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Redox Proteomics Identification of Oxidatively Modified Proteins in Alzheimer’s Disease Brain and in Brain from a Rodent Model of Familial Parkinson’s Disease: Insights into Potential Mechanisms of Neurodegeneration

  • Rukhsana Sultana
  • H. Fai Poon
  • D. Allan Butterfield
Conference paper
Part of the Advances in Behavioral Biology book series (ABBI, volume 57)

Keywords

Oxidative Modification Neurobiol Aging Proteomic Identification Redox Proteomics Oxidatively Modify Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Butterfield DA. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer’s disease brain—a review. Free Radic Res 2002;36(12):1307–1313PubMedCrossRefGoogle Scholar
  2. 2.
    Butterfield DA, Castegna A, Lauderback CM, Drake J. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer’s disease brain contribute to neuronal death. Neurobiol Aging 2002;23(5):655–664PubMedCrossRefGoogle Scholar
  3. 3.
    Butterfield DA, Drake J, Pocernich C, Castegna A. Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid beta-peptide. Trends Mol Med 2001;7(12):548–554PubMedCrossRefGoogle Scholar
  4. 4.
    Butterfield DA, Lauderback CM, Lipid peroxidation and protein oxidation in Alzheimer’s disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med 2002;32(11):1050–1060PubMedCrossRefGoogle Scholar
  5. 5.
    Markesbery WR. Oxidative stress hypothesis in Alzheimer’s disease. Free Radic Biol Med 1997;23(1):134–147PubMedCrossRefGoogle Scholar
  6. 6.
    Pocernich CB, Cardin AL, Racine CL, et al. Glutathione elevation and its protective role in acrolein-induced protein damage in synaptosomal membranes: relevance to brain lipid peroxidation in neurodegenerative disease. Neurochem Int 2001;39(2):141–149PubMedCrossRefGoogle Scholar
  7. 7.
    Lovell MA, Xie C, Markesbery WR, Acrolein is increased in Alzheimer’s disease brain and is toxic to primary hippocampal cultures. Neurobiol Aging 2001;22(2):187–194PubMedCrossRefGoogle Scholar
  8. 8.
    Mark RJ, Lovell MA, Markesbery WR, et al. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J Neurochem 1997;68(1):255–264PubMedGoogle Scholar
  9. 9.
    Smith MA, Richey PL, Taneda S, et al. Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer’s disease. Ann N Y Acad Sci 1994;738:447–454PubMedCrossRefGoogle Scholar
  10. 10.
    Castegna A, Thongboonkerd V, Klein JB, et al. Proteomic identification of nitrated proteins in Alzheimer’s disease brain. J Neurochem 2003;85(6):1394–1401PubMedCrossRefGoogle Scholar
  11. 11.
    Smith MA, Richey Harris PL, Sayre LM, et al. Widespread peroxynitrite-mediated damage in Alzheimer’s disease. J Neurosci 1997;17(8):2653–2657PubMedGoogle Scholar
  12. 12.
    Smith MA, Sayre LM, Monnier VM, Perry G. Oxidative posttranslational modifications in Alzheimer disease: a possible pathogenic role in the formation of senile plaques and neurofibrillary tangles. Mol Chem Neuropathol 1996;28(1-3):41–48PubMedGoogle Scholar
  13. 13.
    Sultana R, Poon HF, Cai J, et al. Identification of nitrated proteins in Alzheimer’s disease brain using redox proteomics approach. Neurobiol Dis 2006;22(1):76–87PubMedCrossRefGoogle Scholar
  14. 14.
    Butterfield DA, Stadtman ER. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol 1997;2:161–191CrossRefGoogle Scholar
  15. 15.
    Berlett BS, Stadtman ER, Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997;272(33):20313–20316PubMedCrossRefGoogle Scholar
  16. 16.
    Butterfield DA, Hensley K, Cole P, et al. Oxidatively induced structural alteration of glutamine synthetase assessed by analysis of spin label incorporation kinetics: relevance to Alzheimer’s disease. J Neurochem 1997;68(6):2451–2457PubMedGoogle Scholar
  17. 17.
    Lauderback CM, Hackett JM, Huang FF, 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 Abeta1-42. J Neurochem 2001;78(2):413–416PubMedCrossRefGoogle Scholar
  18. 18.
    Sultana R, Butterfield DA, Oxidatively modified GST and MRP1 in Alzheimer’s disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res 2004;29:2215–2220PubMedCrossRefGoogle Scholar
  19. 19.
    Butterfield DA. Proteomics: a new approach to investigate oxidative stress in Alzheimer’s disease brain. Brain Res 2004;1000(1-2):1–7PubMedCrossRefGoogle Scholar
  20. 20.
    Butterfield DA, Perluigi M, Sultana R. Oxidative stress in Alzheimer’s disease brain: new insights from redox proteomics. Eur J Pharmacol 2006;545(1):39–50PubMedCrossRefGoogle Scholar
  21. 21.
    Dalle-Donne I, Scaloni A, Butterfield DA, Redox Proteomics: From protein Modifications to Cellular Dysfunction and Diseases. Wiley, Hoboken, NJ, 2006Google Scholar
  22. 22.
    Rabilloud T. Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics 2002;2:3–10PubMedCrossRefGoogle Scholar
  23. 23.
    Tilleman K, Stevens T, Spittaels I, et al. Differential expression of brain proteins in glycogen synthase kinase-3 transgenic mice: a proteomics point of view. Proteomics 2002;2:94–104PubMedCrossRefGoogle Scholar
  24. 24.
    Kaji H, Tsuji T, Mawuenyega KG, et al. Profiling of Caenorhabditis elegans proteins using two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-time of flight-mass spectrometry. Electrophoresis 2000;21(9):1755–1765PubMedCrossRefGoogle Scholar
  25. 25.
    Santoni V, Molloy M, Rabilloud T. Membrane proteins and proteomics: un amour impossible? Electrophoresis 2000;21(6):1054–1070PubMedCrossRefGoogle Scholar
  26. 26.
    Herbert B. Advances in protein solubilization for two-dimensional gel electrophoresis. Electrophoresis 1999;20:660–663PubMedCrossRefGoogle Scholar
  27. 27.
    Molloy MP. Two-dimensional electrophoresis of membrane proteins using immobilized pH gradients, Anal Biochem 2000;280(1):1–10PubMedCrossRefGoogle Scholar
  28. 28.
    Aebersold R, Goodlett DR, Mass spectrometry in proteomics. Chem Rev 2001;101(2):269–295PubMedCrossRefGoogle Scholar
  29. 29.
    Hoogland C, Sanchez C, Tonella L, et al. The 1999 SWISS-2DPAGE database update. Nucleic Acids Res 2000;28(1):286–288PubMedCrossRefGoogle Scholar
  30. 30.
    Aksenova M, Butterfield DA, Zhang SX, et al. Increased protein oxidation and decreased creatine kinase BB expression and activity after spinal cord contusion injury. J Neurotrauma 2002;19(4):491–502PubMedCrossRefGoogle Scholar
  31. 31.
    Boyd-Kimball D, Castegna A, Sultana R, et al. Proteomic identification of proteins oxidized by Abeta(1-42) in synaptosomes: implications for Alzheimer’s disease. Brain Res 2005;1044(2):206–215PubMedCrossRefGoogle Scholar
  32. 32.
    Butterfield DA, Poon HF, St Clair D, et al. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer’s disease. Neurobiol Dis 2006;22(2):223–232PubMedCrossRefGoogle Scholar
  33. 33.
    Sultana R, Boyd-Kimball D, Poon HF, et al. Oxidative modification and down-regulation of Pin 1 Alzheimer’s disease hippocampus: a redox proteomics analysis. Neurobiol Aging 2006;27(7):918–925PubMedCrossRefGoogle Scholar
  34. 34.
    Sultana R, Boyd-Kimbal Dl, Poon HF, 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. Neurobiol Aging 2006;27:1564–1576PubMedCrossRefGoogle Scholar
  35. 35.
    Grundke-Iqbal I, Iqbal K, Quinlan M, et al. Microtubule-associated protein tau: a component of Alzheimer paired helical filaments. J Biol Chem 1986;261(13):6084–6089PubMedGoogle Scholar
  36. 36.
    Selkoe DJ. Presenilin, notch, and the genesis and treatment of Alzheimer’s disease. Proc Natl Acad Sci U S A 2001;98(20):11039–11041PubMedCrossRefGoogle Scholar
  37. 37.
    Aksenov MY, Aksenova MV, Butterfield DA, et al. Protein oxidation in the brain in Alzheimer’s disease. Neuroscience 2001;103(2):373–383PubMedCrossRefGoogle Scholar
  38. 38.
    Drake J, Link CD, Butterfield DA, Oxidative stress precedes fibrillar deposition of Alzheimer’s disease amyloid beta-peptide (1-42) in a transgenic Caenorhabditis elegans model. Neurobiol Aging 2003;24(3):415–420PubMedCrossRefGoogle Scholar
  39. 39.
    Lambert MP, Viola KL, Chromy BA, et al. Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies. J Neurochem 2001;79(3):595–605PubMedCrossRefGoogle Scholar
  40. 40.
    Oda T, Wals P, Osterburg HH, et al. Clusterin (apoJ) alters the aggregation of amyloid beta-peptide (Abeta1-42) and forms slowly sedimenting Abeta complexes that cause oxidative stress. Exp Neurol 1995;136(1):22–31PubMedCrossRefGoogle Scholar
  41. 41.
    Hensley K, Hall K, Subramaniam R, et al. Brain regional correspondence between Alzheimer’s disease histopathology and biomarkers of protein oxidation. J Neurochem 1995;65(5):2146–2156PubMedGoogle Scholar
  42. 42.
    Boyd-Kimball D, Sultana R, Mohmmad-Abdul H, Butterfield DA, Rodent Abeta(1-42) exhibits oxidative stress properties similar to those of human Abeta(1-42): implications for proposed mechanisms of toxicity. J Alzheimers Dis 2004;6(5):515–525PubMedGoogle Scholar
  43. 43.
    Yatin SM, Varadarajan S, Butterfield DA. Vitamin E prevents Alzheimer’s amyloid beta-peptide (1-42)-induced neuronal protein oxidation and reactive oxygen species production. J Alzheimers Dis 2000;2(2):123–131PubMedGoogle Scholar
  44. 44.
    Markesbery WR, Lovell MA. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer’s disease. Neurobiol Aging 1998;19(1):33–36PubMedCrossRefGoogle Scholar
  45. 45.
    Subramaniam R, Roediger F, Jordan B, et al. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. J Neurochem 1997;69(3):1161–1169PubMedGoogle Scholar
  46. 46.
    Butterfield DA, Pocernich CB. The glutamatergic system and Alzheimer’s disease: therapeutic implications. CNS Drugs 2003;17(9):641–652PubMedCrossRefGoogle Scholar
  47. 47.
    Paumi CM, Wright M, Townsend AJ, Morrow CS, Multidrug resistance protein (MRP) 1 and MRP3 attenuate cytotoxic and transactivating effects of the cyclopentenone prostaglandin, 15-deoxy-delta(12,14)prostaglandin J2 in MCF7 breast cancer cells. Biochemistry 2003;42(18):5429–5437PubMedCrossRefGoogle Scholar
  48. 48.
    Castegna A, Aksenov M, Aksenova M, 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 Radic Biol Med 2002;33(4):562–571PubMedCrossRefGoogle Scholar
  49. 49.
    Castegna A, Aksenov M, Thongboonkerd V, et al. Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part II. Dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 2002;82(6):1524–1532PubMedCrossRefGoogle Scholar
  50. 50.
    Small GW, Okonek A, Mandelkern MA, et al. Age-associated memory loss: initial neuropsychological and cerebral metabolic findings of a longitudinal study. Int Psychogeriatr 1994;6(1):23–44; discussion 60–22PubMedCrossRefGoogle Scholar
  51. 51.
    Mazzola JL, Sirover MA, Reduction of glyceraldehyde-3-phosphate dehydrogenase activity in Alzheimer’s disease and in Huntington’s disease fibroblasts. J Neurochem 2001;76(2):442–449PubMedCrossRefGoogle Scholar
  52. 52.
    Hoyer S. Causes and consequences of disturbances of cerebral glucose metabolism in sporadic Alzheimer disease: therapeutic implications. Adv Exp Med Biol 2004;541:135–152PubMedGoogle Scholar
  53. 53.
    Planel E, Miyasaka T, Launey T, et al. Alterations in glucose metabolism induce hypothermia leading to tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer’s disease. J Neurosci 2004;24(10):2401–2411PubMedCrossRefGoogle Scholar
  54. 54.
    Masliah E, Alford M, DeTeresa R, et al. Deficient glutamate transport is associated with neurodegeneration in Alzheimer’s disease. Ann Neurol 1995;40:759-766CrossRefGoogle Scholar
  55. 55.
    Pickart CM, Fushman D, Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 2004;8(6):610–616PubMedCrossRefGoogle Scholar
  56. 56.
    Wilkinson KD, Tashayev VL, O’Connor LB, et al. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry 1995;34(44):14535–14546PubMedCrossRefGoogle Scholar
  57. 57.
    Choi J, Levey AI, Weintraub ST, et al. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson’s and Alzheimer’s diseases. J Biol Chem 2004;279(13):13256–13264PubMedCrossRefGoogle Scholar
  58. 58.
    Butterfield DA, Boyd-Kimball D, Castegna A. Proteomics in Alzheimer’s disease: insights into potential mechanisms of neurodegeneration. J Neurochem 2003;86(6):1313–1327PubMedCrossRefGoogle Scholar
  59. 59.
    Hyun DH, Lee MH, Halliwell B, Jenner P. Proteasomal dysfunction induced by 4-hydroxy-2,3-trans-nonenal, an end-product of lipid peroxidation: a mechanism contributing to neurodegeneration? J Neurochem 2002;83(2):360–370PubMedCrossRefGoogle Scholar
  60. 60.
    Castegna A, Thongboonkerd V, Klein J, et al. Proteomic analysis of brain proteins in the gracile axonal dystrophy (GAD) mouse, a syndrome that emanates from dysfunctional ubiquitin carboxyl-terminal hydrolase L-1, reveals oxidation of key proteins. J Neurochem 2004;88(6):1540–1546PubMedGoogle Scholar
  61. 61.
    Daleke SL, Lyles JV. Identification and purification of aminophospholipid flippases. Biochim Biophys Acta 2000;1486(1):108–127PubMedGoogle Scholar
  62. 62.
    Davies P. Challenging the cholinergic hypothesis in Alzheimer disease. JAMA 1999;281(15):1433–1434PubMedCrossRefGoogle Scholar
  63. 63.
    Castegna A, Lauderback CM, Mohmmad-Abdul H, Butterfield DA. Modulation of phospholipid asymmetry in synaptosomal membranes by the lipid peroxidation products, 4-hydroxynonenal and acrolein: implications for Alzheimer’s disease. Brain Res 2004;1004(1-2):193–197PubMedCrossRefGoogle Scholar
  64. 64.
    Mohmmad-Abdul H, Butterfield D. Protection against amyloid beta-peptide (1-42)-induced loss of phospholipid asymmetry in synaptosomal membranes by tricyclodecan-9-xanthogenate (D609) and ferulic acid ethyl ester: implications for Alzheimer’s disease. Biochim Biophys Acta 2005;1741(1-2):140–48PubMedGoogle Scholar
  65. 65.
    Hamajima N, Matsuda K, Sakata S, et al. A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene 1996;180:157–163PubMedCrossRefGoogle Scholar
  66. 66.
    Kato K, Hamajima N, Inagaki H, et al. Post-meiotic expression of the mouse dihydropyrimidinase-related protein 3 (DRP-3) gene during spermiogenesis. Mol Reprod Dev 1998;51(1):105–111PubMedCrossRefGoogle Scholar
  67. 67.
    Wang LH, Strittmatter SM. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 1996;16(19):6197–6207PubMedGoogle Scholar
  68. 68.
    Lubec G, Nonaka M, Krapfenbauer K, et al. Expression of the dihydropyrimidinase related protein 2 (DRP-2) in Down syndrome and Alzheimer’s disease brain is downregulated at the mRNA and dysregulated at the protein level. J Neural Transm Suppl 1999;57:161–177PubMedGoogle Scholar
  69. 69.
    Weitzdoerfer R, Fountoulakis M, Lubec G. Aberrant expression of dihydropyrimidinase related proteins-2, -3 and -4 in fetal Down syndrome brain. J Neural Transm Suppl 2001;61:95–107PubMedGoogle Scholar
  70. 70.
    Johnston-Wilson NL, Sims CD, Hofmann JP, et al. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder; the Stanley Neuropathology Consortium. Mol Psychiatry 2000;5(2):142–149PubMedCrossRefGoogle Scholar
  71. 71.
    Coleman PD, Flood DG, Neuron numbers and dendritic extent in normal aging and Alzheimer’s disease. Neurobiol Aging 1987;8(6):521–545PubMedCrossRefGoogle Scholar
  72. 72.
    Schutkowski M, Bernhardt A, Zhou XZ, et al. Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition. Biochemistry 1998;37(16):5566–5575PubMedCrossRefGoogle Scholar
  73. 73.
    Zhou XZ, Kops O, Werner A, et al. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 2000;6(4):873–883PubMedCrossRefGoogle Scholar
  74. 74.
    Holzer M, Gartner U, Stobe A, et al. Inverse association of Pin1 and tau accumulation in Alzheimer’s disease hippocampus. Acta Neuropathol (Berl) 2002;104(5):471–481Google Scholar
  75. 75.
    Kurt MA, Davies DC, Kidd M, et al. Hyperphosphorylated tau and paired helical filament-like structures in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Neurobiol Dis 2003;14(1):89–97PubMedCrossRefGoogle Scholar
  76. 76.
    Ramakrishnan P, Dickson DW, Davies P. Pin1 colocalization with phosphorylated tau in Alzheimer’s disease and other tauopathies. Neurobiol Dis 2003;14(2):251–264PubMedCrossRefGoogle Scholar
  77. 77.
    Arendt T. Synaptic plasticity and cell cycle activation in neurons are alternative effector pathways: the ‘Dr. Jekyll and Mr. Hyde concept’ of Alzheimer’s disease or the yin and yang of neuroplasticity. Prog Neurobiol 2003;71(2-3):83–248PubMedCrossRefGoogle Scholar
  78. 78.
    Butterfield DA,. Abdul HM, Opii W, et al. Pin1 in Alzheimer’s disease. J Neurochem 2006;98(6):1697–1706PubMedCrossRefGoogle Scholar
  79. 79.
    Sultana R, Butterfield DA. Regional expression of key cell cycle proteins in brain from subjects with amnestic mild cognitive impairment. Neurochem Res 2007;32:655–662PubMedCrossRefGoogle Scholar
  80. 80.
    Beckers CJ, Block MR, Glick BS, et al. Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein. Nature 1989;339(6223):397–398PubMedCrossRefGoogle Scholar
  81. 81.
    Stenbeck G. Soluble NSF-attachment proteins. Int J Biochem Cell Biol 1998;30(5):573-577PubMedCrossRefGoogle Scholar
  82. 82.
    Sly WS, Hu PY. Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem 1995;64:375–401PubMedCrossRefGoogle Scholar
  83. 83.
    Meier-Ruge W, Iwangoff P, Reichlmeier K. Neurochemical enzyme changes in Alzheimer’s and Pick’s disease. Arch Gerontol Geriatr 1984;3(2):161–165PubMedCrossRefGoogle Scholar
  84. 84.
    Boyd-Kimball D, Poon HF, Lynn BC, et al. Proteomic identification of proteins specifically oxidized in Caenorhabditis elegans expressing human Abeta(1-42): implications for Alzheimer’s disease. Neurobiol Aging 2006;27(9):1239–1249PubMedCrossRefGoogle Scholar
  85. 85.
    Boyd-Kimball D, Sultana R, Poon HF, et al. Proteomic identification of proteins specifically oxidized by intracerebral injection of Abeta(1-42) into rat brain: implications for Alzheimer’s disease. Neuroscience 2005;132(2):313–324PubMedCrossRefGoogle Scholar
  86. 86.
    Boyd-Kimball D, Sultana R, Poon HF, et al. Gamma-glutamylcysteine ethyl ester protection of proteins from Abeta(1-42)-mediated oxidative stress in neuronal cell culture: a proteomics approach. J Neurosci Res 2005;79(5):707–713PubMedCrossRefGoogle Scholar
  87. 87.
    Sultana R, Newman SF, Abdul HM, et al. Protective effect of D609 against amyloid-beta1-42-induced oxidative modification of neuronal proteins: redox proteomics study. J Neurosci Res 2006;84(2):409–417PubMedCrossRefGoogle Scholar
  88. 88.
    Eriksen JL, Dawson TM, Dickson DW, Petrucelli L. Caught in the act: alpha-synuclein is the culprit in Parkinson’s disease. Neuron 2003;40(3):453–456PubMedCrossRefGoogle Scholar
  89. 89.
    Dawson TM, Dawson VL. Molecular pathways of neurodegeneration in Parkinson’s disease. Science 2003;302(5646):819–822PubMedCrossRefGoogle Scholar
  90. 90.
    Kruger R, Kuhn W, Muller T, et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease. Nat Genet 1998;18(2):106–108PubMedCrossRefGoogle Scholar
  91. 91.
    Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science 1997;276(5321):2045–2047PubMedCrossRefGoogle Scholar
  92. 92.
    Alam ZI, Daniel SE, Lees AJ, et al. A generalised increase in protein carbonyls in the brain in Parkinson’s but not incidental Lewy body disease. J Neurochem 1997;69(3):1326–1329PubMedCrossRefGoogle Scholar
  93. 93.
    Floor E, Wetzel MG. Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 1998;70(1):268–275PubMedCrossRefGoogle Scholar
  94. 94.
    Jenner P. Oxidative stress in Parkinson’s disease. Ann Neurol 2003;53(suppl 3):S26–S36PubMedCrossRefGoogle Scholar
  95. 95.
    Yoritaka A, Hattori N, Uchida K, et al. Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc Natl Acad Sci USA 1996;93(7):2696–2701PubMedCrossRefGoogle Scholar
  96. 96.
    Ostrerova-Golts N, Petrucelli L, Hardy J, et al. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. J Neurosci 2000;20(16):6048–6054PubMedGoogle Scholar
  97. 97.
    Lee M, Hyun D, Halliwell B, Jenner P. Effect of the overexpression of wild-type or mutant alpha-synuclein on cell susceptibility to insult. J Neurochem 2001;76(4):998–1009PubMedCrossRefGoogle Scholar
  98. 98.
    Neumann M, Kahle PJ, Giasson BI, et al. Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleinopathies. J Clin Invest 2002;110(10):1429–1439PubMedCrossRefGoogle Scholar
  99. 99.
    Giasson BI, Duda JE, Quinn SM, et al. Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron 2002;34(4):521–533PubMedCrossRefGoogle Scholar
  100. 100.
    Kahle PJ, Neumann M, Ozmen L, et al. Selective insolubility of alpha-synuclein in human Lewy body diseases is recapitulated in a transgenic mouse model. Am J Pathol 2001;159(6):2215–2225PubMedGoogle Scholar
  101. 101.
    Poon HF, Frasier M, Shreve N, et al. Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice: a model of familial Parkinson’s disease. Neurobiol Dis 2005;18(3):492–498PubMedCrossRefGoogle Scholar
  102. 102.
    Heck RW, Tanhauser SM, Manda R, et al. Catalytic properties of mouse carbonic anhydrase V. J Biol Chem 1994;269(40):24742–24746PubMedGoogle Scholar
  103. 103.
    Shah GN, Hewett-Emmett D, Grubb JH, et al. Mitochondrial carbonic anhydrase CA VB: differences in tissue distribution and pattern of evolution from those of CA VA suggest distinct physiological roles. Proc Natl Acad Sci U S A 2000;97(4):1677–1682PubMedCrossRefGoogle Scholar
  104. 104.
    Kasischke KA, Vishwasrao HD, Fisher PJ, et al. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 2004;305(5680):99–103PubMedCrossRefGoogle Scholar
  105. 105.
    Giege P, Heazlewood JL, Roessner-Tunali U, et al. Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 2003;15(9):2140–2151PubMedCrossRefGoogle Scholar
  106. 106.
    Schapira AH. Mitochondrial dysfunction in neurodegenerative disorders. Biochim Biophys Acta 1998;1366(1-2):225–233PubMedCrossRefGoogle Scholar
  107. 107.
    Schapira AH. Causes of neuronal death in Parkinson’s disease. Adv Neurol 2001;86:155–162PubMedGoogle Scholar
  108. 108.
    Sherer TB, Betarbet R, Greenamyre JT. Environment, mitochondria, and Parkinson’s disease. Neuroscientist 2002;8(3):192–197PubMedGoogle Scholar
  109. 109.
    Ferrante RJ, Hantraye P, Brouillet E, Beal MF. Increased nitrotyrosine immunoreactivity in substantia nigra neurons in MPTP treated baboons is blocked by inhibition of neuronal nitric oxide synthase. Brain Res 1999;823(1-2):177–182PubMedCrossRefGoogle Scholar
  110. 110.
    Pennathur S, Jackson-Lewis V, Przedborski S, Heinecke JW. Mass spectrometric quantification of 3-nitrotyrosine, ortho-tyrosine, and o,o’-dityrosine in brain tissue of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine-treated mice, a model of oxidative stress in Parkinson’s disease. J Biol Chem 1999;274(49):34621–34628PubMedCrossRefGoogle Scholar
  111. 111.
    Sherer TB, Betarbet R, Kim JH, Greenamyre JT. Selective microglial activation in the rat rotenone model of Parkinson’s disease. Neurosci Lett 2003;341(2):87–90PubMedCrossRefGoogle Scholar
  112. 112.
    Sherer TB, Kim JH, Betarbet R, Greenamyre JT. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol 2003;179(1):9–16PubMedCrossRefGoogle Scholar
  113. 113.
    Canet-Aviles RM, Wilson MA, Miller DW, et al. The Parkinson’s disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci U S A 2004;101(24):9103–9108PubMedCrossRefGoogle Scholar
  114. 114.
    Palacino JJ, Sagi D, Goldberg MS, et al. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J Biol Chem 2004;279(18):18614–18622PubMedCrossRefGoogle Scholar
  115. 115.
    Valente EM, Abou-Sleiman PM, Caputo V, et al. Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 2004;304(5674):1158–1160.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Rukhsana Sultana
    • 1
  • H. Fai Poon
  • D. Allan Butterfield
  1. 1.Department of Chemistry; Sanders-Brown Center on AgingUniversity of KentuckyLexingtonUSA

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