Table of Contents
Advances in Geriatrics
Volume 2014, Article ID 527518, 14 pages
http://dx.doi.org/10.1155/2014/527518
Review Article

Oxidative Stress and Proteostasis Network: Culprit and Casualty of Alzheimer’s-Like Neurodegeneration

1Department of Biochemical Sciences, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy
2Department of Chemistry, Center of Membrane Sciences, Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY, USA
3Department of Molecular and Biomedical Pharmacology, Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40356, USA
4Department of Chemistry, Center of Membrane Science, University of Kentucky, Lexington, KY 40506, USA

Received 20 January 2014; Accepted 10 June 2014; Published 8 July 2014

Academic Editor: Ghania Ait-Ghezala

Copyright © 2014 Fabio Di Domenico et al. 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. P. D. Ray, B. Huang, and Y. Tsuji, “Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling,” Cellular Signalling, vol. 24, no. 5, pp. 981–990, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Harman, “Aging: overview,” Annals of the New York Academy of Sciences, vol. 928, pp. 1–21, 2001. View at Google Scholar · View at Scopus
  4. M. Perluigi, A. M. Swomley, and D. A. Butterfield, “Redox proteomics and the dynamic molecular landscape of the aging brain,” Ageing Research Reviews, vol. 13, pp. 75–89, 2014. View at Publisher · View at Google Scholar
  5. D. A. Butterfield, M. Perluigi, T. Reed et al., “Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications,” Antioxidants and Redox Signaling, vol. 17, no. 11, pp. 1610–1655, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. A. Dunlop, U. T. Brunk, and K. J. Rodgers, “Oxidized proteins: mechanisms of removal and consequences of accumulation,” IUBMB Life, vol. 61, no. 5, pp. 522–527, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. R. T. Dean, S. Fu, R. Stocker, and M. J. Davies, “Biochemistry and pathology of radical-mediated protein oxidation,” Biochemical Journal, vol. 324, no. 1, pp. 1–18, 1997. View at Google Scholar · View at Scopus
  8. E. R. Stadtman and R. L. Levine, “Protein oxidation,” Annals of the New York Academy of Sciences, vol. 899, pp. 191–208, 2000. View at Google Scholar · View at Scopus
  9. R. L. Levine, “Carbonyl modified proteins in cellular regulation, aging, and disease,” Free Radical Biology and Medicine, vol. 32, no. 9, pp. 790–796, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. C. D. Smith, J. M. Carney, T. Tatsumo, E. R. Stadtman, R. A. Floyd, and W. R. Markesbery, “Protein oxidation in aging brain,” Annals of the New York Academy of Sciences, vol. 663, pp. 110–119, 1992. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. J. Suzuki, M. Carini, and D. A. Butterfield, “Protein carbonylation,” Antioxidants and Redox Signaling, vol. 12, no. 3, pp. 323–325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. R. L. Levine, J. A. Williams, E. R. Stadtman, and E. Shacter, “Carbonyl assays for determination of oxidatively modified proteins,” Methods in Enzymology, vol. 233, pp. 346–357, 1994. View at Publisher · View at Google Scholar · View at Scopus
  13. P. A. Grimsrud, H. Xie, T. J. Griffin, and D. A. Bernlohr, “Oxidative stress and covalent modification of protein with bioactive aldehydes,” The Journal of Biological Chemistry, vol. 283, no. 32, pp. 21837–21841, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. L. M. Sayre, D. A. Zelasko, P. L. R. Harris, G. Perry, R. G. Salomon, and M. A. Smith, “4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease,” Journal of Neurochemistry, vol. 68, no. 5, pp. 2092–2097, 1997. View at Google Scholar · View at Scopus
  15. M. A. Lovell, C. Xie, and W. R. Markesbery, “Acrolein is increased in Alzheimer's disease brain and is toxic to primary hippocampal cultures,” Neurobiology of Aging, vol. 22, no. 2, pp. 187–194, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Sultana and D. A. Butterfield, “Oxidatively modified GST and MRP1 in Alzheimer's disease brain: implications for accumulation of reactive lipid peroxidation products,” Neurochemical Research, vol. 29, no. 12, pp. 2215–2220, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. 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
  18. G. Spiteller, “The important role of lipid peroxidation processes in aging and age dependent diseases,” Molecular Biotechnology, vol. 37, no. 1, pp. 5–12, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. D. A. Butterfield and J. Kanski, “Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins,” Mechanisms of Ageing and Development, vol. 122, no. 9, pp. 945–962, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. D. A. Butterfield, T. T. Reed, M. Perluigi et al., “Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: implications for the role of nitration in the progression of Alzheimer's disease,” Brain Research, vol. 1148, no. 1, pp. 243–248, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. D. A. Butterfield and E. R. Stadtman, Protein Oxidation Processes in Aging Brain, 1997.
  22. G. Gokulrangan, A. Zaidi, M. L. Michaelis, and C. Schöneich, “Proteomic analysis of protein nitration in rat cerebellum: effect of biological aging,” Journal of Neurochemistry, vol. 100, no. 6, pp. 1494–1504, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. N. A. Fugere, D. A. Ferrington, and L. V. Thompson, “Protein nitration with aging in the rat semimembranosus and soleus muscles,” Journals of Gerontology A: Biological Sciences and Medical Sciences, vol. 61, no. 8, pp. 806–812, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. E. S. Dremina, V. S. Sharov, and C. Schöneich, “Protein tyrosine nitration in rat brain is associated with raft proteins, flotillin-1 and α-tubulin: effect of biological aging,” Journal of Neurochemistry, vol. 93, no. 5, pp. 1262–1271, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. H. F. Poon, V. Calabrese, M. Calvani, and D. A. Butterfield, “Proteomics analyses of specific protein oxidation and protein expression in aged rat brain and its modulation by l-acetylcarnitine: insights into the mechanisms of action of this proposed therapeutic agent for CNS disorders associated with oxidative stress,” Antioxidants and Redox Signaling, vol. 8, no. 3-4, pp. 381–394, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. D. A. Butterfield, G. Liqing, F. di Domenico, and R. A. S. Robinson, “Mass spectrometry and redox proteomics: application in disease,” Mass Spectrometry Reviews, vol. 33, no. 4, pp. 277–301, 2014. View at Publisher · View at Google Scholar
  27. J. J. M. Hoozemans and W. Scheper, “Endoplasmic reticulum: the unfolded protein response is tangled in neurodegeneration,” International Journal of Biochemistry & Cell Biology, vol. 44, no. 8, pp. 1295–1298, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Wang and R. J. Kaufman, “The impact of the unfolded protein response on human disease,” Journal of Cell Biology, vol. 197, no. 7, pp. 857–867, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Chakrabarti, A. W. Chen, and J. D. Varner, “A review of the mammalian unfolded protein response,” Biotechnology and Bioengineering, vol. 108, no. 12, pp. 2777–2793, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. K. M. Doyle, D. Kennedy, A. M. Gorman, S. Gupta, S. J. M. Healy, and A. Samali, “Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders,” Journal of Cellular and Molecular Medicine, vol. 15, no. 10, pp. 2025–2039, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Matus, L. H. Glimcher, and C. Hetz, “Protein folding stress in neurodegenerative diseases: a glimpse into the ER,” Current Opinion in Cell Biology, vol. 23, no. 2, pp. 239–252, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Boelens, S. Lust, F. Offner, M. E. Bracke, and B. W. Vanhoecke, “The endoplasmic reticulum: a target for new anticancer drugs,” In Vivo, vol. 21, no. 2, pp. 215–226, 2007. View at Google Scholar · View at Scopus
  33. R. J. Kaufman, “The cellular response to accumulation of unfolded proteins in the endoplasmic reticulum,” FASEB Journal, vol. 16, article A891, 2002. View at Google Scholar
  34. M. Gething, “Role and regulation of the ER chaperone BiP,” Seminars in Cell and Developmental Biology, vol. 10, no. 5, pp. 465–472, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. R. K. Reddy, C. Mao, P. Baumeister, R. C. Austin, R. J. Kaufman, and A. S. Lee, “Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation,” The Journal of Biological Chemistry, vol. 278, no. 23, pp. 20915–20924, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. P. G. Needham and J. L. Brodsky, “How early studies on secreted and membrane protein quality control gave rise to the ER associated degradation (ERAD) pathway: the early history of ERAD,” Biochimica et Biophysica Acta, vol. 1833, no. 11, pp. 2447–2457, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Yoshida, “ER stress and diseases,” The FEBS Journal, vol. 274, no. 3, pp. 630–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Walter and D. Ron, “The unfolded protein response: From stress pathway to homeostatic regulation,” Science, vol. 334, no. 6059, pp. 1081–1086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. B. D. Roussel, A. J. Kruppa, E. Miranda, D. C. Crowther, D. A. Lomas, and S. J. Marciniak, “Endoplasmic reticulum dysfunction in neurological disease,” The Lancet Neurology, vol. 12, no. 1, pp. 105–118, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. H. P. Harding, Y. Zhang, and D. Ron, “Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase,” Nature, vol. 397, pp. 271–274, 1999. View at Google Scholar
  41. M. Halliday and G. R. Mallucci, “Targeting the unfolded protein response in neurodegeneration: a new approach to therapy,” Neuropharmacology, vol. 76, part A, pp. 169–174, 2014. View at Publisher · View at Google Scholar
  42. K. Haze, H. Yoshida, H. Yanagi, T. Yura, and K. Mori, “Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress,” Molecular Biology of the Cell, vol. 10, no. 11, pp. 3787–3799, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Ciechanover, “Proteolysis: from the lysosome to ubiquitin and the proteasome,” Nature Reviews Molecular Cell Biology, vol. 6, no. 1, pp. 79–87, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Jung and T. Grune, “The proteasome and its role in the degradation of oxidized proteins,” IUBMB Life, vol. 60, no. 11, pp. 743–752, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Lim and J. M. M. Tan, “Role of the ubiquitin proteasome system in Parkinson's disease,” BMC Biochemistry, vol. 8, no. 1, article S13, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Grimm, A. Höhn, and T. Grune, “Oxidative protein damage and the proteasome,” Amino Acids, vol. 42, no. 1, pp. 23–38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Koegl, T. Hoppe, S. Schlenker, H. D. Ulrich, T. U. Mayer, and S. Jentsch, “A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly,” Cell, vol. 96, no. 5, pp. 635–644, 1999. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Jung, B. Catalgol, and T. Grune, “The proteasomal system,” Molecular Aspects of Medicine, vol. 30, no. 4, pp. 191–296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. B. S. Berlett and E. R. Stadtman, “Protein oxidation in aging, disease, and oxidative stress,” The Journal of Biological Chemistry, vol. 272, no. 33, pp. 20313–20316, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. K. J. Davies, “Protein damage and degradation by oxygen radicals I. general aspects.,” The Journal of Biological Chemistry, vol. 262, no. 20, pp. 9895–9901, 1987. View at Google Scholar · View at Scopus
  51. J. Cervera and R. L. Levine, “Modulation of the hydrophobicity of glutamine synthetase by mixed-function oxidation,” FASEB Journal, vol. 2, no. 10, pp. 2591–2595, 1988. View at Google Scholar · View at Scopus
  52. K. J. Davies, “Degradation of oxidized proteins by the 20S proteasome,” Biochimie, vol. 83, no. 3-4, pp. 301–310, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Ghavami, S. Shojaei, B. Yeganeh et al., “Autophagy and apoptosis dysfunction in neurodegenerative disorders,” Progress in Neurobiology, vol. 112, pp. 24–49, 2014. View at Google Scholar
  54. N. Mizushima, B. Levine, A. M. Cuervo, and D. J. Klionsky, “Autophagy fights disease through cellular self-digestion,” Nature, vol. 451, no. 7182, pp. 1069–1075, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Dasuri, L. Zhang, and J. N. Keller, “Oxidative stress, neurodegeneration, and the balance of protein degradation and protein synthesis,” Free Radical Biology and Medicine, vol. 62, pp. 170–185, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Yang and D. J. Klionsky, “Mammalian autophagy: core molecular machinery and signaling regulation,” Current Opinion in Cell Biology, vol. 22, no. 2, pp. 124–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. García-Arencibia, W. E. Hochfeld, P. P. C. Toh, and D. C. Rubinsztein, “Autophagy, a guardian against neurodegeneration,” Seminars in Cell & Developmental Biology, vol. 21, no. 7, pp. 691–698, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Manjithaya, T. Y. Nazarko, J. Farré, and S. Suresh, “Molecular mechanism and physiological role of pexophagy,” FEBS Letters, vol. 584, no. 7, pp. 1367–1373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. D. S. Arroyo, E. A. Gaviglio, J. M. P. Ramos, C. Bussi, M. C. Rodriguez-Galan, and P. Iribarren, “Autophagy in inflammation, infection, neurodegeneration and cancer,” International Immunopharmacology, vol. 18, no. 1, pp. 55–65, 2014. View at Publisher · View at Google Scholar
  60. B. Ravikumar, S. Sarkar, J. E. Davies et al., “Regulation of mammalian autophagy in physiology and pathophysiology,” Physiological Reviews, vol. 90, pp. 1383–1435, 2010. View at Publisher · View at Google Scholar
  61. D. J. Metcalf, M. García-Arencibia, W. E. Hochfeld, and D. C. Rubinsztein, “Autophagy and misfolded proteins in neurodegeneration,” Experimental Neurology, vol. 238, no. 1, pp. 22–28, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. V. J. Lavallard, A. J. Meijer, P. Codogno, and P. Gual, “Autophagy, signaling and obesity,” Pharmacological Research, vol. 66, no. 6, pp. 513–525, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Glick, S. Barth, and K. F. Macleod, “Autophagy: cellular and molecular mechanisms,” The Journal of Pathology, vol. 221, no. 1, pp. 3–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Sarkar, “Regulation of autophagy by mTOR-dependent and mTOR-independent pathways: autophagy dysfunction in neurodegenerative diseases and therapeutic application of autophagy enhancers,” Biochemical Society Transactions, vol. 41, pp. 1103–1130, 2013. View at Publisher · View at Google Scholar
  65. M. Perluigi, F. di Domenico, and D. A. Buttterfield, “Unraveling the complexity of neurodegeneration in brain of subjects with down syndrome: insights from proteomics,” Proteomics: Clinical Applications, vol. 8, no. 1-2, pp. 73–85, 2014. View at Publisher · View at Google Scholar
  66. M. Perluigi and D. A. Butterfield, “Oxidative stress and down syndrome: a route toward Alzheimer-like dementia,” Current Gerontology and Geriatrics Research, vol. 2012, Article ID 724904, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. H. W. Querfurth and F. M. LaFerla, “Alzheimer's disease,” The New England Journal of Medicine, vol. 362, no. 4, pp. 329–344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. V. H. Cornejo and C. Hetz, “The unfolded protein response in Alzheimer's disease,” Seminars in Immunopathology, vol. 35, no. 3, pp. 277–292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. Y. Ihara, M. Morishima-Kawashima, and R. Nixon, “The ubiquitin-proteasome system and the autophagic-lysosomal system in Alzheimer disease,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 8, 2012. View at Google Scholar · View at Scopus
  70. D. C. Rubinsztein, “The roles of intracellular protein-degradation pathways in neurodegeneration,” Nature, vol. 443, no. 7113, pp. 780–786, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Resende, E. Ferreiro, C. Pereira, and C. R. Oliveira, “ER stress is involved in Aβ-induced GSK-3β activation and tau phosphorylation,” Journal of Neuroscience Research, vol. 86, no. 9, pp. 2091–2099, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. J. J. M. Hoozemans, R. Veerhuis, E. S. van Haastert et al., “The unfolded protein response is activated in Alzheimer's disease,” Acta Neuropathologica, vol. 110, no. 2, pp. 165–172, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Grune and K. J. A. Davies, “The proteasomal system and HNE-modified proteins,” Molecular Aspects of Medicine, vol. 24, no. 4-5, pp. 195–204, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. B. Friguet and L. I. Szweda, “Inhibition of the multicatalytic proteinase (proteasome) by 4-hydroxy-2-nonenal cross-linked protein,” FEBS Letters, vol. 405, no. 1, pp. 21–25, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Reinheckel, N. Sitte, O. Ullrich, U. Kuckelkorn, K. J. A. Davies, and T. Grune, “Comparative resistance of the 20 S and 26 S proteasome to oxidative stress,” Biochemical Journal, vol. 335, part 3, pp. 637–642, 1998. View at Google Scholar · View at Scopus
  76. T. Reinheckel, O. Ullrich, N. Sitte, and T. Grune, “Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress,” Archives of Biochemistry and Biophysics, vol. 377, no. 1, pp. 65–68, 2000. View at Publisher · View at Google Scholar · View at Scopus
  77. N. Chondrogianni and E. S. Gonos, “Proteasome dysfunction in mammalian aging: steps and factors involved,” Experimental Gerontology, vol. 40, no. 12, pp. 931–938, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. J. N. Keller, K. B. Hanni, and W. R. Markesbery, “Impaired proteasome function in Alzheimer's disease,” Journal of Neurochemistry, vol. 75, no. 1, pp. 436–439, 2000. View at Publisher · View at Google Scholar · View at Scopus
  79. L. A. Pasquini, M. B. Moreno, A. M. Adamo, J. M. Pasquini, and E. F. Soto, “Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activates caspase-3 in cultured cerebellar granule cells,” Journal of Neuroscience Research, vol. 59, no. 5, pp. 601–611, 2000. View at Publisher · View at Google Scholar
  80. F. di Domenico, G. Pupo, A. Tramutola et al., “Redox proteomics analysis of HNE-modified proteins in Down syndrome brain: clues for understanding the development of Alzheimer disease,” Free Radical Biology & Medicine, vol. 71, pp. 270–280, 2014. View at Publisher · View at Google Scholar
  81. F. di Domenico, R. Coccia, A. Cocciolo et al., “Impairment of proteostasis network in Down syndrome prior to the development of Alzheimer's disease neuropathology: redox proteomics analysis of human brain,” Biochimica et Biophysica Acta, vol. 1832, no. 8, pp. 1249–1259, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Morawe, C. Hiebel, A. Kern, and C. Behl, “Protein homeostasis, aging and Alzheimer's disease,” Molecular Neurobiology, vol. 46, no. 1, pp. 41–54, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. J. E. Hamos, B. Oblas, D. Pulaski-Salo, W. J. Welch, D. G. Bole, and D. A. Drachman, “Expression of heat shock proteins in Alzheimer's disease,” Neurology, vol. 41, no. 3, pp. 345–350, 1991. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Cisse, G. Perry, G. Lacoste-Royal, T. Cabana, and D. Gauvreau, “Immunochemical identification of ubiquitin and heat-shock proteins in corpora amylacea from normal aged and Alzheimer's disease brains,” Acta Neuropathologica, vol. 85, no. 3, pp. 233–240, 1993. View at Google Scholar · View at Scopus
  85. F. di Domenico, R. Sultana, G. F. Tiu et al., “Protein levels of heat shock proteins 27, 32, 60, 70, 90 and thioredoxin-1 in amnestic mild cognitive impairment: an investigation on the role of cellular stress response in the progression of Alzheimer disease,” Brain Research, vol. 1333, pp. 72–81, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Magrané, R. C. Smith, K. Walsh, and H. W. Querfurth, “Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons,” The Journal of Neuroscience, vol. 24, no. 7, pp. 1700–1706, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. D. Boyd-Kimball, A. Castegna, R. Sultana et al., “Proteomic identification of proteins oxidized by Aβ(1–42) in synaptosomes: implications for Alzheimer’s disease,” Brain Research, vol. 1044, no. 2, pp. 206–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Barone, F. di Domenico, R. Sultana et al., “Heme oxygenase-1 posttranslational modifications in the brain of subjects with Alzheimer disease and mild cognitive impairment,” Free Radical Biology and Medicine, vol. 52, no. 11-12, pp. 2292–2301, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. M. D. Maines, “The heme oxygenase system: a regulator of second messenger gases,” Annual Review of Pharmacology and Toxicology, vol. 37, pp. 517–554, 1997. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Mancuso, “Heme oxygenase and its products in the nervous system,” Antioxidants and Redox Signaling, vol. 6, no. 5, pp. 878–887, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Hui, D. Wang, W. Li et al., “Long-term overexpression of heme oxygenase 1 promotes tau aggregation in mouse brain by inducing tau phosphorylation,” Journal of Alzheimer's Disease, vol. 26, no. 2, pp. 299–313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. H. M. Schipper, A. Gupta, and W. A. Szarek, “Suppression of glial HO-1 activitiy as a potential neurotherapeutic intervention in AD,” Current Alzheimer Research, vol. 6, no. 5, pp. 424–430, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. J. J. Yerbury, E. M. Stewart, A. R. Wyatt, and M. R. Wilson, “Quality control of protein folding in extracellular space,” EMBO Reports, vol. 6, no. 12, pp. 1131–1136, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Thambisetty and S. Lovestone, “Blood-based biomarkers of Alzheimers disease: challenging but feasible,” Biomarkers in Medicine, vol. 4, no. 1, pp. 65–79, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Cocciolo, F. Di Domenico, R. Coccia et al., “Decreased expression and increased oxidation of plasma haptoglobin in Alzheimer disease: insights from redox proteomics,” Free Radical Biology and Medicine, vol. 53, no. 10, pp. 1868–1876, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Di Domenico, R. Coccia, D. A. Butterfield, and M. Perluigi, “Circulating biomarkers of protein oxidation for Alzheimer disease: expectations within limits,” Biochimica et Biophysica Acta: Proteins and Proteomics, vol. 1814, no. 12, pp. 1785–1795, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. 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
  98. D. A. Butterfield, J. Drake, C. Pocernich, and A. Castegna, “Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid β-peptide,” Trends in Molecular Medicine, vol. 7, no. 12, pp. 548–554, 2001. View at Publisher · View at Google Scholar · View at Scopus
  99. 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 Publisher · View at Google Scholar · View at Scopus
  100. Q. Ding, W. R. Markesbery, V. Cecarini, and J. N. Keller, “Decreased RNA, and increased RNA oxidation, in ribosomes from early Alzheimer's disease,” Neurochemical Research, vol. 31, no. 5, pp. 705–710, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. E. M. Sajdel-Sulkowska and C. A. Marotta, “Alzheimer's disease brain: alterations in RNA levels and in a ribonuclease-inhibitor complex,” Science, vol. 225, no. 4665, pp. 947–949, 1984. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Perluigi, R. Sultana, G. Cenini et al., “Redox proteomics identification of 4-hydroxynonenalmodified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis,” Proteomics—Clinical Applications, vol. 3, no. 6, pp. 682–693, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. T. V. Pestova and C. U. T. Hellen, “The structure and function of initiation factors in eukaryotic protein synthesis,” Cellular and Molecular Life Sciences, vol. 57, no. 4, pp. 651–674, 2000. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Schutkowski, A. Bernhardt, X. Z. Zhou et al., “Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition,” Biochemistry, vol. 37, no. 16, pp. 5566–5575, 1998. View at Publisher · View at Google Scholar · View at Scopus
  105. D. A. Butterfield, H. M. Abdul, W. Opii et al., “Pin1 in Alzheimer's disease,” Journal of Neurochemistry, vol. 98, no. 6, pp. 1697–1706, 2006. View at Publisher · View at Google Scholar · View at Scopus
  106. Y. C. Liou, A. Ryo, H. K. Huang et al., “Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 3, pp. 1335–1340, 2002. View at Publisher · View at Google Scholar · View at Scopus
  107. R. Sultana, D. Boyd-Kimball, H. F. Poon et al., “Redox proteomics identification of oxidized proteins in Alzheimer's disease hippocampus and cerebellum: an approach to understand pathological and biochemical alterations in AD,” Neurobiology of Aging, vol. 27, no. 11, pp. 1564–1576, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. P. Ramakrishnan, D. W. Dickson, and P. Davies, “Pin1 colocalization with phosphorylated tau in Alzheimer's disease and other tauopathies,” Neurobiology of Disease, vol. 14, no. 2, pp. 251–564, 2003. View at Publisher · View at Google Scholar · View at Scopus
  109. X. Z. Zhou, O. Kops, A. Werner et al., “Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and Tau proteins,” Molecular Cell, vol. 6, no. 4, pp. 873–883, 2000. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Cenini, A. L. S. Dowling, T. L. Beckett et al., “Association between frontal cortex oxidative damage and beta-amyloid as a function of age in Down syndrome,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1822, no. 2, pp. 130–138, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. F. Di Domenico, R. Sultana, A. Ferree et al., “Redox proteomics analyses of the influence of co-expression of wild-type or mutated LRRK2 and Tau on C. elegans protein expression and oxidative modification: relevance to parkinson disease,” Antioxidants and Redox Signaling, vol. 17, no. 11, pp. 1490–1506, 2012. View at Publisher · View at Google Scholar · View at Scopus
  112. D. Necchi, S. Lomoio, and E. Scherini, “Dysfunction of the ubiquitin-proteasome system in the cerebellum of aging Ts65Dn mice,” Experimental Neurology, vol. 232, no. 2, pp. 114–118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  113. Z. Kouchi, H. Sorimachi, K. Suzuki, and S. Ishiura, “Proteasome inhibitors induce the association of Alzheimer's amyloid precursor protein with Hsc73,” Biochemical and Biophysical Research Communications, vol. 254, no. 3, pp. 804–810, 1999. View at Publisher · View at Google Scholar · View at Scopus
  114. S. S. Vembar and J. L. Brodsky, “One step at a time: endoplasmic reticulum-associated degradation,” Nature Reviews Molecular Cell Biology, vol. 9, no. 12, pp. 944–957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. D. A. Butterfield, A. Gnjec, H. F. Poon et al., “Redox proteomics identification of oxidatively modified brain proteins in inherited Alzheimer's disease: an initial assessment,” Journal of Alzheimer's Disease, vol. 10, no. 4, pp. 391–397, 2006. View at Google Scholar · View at Scopus
  116. A. Castegna, M. Aksenov, M. Aksenova et al., “Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1,” Free Radical Biology and Medicine, vol. 33, no. 4, pp. 562–571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  117. A. N. Hegde, “The ubiquitin-proteasome pathway and synaptic plasticity,” Learning and Memory, vol. 17, no. 7, pp. 314–327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Di Fonzo, H. F. Chien, M. Socal et al., “ATP13A2 missense mutations in juvenile parkinsonism and young onset Parkinson disease,” Neurology, vol. 68, no. 19, pp. 1557–1562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. R. Zoncu, L. Bar-Peled, A. Efeyan, S. Wang, Y. Sancak, and D. M. Sabatini, “mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase,” Science, vol. 334, no. 6056, pp. 678–683, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. S. Grimm, L. Ernst, N. Grötzinger et al., “Cathepsin D is one of the major enzymes involved in intracellular degradation of AGE-modified proteins,” Free Radical Research, vol. 44, no. 9, pp. 1013–1026, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. P. Benes, V. Vetvicka, and M. Fusek, “Cathepsin D-Many functions of one aspartic protease,” Critical Reviews in Oncology/Hematology, vol. 68, no. 1, pp. 12–28, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. U. Bandyopadhyay, S. Sridhar, S. Kaushik, R. Kiffin, and A. M. Cuervo, “Identification of regulators of chaperone-mediated autophagy,” Molecular Cell, vol. 39, no. 4, pp. 535–547, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. R. Kiffin, C. Christian, E. Knecht, and A. M. Cuervo, “Activation of chaperone-mediated autophagy during oxidative stress,” Molecular Biology of the Cell, vol. 15, no. 11, pp. 4829–4840, 2004. View at Publisher · View at Google Scholar · View at Scopus
  124. G. Joshi, R. Sultana, M. Perluigi, and D. A. Butterfield, “In vivo protection of synaptosomes from oxidative stress mediated by Fe2+/H2O2 or 2,2-azobis-(2-amidinopropane) dihydrochloride by the glutathione mimetic tricyclodecan-9-yl-xanthogenate,” Free Radical Biology and Medicine, vol. 38, no. 8, pp. 1023–1031, 2005. View at Publisher · View at Google Scholar · View at Scopus