidative stress after neonatal hypoxia-ischemia. Int J Dev Neurosci 2008;26:87-92.
7. Ditelberg JS, Sheldon RA, Epstein CJ, Ferriero DM. Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatr Res 1996;39:204-8.
8. Sawe N, Steinberg G, Zhao H. Dual roles of the MAPK/ERK1/2 cell signaling pathway after stroke. J Neurosci Res 2008;86:1659-69.
9. Wick A, Wick W, Waltenberger J, Weller M, Dichgans J, Schulz JB. Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J Neurosci 2002;22:6401-7.
10. Gonzalez-Zulueta M, Feldman AB, Klesse LJ, et al. Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 2000;97:436-41.
11. Jones NM, Bergeron M. Hypoxia-induced ischemic tolerance in neonatal rat brain involves enhanced ERK1/2 signaling. J Neurochem 2004;89:157-67.
12. Zhao H, Sapolsky RM, Steinberg GK. Phosphoinositide-3-kinase/akt survival signal pathways are implicated in neuronal survival after stroke. Mol Neurobiol 2006;34:249-70.
13. Guyton KZ, Liu Y, Gorospe M, Xu Q, Holbrook NJ. Activation of mitogenactivated protein kinase by H2O2. Role in cell survival following oxidant injury. J Biol Chem 1996;271:4138-42.
14. Leslie NR. The redox regulation of PI 3-kinase-dependent signaling. Antioxid Redox Signal 2006;8:1765-74.
15. Chandel NS, McClintock DS, Feliciano CE, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000;275:25130-8.
16. Sheldon RA, Sedik C, Ferriero DM. Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res 1998;810:114-22.
17. Mebratu Y, Tesfaigzi Y. How ERK1/2 activation controls cell proliferation and cell death: is subcellular localization the answer? Cell Cycle 2009;8:1168-75.
18. Ma MC, Qian H, Ghassemi F, Zhao P, Xia Y. Oxygen-sensitive {Δ}-opioid receptor-regulated survival and death signals: novel insights into neuronal preconditioning and protection. J Biol Chem 2005;280:16208-18.
19. Gu Z, Jiang Q, Zhang G, Cui Z, Zhu Z. Diphosphorylation of extracellular signal-regulated kinases and c-Jun N-terminal protein kinases in brain ischemic tolerance in rat. Brain Res 2000;860:157-60.
20. Gu Z, Jiang Q, Zhang G. Extracellular signal-regulated kinase and c-Jun N-terminal protein kinase in ischemic tolerance. Neuroreport 2001;12:3487-91.
21. Choi JS, Kim HY, Cha JH, Lee MY. Ischemic preconditioning-induced activation of ERK1/2 in the rat hippocampus. Neurosci Lett 2006;409:187-91.
22. Ravati A, Ahlemeyer B, Becker A, Krieglstein J. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 2000;866:23-32.
23. Furuichi T, Liu W, Shi H, Miyake M, Liu KJ. Generation of hydrogen peroxide during brief oxygen-glucose deprivation induces preconditioning neuronal protection in primary cultured neurons. J Neurosci Res 2005;79:816-24.
24. Simerabet M, Robin E, Aristi I, et al. Preconditioning by an in situ administration of hydrogen peroxide: involvement of reactive oxygen species and mitochondrial ATP-dependent potassium channel in a cerebral ischemiareperfusion model. Brain Res 2008;1240:177-84.
25. Chang S, Jiang X, Zhao C, Lee C, Ferriero DM. Exogenous low dose hydrogen peroxide increases hypoxia-inducible factor-1alpha protein expression and induces preconditioning protection against ischemia in primary cortical neurons. Neurosci Lett 2008;441:134-8.
26. Khanna S, Roy S, Maurer M, Ratan RR, Sen CK. Oxygen-sensitive reset of hypoxia-inducible factor transactivation response: prolyl hydroxylases tune the biological normoxic set point. Free Radic Biol Med 2006;40: 2147-54.
27. Luo Y, DeFranco DB. Opposing roles for ERK1/2 in neuronal oxidative toxicity: distinct mechanisms of ERK1/2 action at early versus late phases of oxidative stress. J Biol Chem 2006;281:16436-42.
28. Wu HW, Li HF, Wu XY, Zhao J, Guo J. Reactive oxygen species mediate ERK activation through different Raf-1-dependent signaling pathways following cerebral ischemia. Neurosci Lett 2008;432:83-7.
29. Guo J, Wu HW, Hu G, Han X, De W, Sun YJ. Sustained activation of Srcfamily tyrosine kinases by ischemia: a potential mechanism mediating extracellular signal-regulated kinase cascades in hippocampal dentate gyrus. Neuroscience 2006;143:827-36.
30. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 2000;48:285-96.
31. Baranova O, Miranda LF, Pichiule P, Dragatsis I, Johnson RS, Chavez JC. Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 2007;27:6320-32.
32. Helton R, Cui J, Scheel JR, et al. Brain-specific knock-out of hypoxiainducible factor-1alpha reduces rather than increases hypoxic-ischemic damage. J Neurosci 2005;25:4099-107.
33. Sheldon RA, Osredkar D, Lee CL, Jiang X, Mu D, Ferriero DM. HIF-1 alpha-deficient mice have increased brain injury after neonatal hypoxiaischemia. Dev Neurosci 2009;31:452-8.
34. Minet E, Arnould T, Michel G, et al. ERK activation upon hypoxia: involvement in HIF-1 activation. FEBS Lett 2000;468:53-8.
35. Mylonis I, Chachami G, Samiotaki M, et al. Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxiainducible factor-1alpha. J Biol Chem 2006;281:33095-106.
36. Li L, Xiong Y, Qu Y, et al. The requirement of extracellular signal-related protein kinase pathway in the activation of hypoxia inducible factor 1 alpha in the developing rat brain after hypoxia-ischemia. Acta Neuropathol 2008;115:297-303.
37. Wang X, Zhu C, Qiu L, Hagberg H, Sandberg M, Blomgren K. Activation of ERK1/2 after neonatal rat cerebral hypoxia-ischaemia. J Neurochem 2003;86:351-62.
38. Han BH, Holtzman DM. BDNF protects the neonatal brain from hypoxicischemic injury in vivo via the ERK pathway. J Neurosci 2000;20:5775-81.
39. Mirault ME, Tremblay A, Furling D, et al. Transgenic glutathione peroxidase mouse models for neuroprotection studies. Ann N Y Acad Sci 1994;738:104-15.
40. Sury MD, Agarinis C, Widmer HR, Leib SL, Christen S. JNK is activated but does not mediate hippocampal neuronal apoptosis in experimental neonatal pneumococcal meningitis. Neurobiol Dis 2008;32:142-50.
41. Sury MD, Frese-Schaper M, M?lemann MK, et al. Evidence that N-acetylcysteine inhibits TNF-alpha-induced cerebrovascular endothelin-1 upregulation via inhibition of mitogen-and stress-activated protein kinase. Free Radic Biol Med 2006;41:1372-83.
42. Lahiri DK, Ge Y. Electrophoretic mobility shift assay for the detection of specific DNA-protein complex in nuclear extracts from the cultured cells and frozen autopsy human brain tissue. Brain Res Brain Res Protoc 2000;5:257-65.
43. Tang X, Falls DL, Li X, Lane T, Luskin MB. Antigen-retrieval procedure for bromodeoxyuridine immunolabeling with concurrent labeling of nuclear DNA and antigens damaged by HCl pretreatment. J Neurosci 2007;27:5837-44.