The role of iron as a mediator of oxidative stress in Alzheimer disease

BioFactors

Volumn 38, Issue 2, 2012, Pages 133-138

  Castellani, Rudy J ^a   Moreira, Paula I ^b   Perry, George ^c,d   Zhu, Xiongwei ^d  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c University of San Antonio   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer disease; Chelation; Neurodegeneration; Oxidative stress; Redox active iron

Indexed keywords

IRON; REACTIVE OXYGEN METABOLITE;

ALZHEIMER DISEASE; CENTRAL NERVOUS SYSTEM; HUMAN; METABOLIC REGULATION; NEUROPATHOLOGY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

ALZHEIMER DISEASE; ANIMALS; HUMANS; IRON; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84862817976     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1010     Document Type: Review

References (93)

1. Marlatt, M. W., Webber, K. M., Moreira, P. I., et al. ( 2005). Therapeutic opportunities in Alzheimer disease: one for all or all for one? Curr. Med. Chem., 12, 1137-1147.
2. Shah, R. S., Lee, H. G., Xiongwei, Z., Perry, G., Smith, M. A., and Castellani, R. J. ( 2008). Current approaches in the treatment of Alzheimer's disease. Biomed. Pharmacother., 62, 199-207.
3. Castellani, R. J. and Smith, M. A. Compounding artefacts with uncertainty, and an amyloid cascade hypothesis that is "too big to fail." J. Pathol., 224, 147-152.
4. Castellani, R. J., Lee, H. G., Zhu, X., Perry, G., and Smith, M. A. ( 2008). Alzheimer disease pathology as a host response. J. Neuropathol. Exp. Neurol., 67, 523-531.
5. Castellani, R. J., Lee, H. G., Zhu, X., Nunomura, A., Perry, G., and Smith, M. A. ( 2006). Neuropathology of Alzheimer disease: pathogenomonic but not pathogenic. Acta Neuropathol. (Berl). 111, 503-509.
6. Woods, J., Snape, M., and Smith, M. A. ( 2007). The cell cycle hypothesis of Alzheimer's disease: suggestions for drug development. Biochim. Biophys. Acta, 1772, 503-508.
7. Smith, M. A., Harris, P. L., Sayre, L. M., and Perry, G. ( 1997). Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc. Natl. Acad. Sci. USA, 94, 9866-9868.
8. Rouault, T. A. ( 2001). Systemic iron metabolism: a review and implications for brain iron metabolism. Pediatr. Neurol., 25, 130-137.
9. Rouault, T. A. ( 2001). Iron on the brain. Nat. Genet., 28, 299-300.
10. Roy, C. N. and Andrews, N. C. ( 2001). Recent advances in disorders of iron metabolism: mutations, mechanisms and modifiers. Hum. Mol. Genet., 10, 2181-2186.
11. Moos, T. ( 1996). Immunohistochemical localization of intraneuronal transferrin receptor immunoreactivity in the adult mouse central nervous system. J. Comp. Neurol., 375, 675-692.
12. Kawamata, T., Tooyama, I., Yamada, T., Walker, D. G., and McGeer, P. L. ( 1993). Lactotransferrin immunocytochemistry in Alzheimer and normal human brain. Am. J. Pathol., 142, 1574-1585.
13. Leveugle, B., Spik, G., Perl, D. P., Bouras, C., Fillit, H. M., and Hof, P. R. ( 1994). The iron-binding protein lactotransferrin is present in pathologic lesions in a variety of neurodegenerative disorders: a comparative immunohistochemical analysis. Brain Res., 650, 20-31.
14. Patel, B. N., Dunn, R. J., and David S. ( 2000). Alternative RNA splicing generates a glycosylphosphatidylinositol-anchored form of ceruloplasmin in mammalian brain. J. Biol. Chem., 275, 4305-4310.
15. Klomp, L. W. and Gitlin, J. D. ( 1996). Expression of the ceruloplasmin gene in the human retina and brain: implications for a pathogenic model in aceruloplasminemia. Hum. Mol. Genet., 5, 1989-1996.
16. Gonzalez-Cuyar, L. F., Perry, G., Miyajima, H., et al. ( 2008). Redox active iron accumulation in aceruloplasminemia. Neuropathology, 28, 466-471.
17. Castellani, R. J., Smith, M. A., Nunomura, A., Harris, P. L., and Perry, G. ( 1999). Is increased redox-active iron in Alzheimer disease a failure of the copper-binding protein ceruloplasmin? Free Radic. Biol. Med., 26, 1508-1512.
18. Crowe, A. and Morgan, E. H. ( 1992). Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res., 592, 8-16.
19. Bowman, B. H., Jansen, L., Yang, F., et al. ( 1995). Discovery of a brain promoter from the human transferrin gene and its utilization for development of transgenic mice that express human apolipoprotein E alleles. Proc. Natl. Acad. Sci. USA, 92, 12115-12119.
20. Lieu, P. T., Heiskala, M., Peterson, P. A., and Yang, Y. ( 2001). The roles of iron in health and disease. Mol. Aspects Med., 22, 1-87.
21. Double, K. L., Zecca, L., Costi, P., et al. ( 2000). Structural characteristics of human substantia nigra neuromelanin and synthetic dopamine melanins. J. Neurochem., 75, 2583-2589.
22. Castellani, R. J., Siedlak, S. L., Perry, G., and Smith, M. A. ( 2000). Sequestration of iron by Lewy bodies in Parkinson's disease. Acta Neuropathol., 100, 111-114.
23. Hentze, M. W. and Kuhn, L. C. ( 1996). Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA, 93, 8175-8182.
24. Connor, J. R., Menzies, S. L., Burdo, J. R., and Boyer, P. J. ( 2001). Iron and iron management proteins in neurobiology. Pediatr. Neurol., 25, 118-129.
25. Calabrese, V., Scapagnini, G., Ravagna, A., Fariello, R. G., Giuffrida Stella, A. M., and Abraham, N. G. ( 2002). Regional distribution of heme oxygenase, HSP70, and glutathione in brain: relevance for endogenous oxidant/antioxidant balance and stress tolerance. J. Neurosci. Res., 68, 65-75.
26. Maines, M. D. ( 2000). The heme oxygenase system and its functions in the brain. Cell Mol. Biol. (Noisy-le-grand), 46, 573-585.
27. Marcus, D. L., Thomas, C., Rodriguez, C., et al. ( 1998). Increased peroxidation and reduced antioxidant enzyme activity in Alzheimer's disease. Exp. Neurol., 150, 40-44.
28. Sayre, L. M., Zelasko, D. A., Harris, P. L., Perry, G., Salomon, R. G., and Smith, M. A. ( 1997). 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem., 68, 2092-2097.
29. Smith, M. A., Richey Harris, P. L., Sayre, L. M., Beckman, J. S., and Perry, G. ( 1997). Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci., 17, 2653-2657.
30. Smith, M. A., Taneda, S., Richey, P. L., et al. ( 1994). Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc. Natl. Acad. Sci. USA, 91, 5710-5714.
31. Smith, M. A., Perry, G., Richey, P. L., et al. ( 1996). Oxidative damage in Alzheimer's. Nature, 382, 120-121.
32. Nunomura, A., Perry, G., Pappolla, M.A., et al. ( 1999). RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J. Neurosci., 19, 1959-1964.
33. Zhou, Y., Richardson, J. S., Mombourquette, M. J., and Weil, J. A. ( 1995). Free radical formation in autopsy samples of Alzheimer and control cortex. Neurosci. Lett., 195, 89-92.
34. Martins, R. N., Harper, C. G., Stokes, G. B., and Masters, C. L. ( 1986). Increased cerebral glucose-6-phosphate dehydrogenase activity in Alzheimer's disease may reflect oxidative stress. J. Neurochem., 46, 1042-1045.
35. Pappolla, M. A., Omar, R. A., Kim, K. S., and Robakis, N. K. ( 1992). Immunohistochemical evidence of oxidative [corrected] stress in Alzheimer's disease. Am. J. Pathol., 140, 621-628.
36. Lovell, M. A., Robertson, J. D., Teesdale, W. J., Campbell, J. L., and Markesbery, W.R. ( 1998). Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci., 158, 47-52.
37. Hall, E. D., Oostveen, J. A., Dunn, E., and Carter, D. B. ( 1995). Increased amyloid protein precursor and apolipoprotein E immunoreactivity in the selectively vulnerable hippocampus following transient forebrain ischemia in gerbils. Exp. Neurol., 135, 17-27.
38. Shi, J., Perry, G, Smith, M. A., and Friedland, R. P. ( 2000). Vascular abnormalities: the insidious pathogenesis of Alzheimer's disease. Neurobiol. Aging, 21, 357-361.
39. Abe, K., St George-Hyslop, P. H., Tanzi, R. E., and Kogure, K. ( 1991). Induction of amyloid precursor protein mRNA after heat shock in cultured human lymphoblastoid cells. Neurosci. Lett., 125, 169-171.
40. Jendroska, K., Poewe, W., Daniel, S. E., et al. ( 1995). Ischemic stress induces deposition of amyloid beta immunoreactivity in human brain. Acta Neuropathol. (Berl). 90, 461-466.
41. Murakami, N., Yamaki, T., Iwamoto, Y., et al. ( 1998). Experimental brain injury induces expression of amyloid precursor protein, which may be related to neuronal loss in the hippocampus. J. Neurotrauma, 15, 993-1003.
42. Shi, J., Xiang, Y., and Simpkins, J. W. ( 1997). Hypoglycemia enhances the expression of mRNA encoding beta-amyloid precursor protein in rat primary cortical astroglial cells. Brain Res., 772, 247-251.
43. Mattson, M. P. and Pedersen, W. A. ( 1998). Effects of amyloid precursor protein derivatives and oxidative stress on basal forebrain cholinergic systems in Alzheimer's disease. Int. J. Dev. Neurosci., 16, 737-753.
44. Gabuzda, D., Busciglio, J., Chen, L. B., Matsudaira, P., and Yankner, B. A. ( 1994). Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J. Biol. Chem., 269, 13623-13628.
45. Misonou, H., Morishima-Kawashima, M., and Ihara, Y. ( 2000). Oxidative stress induces intracellular accumulation of amyloid beta-protein (Abeta) in human neuroblastoma cells. Biochemistry (Mosc). 39, 6951-6959.
46. Olivieri, G., Hess, C., Savaskan, E., et al. ( 2001). Melatonin protects SHSY5Y neuroblastoma cells from cobalt-induced oxidative stress, neurotoxicity and increased beta-amyloid secretion. J. Pineal Res., 31, 320-325.
47. Frederikse, P. H., Garland, D., Zigler, J. S.Jr., and Piatigorsky, J. ( 1996). Oxidative stress increases production of beta-amyloid precursor protein and beta-amyloid (Abeta) in mammalian lenses, and Abeta has toxic effects on lens epithelial cells. J. Biol. Chem., 271, 10169-10174.
48. Paola, D., Domenicotti, C., Nitti, M., et al. ( 2000). Oxidative stress induces increase in intracellular amyloid beta-protein production and selective activation of betaI and betaII PKCs in NT2 cells. Biochem. Biophys. Res. Commun., 268, 642-646.
49. Atwood, C. S., Scarpa, R. C., Huang, X., et al. ( 2000). Characterization of copper interactions with alzheimer amyloid beta peptides: identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochemistry, 75, 1219-1233.
50. Atwood, C. S., Moir, R. D., Huang, X., et al. ( 1998). Dramatic aggregation of Alzheimer abeta by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem., 273, 12817-12826.
51. Curtain, C. C., Ali, F., Volitakis, I., et al. ( 2001). Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J. Biol. Chem., 276, 20466-20473.
52. Huang, X., Atwood, C. S., Hartshorn, M. A., et al. ( 1999). The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry (Mosc). 38, 7609-7616.
53. Dikalov, S. I., Vitek, M. P., Maples, K. R., and Mason, R. P. ( 1999). Amyloid beta peptides do not form peptide-derived free radicals spontaneously, but can enhance metal-catalyzed oxidation of hydroxylamines to nitroxides. J. Biol. Chem., 274, 9392-9399.
54. Perry, G., Nunomura, A., Raina, A. K., and Smith MA. ( 2000). Amyloid-beta junkies. Lancet, 355, 757.
55. Smith, M. A., Joseph, J. A., and Perry, G. Arson. ( 2000). Tracking the culprit in Alzheimer's disease. Ann. N. Y. Acad. Sci., 924, 35-38.
56. Joseph, J., Shukitt- Hale, B., Denisova, N. A., Martin, A., Perry, G., Smith, M. A. ( 2001). Copernicus revisited: amyloid beta in Alzheimer's disease. Neurobiol. Aging, 22, 131-146.
57. Rottkamp, C. A., Raina, A. K., Zhu, X., et al. ( 2001). Redox-active iron mediates amyloid-beta toxicity. Free Radic. Biol. Med., 30, 447-450.
58. Rottkamp, C. A., Atwood, C. S., Joseph, J. A., Nunomura, A., Perry, G., and Smith, M. A. ( 2002). The state versus amyloid-beta: the trial of the most wanted criminal in Alzheimer disease. Peptides, 23, 1333-1341.
59. Cullen, K. M. ( 1997). Perivascular astrocytes within Alzheimer's disease plaques. Neuroreport, 8, 1961-1966.
60. Dunn, C. J. ( 1991) Cytokines as mediators of chronic inflammatory disease. In Cytokines and Inflammation. ( Kimball, E. S. ed.) pp. 1-33, CRC Pres, Inc., Boca Raton, FL.
61. Yoshida, T., Tanaka, M., Sotomatsu, A., Hirai, S., and Okamoto, K. ( 1998). Activated microglia cause iron-dependent lipid peroxidation in the presence of ferritin. Neuroreport, 9, 1929-1933.
62. Cadman, E. D., Witte, D. G., and Lee, C. M. ( 1994). Regulation of the release of interleukin-6 from human astrocytoma cells. J. Neurochem., 63, 980-987.
63. Sayre, L. M., Perry, G., Harris, P. L., Liu, Y., Schubert, K. A., and Smith, M. A. ( 2000). In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: a central role for bound transition metals. J. Neurochem., 74, 270-279.
64. Shan, X., Tashiro, H., and Lin, C. L. ( 2003). The identification and characterization of oxidized RNAs in Alzheimer's disease. J. Neurosci., 23, 4913-4921.
65. Honda, K., Smith, M. A., Zhu, X., et al. ( 2005). Ribosomal RNA in Alzheimer disease is oxidized by bound redox-active iron. J. Biol. Chem., 280, 20978-20986.
66. Castellani, R. J., Nunomura, A., Rolston, R. K., et al. ( 2008). Sublethal RNA oxidation as a mechanism for neurodegenerative disease. Int J Mol Sci, 9, 789-806.
67. Nunomura, A., Hofer, T., Moreira, P. I., Castellani, R. J., Smith, M. A., and Perry, G. ( 2009). RNA oxidation in Alzheimer disease and related neurodegenerative disorders. Acta Neuropathol., 118, 151-166.
68. Nunomura, A., Chiba, S., Kosaka, K., et al. ( 2002). Neuronal RNA oxidation is a prominent feature of dementia with Lewy bodies. Neuroreport, 13, 2035-2039.
69. Castellani, R. J., Smith, M. A., Perry, G., and Friedland, R. P. ( 2004). Cerebral amyloid angiopathy: major contributor or decorative response to Alzheimer's disease pathogenesis. Neurobiol Aging, 25, 599-602; discussion 603-594.
70. Schrag, M., Crofton, A., Zabel, M., et al. Effect of cerebral amyloid angiopathy on brain iron, copper, and zinc in Alzheimer's disease. J. Alzheimers Dis., 24, 137-149.
71. Hirai, K., Aliev, G., Nunomura, A., et al. ( 2001). Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci., 21, 3017-3023.
72. Mikhaylova, A., Davidson, M., Toastmann, H., et al. ( 2005). Detection, identification and mapping of iron anomalies in brain tissue using X-ray absorption spectroscopy. J. R. Soc. Interface, 2, 33-37.
73. Collingwood, J. F., Mikhaylova, A., Davidson, M., et al. ( 2005). In situ characterization and mapping of iron compounds in Alzheimer's disease tissue. J Alzheimers Dis., 7, 267-272.
74. Collingwood, J. F., Mikhaylova, A., Davidson, M. R., et al. ( 2005). High-resolution x-ray absorption spectroscopy studies of metal compounds in neurodegenerative brain tissue. J. Phys. Conf. Ser., 17, 54-60.
75. Dobson, J. and Grassi, P. ( 1996). Magnetic properties of human hippocampal tissue-evaluation of artefact and contamination sources. Brain Res. Bull., 39, 255-259.
76. Schultheiss-Grassi, P. P., Wessiken, R., and Dobson, J. ( 1999). TEM investigations of biogenic magnetite extracted from the human hippocampus. Biochim. Biophys. Acta, 1426, 212-216.
77. Kirschvink, J. L., Kobayashi-Kirschvink, A., and Woodford, B. J. ( 1992). Magnetite biomineralization in the human brain. Proc. Natl. Acad. Sci. USA, 89, 7683-7687.
78. Hautot, D., Pankhurst, Q. A., Khan, N., and Dobson, J. ( 2003). Preliminary evaluation of nanoscale biogenic magnetite in Alzheimer's disease brain tissue. Proceedings, 270( Suppl 1), S62-S64.
79. Dobson, J. ( 2001). Nanoscale biogenic iron oxides and neurodegenerative disease. FEBS Lett., 496, 1-5.
80. Dobson, J. ( 2004). Magnetic iron compounds in neurological disorders. Ann. N. Y. Acad. Sci., 1012, 183-192.
81. Timmel, C. R., Till, U., Brocklehurst, B., Mclauchlan, K. A., and Hore, P. J. ( 1998). Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys., 95, 71-89.
82. Scaiano, J. C., Monahan, S., and Renaud, J. ( 1997). Dramatic effect of magnetite particles on the dynamics of photogenerated free radicals. Photochem. Photobiol., 65, 759-762.
83. Bush, A. I. ( 2002). Metal complexing agents as therapies for Alzheimer's disease. Neurobiol. Aging, 23, 1031-1038.
84. Shachar, D. B., Kahana, N., Kampel, V., Warshawsky, A., and Youdim, M. B. ( 2004). Neuroprotection by a novel brain permeable iron chelator, VK-28, against 6-hydroxydopamine lession in rats. Neuropharmacology, 46, 254-263.
85. Bartzokis, G., Tishler, T. A., Lu, P. H., et al. ( 2007). Brain ferritin iron may influence age- and gender-related risks of neurodegeneration. Neurobiol. Aging, 28, 414-423.
86. Jack, C. R.Jr., Wengenack, T. M., Reyes, D.A., et al. ( 2005). In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer's transgenic mice. J. Neurosci., 25, 10041-10048.
87. Ritchie, C. W., Bush, A. I., Mackinnon, A., et al. ( 2003). Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Abeta amyloid deposition and toxicity in Alzheimer disease: a pilot phase 2 clinical trial. Arch. Neurol., 60, 1685-1691.
88. McLachlan, D. R., Kruck, T. P., Lukiw, W. J., and Krishnan, S. S. ( 1991). Would decreased aluminum ingestion reduce the incidence of Alzheimer's disease? CMAJ, 145, 793-804.
89. Liu, G., Garrett M. R., Men, P., Zhu, X., Perry, G., and Smith, M. A. ( 2005). Nanoparticle and other metal chelation therapeutics in Alzheimer disease. Biochim. Biophys. Acta, 1741, 246-252.
90. Smith, M. A., Atwood, C. S., Joseph, J. A., and Perry, G. ( 2002). Predicting the failure of amyloid-beta vaccine. Lancet, 359, 1864-1865.
91. Lee, H. G., Casadesus, G., Zhu, X., Takeda, A., Perry, G., and Smith, M. A. ( 2004). Challenging the amyloid cascade hypothesis: senile plaques and amyloid-beta as protective adaptations to Alzheimer disease. Ann. N. Y. Acad. Sci., 1019, 1-4.
92. Kaur, D., Yantiri, F., Rajagopalan, S., et al. ( 2003). Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease. Neuron, 37, 899-909.
93. Cherny, R. A., Atwood, C. S., Xilinas, M. E., et al. ( 2001). Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron, 30, 665-676.