Neurons lacking iron regulatory protein-2 are highly resistant to the toxicity of hemoglobin

Neurobiology of Disease

Volumn 31, Issue 2, 2008, Pages 242-249

  Regan, Raymond F ^a   Chen, Mai ^a   Li, Zhi ^a   Zhang, Xuefeng ^a   Benvenisti Zarom, Luna ^a   Chen Roetling, Jing ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Cell culture; Free radical; Hemoglobin toxicity; Intracerebral hemorrhage; Iron; Oxidative stress; Stroke

Indexed keywords

HEME OXYGENASE 1; HEMOGLOBIN; IRON REGULATORY PROTEIN 2; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN HEMORRHAGE; CONTROLLED STUDY; GENE DELETION; KNOCKOUT MOUSE; MOUSE; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROKE;

ANIMALS; ASTROCYTES; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; CEREBRAL HEMORRHAGE; DRUG RESISTANCE; FEMALE; FERRITINS; GENETIC PREDISPOSITION TO DISEASE; HEME OXYGENASE-1; HEMOGLOBINS; IRON METABOLISM DISORDERS; IRON REGULATORY PROTEIN 2; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NEURONS; OXIDATIVE STRESS; PROTEIN BINDING;

EID: 47149093139     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.04.008     Document Type: Article

References (60)

1. Arosio P., and Levi S. Ferritin, iron homeostasis, and oxidative damage. Free Radic. Biol. Med. 33 (2002) 457-463
2. Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., and Vercellotti G.M. Ferritin: a cytoprotective strategem of endothelium. J. Biol. Chem. 267 (1992) 18148-18153
3. Beaumont C., Dugast I., Renaudie F., Souroujon M., and Grandchamp B. Transcriptional regulation of ferritin H and L subunits in adult erythroid and liver cells from the mouse. Unambiguous identification of mouse ferritin subunits and in vitro formation of ferritin shells. J. Biol. Chem. 264 (1989) 7498-7504
4. Bishop G.M., and Robinson S.R. Quantitative analysis of cell death and ferritin expression in response to cortical iron: implications for hypoxia-ischemia and stroke. Brain Res. 907 (2001) 175-187
5. Brewer G.J. Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42 (1995) 674-683
6. Browne P., Shalev O., and Hebbel R.P. The molecular pathobiology of cell membrane iron: the sickle red cell as a model. Free Radic. Biol. Med. 24 (1998) 1040-1048
7. Cheepsunthorn P., Palmer C., and Connor J.R. Cellular distribution of ferritin subunits in postnatal rat brain. J. Comp. Neurol. 400 (1998) 73-86
8. Chen J., and Regan R.F. Heme oxygenase-2 gene deletion increases astrocyte vulnerability to hemin. Biochem. Biophys. Res. Commun. 318 (2004) 88-94
9. Chen-Roetling J., and Regan R.F. Effect of heme oxygenase-1 on the vulnerability of astrocytes and neurons to hemoglobin. Biochem. Biophys. Res. Commun. 350 (2006) 233-237
10. Cozzi A., Corsi B., Levi S., Santambrogio P., Biasiotto G., and Arosio P. Analysis of the biologic functions of H- and L-ferritins in HeLa cells by transfection with siRNAs and cDNAs: evidence for a proliferative role of L-ferritin. Blood 103 (2004) 2377-2383
11. Festa M., Colonna A., Pietropaolo C., and Ruffo A. Oxalomalate, a competitive inhibitor of aconitase, modulates the RNA-binding activity of iron-regulatory proteins. Biochem. J. 348 Pt 2 (2000) 315-320
12. Goldstein L., Teng Z.P., Zeserson E., Patel M., and Regan R.F. Hemin induces an iron-dependent, oxidative injury on human neuron-like cells. J. Neurosci. Res. 73 (2003) 113-121
13. Gutteridge J.M.C. Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Lett. 201 (1986) 291-295
14. Gwag B.J., Lobner D., Koh J.Y., Wie M.B., and Choi D.W. Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience 68 (1995) 615-619
15. Halliwell B., and Gutteridge J.M.C. Free Radicals in Biology and Medicine (1999), Oxford University Press, Oxford 936
16. Hansen T.M., Nielsen H., Bernth N., and Moos T. Expression of ferritin protein and subunit mRNAs in normal and iron deficient rat brain. Brain Res. Mol. Brain Res. 65 (1999) 186-197
17. Harrison P.M., and Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275 (1996) 161-203
18. Hintze K.J., and Theil E.C. DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 15048-15052
19. Hua Y., Nakamura T., Keep R.F., Wu J., Schallert T., Hoff J.T., and Xi G. Long-term effects of experimental intracerebral hemorrhage: the role of iron. J. Neurosurg. 104 (2006) 305-312
20. Huang F.P., Xi G., Keep R.F., Hua Y., Nemoianu A., and Hoff J.T. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J. Neurosurg. 96 (2002) 287-293
21. Iwasaki K., Mackenzie E.L., Hailemariam K., Sakamoto K., and Tsuji Y. Hemin-mediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells. Mol. Cell. Biol. 26 (2006) 2845-2856
22. Kakhlon O., and Cabantchik Z.I. The labile iron pool: characterization, measurement, and participation in cellular processes(1). Free Radic. Biol. Med. 33 (2002) 1037-1046
23. Koeppen A.H., Dickson A.C., and McEvoy J.A. The cellular reactions to experimental intracerebral hemorrhage. J. Neurol. Sci. 134 (1995) 102-112 Suppl
24. Koeppen A.H., Dickson A.C., and Smith J. Heme oxygenase in experimental intracerebral hemorrhage: the benefit of tin-mesoporphyrin. J. Neuropathol. Exp. Neurol. 63 (2004) 587-597
25. Koh J.Y., and Choi D.W. Vulnerability of cultured cortical neurons to damage by excitotoxins: differential susceptibility of neurons containing NADPH-diaphorase. J. Neurosci. 8 (1988) 2153-2163
26. Kress G.J., Dineley K.E., and Reynolds I.J. The relationship between intracellular free iron and cell injury in cultured neurons, astrocytes, and oligodendrocytes. J. Neurosci. 22 (2002) 5848-5855
27. Kushner J.P., Porter J.P., and Olivieri N.F. Secondary iron overload. Hematology 2001 (2001) 47-61
28. Lamb N.J., Quinlan G.J., Mumby S., Evans T.W., and Gutteridge J.M.C. Haem oxygenase shows pro-oxidant activity in microsomal and cellular systems: implications for the release of low-molecular-mass iron. Biochem. J. 344 (1999) 153-158
29. LaVaute T., Smith S., Cooperman S., Iwai K., Land W., Meyron-Holtz E., Drake S.K., Miller G., Abu-Asab M., Tsokos M., Switzer III R., Grinberg A., Love P., Tresser N., and Rouault T.A. Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat. Genet. 27 (2001) 209-214
30. +-ATPase: protection by tin protoporphyrin. Neurochem. Res. 14 (1989) 861-864
31. Levi S., Yewdall S.J., Harrison P.M., Santambrogio P., Cozzi A., Rovida E., Albertini A., and Arosio P. Evidence of H- and L-chains have cooperative roles in the iron-uptake mechanism of human ferritin. Biochem. J. 288 (1992) 591-596
32. Lin F., and Girotti A.W. Hemin-enhanced resistance of human leukemia cells to oxidative killing: antisense determination of ferritin involvement. Arch. Biochem. Biophys. 352 (1998) 51-58
33. Malecki E.A., Cable E.E., Isom H.C., and Connor J.R. The lipophilic iron compound TMH-ferrocene [(3,5,5-trimethylhexanoyl)ferrocene] increases iron concentrations, neuronal L-ferritin, and heme oxygenase in brains of BALB/c mice. Biol. Trace Elem. Res. 86 (2002) 73-84
34. Masuda T., Hida H., Kanda Y., Aihara N., Ohta K., Yamada K., and Nishino H. Oral administration of metal chelator ameliorates motor dysfunction after a small hemorrhage near the internal capsule in rat. J. Neurosci. Res. 85 (2007) 213-222
35. Meyron-Holtz E.G., Ghosh M.C., Iwai K., LaVaute T., Brazzolotto X., Berger U.V., Land W., Ollivierre-Wilson H., Grinberg A., Love P., and Rouault T.A. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. Embo J. 23 (2004) 386-395
36. Moos T., and Morgan E.H. The metabolism of neuronal iron and its pathogenic role in neurological disease: review. Ann. N. Y. Acad. Sci. 1012 (2004) 14-26
37. Muñoz A.M., Rey P., Parga J., Guerra M.J., and Labandeira-Garcia J.L. Glial overexpression of heme oxygenase-1: a histochemical marker for early stages of striatal damage. J. Chem. Neuroanat. 29 (2005) 113-126
38. Nakamura T., Keep R.F., Hua Y., Schallert T., Hoff J.T., and Xi G. Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J. Neurosurg. 100 (2004) 672-678
39. Ohashi T., Mizutani A., Murakami A., Kojo S., Ishii T., and Taketani S. Rapid oxidation of dichlorofluorescin with heme and hemoproteins: formation of fluorescein is independent of the generation of reactive oxygen species. FEBS Lett. 511 (2002) 21-27
40. Porter J.B., and Huehns E.R. The toxic effects of desferrioxamine. Baillieres Clin. Haematol. 2 (1989) 459-474
41. Qi Y., Jamindar T.M., and Dawson G. Hypoxia alters iron homeostasis and induces ferritin synthesis in oligodendrocytes. J. Neurochem. 64 (1995) 2458-2464
42. Qu Y., Chen J., Benvenisti-Zarom L., Ma X., and Regan R.F. Effect of targeted deletion of the heme oxygenase-2 gene on hemoglobin toxicity in the striatum. J. Cereb. Blood Flow Metab. 25 (2005) 1466-1475
43. Qu Y., Chen-Roetling J., Benvenisti-Zarom L., and Regan R.F. Attenuation of oxidative injury after induction of experimental intracerebral hemorrhage in heme oxygenase-2 knockout mice. J. Neurosurg. 106 (2007) 428-435
44. Regan R.F., Chen J., and Benvenisti-Zarom L. Heme oxygenase-2 gene deletion attenuates oxidative stress in neurons exposed to extracellular hemin. BMC Neurosci. 5 (2004) 34
45. Regan R.F., and Choi D.W. The effect of NMDA, AMPA/kainate, and calcium channel antagonists on traumatic cortical neuronal injury in culture. Brain Res. 633 (1994) 236-242
46. Regan R.F., Kumar N., Gao F., and Guo Y.P. Ferritin induction protects cortical astrocytes from heme-mediated oxidative injury. Neuroscience 113 (2002) 985-994
47. Regan R.F., and Panter S.S. Neurotoxicity of hemoglobin in cortical cell culture. Neurosci. Lett. 153 (1993) 219-222
48. Regan R.F., and Rogers B. Delayed treatment of hemoglobin neurotoxicity. J. Neurotrauma 20 (2003) 111-120
49. Rogers B., Yakopson V., Teng Z.P., Guo Y., and Regan R.F. Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Rad. Biol. Med. 35 (2003) 872-881
50. Royall J.A., and Ischiropoulos H. Evaluation of 2′,7′-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch. Biochem. Biophys. 302 (1993) 348-355
51. Sadrzadeh S.M.H., Anderson D.K., Panter S.S., Hallaway P.E., and Eaton J.W. Hemoglobin potentiates central nervous system damage. J. Clin. Invest. 79 (1987) 662-664
52. Santamaria R., Irace C., Festa M., Maffettone C., and Colonna A. Induction of ferritin expression by oxalomalate. Biochim. Biophys. Acta 1691 (2004) 151-159
53. Song S., Hua Y., Keep R.F., Hoff J.T., and Xi G. A new hippocampal model for examining intracerebral hemorrhage-related neuronal death: effects of deferoxamine on hemoglobin-induced neuronal death. Stroke 38 (2007) 2861-2863
54. Tampo Y. Studies on membrane factors in iron-supported lipid peroxidation. Yakugaku Zasshi 120 (2000) 387-396
55. Torti F.M., and Torti S.V. Regulation of ferritin genes and protein. Blood 99 (2002) 3505-3516
56. Wagner K.R., Sharp F.R., Ardizzone T.D., Lu A., and Clark J.F. Heme and iron metabolism: role in cerebral hemorrhage. J. Cereb. Blood Flow Metab. 23 (2003) 629-652
57. Wang W., Di X., D'Agostino Jr. R.B., Torti S.V., and Torti F.M. Excess capacity of the iron regulatory protein system. J. Biol. Chem. 282 (2007) 24650-24659
58. Wu J., Hua Y., Keep R.F., Nakemura T., Hoff J.T., and Xi G. Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke 34 (2003) 2964-2969
59. Xi G.H., Keep R.F., and Hoff J.T. Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J. Neurosurg. 89 (1998) 991-996
60. Yoshida T., and Migita C.T. Mechanism of heme degradation by heme oxygenase. J. Inorg. Biochem. 82 (2000) 33-41