Nitric oxide induces hypoxia ischemic injury in the neonatal brain via the disruption of neuronal iron metabolism

Redox Biology

Volumn 6, Issue , 2015, Pages 112-121

  Lu, Qing ^a   Harris, Valerie A ^a   Rafikov, Ruslan ^b   Sun, Xutong ^b   Kumar, Sanjiv ^a   Black, Stephen M ^b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Hydroxyl radical; Hypoxia ischemia; Iron; Neonatal brain; Neuronal cell death; Nitric oxide

Indexed keywords

ACONITATE HYDRATASE; FERRITIN; HYDROXYL RADICAL; IRON; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TRANSFERRIN RECEPTOR; CULTURE MEDIUM; DEFEROXAMINE; GLUCOSE; N(G) NITROARGININE METHYL ESTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOTOXICITY; ENZYME ACTIVITY; HIPPOCAMPAL SLICE; HOMEOSTASIS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VITRO STUDY; IN VIVO STUDY; INVESTIGATIVE PROCEDURES; IRON METABOLISM; IRON STORAGE; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEWBORN; NEWBORN DISEASE; NONHUMAN; OXYGEN GLUCOSE DEPRIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DEATH; CELL HYPOXIA; CHEMICALLY INDUCED; CHEMISTRY; CULTURE MEDIUM; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; METABOLISM; MICROTOMY; NERVE CELL; PATHOLOGY; SPRAGUE DAWLEY RAT; TISSUE CULTURE TECHNIQUE;

ACONITATE HYDRATASE; ANIMALS; ANIMALS, NEWBORN; CELL DEATH; CELL HYPOXIA; CULTURE MEDIA; DEFEROXAMINE; FERRITINS; GENE EXPRESSION REGULATION; GLUCOSE; HIPPOCAMPUS; HYDROXYL RADICAL; HYPOXIA-ISCHEMIA, BRAIN; IRON; MICROTOMY; NEURONS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFERRIN; TISSUE CULTURE TECHNIQUES;

EID: 84937806176     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.06.007     Document Type: Article

References (83)

1. Ferriero D.M. Neonatal brain injury. N. Engl. J. Med. 2004, 351(19):1985-1995. http://www.ncbi.nlm.nih.gov/pubmed/15525724, 10.1056/NEJMra041996.
2. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 1999, 79(4):1431-1568. http://www.ncbi.nlm.nih.gov/pubmed/10508238.
3. Martin L.J., Brambrink A.M., Price A.C., Kaiser A., Agnew D.M., Ichord R.N., et al. Neuronal death in newborn striatum after hypoxia-ischemia is necrosis and evolves with oxidative stress. Neurobiol. Dis. 2000, 7(3):169-191. http://www.ncbi.nlm.nih.gov/pubmed/10860783, 10.1006/nbdi.2000.0282.
4. Clarkson A.N., Sutherland B.A., Appleton I. The biology and pathology of hypoxia-ischemia: an update. Arch. Immunol. Ther. Exp. (Warsz.) 2005, 53(3):213-225. http://www.ncbi.nlm.nih.gov/pubmed/15995582.
5. Lu Q., Wainwright M.S., Harris V.A., Aggarwal S., Hou Y., Rau T., et al. Increased NADPH oxidase-derived superoxide is involved in the neuronal cell death induced by hypoxia-ischemia in neonatal hippocampal slice cultures. Free Radic. Biol. Med. 2012, 53(5):1139-1151. http://www.ncbi.nlm.nih.gov/pubmed/22728269, 10.1016/j.freeradbiomed.2012.06.012.
6. Lu Q., Rau T.F., Harris V., Johnson M., Poulsen D.J., Black S.M. Increased p38 mitogen-activated protein kinase signaling is involved in the oxidative stress associated with oxygen and glucose deprivation in neonatal hippocampal slice cultures. Eur. J. Neurosci. 2011, 34(7):1093-1101. http://www.ncbi.nlm.nih.gov/pubmed/21939459, 10.1111/j.1460-9568.2011.07786.x.
7. Sheldon R.A., Jiang X., Francisco C., Christen S., Vexler Z.S., Täuber M.G., et al. Manipulation of antioxidant pathways in neonatal murine brain. Pediatr. Res. 2004, 56(4):656-662. http://www.ncbi.nlm.nih.gov/pubmed/15295091, 10.1203/01.PDR.0000139413.27864.50.
8. Jiang X., Mu D., Manabat C., Koshy A.A., Christen S., Täuber M.G., et al. Differential vulnerability of immature murine neurons to oxygen-glucose deprivation. Exp. Neurol. 2004, 190(1):224-232. http://www.ncbi.nlm.nih.gov/pubmed/15473995, 10.1016/j.expneurol.2004.07.010.
9. Moos T. Developmental profile of non-heme iron distribution in the rat brain during ontogenesis. Brain Res. Dev. Brain Res. 1995, 87(2):203-213. http://www.ncbi.nlm.nih.gov/pubmed/7586503.
10. Moos T., Rosengren Nielsen T. Ferroportin in the postnatal rat brain: implications for axonal transport and neuronal export of iron. Semin. Pediatr. Neurol. 2006, 13(3):149-157. http://www.ncbi.nlm.nih.gov/pubmed/17101453, 10.1016/j.spen.2006.08.003.
11. Moos T., Oates P.S., Morgan E.H. Expression of the neuronal transferrin receptor is age dependent and susceptible to iron deficiency. J. Comp. Neurol. 1998, 398(3):420-430. http://www.ncbi.nlm.nih.gov/pubmed/9714152.
12. Morgan E.H., Moos T. Mechanism and developmental changes in iron transport across the blood-brain barrier. Dev. Neurosci. 2002, 24(2-3):106-113. http://www.ncbi.nlm.nih.gov/pubmed/12401948.
13. Lipinski B. Hydroxyl radical and its scavengers in health and disease. Oxid. Med. Cell Longev. 2011, 2011:809696. http://www.ncbi.nlm.nih.gov/pubmed/21904647, 10.1155/2011/809696.
14. Edelman G.M., Gally J.A. Nitric oxide: linking space and time in the brain. Proc. Natl. Acad. Sci. USA 1992, 89(24):11651-11652. http://www.ncbi.nlm.nih.gov/pubmed/1334544, 10.1073/pnas.89.24.11651.
15. Mongin A.A., Dohare P., Jourd'heuil D. Selective vulnerability of synaptic signaling and metabolism to nitrosative stress. Antioxid. Redox Signal. 2012, 17(7):992-1012. http://www.ncbi.nlm.nih.gov/pubmed/22339371, 10.1089/ars.2012.4559.
16. Dachtler J., Hardingham N.R., Fox K. The role of nitric oxide synthase in cortical plasticity is sex specific. J. Neurosci. 2012, 32(43):14994-14999. http://www.ncbi.nlm.nih.gov/pubmed/23100421, 10.1523/JNEUROSCI.3189-12.2012.
17. Tórtora V., Quijano C., Freeman B., Radi R., Castro L. Mitochondrial aconitase reaction with nitric oxide, S-nitrosoglutathione, and peroxynitrite: mechanisms and relative contributions to aconitase inactivation. Free Radic. Biol. Med. 2007, 42(7):1075-1088. http://www.ncbi.nlm.nih.gov/pubmed/17349934, 10.1016/j.freeradbiomed.2007.01.007.
18. Castro L.A., Robalinho R.L., Cayota A., Meneghini R., Radi R. Nitric oxide and peroxynitrite-dependent aconitase inactivation and iron-regulatory protein-1 activation in mammalian fibroblasts. Arch. Biochem. Biophys. 1998, 359(2):215-224. http://www.ncbi.nlm.nih.gov/pubmed/9808763, 10.1006/abbi.1998.0898.
19. Cairo G., Ronchi R., Recalcati S., Campanella A., Minotti G. Nitric oxide and peroxynitrite activate the iron regulatory protein-1 of J774A.1 macrophages by direct disassembly of the Fe-S cluster of cytoplasmic aconitase. Biol. Chem. 2002, 41(23):7435-7442. http://www.ncbi.nlm.nih.gov/pubmed/12044177, 10.1021/bi025756k.
20. Cronberg T., Rytter A., Asztély F., Söder A., Wieloch T. Glucose but not lactate in combination with acidosis aggravates ischemic neuronal death in vitro. Stroke 2004, 35(3):753-757. http://www.ncbi.nlm.nih.gov/pubmed/14963271, 10.1161/01.STR.0000117576.09512.32.
21. Gardner P.R., Raineri I., Epstein L.B., White C.W. Superoxide radical and iron modulate aconitase activity in mammalian cells. J. Biol. Chem. 1995, 270(22):13399-13405. http://www.ncbi.nlm.nih.gov/pubmed/7768942, 10.1074/jbc.270.22.13399.
22. Lee D.H., Zhou L.J., Zhou Z., Xie J.X., Jung J.U., Liu Y., Xi C.X., Mei L., Xiong W.C. Neogenin inhibits HJV secretion and regulates BMP-induced hepcidin expression and iron homeostasis. Blood 2010, 115(15):3136-3145. http://www.ncbi.nlm.nih.gov/pubmed/20065295, 10.1182/blood-2009-11-251199.
23. Casanova M.F., Comparini S.O., Kim R.W., Kleinman J.E. Staining intensity of brain iron in patients with schizophrenia: a postmortem study. J. Neuropsychiatry Clin. Neurosci. 1992, 4(1):36-41. http://www.ncbi.nlm.nih.gov/pubmed/1627959, 10.1176/jnp.4.1.36.
24. Pieper G.M., Felix C.C., Kalyanaraman B., Turk M., Roza A.M. Detection by ESR of DMPO hydroxyl adduct formation from islets of langerhans. Free Radic. Biol. Med. 1995, 19(2):219-225. http://www.ncbi.nlm.nih.gov/pubmed/7649493.
25. Hentze M.W., Kühn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 1996, 93(16):8175-8182. http://www.ncbi.nlm.nih.gov/pubmed/8710843, 10.1073/pnas.93.16.8175.
26. Henderson B.R. Iron regulatory proteins 1 and 2. Bioessays 1996, 18(9):739-746. http://www.ncbi.nlm.nih.gov/pubmed/8831290, 10.1002/bies.950180909.
27. Mascotti D.P., Rup D., Thach R.E. Regulation of iron metabolism: translational effects mediated by iron, heme, and cytokines. Annu. Rev. Nutr. 1995, 15:239-261. http://www.ncbi.nlm.nih.gov/pubmed/8527220, 10.1146/annurev.nu.15.070195.001323.
28. Kühn L.C. Molecular regulation of iron proteins. Baillieres Clin. Haematol. 1994, 7(4):763-785. http://www.ncbi.nlm.nih.gov/pubmed/7881153, 10.1016/S0950-3536(05)80123-4.
29. Piñero D.J., Hu J., Connor J.R. Alterations in the interaction between iron regulatory proteins and their iron responsive element in normal and Alzheimer's diseased brains. Cell. Mol. Biol. Noisy le Grand 2000, 46(4):761-776. http://www.ncbi.nlm.nih.gov/pubmed/10875438.
30. du Plessis A.J., Johnston M.V. Hypoxic-ischemic brain injury in the newborn. cellular mechanisms and potential strategies for neuroprotection. Clin. Perinatol. 1997, 24(3):627-654. http://www.ncbi.nlm.nih.gov/pubmed/9394864.
31. Fenichel G.M. Hypoxic-ischemic encephalopathy in the newborn. Arch. Neurol. 1983, 40(5):261-266. http://www.ncbi.nlm.nih.gov/pubmed/6405725, 10.1001/archneur.1983.04050050029002.
32. Vannucci R.C., Perlman J.M. Interventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics 1997, 100(6):1004-1014. http://www.ncbi.nlm.nih.gov/pubmed/9374573, 10.1542/peds.100.6.1004.
33. Volpe J. Hypoxic-ishcemic encephalopathy. Neurology of the Newborn 1995, WB Saunders, Philadelphia.
34. Ferriero D.M., Arcavi L.J., Simon R.P. Ontogeny of excitotoxic injury to nicotinamide adenine dinucleotide phosphate diaphorase reactive neurons in the neonatal rat striatum. Neuroscience 1990, 36(2):417-424. http://www.ncbi.nlm.nih.gov/pubmed/2145527, 10.1016/0306-4522(90)90437-9.
35. Ferriero D.M., Sheldon R.A., Black S.M., Chuai J. Selective destruction of nitric oxide synthase neurons with quisqualate reduces damage after hypoxia-ischemia in the neonatal rat. Pediatr. Res. 1995, 38(6):912-918. http://www.ncbi.nlm.nih.gov/pubmed/8618793, 10.1203/00006450-199512000-00014.
36. Ferriero D.M., Holtzman D.M., Black S.M., Sheldon R.A. Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury. Neurobiol. Dis. 1996, 3(1):64-71. http://www.ncbi.nlm.nih.gov/pubmed/9173913, 10.1006/nbdi.1996.0006.
37. Burke R.E., Baimbridge K.G. Relative loss of the striatal striosome compartment, defined by calbindin-D28k immunostaining, following developmental hypoxic-ischemic injury. Neuroscience 1993, 56(2):305-315. http://www.ncbi.nlm.nih.gov/pubmed/8247262, 10.1016/0306-4522(93)90333-B.
38. Nowicki J.P., Duval D., Poignet H., Scatton B. Nitric oxide mediates neuronal death after focal cerebral ischemia in the mouse. Eur. J. Pharmacol. 1991, 204(3):339-340. http://www.ncbi.nlm.nih.gov/pubmed/1773832, 10.1016/0014-2999(91)90862-K.
39. Yamamoto S., Golanov E.V., Berger S.B., Reis D.J. Inhibition of nitric oxide synthesis increases focal ischemic infarction in rat. J. Cereb. Blood Flow Metab. 1992, 12(5):717-726. http://www.ncbi.nlm.nih.gov/pubmed/1380515, 10.1038/jcbfm.1992.102.
40. Depré C., Fiérain L., Hue L. Activation of nitric oxide synthase by ischaemia in the perfused heart. Cardiovasc. Res. 1997, 33(1):82-87. http://www.ncbi.nlm.nih.gov/pubmed/9059531, 10.1016/S0008-6363(96)00176-9.
41. Wada K., Chatzipanteli K., Busto R., Dietrich W.D. Role of nitric oxide in traumatic brain injury in the rat. J. Neurosurg. 1998, 89(5):807-818. http://www.ncbi.nlm.nih.gov/pubmed/9817419, 10.3171/jns.1998.89.5.0807.
42. Brevetti L.S., Chang D.S., Tang G.L., Sarkar R., Messina L.M. Overexpression of endothelial nitric oxide synthase increases skeletal muscle blood flow and oxygenation in severe rat hind limb ischemia. J. Vasc. Surg. 2003, 38(4):820-826. http://www.ncbi.nlm.nih.gov/pubmed/14560236, 10.1016/S0741-5214(03)00555-X.
43. Dawson T.M., Bredt D.S., Fotuhi M., Hwang P.M., Snyder S.H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 1991, 88(17):7797-7801. http://www.ncbi.nlm.nih.gov/pubmed/1715581, 10.1073/pnas.88.17.7797.
44. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 1991, 88(14):6368-6371. http://www.ncbi.nlm.nih.gov/pubmed/1648740, 10.1073/pnas.88.14.6368.
45. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 1993, 75(7):1273-1286. http://www.ncbi.nlm.nih.gov/pubmed/7505721, 10.1016/0092-8674(93)90615-W.
46. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994, 265(5180):1883-1885. http://www.ncbi.nlm.nih.gov/pubmed/7522345, 10.1126/science.7522345.
47. Huang Z., Huang P.L., Ma J., Meng W., Ayata C., Fishman M.C., et al. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J. Cereb. Blood Flow Metab. 1996, 16(5):981-987. http://www.ncbi.nlm.nih.gov/pubmed/8784243, 10.1097/00004647-199609000-00023.
48. Black S.M., Bedolli M.A., Martinez S., Bristow J.D., Ferriero D.M., Soifer S.J. Expression of neuronal nitric oxide synthase corresponds to regions of selective vulnerability to hypoxia-ischaemia in the developing rat brain. Neurobiol. Dis. 1995, 2(3):145-155. http://www.ncbi.nlm.nih.gov/pubmed/9173998, 10.1006/nbdi.1995.0016.
49. Li L.L., Ginet V., Liu X., Vergun O., Tuittila M., Mathieu M., et al. The nNOS-p38MAPK pathway is mediated by NOS1AP during neuronal death. J. Neurosci. 2013, 33(19):8185-8201. http://www.ncbi.nlm.nih.gov/pubmed/23658158, 10.1523/JNEUROSCI.4578-12.2013.
50. Tribe R.M., Poston L. Oxidative stress and lipids in diabetes: a role in endothelium vasodilator dysfunction?. Vasc. Med. 1996, 1(3):195-206. http://www.ncbi.nlm.nih.gov/pubmed/9546938.
51. Ronson R.S., Nakamura M., Vinten-Johansen J. The cardiovascular effects and implications of peroxynitrite. Cardiovasc. Res. 1999, 44(1):47-59. http://www.ncbi.nlm.nih.gov/pubmed/10615389, 10.1016/S0008-6363(99)00184-4.
52. Lynch J.K., Nelson K.B. Epidemiology of perinatal stroke. Curr. Opin. Pediatr. 2001, 13(6):499-505. http://www.ncbi.nlm.nih.gov/pubmed/11753097, 10.1097/00008480-200112000-00002.
53. Johnston M.V., Trescher W.H., Ishida A., Nakajima W. Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr. Res. 2001, 49(6):735-741. http://www.ncbi.nlm.nih.gov/pubmed/11385130, 10.1203/00006450-200106000-00003.
54. Johnston M.V., Trescher W.H., Ishida A., Nakajima W. Novel treatments after experimental brain injury. Semin. Neonatol. 2000, 5(1):75-86. http://www.ncbi.nlm.nih.gov/pubmed/10802752, 10.1053/siny.1999.0116.
55. Halliwell B. Reactive oxygen species and the central nervous system. J. Neurochem. 1992, 59(5):1609-1623. http://www.ncbi.nlm.nih.gov/pubmed/1402908, 10.1111/j.1471-4159.1992.tb10990.x.
56. Khan J.Y., Black S.M. Developmental changes in murine brain antioxidant enzymes. Pediatr. Res. 2003, 54(1):77-82. http://www.ncbi.nlm.nih.gov/pubmed/12646716, 10.1203/01.PDR.0000065736.69214.20.
57. Kinouchi H., Epstein C.J., Mizui T., Carlson E., Chen S.F., Chan P.H. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc. Natl. Acad. Sci. USA 1991, 88(24):11158-11162. http://www.ncbi.nlm.nih.gov/pubmed/1763030, 10.1073/pnas.88.24.11158.
58. Chan P.H., Epstein C.J., Li Y., Huang T.T., Carlson E., Kinouchi H., et al. Transgenic mice and knockout mutants in the study of oxidative stress in brain injury. J. Neurotrauma 1995, 12(5):815-824. http://www.ncbi.nlm.nih.gov/pubmed/8594209, 10.1089/neu.1995.12.815.
59. Chan P.H., Kawase M., Murakami K., Chen S.F., Li Y., Calagui B., et al. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J. Neurosci. 1998, 18(20):8292-8299. http://www.ncbi.nlm.nih.gov/pubmed/9763473.
60. Fullerton H.J., Ditelberg J.S., Chen S.F., Sarco D.P., Chan P.H., Epstein C.J., et al. Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann. Neurol. 1998, 44(3):357-364. http://www.ncbi.nlm.nih.gov/pubmed/9749602, 10.1002/ana.410440311.
61. Beard J.L., Connor J.R., Jones B.C. Iron in the brain. Nutr. Rev. 1993, 51(6):157-170. http://www.ncbi.nlm.nih.gov/pubmed/8371846, 10.1111/j.1753-4887.1993.tb03096.x.
62. Beard J.L., Connor J.D., Jones B.C. Brain iron: location and function. Prog. Food Nutr. Sci. 1993, 17(3):183-221. http://www.ncbi.nlm.nih.gov/pubmed/7901870.
63. Beard J. Iron deficiency alters brain development and functioning. J. Nutr. 2003, 133(5 Suppl. 1):1468S-1472S. http://www.ncbi.nlm.nih.gov/pubmed/12730445.
64. Halliwell B., Aeschbach R., Löliger J., Aruoma O.I. The characterization of antioxidants. Food Chem. Toxicol. 1995, 33(7):601-617. http://www.ncbi.nlm.nih.gov/pubmed/7628797, 10.1016/0278-6915(95)00024-V.
65. Halliwell B. The antioxidant paradox. Lancet 2000, 355(9210):1179-1180. http://www.ncbi.nlm.nih.gov/pubmed/10791396, 10.1016/S0140-6736(00)02075-4.
66. Nappi A.J., Vass E. Hydroxyl radical formation via iron-mediated Fenton chemistry is inhibited by methylated catechols. Biochim. Biophys. Acta 1998, 1425(1):159-167.
67. Connor J.R. Iron acquisition and expression of iron regulatory proteins in the developing brain: manipulation by ethanol exposure, iron deprivation and cellular dysfunction. Dev. Neurosci. 1994, 16(5-6):233-247. http://www.ncbi.nlm.nih.gov/pubmed/7768202, 10.1159/000112115.
68. Connor J.R. Iron regulation in the brain at the cell and molecular level. Adv. Exp. Med. Biol. 1994, 356:229-238. http://www.ncbi.nlm.nih.gov/pubmed/7887227, 10.1007/978-1-4615-2554-7_25.
69. Palmer C., Menzies S.L., Roberts R.L., Pavlick G., Connor J.R. Changes in iron histochemistry after hypoxic-ischemic brain injury in the neonatal rat. J. Neurosci. Res. 1999, 56(1):60-71. http://www.ncbi.nlm.nih.gov/pubmed/10213476.
70. Dietrich R.B., Bradley W.G. Iron accumulation in the basal ganglia following severe ischemic-anoxic insults in children. Radiology 1988, 168(1):203-206. http://www.ncbi.nlm.nih.gov/pubmed/3380958, 10.1148/radiology.168.1.3380958.
71. Hamilton K.O., Stallibrass L., Hassan I., Jin Y., Halleux C., Mackay M. The transport of two iron chelators, desferrioxamine B and L1, across Caco-2 monolayers. Br. J. Haematol. 1994, 86(4):851-857. http://www.ncbi.nlm.nih.gov/pubmed/7918082, 10.1111/j.1365-2141.1994.tb04841.x.
72. Palmer C., Roberts R.L., Bero C. Deferoxamine posttreatment reduces ischemic brain injury in neonatal rats. Stroke 1994, 25(5):1039-1045. http://www.ncbi.nlm.nih.gov/pubmed/8165675, 10.1161/01.STR.25.5.1039.
73. Sarco D.P., Becker J., Palmer C., Sheldon R.A., Ferriero D.M. The neuroprotective effect of deferoxamine in the hypoxic-ischemic immature mouse brain. Neurosci. Lett. 2000, 282(1-2):113-116. http://www.ncbi.nlm.nih.gov/pubmed/10713409, 10.1016/S0304-3940(00)00878-8.
74. Ponka P. Hereditary causes of disturbed iron homeostasis in the central nervous system. Ann. N. Y. Acad. Sci. 2004, 1012:267-281. http://www.ncbi.nlm.nih.gov/pubmed/15105272, 10.1196/annals.1306.022.
75. Gruer M.J., Artymiuk P.J., Guest J.R. The aconitase family: three structural variations on a common theme. Trends Biochem. Sci. 1997, 22(1):3-6. http://www.ncbi.nlm.nih.gov/pubmed/9020582, 10.1016/S0968-0004(96)10069-4.
76. Paraskeva E., Hentze M.W. Iron-sulphur clusters as genetic regulatory switches: the bifunctional iron regulatory protein-1. FEBS Lett. 1996, 389(1):40-43. http://www.ncbi.nlm.nih.gov/pubmed/8682202, 10.1016/0014-5793(96)00574-1.
77. Drapier J.C. Interplay between NO and [Fe-S] clusters: relevance to biological systems. Methods 1997, 11(3):319-329. http://www.ncbi.nlm.nih.gov/pubmed/9073575, 10.1006/meth.1996.0426.
78. Cairo G., Pietrangelo A. Nitric-oxide-mediated activation of iron-regulatory protein controls hepatic iron metabolism during acute inflammation. Eur. J. Biochem. 1995, 232(2):358-363. http://www.ncbi.nlm.nih.gov/pubmed/7556182, 10.1111/j.1432-1033.1995.358zz.x.
79. Oria R., Sánchez L., Houston T., Hentze M.W., Liew F.Y., Brock J.H. Effect of nitric oxide on expression of transferrin receptor and ferritin and on cellular iron metabolism in K562 human erythroleukemia cells. Blood 1995, 85(10):2962-2966. http://www.ncbi.nlm.nih.gov/pubmed/7742556.
80. Pantopoulos K., Hentze M.W. Nitric oxide signaling to iron-regulatory protein: direct control of ferritin mRNA translation and transferrin receptor mRNA stability in transfected fibroblasts. Proc. Natl. Acad. Sci. USA 1995, 92(5):1267-1271. http://www.ncbi.nlm.nih.gov/pubmed/7533289, 10.1073/pnas.92.5.1267.
81. Ponka P. Cellular iron metabolism. Kidney Int. Suppl. 1999, 69:S2-11. http://www.ncbi.nlm.nih.gov/pubmed/10084280, 10.1046/j.1523-1755.1999.055Suppl.69002.x.
82. Chen Q., Xiao D.S. Long-term aerobic exercise increases redox-active iron through nitric oxide in rat hippocampus. Nitric Oxide 2014, 36:1-10. http://www.ncbi.nlm.nih.gov/pubmed/24184442, 10.1016/j.niox.2013.10.009.
83. Verma N., Pink M., Petrat F., Rettenmeier A.W., Schmitz-Spanke S. Proteomic analysis of human bladder epithelial cells by 2D blue native SDS-PAGE reveals TCDD-induced alterations of calcium and iron homeostasis possibly mediated by nitric oxide. J. Proteome Res. 2015, 14(1):202-213. http://www.ncbi.nlm.nih.gov/pubmed/25348606, 10.1021/pr501051f.