Table of Contents
Journal of Amino Acids
Volume 2011, Article ID 198430, 10 pages
http://dx.doi.org/10.4061/2011/198430
Review Article

Methionine-35 of Aβ(1–42): Importance for Oxidative Stress in Alzheimer Disease

1Department of Chemistry, University of Kentucky, Lexington, KY 40506-0055, USA
2Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506-0055, USA
3Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40506-0055, USA

Received 1 January 2011; Accepted 14 April 2011

Academic Editor: Andreas Wyttenbach

Copyright © 2011 D. Allan Butterfield and Rukhsana Sultana. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. Selkoe, “Alzheimer's disease: genes, proteins, and therapy,” Physiological Reviews, vol. 81, no. 2, pp. 741–766, 2001. View at Google Scholar · View at Scopus
  2. L. Bertram, “Alzheimer's disease genetics current status and future perspectives,” International Review of Neurobiology, vol. 84, pp. 167–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Bertram and R. E. Tanzi, “Genome-wide association studies in Alzheimer's disease,” Human Molecular Genetics, vol. 18, no. R2, pp. R137–R145, 2009. View at Google Scholar
  4. T. M. Feulner, S. M. Laws, P. Friedrich et al., “Examination of the current top candidate genes for AD in a genome-wide association study,” Molecular Psychiatry, vol. 15, no. 7, pp. 756–766, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Harold, R. Abraham, P. Hollingworth et al., “Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease,” Nature Genetics, vol. 41, no. 10, pp. 1088–1093, 2009. View at Google Scholar
  6. S. A. Frautschy, A. Baird, and G. M. Cole, “Effects of injected Alzheimer beta-amyloid cores in rat brain,” Proceedings of the National Academy of Sciences, vol. 88, no. 19, pp. 8362–8366, 1991. View at Google Scholar
  7. D. A. Butterfield and C. M. Lauderback, “Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress,” Free Radical Biology & Medicine, vol. 32, no. 11, pp. 1050–1060, 2002. View at Google Scholar
  8. K. V. Subbarao, J. S. Richardson, and L. S. Ang, “Autopsy samples of Alzheimer's cortex show increased peroxidation in vitro,” Journal of Neurochemistry, vol. 55, no. 1, pp. 342–345, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Y. Aksenov, M. V. Aksenova, D. A. Butterfield, J. W. Geddes, and W. R. Markesbery, “Protein oxidation in the brain in Alzheimer's disease,” Neuroscience, vol. 103, no. 2, pp. 373–383, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Hensley, N. Hall, R. Subramaniam et al., “Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation,” Journal of Neurochemistry, vol. 65, no. 5, pp. 2146–2156, 1995. View at Google Scholar · View at Scopus
  11. D. A. Butterfield, T. Reed, S. F. Newman, and R. Sultana, “Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment,” Free Radical Biology and Medicine, vol. 43, no. 5, pp. 658–677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. W. R. Markesbery, “Oxidative stress hypothesis in Alzheimer's disease,” Free Radical Biology and Medicine, vol. 23, no. 1, pp. 134–147, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Nunomura, P. I. Moreira, H. G. Lee et al., “Neuronal death and survival under oxidative stress in Alzheimer and Parkinson diseases,” CNS & Neurological Disorders—Drug Targets, vol. 6, no. 6, pp. 411–423, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. S. M. Yatin, S. Varadarajan, C. D. Link, and D. A. Butterfield, “In vitro and in vivo oxidative stress associated with Alzheimer's amyloid beta-peptide (1–42),” Neurobiology of Aging, vol. 20, no. 3, pp. 325–330, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Lyras, R. H. Perry, E. K. Perry et al., “Oxidative damage to proteins, lipids, and DNA in cortical brain regions from patients with dementia with Lewy bodies,” Journal of Neurochemistry, vol. 71, no. 1, pp. 302–312, 1998. View at Google Scholar · View at Scopus
  16. I. Dalle-Donne, A. Scaloni, and D. A. Butterfield, Redox Proteomics: From Protein Modifications to Cellular Dysfunction and Diseases, John Wiley and Sons, Hoboken, NJ, USA, 2006.
  17. R. Sultana, M. Perluigi, and D. A. Butterfield, “Protein oxidation and lipid peroxidation in brain of subjects with Alzheimer's disease: insights into mechanism of neurodegeneration from redox proteomics,” Antioxidants and Redox Signaling, vol. 8, no. 11-12, pp. 2021–2037, 2006. View at Google Scholar · View at Scopus
  18. J. Choi, A. I. Levey, S. T. Weintraub et al., “Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases,” The Journal of Biological Chemistry, vol. 279, no. 13, pp. 13256–13264, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. M. A. Smith, P. L. Richey Harris, L. M. Sayre, J. S. Beckman, and G. Perry, “Widespread peroxynitrite-mediated damage in Alzheimer's disease,” Journal of Neuroscience, vol. 17, no. 8, pp. 2653–2657, 1997. View at Google Scholar · View at Scopus
  20. W. R. Markesbery, R. J. Kryscio, M. A. Lovell, and J. D. Morrow, “Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment,” Annals of Neurology, vol. 58, no. 5, pp. 730–735, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Yao, V. Zhukareva, S. Sung et al., “Enhanced brain levels of 8,12-iso-iPF2alpha-VI differentiate AD from frontotemporal dementia,” Neurology, vol. 61, no. 4, pp. 475–478, 2003. View at Google Scholar · View at Scopus
  22. X. Liu, M. A. Lovell, and B. C. Lynn, “Development of a method for quantification of acrolein-deoxyguanosine adducts in DNA using isotope dilution-capillary LC/MS/MS and its application to human brain tissue,” Analytical Chemistry, vol. 77, no. 18, pp. 5982–5989, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. D. A. Butterfield, J. Drake, C. Pocernich, and A. Castegna, “Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide,” Trends in Molecular Medicine, vol. 7, no. 12, pp. 548–554, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. C. M. Lauderback, J. M. Hackett, F. F. Huang et al., “The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Aβ1–42,” Journal of Neurochemistry, vol. 78, no. 2, pp. 413–416, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. J. B. Owen, R. Sultana, C. D. Aluise et al., “Oxidative modification to LDL receptor-related protein 1 in hippocampus from subjects with Alzheimer disease: implications for Aß accumulation in AD brain,” Free Radical Biology & Medicine, vol. 49, no. 11, pp. 1798–1803, 2010. View at Google Scholar
  26. J. N. Keller, F. A. Schmitt, S. W. Scheff et al., “Evidence of increased oxidative damage in subjects with mild cognitive impairment,” Neurology, vol. 64, no. 7, pp. 1152–1156, 2005. View at Google Scholar · View at Scopus
  27. R. Sultana, M. Perluigi, and D. A. Butterfield, “Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Aβ(1–42),” Journal of Chromatography B, vol. 833, no. 1, pp. 3–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. D. A. Butterfield, H. F. Poon, D. S. T. Clair et al., “Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer'disease,” Neurobiology of Disease, vol. 22, no. 2, pp. 223–232, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. D. A. Butterfield, T. Reed, M. Perluigi et al., “Elevated protein-bound levels of the lipid peroxidation product, 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment,” Neuroscience Letters, vol. 397, no. 3, pp. 170–173, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Lovell and W. R. Markesbery, “Oxidatively modified RNA in mild cognitive impairment,” Neurobiology of Disease, vol. 29, no. 2, pp. 169–175, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Varadarajan, S. Yatin, M. Aksenova, and D. A. Butterfield, “Review: Alzheimer's amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity,” Journal of Structural Biology, vol. 130, no. 2-3, pp. 184–208, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. S. V. Jovanovic, D. Clements, and K. MacLeod, “Biomarkers of oxidative stress are significantly elevated in Down syndrome,” Free Radical Biology and Medicine, vol. 25, no. 9, pp. 1044–1048, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. S. M. Yatin, S. Varadarajan, and D. A. Butterfield, “Vitamin E prevents Alzheimer's amyloid beta-peptide (1–42)-induced neuronal protein oxidation and reactive oxygen species production,” Journal of Alzheimer's Disease, vol. 2, no. 2, pp. 123–131, 2000. View at Google Scholar
  34. R. A. Quintanilla, F. J. Muñoz, MJ Metcalfe et al., “Trolox and 17beta-estradiol protect against amyloid beta-peptide neurotoxicity by a mechanism that involves modulation of the Wnt signaling pathway,” The Journal of Biological Chemistry, vol. 280, no. 12, pp. 11615–11625, 2005. View at Google Scholar
  35. R. Subramaniam, F. Roediger, B. Jordan et al., “The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins,” Journal of Neurochemistry, vol. 69, no. 3, pp. 1161–1169, 1997. View at Google Scholar · View at Scopus
  36. G. Olivieri, C. Hess, E. Savaskan et al., “Melatonin protects SHSY5Y neuroblastoma cells from cobalt-induced oxidative stress, neurotoxicity and increased beta-amyloid secretion,” Journal of Pineal Research, vol. 31, no. 4, pp. 320–325, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Pappolla, Y. J. Chyan, B. Poeggeler et al., “Alzheimer beta protein mediated oxidative damage of mitochondrial DNA: prevention by melatonin,” Journal of Pineal Research, vol. 27, no. 4, pp. 226–229, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Drake, C. D. Link, and D. A. Butterfield, “Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid beta-peptide (1–42) in a transgenic Caenorhabditis elegans model,” Neurobiology of Aging, vol. 24, no. 3, pp. 415–420, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. C. C. Glabe, “Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Aβ,” Sub-Cellular Biochemistry, vol. 38, pp. 167–177, 2005. View at Google Scholar · View at Scopus
  40. C. Caspersen, N. Wang, J. Yao et al., “Mitochondrial Aß A potential focal point for neuronal metabolic dysfunction in Alzheimer's disease,” The FASEB Journal, vol. 19, no. 14, pp. 2040–2041, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Manczak, T. S. Anekonda, E. Henson, B. S. Park, J. Quinn, and P. H. Reddy, “Mitochondria are a direct site of Aβ accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression,” Human Molecular Genetics, vol. 15, no. 9, pp. 1437–1449, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Boyd-Kimball, H. M. Abdul, T. Reed, R. Sultana, and D. A. Butterfield, “Role of phenylalanine 20 in Alzheimer's amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity,” Chemical Research in Toxicology, vol. 17, no. 12, pp. 1743–1749, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Behl and B. Moosmann, “Oxidative nerve cell death in Alzheimer's disease and stroke: antioxidants as neuroprotective compounds,” Biological Chemistry, vol. 383, no. 3-4, pp. 521–536, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Nishida, S. Ito, S. Ohtsuki et al., “Depletion of vitamin E increases amyloid beta accumulation by decreasing its clearances from brain and blood in a mousemodel of Alzheimer disease,” The Journal of Biological Chemistry, vol. 284, no. 48, pp. 33400–33408, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Varadarajan, J. Kanski, M. Aksenova, C. Lauderback, and D. A. Butterfield, “Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's A beta (1–42) and A beta (25–35),” Journal of the American Chemical Society, vol. 123, no. 24, pp. 5625–5631, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. D. A. Butterfield and D. Boyd-Kimball, “The critical role of methionine 35 in Alzheimer's amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity,” International Journal of Biochemistry, Biophysics and Molecular Biology, vol. 1703, no. 2, pp. 149–156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. C. J. Pike, A. J. Walencewicz-Wasserman, J. Kosmoski, D. H. Cribbs, C. G. Glabe, and C. W. Cotman, “Structure-activity analyses of beta-amyloid peptides: contributions of the beta 25-35 region to aggregation and neurotoxicity,” Journal of Neurochemistry, vol. 64, no. 1, pp. 253–265, 1995. View at Google Scholar · View at Scopus
  48. D. Pogocki and C. Schöneich, “Redox properties of Met in neurotoxic β-amyloid peptide. A molecular modeling study,” Chemical Research in Toxicology, vol. 15, no. 3, pp. 408–418, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Schöneich, D. Pogocki, G. L. Hug, and K. Bobrowski, “Free radical reactions of methionine in peptides: mechanisms relevant to beta-amyloid oxidation and alzheimer's disease,” Journal of the American Chemical Society, vol. 125, no. 45, pp. 13700–13713, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Brot and H. Weissbach, “Biochemistry of methionine sulfoxide residues in proteins,” BioFactors, vol. 3, no. 2, pp. 91–96, 1991. View at Google Scholar · View at Scopus
  51. S. R. Labrenz, M. A. Calmann, G. A. Heavner, and G. Tolman, “The oxidation of methionine-54 of epoetinum alfa does not affect molecular structure or stability, but does decrease biological activity,” Journal of Pharmaceutical Science and Technology, vol. 62, no. 3, pp. 211–223, 2008. View at Google Scholar · View at Scopus
  52. E. R. Stadtman, “Cyclic oxidation and reduction of methionine residues of proteins in antioxidant defense and cellular regulation,” Archives of Biochemistry and Biophysics, vol. 423, no. 1, pp. 2–5, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Luo and R. L. Levine, “Methionine in proteins defends against oxidative stress,” The FASEB Journal, vol. 23, no. 2, pp. 464–472, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Mary, S. Vougier, C. R. Picot, M. Perichon, I. Petropoulos, and B. Friguet, “Enzymatic reactions involved in the repair of oxidized proteins,” Experimental Gerontology, vol. 39, no. 8, pp. 1117–1123, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. E. R. Stadtman, J. Moskovitz, and R. L. Levine, “Oxidation of methionine residues of proteins: biological consequences,” Antioxidants and Redox Signaling, vol. 5, no. 5, pp. 577–582, 2003. View at Google Scholar · View at Scopus
  56. S. P. Gabbita, M. Y. Aksenov, M. A. Lovell, and W. R. Markesbery, “Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain,” Journal of Neurochemistry, vol. 73, no. 4, pp. 1660–1666, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Naslund, A. Schierhorn, U. Hellman et al., “Relative abundance of Alzheimer Aß amyloid peptide variants in Alzheimer disease and normal aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 18, pp. 8378–8382, 1994. View at Google Scholar · View at Scopus
  58. C. Schöneich, “Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease,” Biochimica et Biophysica Acta, vol. 1703, no. 2, pp. 111–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. M. E. Clementi, M. Pezzotti, F. Orsini et al., “Alzheimer's amyloid beta-peptide (1–42) induces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35,” Biochemical and Biophysical Research Communications, vol. 342, no. 1, pp. 206–213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. X. L. Dai, Y. X. Sun, and Z. F. Jiang, “Attenuated cytotoxicity but enhanced βfibril of a mutant amyloid β-peptide with a methionine to cysteine substitution,” The FEBS Letters, vol. 581, no. 7, pp. 1269–1274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M. M. Murray, S. L. Bernstein, V. Y. Nyugen, M. M. Condron, D. B. Teplow, and M. T. Bowers, “Amyloid beta protein: a beta40 Inhibits A β42 oligomerization,” Journal of the American Chemical Society, vol. 131, no. 18, pp. 6316–6317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. D. A. Butterfield, V. Galvan, M. B. Lange et al., “In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid beta-peptide of APP,” Free Radical Biology and Medicine, vol. 48, no. 1, pp. 136–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. V. Galvan, J. Zhang, O. F. Gorostiza et al., “Long-term prevention of Alzheimer's disease-like behavioral deficits in PDAPP mice carrying a mutation in Asp664,” Behavioural Brain Research, vol. 191, no. 2, pp. 246–255, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. V. Galvan, O. F. Gorostiza, S. Banwait et al., “Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7130–7135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. D. C. Lu, S. Rabizadeh, S. Chandra et al., “A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor,” Nature Medicine, vol. 6, no. 4, pp. 397–404, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Madeira, J. M. Pommet, A. Prochiantz, and B. Allinquant, “SET protein (TAF1beta;, I2PP2A) is involved in neuronal apoptosis induced by an amyloid precursor protein cytoplasmic subdomain,” The FASEB Journal, vol. 19, no. 13, pp. 1905–1907, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Nikolaev, T. McLaughlin, D. D. M. O'Leary, and M. Tessier-Lavigne, “APP binds DR6 to trigger axon pruning and neuron death via distinct caspases,” Nature, vol. 457, no. 7232, pp. 981–989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Wan, G. Nie, J. Zhang et al., “β-Amyloid peptide increases levels of iron content and oxidative stress in human cell and Caenorhabditis elegans models of Alzheimer disease,” Free Radical Biology & Medicine, vol. 50, no. 1, pp. 122–129, 2011. View at Google Scholar
  69. M. E. Clementi, G. E. Martorana, M. Pezzotti, B. Giardina, and F. Misiti, “Methionine 35 oxidation reduces toxic effects of the amyloid beta-protein fragment (31–35) on human red blood cell,” The International Journal of Biochemistry & Cell Biology, vol. 36, no. 10, pp. 2066–2076, 2004. View at Google Scholar · View at Scopus
  70. M. Palmblad, A. Westlind-Danielsson, and J. Bergquist, “Oxidation of methionine 35 attenuates formation of amyloid β-peptide 1–40 oligomers,” The Journal of Biological Chemistry, vol. 277, no. 22, pp. 19506–19510, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Misiti, M. E. Clementi, and B. Giardina, “Oxidation of methionine 35 reduces toxicity of the amyloid beta-peptide(1–42) in neuroblastoma cells (IMR-32) via enzyme methionine sulfoxide reductase A expression and function,” Neurochemistry International, vol. 56, no. 4, pp. 597–602, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. A. S. Johansson, J. Bergquist, C. Volbracht et al., “Attenuated amyloid-β aggregation and neurotoxicity owing to methionine oxidation,” NeuroReport, vol. 18, no. 6, pp. 559–563, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. K. J. Barnham, G. D. Ciccotosto, A. K. Tickler et al., “Neurotoxic, Redox-competent Alzheimer's ß-amyloid Is released from lipid membrane by methionine oxidation,” The Journal of Biological Chemistry, vol. 278, no. 44, pp. 42959–42965, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. C. C. Curtain, F. Ali, I. Volitakis et al., “Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits,” The Journal of Biological Chemistry, vol. 276, no. 23, pp. 20466–20473, 2001. View at Publisher · View at Google Scholar · View at Scopus
  75. D. G. Smith, R. Cappai, and K. J. Barnham, “The Redox chemistry of the Alzheimer's disease amyloid beta peptide,” Biochimica et Biophysica Acta, vol. 1768, no. 8, pp. 1976–1990, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. W. F. Cerpa, M. I. Barría, M. A. Chacón et al., “The N-terminal copper-binding domain of the amyloid precursor protein protects against Cu2+ neurotoxicity in vivo,” The FASEB Journal, vol. 18, no. 14, pp. 1701–1703, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Huang, C. S. Atwood, M. A. Hartshorn et al., “The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction,” Biochemistry, vol. 38, no. 24, pp. 7609–7616, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Jomova, D. Vondrakova, M. Lawson, and M. Valko, “Metals, oxidative stress and neurodegenerative disorders,” Molecular and Cellular Biochemistry, vol. 345, no. 1-2, pp. 91–104, 2010. View at Google Scholar
  79. T. Kowalik-Jankowska, M. Ruta-Dolejsz, K. Wisniewska, L. Lankiewicz, and H. Kozlowski, “Possible involvement of Copper(II) in Alzheimer disease,” Environmental Health Perspectives, vol. 110, supplement 5, pp. 869–870, 2002. View at Google Scholar · View at Scopus
  80. A. I. Bush, “Drug development based on the metals hypothesis of Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 15, no. 2, pp. 223–240, 2008. View at Google Scholar · View at Scopus
  81. A. R. White, T. Du, K. M. Laughton et al., “Degradation of the Alzheimer disease amyloid beta-peptide by metal-dependent up-regulation of metalloprotease activity,” The Journal of Biological Chemistry, vol. 281, no. 26, pp. 17670–17680, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. R. A. Cherny, C. S. Atwood, M. E. Xilinas et al., “Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice,” Neuron, vol. 30, no. 3, pp. 665–676, 2001. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Opazo, S. Luza, V. L. Villemagne et al., “Radioiodinated clioquinol as a biomarker for beta-amyloid: Zn complexes in Alzheimer's disease,” Aging Cell, vol. 5, no. 1, pp. 69–79, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. C. W. Ritchie, A. I. Bush, A. Mackinnon et al., “Metal-protein attenuation with iodochlorhydroxyquin (Clioquinol) targeting Aß amyloid deposition and toxicity in alzheimer disease,” Archives of Neurology, vol. 60, no. 12, pp. 1685–1691, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Kanski, M. Aksenova, and D. A Butterfield, “The hydrophobic environment of Met35 of Alzheimer's Aβ(1–42) is important for the neurotoxic and oxidative properties of the peptide,” Neurotoxicity Research, vol. 4, no. 3, pp. 219–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Halliwell and J. M. C. Gutteridge, “Biologically relevant metal ion-dependent hydroxyl radical generation. An update,” The FEBS Letters, vol. 307, no. 1, pp. 108–112, 1992. View at Publisher · View at Google Scholar · View at Scopus
  87. D. A. Butterfield, A. Castegna, C. M. Lauderback, and J. Drake, “Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death,” Neurobiology of Aging, vol. 23, no. 5, pp. 655–664, 2002. View at Publisher · View at Google Scholar · View at Scopus
  88. R. Sultana, M. Perluigi, and D. A. Butterfield, “Oxidatively modified proteins in Alzheimer's disease (AD), mild cognitive impairment and animal models of AD: role of A beta in pathogenesis,” Acta Neuropathologica, vol. 118, no. 1, pp. 131–150, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. G. D. Ciccotosto, D. Tew, C. C. Curtain et al., “Enhanced toxicity and cellular binding of a modified amyloid beta peptide with a methionine to valine substitution,” The Journal of Biological Chemistry, vol. 279, no. 41, pp. 42528–42534, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. D. Pogocki, “Mutation of the Phe20 residue in Alzheimer's amyloid beta-peptide might decrease its toxicity due to disruption of the Met35-cupric site electron transfer pathway,” Chemical Research in Toxicology, vol. 17, no. 3, pp. 325–329, 2004. View at Google Scholar
  91. P. Brunelle and A. Rauk, “The radical model of Alzheimer's disease: specific recognition of Gly29 and Gly33 by Met35 in a beta-sheet model of A beta: an ONIOM study,” Journal of Alzheimer's Disease, vol. 4, no. 4, pp. 283–289, 2002. View at Google Scholar
  92. J. Kanski, S. Varadarajan, M. Aksenova, and D. A. Butterfield, “Role of glycine-33 and methionine-35 in Alzheimer's amyloid beta-peptide 1–42-associated oxidative stress and neurotoxicity,” Biochimica et Biophysica Acta, vol. 1586, no. 2, pp. 190–198, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. N. A. Avdulov, S. V. Chochina, U. Igbavboa et al., “Amyloid beta-peptides increase annular and bulk fluidity and induce lipid peroxidation in brain synaptic plasma membranes,” Journal of Neurochemistry, vol. 68, no. 5, pp. 2086–2091, 1997. View at Google Scholar · View at Scopus
  94. D. A. Butterfield, K. Hensley, M. Harris, M. Mattson, and J. Carney, “beta-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease,” Biochemical and Biophysical Research Communications, vol. 200, no. 2, pp. 710–715, 1994. View at Google Scholar
  95. P. Maiti, A. Lomakin, G. B. Benedek, and G. Bitan, “Despite its role in assembly, methionine 35 is not necessary for amyloid beta-protein toxicity,” Journal of Neurochemistry, vol. 113, no. 5, pp. 1252–1262, 2010. View at Publisher · View at Google Scholar · View at Scopus